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Thoracic Ultrasound
Thoracic Ultrasound
ERS monograph
ERS monograph 79
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ERS monograph
Contents
Thoracic Ultrasound Number 79
March 2018
Preface ix
Guest Editors xi
Introduction xiii
4. Pneumothorax 43
Nils Petter Oveland
5. Pleural effusion 64
Christopher Merrick, Rachelle Asciak, Anthony Edey, Fabien Maldonado
and Ioannis Psallidas
6. Interstitial syndrome 75
Luna Gargani
7. Pneumonia 87
Gebhard Mathis
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
https://doi.org/10.1183/2312508X.10001318 ix
References
1. Laursen CB, Rahman NM, Volpicelli G. Introduction. In: Laursen CB, Rahman
NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield,
European Respiratory Society, 2018; pp. xiii–xv.
x https://doi.org/10.1183/2312508X.10001318
ERS | monograph
Guest Editors
Christian B. Laursen
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
https://doi.org/10.1183/2312508X.10001018 xi
Najib M. Rahman
Giovanni Volpicelli
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ERS | monograph
Introduction
Christian B. Laursen1,2,3, Najib M. Rahman4,5,6 and Giovanni Volpicelli7
The sinking of RMS Titanic in 1912 led to the invention of a range of devices as a means
of improving the detection of icebergs. During World War I, the technique was further
developed into an active sound device using quartz for the detection of submarines. In
the following decades and during World War II, the technique was further developed and
named sonar (SOund Navigation And Ranging) [1]. The principles and technologies that
lead to the development of sonar were also noticed amongst physicians. In 1940, Gohr
and Wedekind suggested the use of reflected sound for diagnosing tumours, effusions
and abscesses [2]. Dussik was the first to report the clinical use of reflected US as a
medical diagnostic tool in his exploration of whether visualisation of intracranial
structures and ventricular measurements was possible with US waves [3]. Despite Gohr
and Wedekind’s initial suggestions and studies published by other authors, the use of
TUS as a clinical tool was for many years considered to be limited to the assessment
of pleural effusion [2, 4–6]. A description of the use of TUS as a tool for the assessment
of horses with respiratory diseases challenged this dogma. Rantanen reported the use of
TUS for the assessment and diagnosis of such conditions as lung consolidation,
atelectasis, abscesses, pleural effusion, empyema and pneumothorax in horses [7].
Furthermore, Rantanen’s paper contains descriptions of vertical and horizontal
reverberation artefacts as well as the concept of movement of the “pleural blades” during
respiration in normal lungs, and its absence if pneumothorax is present [7]. These signs
and artefacts were later to be considered key concepts in TUS [8]. The subsequent studies
during the 1990s by researchers such as Targhetta and Lichtenstein lead to the birth of
TUS as an essential diagnostic modality in the assessment of patients with known or
suspected disease in the chest [9–14].
A milestone was reached when the first international consensus conference producing
evidence-based recommendations for point-of-care LUS was published in 2012 [8].
This document achieved the great aknowledgement of becoming the most cited article
of the top 50 published in Intensive Care Medicine, the journal of the European
Society of Intensive Care Medicine; it was even more highly cited than other very
1
Dept of Respiratory Medicine, Odense University Hospital, Odense, Denmark. 2Centre for Thoracic Oncology, Odense University
Hospital, Odense, Denmark. 3Institute for Clinical Research, SDU, Odense, Denmark. 4Oxford Centre for Respiratory Medicine, Oxford
University Hospitals NHS Foundation Trust, Oxford, UK. 5Oxford Respiratory Trials Unit, Nuffield Dept of Medicine, University of
Oxford, Oxford, UK. 6Oxford NIHR Biomedical Research Centre, Oxford, UK. 7Dept of Emergency Medicine, San Luigi Gonzaga
University Hospital, Torino, Italy.
Correspondence: Christian B. Laursen, Dept of Respiratory Medicine, Odense University Hospital, Sdr. Boulevard 29, 5000 Odense C,
Denmark. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
https://doi.org/10.1183/2312508X.10000518 xiii
popular topics in critical care, such as the fluid management of shock and the new
definition of acute respiratory distress syndrome [15]. The consensus analysed 320
articles published prior to 2012. The same group of experts is working on the update,
analysing around 700 articles on LUS published from 2012 to the present day. This
demonstrates the great importance and high impact of TUS in various communities,
including, of course, respiratory medicine.
We were thrilled to be asked to be guest editors of this, the very first ERS Monograph on
TUS. A book solely dedicated to the subject is a clear sign that TUS is now considered to
be an essential bedside tool for the modern respiratory physician. Despite this, and the fact
that the number of published studies describing the clinical use of TUS is steadily
increasing, several aspects are yet to be studied and assessed in robust clinical trials. In
comparison with other types of clinical US (e.g. abdominal US, echocardiography) the
extent of international consensus on several key aspects remains limited. Furthermore,
different forms and TUS approaches have been adopted by many different specialities and
societies, making a consensus process even more difficult. In the context of this
Monograph, we chose to use the following definitions:
• TUS: diagnostic ultrasonography of the thorax. The term chest sonography or LUS is
often used synonymously in the literature [8, 16].
In summary, we hope that this ERS Monograph will facilitate increased consensus, research,
implementation and evidence-based use of TUS to the benefit of the high number of
patients being assessed for diseases of the thorax. This technique must surely now be
regarded as essential.
xiv https://doi.org/10.1183/2312508X.10000518
References
1. Ainslie M. Principles of Sonar Performance Modelling. Berlin, Springer, 2010.
2. Gohr H, Wedekind T. Der Ultraschall in der Medizin. Klin Wochenschr 1940; 19: 25.
3. Dussik K. Uber die moglichkeit hochfrequente mechanische schwingungen als diagnostisches hilfsmittel zu
verwerten. Z Neurol Psychiat 1942; 174: 153–168.
4. Dudrick SJ, Joyner CR, Miller LD, et al. Ultrasound in the early diagnosis of pulmonary embolism. Surg Forum
1966; 17: 117–118.
5. Miller LD, Joyner CR, Dudrick SJ, et al. Clinical use of ultrasound in the early diagnosis of pulmonary embolism.
Ann Surg 1967; 166: 381–393.
6. Joyner CR Jr, Miller LD, Dudrick SJ, et al. Reflected ultrasound in the study of diseases of the chest. Trans Am
Clin Climatol Assoc 1967; 78: 28–37.
7. Rantanen NW. Diseases of the thorax. Vet Clin North Am Equine Pract 1986; 2: 49–66.
8. Volpicelli G, Elbarbary M, Blaivas M, et al. International evidence-based recommendations for point-of-care lung
ultrasound. Intensive Care Med 2012; 38: 577–591.
9. Targhetta R, Bourgeois JM, Balmes P. Echography of pneumothorax. Rev Mal Respir 1990; 7: 575–579.
10. Targhetta R, Chavagneux R, Bourgeois JM, et al. Sonographic approach to diagnosing pulmonary consolidation. J
Ultrasound Med 1992; 11: 667–672.
11. Lichtenstein DA. A bedside ultrasound sign ruling out pneumothorax in the critically ill. Lung sliding. CHEST J
1995. 108: 1345.
12. Lichtenstein D, Mézière G, Biderman P, et al. The comet-tail artifact. An ultrasound sign of alveolar-interstitial
syndrome. Am J Respir Crit Care Med 1997; 156: 1640–1646.
13. Lichtenstein D, Meziere G. A lung ultrasound sign allowing bedside distinction between pulmonary edema and
COPD: the comet-tail artifact. Intensive Care Med 1998; 24: 1331–1334.
14. Lichtenstein D, Mezière G, Biderman P, et al. The “lung point”: an ultrasound sign specific to pneumothorax.
Intensive Care Med 2000; 26: 1434–1440.
15. ICM: 50 most cited articles. www.esicm-old.org/news-article/ICM-news-50-MOST-CITED-2012-June-2015. Date
last accessed: January 1, 2018.
16. Mathis G, Sparchez Z, Volpicelli G. Chest sonography. In: Dietrich CF. EFSUMB Course Book. London, EFSUMB,
2010.
17. Noble VE, Nelson BP. Manual of Emergency and Critical Care Ultrasound. Cambridge, Cambridge University
Press, 2011.
18. Minimal Training Requirements for the Practice of Medical Ultrasound in Europe. Appendix 11: Thoracic
Ultrasound. 2008 [cited 2016 01.03.16] http://efsumb.org/guidelines/guidelines01.asp
Disclosures: C.B. Laursen has received personal fees from GE Healthcare for giving lectures at an US course
organised by the company.
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List of abbreviations
The clinical benefits of LUS manifest in patients ranging from the clinically ill to those who
have suffered trauma. Along with the proper hands-on technique at the bedside, the different
US modalities and parameters of the US machine must be understood in order to acquire
high-quality images on the screen for the physician to translate clinically. Unlike other parts
of the body, the normal healthy lungs themselves are not actually visualised using bedside
US, and what is depicted on the screen is not a true representation of the lung. Instead, LUS
can best be described as the interpretation of US artefacts. Accordingly, the basic US
principles and physics behind these artefacts must be understood in order to learn, apply
and teach LUS. These tenets are reflected in both normal lung (e.g. A-lines, mirror artefact
of the liver above the diaphragm) and diseased or injured lung (e.g. B-lines, pneumothorax).
Cite as: Alerhand S, Graumann O, Nelson BP. Physics and basic principles. In: Laursen CB, Rahman NM,
Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018;
pp. 1–13 [https://doi.org/10.1183/2312508X.10006017].
D ue to the poor penetration of US waves through air, LUS was traditionally considered
a difficult modality to incorporate into practice. Eventually, it was realised that LUS is
mostly a study of its artefacts. This concept laid the foundation for its use in diagnostic and
procedural applications. Accordingly, the basic tenets of US physics must be understood in
order to fully implement these techniques and interpret the acquired images. Moreover,
since the structure of normal lung cannot be directly “seen” in a straightforward way as
with other applications, educators must have a firm grasp on US artefacts in order to teach
these concepts in a simple way that learners can appreciate. This chapter will describe
several basic US concepts and principles that will be used throughout the rest of the book.
1
Division of Emergency Ultrasound, Dept of Emergency Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
2
Dept of Radiology, Odense University Hospital, Odense, Denmark. 3Dept of Clinical Medicine, Odense University, Odense, Denmark.
4
Dept of Clinical Medicine, Aarhus University, Aarhus, Denmark.
Correspondence: Bret P. Nelson, Division of Emergency Ultrasound, Dept of Emergency Medicine, Icahn School of Medicine at Mount
Sinai, 1 Gustave L. Levy Place, New York, NY 10029, USA. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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pressure wave. Upon the reflection and return of these echoes to the transducer, the crystal
element is deformed once again. These deformations generate an electric current that the US
machine converts into an image on the screen. The distance of a given structure on the
screen from the US transducer is determined by the time required for the mechanical
energy of its echo to return. The greyscale representation on the screen is determined by the
intensity of that returning signal, with each echo corresponding to a point on the screen.
The sound waves described above consist of a series of repeating mechanical pressure waves
propagating through a medium (figure 1). The peak pressure of a wave (its height when
mapped out graphically) is defined as its amplitude and is measured in decibels (dB). This
amplitude is a measurement of the strength of the echo returning to the US transducer as
mechanical energy. The machine itself processes this information to determine the
brightness of the structure on the screen. Stronger returning echoes (with higher
amplitude) appear as bright white (or hyperechoic) areas on the screen, whereas
weaker echoes (with lower amplitude) appear dark grey (hypoechoic) or black (anechoic)
(figure 2). In between white and black, there exists a wide range on the continuum referred
to as the greyscale.
The velocity of the sound waves is also of critical importance for interpreting the screen
images and teaching LUS. The velocity is defined as the speed of the US wave, measured in
metres per second. Within any given medium through which the US wave passes, this
velocity remains constant. Some media allow faster propagation than others; some
examples are shown in table 1.
Generally speaking, waves propagate faster when molecules are closer in relation to one
another, and they propagate more slowly with decreased density of molecules. The
resistance to molecular movement in a particular tissue type is referred to as its acoustic
impedance. The US machine uses these different propagation speeds to determine the
distance of a structure from the transducer. It accomplishes this by measuring the time
taken for the wave to reach that particular structure and be reflected back to the transducer.
Pressure
Amplitude
Time
0
Period
Figure 1. Sound wave plotted as time versus pressure. Reproduced and modified from [1] with permission.
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Figure 2. A midrange echotexture, like that of a solid organ, is shown on the left. On the right, the image of
the thorax demonstrates areas that are hypoechoic (A), isoechoic (B) and hyperechoic (C) compared with the
image on the left.
and organs, it is much more difficult to obtain accurate sonographic information from
these structures. This will have an impact on the attenuation of US energy through these
structures, as discussed later in this chapter.
Having described the elements determining the screen image’s characteristics (brightness,
depth), we can now turn to the visual quality of this image. This resolution is determined
by the frequency of the US wave, which is defined as the number of times per second that
the wave repeats. It is measured in hertz (Hz), with 1 Hz being equal to one wave-cycle per
second. US waves include any frequencies above audible sound (20–20 000 Hz). Diagnostic
US uses frequencies ranging from 12 to 2 MHz, with 1 MHz being equal to 1 million Hz.
Waves with high frequencies generate images with high resolution. They utilise more
energy and create more waves per second. These waves thus lose energy more rapidly and
have less energy available to penetrate to deeper distances. In contrast, waves with low
frequencies utilise less energy and create fewer waves per second. Accordingly, the images
produced are of lower resolution. Since these waves lose energy less rapidly, more energy
remains available to penetrate more deeply. Frequency is thus directly correlated with
image resolution and indirectly correlated with tissue penetration. The strength of the
returning signal also depends on the surface structure of the organ. For instance, a linear
surface structure of an organ will return much of the signal directly to the transducer and
therefore have a higher signal (figure 3).
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a) b) c) d)
Figure 3. Depiction of an emitted US beam striking and being reflected off a linear surface structure (a),
compared with surface structures of varying angles and orientations (b–d).
the US wave (directly along its path), while lateral resolution refers to structures lying in a
perpendicular plane to the US beam. A beam is very thin and is created by tens to hundreds
of scan lines. Lateral resolution will generally be inferior. Adjusting the depth of the view on
the screen, as well as the width, will indirectly adjust the focal zone of the US beam.
The velocity, and therefore the frequency and wavelength, can also be described by its
property of attenuation. This is defined as the progressive weakness of a sound wave as it
travels through a given medium. This loss of energy begins upon being emitted from the
transducer, all the way through the return of the echo back to the transducer. Similar to
velocity, each tissue medium has a corresponding attenuation coefficient. This value is
determined by several factors including: the density of molecules of the medium, the
number of different interfaces encountered by the wave and the wavelength (table 2).
Waves do not travel well through aerated lung due to scatter and reflection; they travel
much better through tissue with increased density, such as fluid-filled or fibrotic lung. This
helps to differentiate among well-aerated (i.e. healthy), fluid-filled (i.e. pulmonary oedema,
pulmonary contusion) and consolidated (i.e. pneumonia) lung. With a fluid-filled lung, the
fluid within the alveoli will conduct the wave rather than scatter it. The waves thus become
trapped and are reflected within the alveoli to create hyperechoic vertical “B-lines” that
extend from the pleural interface to the bottom of the screen and move with respiration
(figure 4). The degree of fluid within the alveoli or fibrotic lung tissue corresponds to the
number and size of B-lines. B-lines can also coalesce together and appear as a wide belt
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Air 4500
Bone 870
Muscle 350
Liver/kidney 90
Fat 60
Blood 9
Fluid 6
(“lung rockets”). In newborns, wet lung will have this B-line belt appearance, which
disappears when the lungs fill with air.
With regard to interfaces encountered by the emitted wave, fewer interfaces will be
encountered if the lung tissue is homogeneous, and thus less attenuation will occur. With
more heterogeneous lung, more interfaces will be encountered and more attenuation will
occur. In essence, tissue of the same type and density facilitates the transmission of
sound waves.
Moreover, reflection will be greater with larger differences in acoustic impedance between
tissue interfaces. More energy will be lost to this reflection, and less energy therefore
remains to penetrate further and visualise deeper tissue structures. In relation to LUS, air is
Figure 4. B-lines within the lung. More than three B-lines within a given lung field is indicative of
increased density.
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*
*
* *
*
Figure 5. Vertebral bodies (*) visible behind the window of the liver. Normally, air above the diaphragm (D)
blocks their visualisation above the diaphragm. However, when fluid is present above the diaphragm, the
fluid acts as a window to allow visualisation of the vertebral bodies.
not a good tissue medium for sound wave transduction, as it scatters waves in infinite
directions and precludes organised feedback to the transducer. The difference in acoustic
impedance between tissues thus illustrates why US waves do not allow good visualisation of
structures that lie deep to air, as opposed to fluid. For instance, the “spine sign” refers to
visualisation of the spine deep to the lung when the lung is filled with fluid rather than
filled with air (figure 5).
LUS artefacts
Artefacts represent information from returning echoes that does not correspond to accurate
anatomic information. Failure to recognise US artefacts can lead to misinterpretation of the
images. It is therefore of utmost importance to understand these artefacts and recognise
them in the proper clinical context. For further reading on this subject, the reader is
directed to [5].
Acoustic shadowing
This refers to the dark shadow posterior to a structure that extends to the bottom of the
screen. This occurs when the structure has a different tissue density from the tissue that
immediately preceded it along the plane of the emitted beam. The greater the difference in
density and attenuation between interfaced tissues, the more acoustic energy will be reflected.
These surfaces are thus referred to as strong reflectors. With regard to LUS, the US probe
and gel have roughly the same density as liquid. Upon reaching past the pleura, the air will
scatter the US waves in infinite directions. In contrast, relatively less scattering and reflection
of waves will occur with pulmonary oedema or consolidated lung (roughly liquid-dense).
Reverberation
Reverberation occurs when the emitted beam bounces to and fro between two highly
reflective structures. For LUS, this may appear as recurrent bright hyperechoic arcs displayed
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Figure 6. Reverberation artefacts, known as A-lines (arrows), extending to the bottom of the screen, spaced
out at equidistant intervals from one another.
at equidistant intervals from the transducer to the bottom of the screen. These reflections
between the transducer and the pleura generate “A-lines” (figure 6). A distance equal to the
initial index distance between the skin and pleura separates sequential artefactual lines. In
addition, the parietal and visceral pleura, which are closely apposed to one another in
normal lung, will “trap” the emitted beam, which then travels repeatedly back and forth
between the two surfaces. The machine displays this artefact as a hyperechoic white echo
called a comet tail artefact, which will then appear as a “Z-line” (figure 7).
Refraction artefact
A refraction artefact (or edge shadowing) occurs when an emitted sound beam crosses an
interface of differing tissue densities at an oblique angle. An acoustic shadow will appear
posterior to the point at which the beam crossed this tissue interface and changed its direction.
Figure 7. Comet tail artefact. Although they both arise from the pleura, lung comets (arrow) do not extend
all the way down to the bottom of the screen as B-lines do (see figure 4).
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Mirror imaging
Mirror imaging can produce an artefactual object when an emitted beam undergoes
multiple reflections. Two objects will appear on the screen, one on each side of the strong
reflector, with the deeper one being false. The mechanism for mirror imaging begins when
part of the emitted beam is reflected backwards upon encountering a tissue of differing
density. If this wave then encounters another object, the machine will use its amplitude to
depict its presence on the screen. However, the machine will incorrectly assume that the
initial emitted beam had travelled along a linear path to reach this object lying further than
the index tissue. Based on the longer time that the beam travelled before the return of the
echo, the machine will incorrectly duplicate the object as a false object deep to the index
reflection. This artefact can be visualised when viewing the lung–diaphragm–liver interface
in the sagittal plane of the midaxillary line (figure 8). Mirror imaging is very sensitive to
subtle manipulation of transducer orientation, as the linear plane will be changed.
This refers to artefactual brightness deep to an anechoic structure through which low
attenuation occurs. For instance, since there is low attenuation through fluid-filled
structures (higher propagation speed), the beam passing through a pleural effusion will
have more energy remaining with which to continue travelling deeper towards the vertebral
bodies. As a result, the spine sign will be visualised on the screen (figure 5). Adjacent to
the pleural effusion, for instance through the soft-tissue density of the liver, the spine may
not be as well visualised because there will be less acoustic energy remaining for echoes of
the spine to return with sufficient intensity.
This artefact occurs when acoustic energy emitted outside the central axis of the transducer
is reflected back to the probe. The reflection is interpreted by the machine as an echo
Figure 8. US pulses (long arrow) reflected off a bright reflector such as the diaphragm encounter liver
tissue (short solid arrow) and are then reflected back to the diaphragm and then to the transducer. The
device calculates the extended round-trip time as an encounter with liver tissue deeper than the reflector
(dotted arrow), mapping the liver tissue in this deeper, false location.
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returning from the central axis, not from the sides. It therefore creates a false representation
of that structure in the central axis.
A beam width artefact occurs due to the fact that the US beam is actually a few millimetres
thick, as opposed to our conceptualisation that it occupies zero width. As a result, the
opposing lateral sides of this thin beam may visualise tissues at points of differing
echogenicity. These amplitudes will be averaged out by the machine and depicted on the
screen according to that midrange value.
Probe selection
Each available US transducer carries different properties and can be used to evaluate the
lung. To begin with, the transducers vary in the frequency emitted. A linear transducer
emits a beam with a frequency range of 6–12 MHz, a phased array probe has a range of
1–5 MHz and a curvilinear probe has a range of 2–5 MHz. As mentioned previously,
higher frequencies allow high-resolution images of shallower structures, whereas lower
frequencies allow lower-resolution images of deeper structures. The transducer used to
evaluate the lung depends on the specific application. For instance, the linear transducer is
traditionally used for visualising the pleura–lung interface to evaluate for pneumothorax
(PTX) or B-lines. However, in a patient with a larger body habitus, either of the other two
transducers may suffice for deeper penetration through the excess soft tissue.
The piezoelectric effect described earlier manifests differently with the varying US probe
shapes. To evaluate lung tissue with a linear-shaped probe, for example, the crystals at the
tip of the probe are aligned along a flat plane. The US waves are emitted in a straight line,
the echoes return in this same line and the machine generates a rectangular image with
high lateral resolution. In contrast, with a curvilinear probe, the crystals are embedded
along a curved shape. The US beams emitted from the lateral aspects of the transducer fan
outwards, leading to decreased lateral resolution and a pie-shaped image on the screen.
Tenets of US technique
It is best to maintain the body part to be scanned and the US screen in the same visual
plane of the physician. In this way, the physician can manipulate the probe’s position and
orientation while maintaining a line of sight with the structures on the screen.
Once positioned, the US probe must be applied and wielded in such a way as to maximise
the ability of the piezoelectric effect to produce high-quality images. To begin with,
sufficient gel must be placed along the interface between the probe marker and the patient’s
body. Any air residing in this interface will cause the emitted sound waves to scatter at this
initial point, similar to the situation through well-aerated tissue in the lung.
An appropriate technique consists of holding the probe with the first three fingers, as if
holding a pencil, while using the fourth and fifth fingers for stabilisation against the
patient’s body. In this way, the probe can be maintained in its position with the most ease
for the ultrasonographer and with decreased probe pressure against the patient’s body.
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Lung tissue moves with respiration, and by keeping the probe still in its spot, lung tissue
movement with inspiration and expiration can best be visualised.
The three-dimensional (3D) structures of the body being evaluated are seen on the screen
as two-dimensional (2D) images. Therefore, each structure must be scanned in at least two
orthogonal planes.
The raised or otherwise indicated marker on the transducer corresponds to a dot or marker
on the left side of the US screen. Structures in the body located on the side of the probe
marker correspond to objects on the screen on the side of the dot. This enables the
ultrasonographer to relate the orientation of his or her probe to the image orientation on
the screen (figure 9). Another way to ensure correct probe orientation is to tap on one end
of the probe with the fingers while watching for the side of the screen where this contact is
visualised.
The US probe, along with its emitted beam, can be oriented in the x-, y- or z-axis. To
obtain a longitudinal or sagittal view, the probe is oriented along the long axis of the
patient’s body with the probe marker facing cephalad, or towards the head. These cephalad
structures will be seen on the left side of the screen closest to the marker. To obtain a
transverse or axial view, the probe is oriented along the short axis of the patient’s body,
with the probe marker facing towards the patient’s right. Structures on the patient’s right
will be seen on the left side of the screen closest to the marker.
Patient positioning
Different protocols for scanning have been proposed, and many authors and operators have
particular preferences based on the pathology that is being evaluated. For example,
scanning the anterior chest wall with the patient supine is generally sufficient for evaluating
for PTX, in which the gravitationally dependent air will rise to the anterior-most part of
the pleura. Conversely, a comprehensive assessment of the entire lung, especially the
a) b)
*
Figure 9. The probe marker on the screen (a) corresponds to the probe marker on the probe (b) (both
indicated by *).
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posterior, is necessary to assess for pneumonia. This can be accomplished by using the
“lawnmower technique”, which involves dividing up the lung regions into different zones as
part of a standardised protocol.
US imaging modalities
The US machine consists of several modalities that emit US waves differently, receive the
echoes and translate that information uniquely onto the screen. Brightness or B-mode is
the main modality used for diagnostic imaging of the lung. It converts the returning echoes
of varying amplitudes into the greyscale visualised on the screen. It presents a 2D slice of
the 3D structure being visualised.
Motion or M-mode depicts the motion of a given structure in the transducer’s directed
plane over time. This plane is chosen by the operator’s placement and manipulation of a
vertical line through the object of interest. This line remains anchored at the top and centre
of the screen, but its orientation and direction can be adjusted laterally in either the left or
right direction. On the screen, the motion (or nonmotion) of the structure is plotted along
the y-axis, and time in seconds is plotted along the x-axis. This scanning modality can be
used to evaluate the lung for PTX, as demonstrated by the absence of visceral pleural
sliding deep to the nonmoving parietal pleura (a “lung point” in B-mode and “barcode
sign” in M-mode).
Doppler physics allows the differentiation of reflected sound waves towards or away from
the probe. Objects moving towards the transducer produce a higher reflected frequency,
whereas sources moving away from the transducer produce a lower reflected frequency.
These distinctions can be represented either by colour changes (colour Doppler) or by
audible and graphical peaks (spectral Doppler). In the former, red and blue correspond
to sound waves travelling to and away from the probe, respectively, as indicated by the
legend on the side of the screen. Usually, this legend will show red at the top and blue at
the bottom, with the continuum of colours in between. This means that waves moving
towards the transducer (at the top of the screen) will appear red, whereas waves moving
away from the transducer (at the bottom of the screen) will appear blue. This
information adhering to Doppler physics is sensitive to the position and angle of the
transducer relative to the direction of the waves. For instance, if the angle is at 90°, no
signal will be reflected.
Another Doppler modality called power Doppler is most useful for detection of low-flow
states. This flow is represented on the screen by degrees or gradations of the colour red
only, as it does not provide information about the direction of the flow. It averages several
frames of flow over a number of cardiac cycles. It is less dependent on the angle of the
transducer but is more sensitive to motion artefacts.
The US machine itself consists of several operations that can manipulate the display of the
visualised structures on the screen. The focal zone is the area where the narrowest part of
the US beam is focused and provides the highest lateral resolution. Some US machines
allow this focus to be adjusted laterally. The focal depth can also be adjusted on some
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machines by vertically adjusting the marker located on the side of the screen. The focal
zone should be placed at the level of or just below the structure you want evaluate.
The depth can also be adjusted to allow visualisation of deeper structures, or to limit the
depth to better visualise shallow structures. One side of the screen shows a centimetre scale
for indicating depth.
Adjusting the gain parameter allows adjustment of the display brightness of returning
echoes. Increasing the gain will brighten the entire display field on the screen, whereas
decreasing the gain will darken it. It has an equal impact on signal and noise, and does not
change the amount of US energy entering the body. The gain has no effect on the
resolution of images that appear on the screen. In other words, the quality of the image will
remain the same.
Time gain compensation allows the gain to be changed at specific depths as opposed to for
the entire screen. In addition to enhancing the brightness of a certain structure to be
visualised, this parameter corrects for the decreased energy that remains to reach deeper
structures. These deeper structures undergo more attenuation due to their further location
from the transducer, and hence a greater amount of tissue through which emitted waves
a) b)
c)
Figure 10. Time gain compensation controls vary based on the machine manufacturer. For this device, there
is a knob for near gain (a, inset: top), far gain (a, inset: middle) and overall gain (a, inset: bottom). Here we
see the same image with different time gain compensation settings: a) image demonstrating good overall
gain, with consistent echogenicity throughout the image; b) image showing overgain in the far field;
c) image showing overgain in the near field.
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must propagate. Manipulation of the time gain compensation will enhance the brightness
of these deeper structures, because otherwise they would always appear darker than their
more shallow counterparts along the transducer’s imaging plane (figure 10).
Conclusion
LUS can be utilised and interpreted in the medical care of a wide range of patients. In
addition to understanding the basic tenets of US physics, physicians must be well
acquainted with the different sonographic modalities and parameters of the US machine
itself. Furthermore, it is vital to recognise that, unlike other tissues in the body, normal
healthy lung is not actually visualised on the screen. Instead, the lung tissue is seen as
artefacts governed by the aforementioned tenets of US physics. With a proper
understanding of these tenets, LUS can thus be interpreted to great effect for both normal
and diseased lung.
References
1. Ma OJ, Mateer JR, Reardon RF, et al., eds. Ma and Mateer’s Emergency Ultrasound. 3rd Edn. Maidenhead,
McGraw-Hill Education, 2013; p. 31.
2. Hoskins P, Martin K, Thrush A, eds. Diagnostic Ultrasound: Physics and Equipment. Cambridge, Cambridge
University Press, 2010.
3. Postema M. Fundamentals of Medical Ultrasonics. London, Soon Press, 2011.
4. Schmitz G. Ultrasound in medical diagnosis. In: Pike R, Sabatier P, eds. Scattering: Scattering and Inverse Scattering
in Pure and Applied Science. London, Academic Press, 2002, pp. 162–174.
5. Feldman MK, Katyal S, Blackwood MS. US artifacts. Radiographics 2009; 29: 1179–1189.
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| Chapter 2
Technique and protocols
Christian B. Laursen1,2,3, Jesper R. Davidsen1,2,4 and Fergus Gleeson5
Cite as: Laursen CB, Davidsen JR, Gleeson F. Technique and protocols. In: Laursen CB, Rahman NM,
Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018;
pp. 14–30 [https://doi.org/10.1183/2312508X.10006117].
The primary aim of this chapter is to provide the US novice with a description of the basic
concepts and approach needed to be able to perform a systematic FTUS examination, as
well as some basic knowledge regarding a diagnostic examination (TUS). The reading of
this chapter does not replace theoretical and practical training, or a competency assessment
prior to performing unsupervised examinations in clinical practice.
The chapter will provide a brief overview of the basics of sonoanatomy of the thorax, a
stepwise approach to the techniques and protocols for performing FTUS, and some of the
basic differences and principles when performing TUS. Descriptions of more detailed
sonoanatomy, pathology and specialised techniques are addressed in subsequent chapters in
this Monograph describing specific conditions and examination techniques.
1
Dept of Respiratory Medicine, Odense University Hospital, Odense, Denmark. 2Centre for Thoracic Oncology, Odense University
Hospital, Odense, Denmark. 3Institute for Clinical Research, SDU, Odense, Denmark. 4South Danish Center for Interstitial Lung
Diseases (SCILS), Odense University Hospital, Odense, Denmark. 5Dept of Radiology, Churchill Hospital, Oxford University Hospitals
NHS Foundation Trust, Oxford, UK.
Correspondence: Christian B. Laursen, Dept of Respiratory Medicine, Odense University Hospital, Søndre Boulevard 29, 5000 Odense C,
Denmark. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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Chest wall
Structures such as skin, s.c. tissue, muscles and connective tissue are visible just beneath the
transducer. The connective tissue appears hyperechoic, and often more hyperechoic
horizontal linear structures can be seen, representing connective tissue, such as muscle
fascia. The two ribs aligning the ICS are visible as two hyperechoic lines with an
underlying shadow (figure 2) [1, 2].
Pleura
Placed just below and between the two ribs, a hyperechoic horizontal line is seen
representing the visceral and parietal pleura. Most conventional clinical US machines are
not able to differentiate the two pleural surfaces from each other. The combined surfaces
are termed the pleural line (figure 2) [1, 3, 4].
Since several structures as well as the pleural line may appear as a horizontal hyperechoic
(white) line on the US screen, it is essential to be able to identify which of these lines
represents the pleura. LICHTENSTEIN et al. [4] described how to use the “bat sign” in order to
facilitate correct identification of the pleural line. The term “bat sign” is used since the two
ribs adjoining an ICS (hyperechoic surface with posterior shadowing) and the pleural line
resemble a bat flying towards the US screen (figure 3). Thus, the following two steps
Figure 1. A curved low-frequency transducer placed in zone L1. The orientation marker (arrow) is placed
cranially to facilitate identification of the “bat sign” on the US screen.
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Figure 2. Normal sonoanatomy of the thorax. The muscles, fascia and s.c. tissue of the chest wall (CW) are
placed just below the transducer. The superficial surface of the ribs (R) can be seen as hyperechoic
horizontal lines with posterior shadowing (*). The visceral and parietal pleura can be seen as a hyperechoic
horizontal line, the pleural line (PL), just below the ribs. The area below the pleural line (“L”) is due to
artefact generation and does not represent the air-filled lung, which cannot be visualised using US.
should be performed prior to assessing the pleura line: 1) ensure that the scanning plane is
vertical and the orientation marker is placed cranially (figure 1); and 2) use the “bat sign”
sign to identify the pleural line (figure 3).
Once this is done, the transducer can be rotated approximately 90° (depending on the
angle of the ribs at the area being scanned) counterclockwise to avoid the ribs and visualise
the entire pleural line in the ICS.
The presence or absence of three findings is of importance when assessing the pleural line:
1) lung sliding, 2) the lung pulse and 3) B-line(s).
Figure 3. Identification of the “bat sign” is performed to identify the pleural line (PL) as being placed just
below the two ribs (R). The ribs with posterior shadowing represent the bat’s wings and the pleural line
represents the head of the bat.
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Lung sliding
Lung sliding is seen as a horizontal movement of the pleural line in synchrony with the
respiratory cycle, indicating a sliding movement of the visceral pleura against the parietal
pleura [3, 5]. Lung sliding is due to the up-and-down movement of the visceral pleura in
synchrony with the piston-like respiratory movement of the diaphragm [6]. Several factors
may affect the magnitude of lung sliding (e.g. lung zone scanned, patient tidal volume,
underlying disease and intubation) [6–8]. When air separates the two pleural layers (e.g.
pneumothorax (PTX)), the movement disappears and cannot be detected with US. In such
cases, the pleural line represents only the parietal pleura, which is still visible but does not
slide since it is fixed to the chest wall [5, 9]. Apart from PTX, other conditions may also
cause absence of lung sliding (e.g. fibrotic involvement in interstitial lung diseases, prior
pleural empyema or sequelae from a prior intrathoracic operation) [6–8, 10, 11].
Lung pulse
As well as lung sliding in synchrony with the respiratory cycle, the pleural line may also
move in synchrony with the cardiac pulse. This movement, termed the “lung pulse”, is
caused by the force of the cardiac pulsation being transmitted to the lung and hence to the
visceral pleura [3, 7]. The lung pulse is not always present in healthy persons and is
generally easiest to visualise in areas where the lung is in close contact with the
pericardium and heart. Like lung sliding, the lung pulse indicates that the visceral and
parietal pleural surfaces are juxtaposed at the location of the probe [7, 8, 12].
B-lines
A B-line has been defined as a hyperechoic, laser-like, vertical reverberation artefact
originating from the pleural line. B-lines are continuous from the pleural line to the bottom
edge of the screen and do not fade in intensity [3, 13, 14]. Other reverberation artefacts
may also originate from the pleural line, but, in contrast to B-lines, they fade out relatively
quickly and do not continue to the bottom edge of the screen (figure 4) [3, 4]. If lung
sliding is present, B-lines move in synchrony with the sliding [15]. B-lines are discussed in
more detail in another chapter in this Monograph [16].
Figure 4. A B-line can be seen to originate at the pleural line (PL) and extends vertically to the bottom of
the screen without fading. Another vertical artefact can also be seen (“Z”). However, this quickly fades when
extending vertically and does thus not fulfil the criteria for a B-line. Such artefacts have been termed
Z-lines by LICHTENSTEIN et al. [7].
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Lung
The normal air-filled lung cannot be visualised using conventional 2D-mode US. Due to
the difference in acoustic impedance, the US signal is reflected at the surface of the lung
(visceral pleura). The reflection is seen as a hyperechoic line with posterior shadowing. In
persons with normal, aerated lung tissue, any structures that can be seen on the US screen
below the pleural line are thus due to artefact generation [1, 3, 4].
Diaphragm
The superficial part of the diaphragm can be recognised as a hyperechoic “double line”
located just below the ribs. The more hypoechoic area between the lines represents the
muscle fibres of the diaphragm. As the diaphragm contracts, movement and thickening of
the fibres can be observed [17]. The more central portion or tendinous component of the
diaphragm can be visualised when using either the liver or the spleen as an acoustic
window [18–21].
Focused TUS
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diagnostic accuracy for many of the common conditions seen in a variety of emergency
settings [3, 10, 24, 26–34]. When used as part of whole-body ultrasonography, FTUS has
been shown to help identify patients with missed life-threatening conditions, and it
significantly increased the proportion of correctly diagnosed and treated patients admitted
to an emergency department with respiratory symptoms [35, 36]. FTUS, alongside other
forms of focused US, should be used as an integrated part of the clinical assessment of
these patients.
Several different FTUS protocols and approaches have been described; however, no
international consensus for the use of one specific protocol has been obtained [3]. Many
protocols divide the thorax into a number of scanning points, areas or zones that are
assessed using US, but the number of zones varies significantly for each protocol [4, 9, 12,
13, 31, 37–48]. The number of areas or zones scanned is of importance, since diagnostic
criteria for some conditions (e.g. interstitial syndrome) are defined by the number of zones
in which specific findings are represented. In this way, the number of areas or zones may
potentially affect the diagnostic accuracy when compared with other protocols or with use
in other settings [3, 24, 31, 49]. As well as the protocols describing FTUS, several other
studies have described the use of FTUS principles as an integrated part of a whole-body
ultrasonography approach in which several organs or structures are assessed in a given
patient population or clinical setting [4, 34, 35, 50–54]. Many studies have used an
eight-scanning-areas approach, as described by VOLPICELLI et al. [44], for assessing the
anterior and lateral thoracic surfaces; similarly, the definition of interstitial syndrome is also
based on these principles [3, 44]. However, this approach does not include assessment of
the posterior thoracic surface, which is why posteriorly positioned pathology may be
missed using this protocol [44]. LAURSEN et al. [35] modified the protocol to a 14-zone
scanning protocol by adding assessment of the posterior surfaces using principles described
previously by LICHTENSTEIN et al. [4], and this has subsequently been validated in
prospective studies in a variety of settings [35, 36, 55, 56]. The use of this 14-zone FTUS
approach alongside FoCUS and limited-compression ultrasonography of the deep veins has
been validated for assessing patients with respiratory failure in an emergency department
setting [35, 36]. Using the 14-zone approach, each hemithorax is divided into anterior,
lateral and posterior surfaces, which can be further subdivided into smaller squares
representing a scanning zone. Each of these scanning zones should be assessed using FTUS.
Each of the scanning zones can be denoted from 1R to 7R on the right and from 1L to 7L
on the left (figure 5) [35]. As described in subsequent sections, when assessing the thoracic
lateral and posterior surfaces, it is of paramount importance to begin the assessment with
identification of the upper abdominal structures and diaphragm. This is done in order to
avoid mistaking abdominal structures as thoracic structures and vice versa (e.g. fluid in the
stomach wrongly diagnosed as pleural effusion). To facilitate this approach, caudal zones
(e.g. zones 3 and 5) have lower numbers than cranial zones (e.g. zones 4, 6 and 7) [35].
Predefined questions
FTUS should be performed in a focused manner in order to answer specific and clinically
relevant yes/no questions [22]. The FTUS protocol aims to answer the following four
predefined yes/no questions: 1) Is a PTX present? 2) Is a pleural effusion present? 3) Is
interstitial syndrome present? 4) Is obvious pathology present?
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R7 L7
R1 L1
R4 L4 R6 L6
R2 L2
R3 L3 R5 L5
Figure 5. Focused TUS (FTUS) scanning zones using a 14-zone approach. The numbers of the zones denote
the optimal scanning sequence. When scanning the lateral and posterior surfaces of the thorax, the
examination should begin in the most caudal zones (e.g. zones 3 and 5) to ensure accurate identification of
the border (diaphragm) between the chest and upper abdomen.
Several studies have documented that FTUS has a high diagnostic accuracy for conditions
included as part of the predefined questions [10, 28, 35, 36, 54, 57–61]. It is, however, of
importance to underline that FTUS has not been validated for a number of other conditions
(e.g. pulmonary embolism, malignancy, chest wall pathology), and it has not been determined
whether there is a substantial difference in diagnostic accuracy when FTUS is compared
directly with TUS. Any incidental FTUS findings should therefore generally be referred to
TUS performed by a trained expert. The same principles apply when reporting FTUS
findings; terms such as “normal examination” should generally be avoided, since they imply
the performance of TUS. FTUS reporting should be limited to answering the predefined
questions: “No signs of PTX, pleural effusion or interstitial syndrome.”
Basic US principles have been addressed in the previous chapter in this Monograph [62]. A
few key aspects regarding FTUS are mentioned in the following sections.
Choice of transducer
A curved low-frequency transducer is generally the preferred transducer for FTUS as it has
an acceptable image quality for both superficial and deep structures and can be used to
answer the focused questions. In some scenarios, the use of other transducers can be
considered, such as a microconvex transducer, linear transducer or phased array transducer.
Microconvex transducer
A microconvex transducer is an acceptable all-around transducer for FTUS. Due to its small
size, it is often easier to use when the patient can only be examined in the supine position
(e.g. emergency setting, intensive care unit (ICU)) or when scanning children [3, 4].
Linear transducer
A linear transducer generates excellent images of superficial structures, such as ribs and the
pleura, but deeper structures can be difficult to assess. It excels when the only clinically
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If a dedicated FTUS pre-set is available, then this should be used. In the absence of such a
pre-set, an abdominal pre-set can be used when using a curved transducer, or a
musculoskeletal pre-set when using a linear transducer. The presence or absence of US
artefacts plays a pivotal role when performing FTUS. Software (e.g. harmonics, cross-beam)
minimising artefacts should generally be switched off when performing FTUS [3].
Normally, the only mode needed for FTUS is B-mode.
Patient positioning
Initially, the anterior and lateral surfaces of each hemithorax are scanned with the patient in
the supine position. Subsequently, the patient is asked to sit up and the zones on the
posterior surface are scanned. Some patients with acute respiratory failure cannot be placed
in a supine position due to severe dyspnoea. Anterior, lateral and posterior surfaces are then
scanned with the patient in the sitting position. The patient position will affect the position
of free air (e.g. PTX) and free fluid (e.g. simple pleural effusion) in the pleural cavities, and
patient positioning is therefore of importance when assessing the patient for these two
conditions. The supine position is the recommended position for assessing the presence of
PTX, since the air will tend to be placed anteriorly in the chest cavity, an area that is easily
assessable using FTUS. If the patient is placed in the sitting position, a small PTX can be
missed if the air is located solely at the apex of the chest cavity, an area that is more difficult
to assess using US [3]. In comparison, patients should be placed in the sitting position when
scanning to detect a pleural effusion, in which case the fluid will tend to be in the lower
posterior zones. Some critically ill patients may, however, not be able to sit up to enable
assessment of the posterior zones. In this case, the posterior surfaces can be scanned either
directly or indirectly (see section on Supplementary scanning techniques).
Once the machine has been prepared for the examination and the patient has been
positioned in the most optimal position possible, the FTUS examination can be performed.
The transducer is placed in the first of the scanning zones in the vertical plane above an
ICS with the orientation marker facing cranially (figure 1). The operator then notes
whether PTX, pleural effusion, multiple B-lines or other obvious pathology is present. Once
this has been assessed, the transducer is moved to the next scanning zone, and this
approach continues until all accessible zones have been scanned.
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Each zone scanned as part of the 14-zone FTUS protocol has some special characteristics
and potential pitfalls. Some of these are described for each zone.
Zones R1 and L1
Transducer placement: the transducer should be placed in the second ICS a few centimetres
lateral to the sternum. If the transducer is placed too far laterally, additional tissue (e.g.
muscle, breast) will be present between the transducer and the pleura, possibly decreasing
image quality.
Zone findings: these resemble the basic sonoanatomy pattern described previously (figure 2).
Zone R2
Transducer placement: when moving the transducer from zone R1 to R2, the transducer is
moved to ICS4 a few centimetres lateral to the sternum. The anatomical landmark is the
lower edge of the pectoralis muscle or breast tissue. In most persons, this point corresponds
to the anterior phrenicocostal sinus, and both the pleural line and the superficial part of
the diaphragm can be visualised. In some patients, pericardium or mediastinal tissue will
be visible instead of the pleural line. Moving the transducer a few centimetres laterally will
often allow visualisation of the pleural line.
Zone findings: zone R2 findings consist of the pleural line on the left of the screen and the
diaphragm and liver on the right of the screen.
Zone L2
Transducer placement: when moving the transducer from zone L1 to L2, the transducer
should gradually be moved caudally one ICS at a time until the pericardium and heart
appear on the right side of the screen. This approach reduces the risk of misinterpreting
the pericardium as the pleural line. In patients with hyperinflation of the lungs or
emphysema, the lung may obscure the view of the pericardium and heart. Zone L2 findings
then often resemble the findings in zone R2.
Zone findings: zone L2 findings consist of the pleural line on the left of the screen and the
pericardium and heart on the right.
Zone R3
Transducer placement: assessment of zone R3 should always begin with identification of the
liver, right kidney and diaphragm. Most often, this can be done by placing the transducer in
the midaxillary line on the lower part of the chest. Once the liver has been identified, the
pleural line can be identified either by asking the patient to take a deep breath or by
gradually moving the transducer to an ICS cranially until the pleural line can be visualised.
Zone findings: zone R3 findings consist of the pleural line on the left of the screen and
abdominal structures on the right of the screen (figure 6). When the patient takes a deep
breath, the pleural line is seen moving in from the left with “removal” of the liver due to
posterior shadowing and movement of the diaphragm. This finding is also termed the
“curtain sign” since it resembles a curtain being drawn, obscuring the view to the
abdominal structures [63–67].
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Zone L3
Transducer placement: assessment of zone L3 should also always begin with identification
of the structures in the upper abdomen (e.g. spleen, left kidney) and diaphragm. Since the
spleen is smaller and more posteriorly located than the liver, the transducer should be
placed more posteriorly in zone L3 than when assessing zone R3. Most often, this can be
done by placing the transducer in the posterior axillary line on the lower part of the chest.
In the supine patient, this can be achieved by simply resting the hand with the transducer
on the underlying mattress and then scanning the left side of the thorax at that point. Once
the spleen and left kidney have been identified, the pleural line can be identified either by
asking the patient to take a deep breath or by gradually moving the transducer to an ICS
cranially until the pleural line can be visualised.
Zone findings: zone L3 findings consist of the pleural line on the left of the screen and the
spleen (and left kidney) on the right of the screen. Movement of the lung during breathing
also appears as the “curtain sign” on the left side. When fluid is present in the stomach, it
can sometimes also be seen, even though a more posterior approach has been used.
Zones R4 and L4
Transducer placement: the transducer should be placed in approximately ICS3 in the
midaxillary line. This is often the area with the shortest distance between the transducer
and the pleural line. When scanning zone 4, there is often a tendency to have the
transducer footprint tilted in a cranial direction; in the corresponding US image, the pleural
line will be angulated rather than horizontal. If this is the case, the transducer should be
tilted until the pleural line is horizontally placed.
Zone findings: zone 4 findings on both sides resemble the basic pattern described
previously (figure 2).
Zones R5 and L5
Transducer placement: assessment of zones R5 and L5 should always begin with
identification of the upper abdominal structures (e.g. liver/spleen, right/left kidney) and
Figure 6. Sonoanatomy when assessing zone R3 and the upper abdomen on the right side. The liver (Lvr),
right kidney (RK) and diaphragm (D) can be visualised. The pleural line (PL) is seen in the top left corner
with posterior shadowing (*). The movement of the pleural line causes the shadowing to obscure the view to
the upper abdomen when the patient takes a deep breath. This is known as the “curtain sign”.
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diaphragm. This can be done by placing the transducer at the lower part of the chest at a
vertical line corresponding to the tip of the scapulae (inferior angle). If the transducer is
placed too medially, the distance between the transducer and the pleura will be longer, and
since the surface of the pleura is no longer perpendicular to the surface of the thorax, the
pleural line will often appear thickened, mimicking pathology. Once the liver has been
identified, the pleural line can be identified either by asking the patient to take a deep
breath or by gradually moving the transducer to an ICS cranially until the pleural line can
be visualised.
Zone findings: zone R5 findings consist of the pleural line on the left of the screen and the
liver and upper abdominal structures on the right of the screen.
Zones R6 and L6
Transducer placement: the transducer is placed in the posterior midclavicular line at a level
corresponding to the middle part of the scapulae. The best images can generally be
obtained by placing the transducer as close to the medial border of the scapulae as possible.
An additional area of the pleura can be assessed in zone 6 if the patient is asked to place
the hand of the side being scanned on the opposite shoulder, causing the scapula to move
and rotate laterally.
Zone findings: these resemble the basic sonoanatomy pattern described previously (figure 2).
When compared with zone 5, the distance between the ribs is shorter and the extent of
lung sliding is often less pronounced.
Zones R7 and L7
Transducer placement: the transducer is placed in the posterior midclavicular line at a level
corresponding to the cranial part of the scapulae. The best images can generally be
obtained by placing the transducer as close to the medial border of the scapulae as possible.
An additional area of the pleura can be assessed in zone 7 if the patient is asked to perform
the same manoeuvre as described for zone R6/L6.
Zone findings: zone 7 findings on both sides resemble the basic pattern described
previously (figure 2). When compared with zone 6, additional muscle tissue is often
present between the transducer and the pleural line, the distance between the ribs is often
even shorter and the extent of lung sliding is often additionally decreased. In patients with
small tidal volumes, lung sliding cannot always be identified in zone 7. If doubt exists as to
whether lung sliding is present or absent, it is often helpful to compare the findings with
zone 7 on the opposite side.
Assessment of the posterior zones is not always possible (e.g. critically ill patients, trauma
patients). The posterior surfaces can then be scanned either directly or indirectly. Direct
assessment can be performed with the patient lying on their side, in a decubitus position,
or alternatively the transducer can be inserted in between the mattress and the patient,
making it possible to scan at least part of the posterior surface. The indirect approach
involves use of the liver and spleen as acoustic windows in order to identify the presence of
the “spine sign” [22].
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In patients with pathology in the lower posterior part of the pleural cavity (e.g. pleural
effusion, consolidation of the lower lobe), the normal air-filled lung is replaced by fluid or
tissue. Since the US signal is no longer reflected, the structures can be assessed using US,
which enables visualisation of the underlying thoracic spine. The visualisation of an
extended part of the thoracic spine is thus an indirect marker of pathology in the lower
posterior part of the pleural cavity. This finding is known as the presence of the “V-line” or
“thoracic spine sign” (figure 7), and has a high diagnostic accuracy for the diagnosis of
clinically relevant pleural effusion in the supine patient [68, 69].
The direction of the US beam is then aimed in a more posterior direction by panning the
transducer. For inexperienced operators, it can be of help to look at the patient and
positioning of the transducer, which is placed in the midaxillary line so that it is pointing
towards the spine. When the correct image has been obtained, the liver, right kidney,
diaphragm and underlying spine can be identified in the same image. The spine is typically
seen as a horizontal, wavy, hyperechoic line where the individual vertebrae can often be
identified. Once this image has been obtained, it can be noted whether the visualised spine
below the liver and kidney can also be identified deep to the diaphragm.
a) b)
Figure 7. The “thoracic spine sign”. a) Normal findings in zone R3. The structures of the upper abdomen
(liver (Lvr) and right kidney (RK)) can be used as an acoustic window to visualise the spine (blue line). Due
to shadowing from the normal aerated right lung, the spine cannot be visualised in the area cranial to the
liver (arrowhead). b) The vertebrae (blue lines) located below the upper abdominal organs can be as in a.
The presence of pleural effusion (Eff ) allows visualisation of the vertebrae (yellow lines) cranial to the liver.
The visualisation of these vertebrae is known as the presence of the “thoracic spine sign”.
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Since FTUS is used in critically ill patients in a variety of settings (e.g. pre-hospital,
emergency department, ICU, operating room), it may not always be possible to perform a
standardised FTUS examination. Thus, the standard protocol may sometimes be modified
for the given setting. By using FTUS in a standardised and systematic approach, its clinical
utility remains high, and the diagnosis and exclusion of important diagnoses, such as PTX,
pleural effusion and interstitial syndrome, are often still possible.
Thoracic ultrasound
Equipment
Often the equipment required for performing FTUS can also be used for TUS. Dedicated
high-end US machines may, however, be needed for increased image quality and
supplementary scanning modes.
Choice of transducer
FTUS can often be performed using only one transducer for the examination. When
performing TUS, changing between different transducers during the examination can be
useful in order to obtain additional information. The interchangeable use of a curved
low-frequency transducer and a high-frequency linear transducer is often an excellent
combination due to optimal image quality when a given structure is assessed. The smaller-
sized microconvex transducers excel as an alternative when the patient can only be
examined in the supine position. Phased array transducers are generally less suitable but
may be of use in patients with complex pleural effusions, since the characteristics of the
transducer make it ideally suited for identifying septa within a pleural effusion. Due to its
small footprint, a phased array transducer is also useful when assessing the mediastinum.
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Pre-set
Since TUS may be performed to assess a wide variety of different deep and superficial
structures, the pre-set should continuously be altered whenever a new organ or anatomical
structure is assessed. If no predefined TUS pre-set is available, an abdominal pre-set is
often useful for deeper structures (e.g. lung, pleural effusion) and a musculoskeletal pre-set
for superficial structures (e.g. chest wall, parietal pleura).
Software
US scanning modes
2D-mode scanning is by far the most widely used mode when performing TUS.
Supplementary M-mode can be used for measuring purposes (e.g. amplitude of
diaphragmatic movement), and is recommended by some experts in cases where there is
doubt as to whether PTX is present or not [4, 5, 70]. Colour Doppler mode assessment is a
useful adjunct to the conventional B-mode scanning. Doppler mode can be used to assess
vascularisation of lung parenchymal pathology, lymph nodes and vessels. Other US modes
that can be used as part of more highly specialised sonography are spectral analysis, CEUS,
elastography and image fusion.
Examination technique
The basic TUS principles are the same as for FTUS. When performing TUS, the entire
surface of the thorax, pleura and lungs is assessed, and each ICS is thoroughly examined in
each zone. The use of scanning zones when performing TUS is used primarily as a tool to
describe and document the position of findings, as an alternative to describing the location
using other anatomical landmarks (e.g. ICS4, midaxillary line). Additionally, the use of the
same scanning zones for FTUS and TUS facilitates the comparison of reports and a
stepwise approach to learning FTUS/TUS, and also strengthens the multidisciplinary use of
FTUS/TUS.
As well as assessment of the thoracic wall, pleural cavities and lungs, the TUS examination
can be supplemented with assessment of other anatomical structures and organs, such as
the neck and supra- and infraclavicular regions, the diaphragm, the upper abdomen, the
mediastinum and the heart. Assessment of these structures is described in later chapters in
this Monograph [71–75]. Patients in which TUS reveals incidental findings in other
adjoining structures (e.g. heart, upper abdomen) should generally be referred for
subsequent assessment and imaging by a relevant specialist trained in diagnostic US (e.g.
echocardiography, diagnostic abdominal US) of the given structure.
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Conclusion
Most literature and published studies regarding FTUS and TUS have been classical
diagnostic accuracy studies and, to a lesser extent, studies assessing clinical impact. The art
of integrating the US examination into the clinical context is seldom discussed, even
though this is probably the most difficult skill to learn. Any physician performing FTUS or
TUS should be well aware of and respect the limitations of the US examination in itself and
the limitations in the physician’s own skills and experience. As well as training in practical
US skills, inexperienced physicians should also focus on the art of integration of imaging
into clinical practice.
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| Chapter 3
Chest wall and parietal pleura
Maged Hassan1,2,3 and Najib M. Rahman1,2,4
US examination of the chest wall and parietal pleura can reveal a number of pathologies and
is useful in various clinical settings. Chest wall pathologies that are identifiable during US
examination include haematomas, abscesses, rib abnormalities and lymph nodes.
Additionally, useful information about pleural infection and neoplasia can be gathered using
US. In addition to its diagnostic potential, US provides guidance for safe execution of
percutaneous sampling and/or drainage of chest wall and pleural abnormalities.
Cite as: Hassan M, Rahman NM. Chest wall and parietal pleura. In: Laursen CB, Rahman NM, Volpicelli G,
eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 31–42
[https://doi.org/10.1183/2312508X.10006217].
P erforming TUS for examination of the chest wall and pleura is indicated in a number
of situations. In many instances, it is used to explore further and examine in more
detail pleural or parietal abnormalities first seen on a chest CT scan. In other situations,
TUS is used up front, particularly for evaluation of patients with localised thoracic lesions.
It is the investigation of choice to first characterise palpable chest wall lesions that are
picked up during clinical examination [1]. In patients with chest trauma, TUS can detect
chest wall, pleural and lung injuries with high sensitivity [2]. TUS is especially valuable in
delineating chest wall/pleural involvement by peripheral pulmonary masses, which has an
important implication for staging. Finally, TUS is usually preferred to CT for guidance of
invasive drainage and biopsy procedures due to its safety profile, live procedural ability and
lower cost [3].
Technical considerations
The exact technique of chest sonographic examination, as well as the physics of TUS, is
covered elsewhere in this Monograph [4, 5]. Generally speaking, examination of the chest
wall and parietal pleura can be achieved with a combination of low-frequency probes
(range 3.5–5 MHz), a convex array (curvilinear) or phased array (sector) probe, and
higher-frequency linear array probes (range 5–7.5 MHz) [6–8].
1
Oxford Centre for Respiratory Medicine, Oxford University Hospitals NHS Foundation Trust, Oxford, UK. 2Oxford Respiratory Trials
Unit, Nuffield Dept of Medicine, University of Oxford, Oxford, UK. 3Chest Diseases Dept, Faculty of Medicine, Alexandria University,
Alexandria, Egypt. 4Oxford NIHR Biomedical Research Centre, Oxford, UK.
Correspondence: Maged Hassan, Oxford Centre for Respiratory Medicine, Churchill Hospital, Old Road, Oxford OX3 7LE, UK. E-mail:
[email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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Chest wall anatomy and pathology are ideally appreciated with a linear probe, given the
superficial position of the chest wall [9]. Some sonographers find the phased array probe
useful when examining the pleura and lung in patients with narrow intercostal spaces [6].
This probe is especially useful for moving structures, such as the heart. The convex probe,
however, is generally the preferred probe for pleural and peripheral lung examinations, and
is particularly superior to the phased array probe during guidance of invasive procedures
[10, 11]. This is because the phased array probe has a narrow footprint, which misses large
parts of the superficial layer of the chest wall and consequently cannot capture a portion of
the invading needle.
Most of the TUS examination of the chest wall and pleura is conducted in the B-mode
[7]. M-mode examination is not particularly useful except for exclusion of pneumothorax
(PTX) following biopsy, given that it is a mode that captures movement. In addition to
grey-scale imaging, colour Doppler is important for delineation of the vascular pattern of
lesions, which is an essential component of characterisation and diagnosis. Doppler is
used to identify the intercostal artery, which is necessary to minimise the risk of vascular
injury during percutaneous invasive interventions [10, 12].
During TUS examination, the authors prefer to orient the scanning probe parallel to the
ribs to obtain the maximum view of the pleura and to avoid the acoustic shadowing
created by the ribs (figure 1b). The perpendicular probe orientation is useful mainly
during examination of the acutely breathless patient in order to identify and quantify
the number of intercostal comet tail artefacts, which is helpful in the diagnosis
of pulmonary oedema [13]. As well as this indication, the parallel orientation should
be followed during examination of the chest wall, pleura and lung to maximise the
acoustic window.
a) b)
1 1
2 2
3 3
4 4 5
6 6
Figure 1. Layers of the chest wall as seen using a high-frequency linear probe. a) Parallel orientation;
b) perpendicular orientation. 1: skin; 2: s.c. fat; 3: muscles; 4: intermuscular septum; 5: outer rib cortex
(with acoustic shadow seen deeper); 6: pleural band.
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CHEST WALL AND PARIETAL PLEURA | M. HASSAN AND N.M. RAHMAN
Chest wall
Anatomy
The chest wall is composed of four layers: the skin, s.c. fat, various layers of chest wall
muscles, and ribs and intercostal muscle [14]. Very detailed anatomical images are made
possible by high-frequency TUS (figure 1a). The skin appears as a thin isoechoic layer
followed by s.c. fat, which is hypoechoic with interposing isoechoic fascial septa [12]. On
TUS, muscles appear as generally hypoechoic with echogenic striae and dots depending on
the orientation of the muscle fibres [12]. Different muscles are separated by dense fascial
septa that appear hyperechoic. The outer cortex of ribs is hyperechoic, and since it causes
reflection of most of the US waves, all deeper structures are obscured and only an anechoic
shadow of the overlying rib (termed an acoustic shadow) is seen (figure 1b).
The intercostal vessels run between intercostal muscles. They run in the middle of the
space in the most medial 5 cm of their course anteriorly and posteriorly. For the rest of the
course, the neurovascular bundle is hidden under the lower border of the superior rib,
which makes it elusive for TUS identification. Some subjects have an aberrant course,
especially in the elderly, and excluding the presence of an unprotected artery in the pleural
space is essential before interventional pleural procedures (figure 2).
Pathology
The majority of chest wall lesions tend to be localised [12]. TUS has the potential to
uncover lesions that are too subtle to be picked up on conventional CXRs. This makes TUS
the investigation of choice in patients with localised pleuritic pain or a palpable lesion [15].
The range of chest wall lesions that can be identified by TUS is summarised in table 1
[1, 7, 10]. As mentioned previously, grey-scale images should ideally be complemented with
colour Doppler scanning for identification of the vascular pattern of a given lesion [12].
a)
Figure 2. Colour Doppler impulse indicating the position of the intercostal artery (arrow) just superficial to
the pleura.
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Fluid formations usually adapt to the shape of the surrounding more rigid structures [10].
Haematomas, commonly seen in trauma patients, can have various degrees of echogenicity
depending on the erythrocyte content and can exhibit denser echoes due to organisation in
older lesions [1]. Chest wall abscesses show heterogeneous echoes, which makes
differentiation from organising haematomas challenging, particularly because of the
tendency of undrained haematomas to be complicated by infection. The presence of a
capsule surrounding the abscess facilitates differentiating the lesion from an organised
haematoma [1].
Malignant infiltration of the chest wall by distinct nodules or by extension from the lung
and pleura is accurately delineated by TUS [20]. Malignant space-occupying lesions
commonly appear hypoechoic with occasional hyperechoic parts (figure 3). Studying the
vascular pattern of a chest wall swelling can suggest malignancy if an irregular pattern is
identified by colour Doppler examination [1]. Colour Doppler is valuable during the
planning of biopsies from a suspected swelling, which is an attractive target for invasive
sampling due to its superficial position.
Infiltration of the chest wall and pleura by peripheral lung cancers has important
implications for staging and subsequent treatment choice. TUS can accurately identify chest
wall infiltration by demonstrating features such as fixation of the tumour during breathing,
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and disruption and infiltration of the parietal pleura (figure 4) [21]. It has been shown that
TUS has superior sensitivity to CT in assessing chest wall involvement by lung cancer when
pathological examination of surgically resected tumours is used as the gold standard [22].
Bony lesions
Chest wall examination by US is usually conducted in the setting of a blunt chest wall
trauma or to evaluate suspected rib deposits. Normal ribs appear as well-defined
hyperechoic curved structures with an acoustic shadow seen deeper to them (figure 1a). A
wide array of manifestations secondary to blunt trauma to the chest wall are identifiable
by US, including rib/sternal fractures, myocardial contusion, PTX and haemothorax
[2, 23, 24].
Rib fractures are more amenable to detection by TUS than by chest radiography, with a
50% increase in diagnostic sensitivity with TUS [7, 19]. Directing TUS examination to
areas of maximum pain helps in delineating rib fractures [1]. Fractures are primarily
diagnosed by the presence of a discontinuity (or a gap) in the outer cortex of the rib, or by
the presence of a “step” if the fracture has become dislocated. Bone fragments can
sometimes be visible on TUS. In nondisplaced fractures, or where there are gaps that are
Needle
Nee d le
dle lengt
length
ngth
ngth
Figure 4. Peripheral lung carcinoma. Clear invasion and destruction of the pleura can be seen. Note the
edge of the normal pleura (arrow).
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smaller than the lateral resolution of the TUS probe, the fissure can be identified by the
presence of a reverberation artefact, known as the “chimney” phenomenon [23]. Auxiliary
findings that lend support to a diagnosis of rib fracture include soft tissue haematoma, an
associated pleural collection, lung contusion and PTX [2, 24]. The presence of s.c.
emphysema is encountered occasionally with rib fractures, and despite being readily
diagnosed clinically, its presence imposes significant limitations on full TUS examination of
deeper structures due to the scattering of US waves by s.c. air (figure 5) [25].
Osteolytic rib deposits are identified as disruptions of the rib cortex, which is replaced by an
inhomogeneous lesion that is invariably associated with an increase in adjacent soft tissue
[7]. Colour Doppler examination may in addition reveal the presence of neovascularisation,
assuming a “corkscrew” or spiral configuration [1]. In addition to its diagnostic value, TUS
can be used to gauge the response to therapy in osteolytic lesions secondary to malignancies
such as multiple myeloma and breast cancer. The superficial location of such structures
renders them easily accessible to serial TUS to monitor changes in size or morphology of
the osteolytic lesion as part of the monitoring of the tumour response.
The intercostal artery does not invariably follow the classical course described in the
anatomic literature but may instead follow an aberrant course in a considerable minority of
cases [26]. TUS has been demonstrated to be an accurate tool at the bedside to screen for a
vulnerable intercostal artery for physicians who perform thoracentesis, chest-drain
insertions and TUS-guided pleural biopsies [27]. This is especially valuable in patients with
increased risk of bleeding. In addition to pre-procedure planning for the intervention site,
TUS can identify any procedure-related bleeding early, which expedites the process of
timely management [28].
Pleura
Anatomy
The pleural membrane is the deepest layer of thoracic wall that is amenable to anatomic
characterisation by TUS. Aerated lung causes scattering of the US impulses, and anatomic
Needle
Nee dle le
lengt
length
ngth
Figure 5. Subcutaneous air at different layers of the chest wall (arrows). Note the two sets of reverberation
artefacts, which are repetitions of the air lines.
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CHEST WALL AND PARIETAL PLEURA | M. HASSAN AND N.M. RAHMAN
The normal pleura is only 0.2–0.4 mm thick [8]. The two layers of pleura are identified as
an echogenic band deeper to the intercostal muscles (figure 1) that is seen to be moving or
shimmering on real-time viewing; this is the so-called “pleural slide”. The thickness of this
echogenic band that represents the pleura is exaggerated by the movement of the two layers
of pleura as well the movement of underlying lung and is usually found to be 2 mm [29].
Care should be taken not to mistake the pleural band for the intermuscular septum, which
occasionally is encountered in subjects with thick chest walls (figure 1a). Gliding of the
pleura is key for correct identification. High-definition US can delineate a two-layered
membrane, which corresponds to the combination of parietal pleura and endothoracic
fascia [30, 31]. An echo-free band is occasionally noted inside the pleural line, and this is
thought to represent the actual pleural space [8]. The normally very thin visceral pleural is
not visualised by TUS due to the fact that it is obscured by the complete reflection of
sound waves off the lung interface [19, 29]. A hypoechoic layer, which corresponds to
extrapleural fat, is normally seen superficial to the parietal pleura, and the thickness of this
layer varies among individuals (figure 1) [6].
A thorough examination of the costal pleura is usually feasible with TUS. The
diaphragmatic pleura is accessible to US examination via the transabdominal approach, and
this is especially true on the right side due to the excellent sonographic window that the
liver provides. Parts of the apical and mediastinal pleurae are partially assessable
sonographically via the supraclavicular and parasternal approaches, respectively. It has been
estimated, based on comparison between multiple CT cuts and full TUS examination, that
the latter can visualise 60–70% of the pleural surface [8].
Pathology
The pleural pathology manifests either as exudation of effusion or pleural swelling [8].
Several benign and malignant processes can be seen by TUS. In addition, TUS can guide
the process of sampling abnormal pleura in cases of suspected malignancy or for
microbiological evaluation of nonresolving or tuberculous infection. Pleural thickening,
nodularity and calcification are among the sonographic features of pleural disease.
Benign disease
Pleuritis can usually be identified on TUS by an abnormally rough crenulated appearance
with some degree of thickening. The abnormal pleura generally looks hypoechoic with loss
of the normal smooth texture. The presence of subpleural consolidation or small pleural
effusions increases diagnostic certainty. Colour Doppler examination is not sensitive
enough to pick up increased pleural vascularity associated with pleural inflammation [29].
CEUS, which remains an experimental technique in pleural disease, has shown promising
results in identifying pleurisy, with some data suggesting sensitivity nearly comparable to
that of contrast-enhanced CT in identifying enhanced pleural inflammation due to
infection [32].
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Figure 6. Significant parietal pleural thickening (arrow) in a patient with chronic rheumatoid pleuritis. A
catheter is seen inside the pleura (arrowhead). The pleural cavity is indicated by crosses joined by dotted lines.
considered alongside other clinical and radiological features, since pleural thickening
associated with empyema or inflammatory pleuritis can reach a significant width (figure 6).
For more subtle thickening, correct measurement can be challenging. A method commonly
used by the authors to measure pleural thickening is as follows. The pleural space is always
examined by aligning the TUS probe parallel to the ribs. Once thickening is identified, the
probe orientation is changed to be perpendicular to the ribs so that the outer cortex of the
ribs is visible. The pleura is then assumed to begin just below the innermost visible
convexity of the rib, and a reasonable measurement can be obtained (figure 7). Pleural
thickening can sometimes be confused with effusion, when there is a hypoechoic strip
Figure 7. Estimation of parietal pleural thickness by US. The pleura is assumed to start from the deepest
part of the rib cortex (arrow). Two crosses denote the extent of the thickening, which is highlighted by the
presence of a thin layer of effusion.
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superficial to the lung that can either be interpreted as a small effusion or as thickening.
Applying colour Doppler may help in the differentiation. The presence of a haphazard
Doppler signal that is intensified with breathing movements, termed the “fluid colour sign”,
favours a diagnosis of pleural effusion [3, 34]. A simple approach to differentiate a small
effusion from pleural thickening is to ask the patient to take a few deep breaths while
observing any changes in the hypoechoic strip. While pleural effusion tends to change in
dimensions with the changes in lung volume, pleural thickening should appear fairly static.
This is better observed with a high-frequency probe.
Among the common benign pleural pathologies that can be assessed by TUS are pleural
plaques. This is a common finding in people who have been exposed to asbestos [35].
Pleural plaques are easily diagnosed on CXR. On TUS, they appear as distinct areas of
thickening with or without calcification, usually at the dorsolateral pleura. Calcification can
be differentiated from noncalcified thickening by the absence of deeper reverberation
artefacts in calcification.
Metastatic disease
Malignant pleural disease occurs more commonly secondary to metastasis rather than
mesothelioma. The most common cancers that infiltrate the pleura are lung cancer, breast
cancer and lymphoma [36]. Malignant pleural disease is now frequently diagnosed by
means of pleural biopsy obtained during local anaesthetic thoracoscopy (LAT) [37], and in
many instances, pleural deposits are micronodular and are too small to be identified by
TUS. Metastases that are ⩾5 mm in diameter can be visualised as hypoechoic/echogenic
polypoid or broad-based nodules [8]. Large metastatic deposits are easily identifiable by
TUS for two reasons. First, metastatic pleural disease is very commonly associated with
pleural effusion [38], which creates an excellent sonographic window. Second, disease
usually is heaviest near the diaphragm and lower costal pleura [38], which are the most
accessible anatomic regions for TUS (figure 8).
Diaphragm
Needle
Nee
Nee
edle le
llength
lengt
eng
ngt
n gth
gt
th
Figure 8. Nodule noted on the diaphragmatic pleura (arrow). This effusion proved to be due to metastatic
adenocarcinoma.
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Mesothelioma
CT is the main radiological investigation for evaluation of mesothelioma. Features such as
circumferential pleural encasement of the lung, involvement of the mediastinal pleura and
pleural nodules superimposed on pleural thickening favour the likelihood of mesothelioma
over metastatic pleural disease [39]. However, these appearances are not specific enough to
confidently exclude pleural metastasis [35]. Definitive differentiation of mesothelioma from
metastatic pleural malignancy based on CT alone is not possible [7]. Using TUS, irregular,
partly angular pleural thickening can be seen. Frequently, mesothelioma appears as
extensive nodular growth with or without chest wall invasion. TUS is highly sensitive to
chest wall and diaphragm invasion, and is superior to CT in this regard. TUS is a useful
tool to direct potential biopsy sites of abnormal pleura.
Sliding of the pleural membranes is a key feature used to confidently exclude the presence
of PTX. In addition, the presence of sliding suggests that the lung is not tethered to the
chest wall, which can be valuable information for physicians planning to perform LAT
[40]. In patients requiring a pleural biopsy, lack of pleural sliding indicates probable failure
of lung collapse after accessing the pleural space, which is necessary to execute LAT [41].
In this situation, input from the pre-procedure TUS can lead to conversion of the
procedure from LAT to an image-guided biopsy [11]. Practitioners who are experienced
with LAT can perform the procedure in the absence of any effusion by inducing PTX
before the procedure. This is ideally performed after confirming the presence of lung
sliding using TUS, and TUS can be used “on table” to confirm the formation of PTX
during the procedure [42].
Conclusion
TUS is a highly useful technique for the diagnosis and sampling of chest wall and pleural
pathologies. As an increasing number of physicians are trained in TUS, it has become a
central part of many diagnostic pathways in the emergency/acute setting, as well as now
being an indispensable tool for specialist management of pleural disease.
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18. Prosch H, Strasser G, Sonka C, et al. Ultraschall (US) und US-gezielte Biopsie supraklavikulärer
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20. Suzuki N, Saitoh T, Kitamura S. Tumor invasion of the chest wall in lung cancer: diagnosis with US. Radiology
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21. Qureshi NR, Rahman NM, Gleeson FV. Thoracic ultrasound in the diagnosis of malignant pleural effusion. Thorax
2009; 64: 139–143.
22. Bandi V, Lunn W, Ernst A, et al. Ultrasound vs CT in detecting chest wall invasion by tumor. Chest 2008; 133:
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24. Ma OJ, Mateer JR. Trauma ultrasound examination versus chest radiography in the detection of hemothorax. Ann
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30. Diacon AH, Theron J, Bolliger CT. Transthoracic ultrasound for the pulmonologist. Curr Opin Pulm Med 2005; 11:
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32. Görg C, Bert T, Görg K. Contrast-enhanced sonography for differential diagnosis of pleurisy and focal pleural
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34. Wu RG, Yuan A, Liaw YS, et al. Image comparison of real-time gray-scale ultrasound and color Doppler
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35. British Thoracic Society Standards of Care Committee. BTS statement on malignant mesothelioma in the UK,
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37. Rahman NM, Ali NJ, Brown G, et al. Local anaesthetic thoracoscopy: British Thoracic Society pleural disease
guideline 2010. Thorax 2010; 65: Suppl. 2, ii54–ii60.
38. Rogrigues-Panadero F. Effusions from malignancy. In: Light RW, Lee YCG, eds. Textbook of Pleural Diseases. 2nd
Edn. Boca Raton, CRC Press, 2008; pp. 323– 340.
39. Metintas M, Ucgun I, Elbek O, et al. Computed tomography features in malignant pleural mesothelioma and other
commonly seen pleural diseases. Eur J Radiol 2002; 41: 1–9.
40. Marchetti G, Valsecchi A, Indellicati D, et al. Ultrasound-guided medical thoracoscopy in the absence of pleural
effusion. Chest 2015; 147: 1008–1012.
41. Hersh CP, Feller-Kopman D, Wahidi M, et al. Ultrasound guidance for medical thoracoscopy: a novel approach.
Respir Int Rev Thorac Dis 2003; 70: 299–301.
42. Corcoran JP, Psallidas I, Hallifax RJ, et al. Ultrasound-guided pneumothorax induction prior to local anaesthetic
thoracoscopy. Thorax 2015; 70: 906–908.
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| Chapter 4
Pneumothorax
Nils Petter Oveland
Pneumothorax (PTX) is common after blunt chest injury, and failure to diagnose and
rapidly treat an enlarging PTX may cause patient death. The anteroposterior supine CXR is
the least sensitive of all plain radiographic techniques for detecting PTX. Occult PTX (i.e. if
missed on CXR) may subsequently be found by CT scans, but both of these diagnostic tools
are not readily available for the patient, include a radiation hazard, and have a time delay
between ordering and obtaining results. TUS is a harmless point-of-care examination to
accurately diagnose PTX. The main message in this chapter is that TUS is a safe and highly
accurate diagnostic tool to diagnose PTX and can be used to assess PTX progression. With
the appropriate training, all clinicians can perform US examinations to detect PTX, which
suggests that this technique should be used as a diagnostic adjunct to the clinical
examination of patients with respiratory distress.
Cite as: Oveland NP. Pneumothorax. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound
(ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 43–63 [https://doi.org/10.1183/
2312508X.10006317].
In the first scenario, you are an air ambulance doctor on call at a level 2 trauma centre.
During your shift, you are dispatched to a hunting accident where a 14-year-old boy has
been shot in the chest and face. When you arrive at the scene 15 min later, the patient is
lying on his back on the ground complaining of general chest pain and facial discomfort
around his right eye. The clinical examination, including auscultation, shows no respiratory
and circulatory instability, but his chest and face have multiple gunshot wounds from the
metal pellets. On the way to the hospital, you perform an in-flight TUS examination, which
shows no sign of blood in the pericardium, abdomen or thorax. However, you suspect a
small PTX in the left lung apex because the normal sliding movement between the two
pleural layers is absent and the tip of the lung reappears on the US screen with each breath
(figure 1a). Although these US signs of abnormal lung sliding and a visible lung point are
subtle, your suspicion is passed on to the trauma surgeon in the emergency department.
The supine CXR shows the metal pellets but no PTX (figure 1b). Subsequent CT scans
confirm the chest injury caused by the gunshot: a small 5 mm-thick apical PTX (figure 1c).
No chest tube is inserted, and the patient is brought to the operating room and intubated
Stavanger University Hospital, Dept of Anaesthesiology and Intensive Care, Stavanger, Norway.
Correspondence: Nils Petter Oveland, Gneisveien 1 C, 4027 Stavanger, Norway. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
https://doi.org/10.1183/2312508X.10006317 43
ERS MONOGRAPH | THORACIC ULTRASOUND
b)
a)
c)
Figure 1. Case scenarios. a) US image of a miniscule apical pneumothorax (PTX) caused by penetrating
trauma. The tip of the lung (thick arrow) has detached from the hyperechoic pleural line (thin arrow) as air
interposes the parietal and visceral pleural layers (i.e. the definition of a PTX). This lung point moves to and
fro along the pleural line, in a manner synchronous with respiration (visible only on video clips). b) CXR
showing the multiple metal pellets from the gunshot. The PTX is not visible. c) CT confirming the small
amount of intrapleural air displayed as a black pocket in the left lung apex (black arrow). The white arrow
shows the lung point. Reproduced and modified from [1] with kind permission from N.P. Oveland.
prior to eye surgery. The patient is closely observed for any clinical deterioration and signs
of tension PTX during surgery.
In the second scenario, you are dispatched to a motorcycle accident where a 55-year-old
male biker has gone off the road and hit a tree at high speed. When you arrive, the
paramedics have placed the patient on a backboard, secured his neck with a collar and
given him high-flow oxygen through a mask. He is anxious and complains of chest pain
and dyspnoea. The clinical examination shows no chest instability, but the respiratory rate
is clearly elevated (40 breaths min−1) with symmetrical breath sounds. Peripheral pulses are
present and the heart rate is 136 beats min−1 with no signs of external bleeding or
long-bone fractures. You perform a rapid sequence intubation, initiate positive-pressure
ventilation using a portable respirator and transport the patient by helicopter to a level 2
trauma centre 15 min away. The trauma team there is notified. The initial assessment and
supine CXR obtained in the emergency department do not show any thoracic injuries. The
CT scan detects unstable L2 and C7 vertebral-body fractures, multiple small rib fractures, a
sternum fracture and bilateral small PTXs in the anterior chest. The surgeon on call wants
the patient transferred by helicopter to a level 1 trauma centre 70 min away because the
vertebral fractures are unstable. You express concern for having a patient in a helicopter
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PNEUMOTHORAX | N.P. OVELAND
with bilateral PTX undergoing positive-pressure ventilation, and advocate the insertion of
chest tubes, but the surgeon disagrees. Because lung auscultation in flight is impossible due
to noise, you use the portable US machine to repeatedly scan the anterior chest of the
patient every 10 min. The PTX is outlined on the patient’s chest with a pen by marking
the US lung point sign (i.e. the edge of the PTX where the lung is still in contact with the
interior chest wall). The patient is transported to the level 1 trauma centre without any
progression of the PTX on either side.
These scenarios show how clinicians are challenged with a diagnostic dilemma when
encountering trauma patients, because a physical examination combined with an
anteroposterior supine CXR is insufficient to diagnose PTX. Emergent CT scans of the
chest can detect all PTX but have disadvantages, such as exposure to radiation. In addition,
in settings such as pre-hospital, battlefield and remote areas, clinicians do not have access
to these diagnostic modalities. Thus, an accurate mobile method for diagnosing PTX is
needed. TUS meets these requirements and can be performed in almost any clinical setting.
First, it is a noninvasive, radiation-free, rapid and repeatable bedside diagnostic test that has
been shown to be more sensitive than, and equally specific as, supine CXR. Second, TUS
can also assess PTX progression, known to be an independent factor of a patient’s later
need for chest-tube insertion. This is potentially helpful in real clinical settings, as it may
enable clinicians to use US to make treatment decisions.
Pneumothorax
Thoracic trauma
Trauma is one of the leading causes of death worldwide (5.1 million deaths in 2010) and
can be characterised as a global epidemic because it accounts for one in every 10 deaths
[2]. Patients with multiple blunt injuries are far more common in civilian practice, but both
penetrating and blunt trauma present significant challenges to national healthcare systems
and necessitate a policy action to prevent them [3]. Chest injury is the direct cause of death
in 25% of blunt trauma victims and a contributing factor in up to another 50% of trauma
deaths [4], which can be explained by the large number of motor vehicle crashes and falls
[2, 5]. One serious consequence of chest trauma is PTX, a potential life-threatening
condition that sometimes requires immediate treatment to prevent patient death [6].
Although the origin of PTX can be spontaneous, it is trauma patients in particular who
present with a respiratory instability that needs immediate diagnosis and treatment.
Therefore, this chapter focuses on the basic clinical and diagnostic aspects of traumatic PTX.
Cardiothoracic anatomy
The thoracic cage is a bony structure that connects the posterior vertebral column and
anterior sternum via the osteocartilaginous ribs. The thorax contains the heart, lungs, great
vessels and oesophagus (figure 2), and is demarcated by the diaphragm inferiorly and
structures of the neck and lung apices superiorly. The aorta, pulmonary artery, pulmonary
veins and vena cava occupy the mediastinum, where they connect to the base of the heart.
The heart is contained within the fibrous pericardium, and its apex projects into the left
thoracic cavity [7]. In the right and left hemithorax, the pleural sac surrounds each lung:
the parietal layer covers the inside of the chest wall and the visceral layer encloses the
lung parenchyma. During ventilation, the visceral pleura is brought into contact with the
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Figure 2. Illustration of a pneumothorax (PTX) in the right lung and detection by an US probe. PTX is caused
by one of the following mechanisms: 1) air leaking from the airways ( proximal or distal conduits) or the
alveolar space, 2) air communication between the pleural space and the atmosphere or 3) the presence of
gas-producing organisms within the pleura. Reproduced and modified from [10] with permission.
parietal pleura, thereby reducing the pleural cavity to a closed, separate space. This
space normally contains only a capillary layer of serous fluid that lubricates the apposed
surfaces and reduces friction between the parietal and visceral pleura [8]. The dynamic
to-and-fro sliding motion between the layers during respiration is the basis of TUS
detection of PTX [9].
Definition
PTX is a common clinical condition where air is present in the pleural space (figure 2).
When air separates the parietal and visceral pleural layers, the negative intrapleural pressure
that keeps the lungs distended is disrupted, leading to a collapse of the elastic lung
parenchyma and expansion of the thoracic cage [11].
Classification
There are different classification categories for PTX (table 1). According to aetiology, PTXs
are classified as spontaneous or traumatic. A PTX is classified as primary spontaneous if no
obvious precipitating factor is present and as secondary spontaneous if the patient has an
underlying disease (e.g. COPD, cystic fibrosis). Traumatic PTX is either iatrogenic (i.e.
caused by transthoracic or transbronchial biopsy, central venous catheterisation, pleural
biopsy, thoracentesis) or noniatrogenic following a blunt or penetrating chest injury [11]. A
PTX can have a wide continuum of severity, ranging from simple asymptomatic PTX
caused by disruption of the pleural space to tension PTX associated with increased
intrathoracic pressure [7]. The increasing use of CT to investigate thoracoabdominal
trauma allows a more precise and three-dimensional evaluation of the thorax. Intrapleural
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Figure 3. Occult pneumothorax after blunt chest trauma. The large amount of intrapleural air anterior to
the right lung was not visible on the supine CXR but was subsequently diagnosed on the CT scan images.
Reproduced and modified from [1] with kind permission from N.P. Oveland.
air not seen on supine CXR is often seen on CT, and this entity is defined as occult PTX
(figure 3) [12].
Epidemiology
In addition to rib fractures and pulmonary contusions, PTX is the most common chest
injury found in patients with blunt trauma [13, 14]. In a population-based study from Italy,
PTX was present in one in every five severely traumatised patients (i.e. an incidence of 81
per 1 million citizens per year) [6]. These results are consistent with a study of chest
injuries from the regional trauma centre in Trondheim, Norway, where the most common
thoracic injury was rib fracture (55%) and the most common internal thoracic injury was
Reproduced and modified from [1] with kind permission from N.P. Oveland.
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PTX (24%) [15]. A high incidence of extrathoracic injuries such as head trauma and
musculoskeletal injuries in the extremities has also been associated with major blunt
trauma [7, 15], and only a minority of patients with PTX (5%) have isolated chest injuries
[4]. Furthermore, PTX is associated with greater on-scene physiological instability (i.e. low
blood pressure and low oxygen saturation) compared with other chest injuries of similar
severity [6]. These findings draw attention to the association between PTX and tension
physiology, as well as the potential benefits of decompression procedures.
Tension PTX
If air is allowed to enter (from the lung or through the chest wall) but not exit the pleural
space via a “one-way valve”-like opening, tension PTX will quickly develop. The increasing
pressure deranges the cardiorespiratory capacity of the patient and makes this an insidious
and life-threatening event. This condition is most often seen in pre-hospital, emergency
department, trauma unit and critical care settings [16]. The instability of trauma patients
with PTX [6] may be explained by the progressive accumulation of air within the pleural
space, which exerts mechanical pressure on internal structures. The affected lung may then
collapse, with a possible shift of the organs to the contralateral thoracic side. Such a
mediastinal shift severely impairs the circulation by pinching the central venous return to
the heart (figure 4) and reduces ventilation by compressing the remaining lung.
Furthermore, the resulting hypotension and hypoxaemia can lead to cardiac arrest, at
which point diagnostic and treatment delays are highly lethal [7, 16, 17]. Thus, PTX is a
notable cause of preventable death (i.e. in ∼16% of pre-hospital trauma cases) [6, 18, 19]
where simple field-friendly interventions may be lifesaving [20].
Figure 4. Tension pneumothorax on the left side. The expanding intrapleural air mass pushes the heart over
the midline into the contralateral right hemithorax, impairing the lung and heart capacity. Image provided
by N.P. Oveland.
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Clinical examination
The physical examination of the chest includes inspection (looking for signs of injury,
symmetry of the thorax, abnormal breathing movements and distended neck veins),
palpation (searching for s.c. emphysema, localised chest pain, crepitation, instability of the
thorax and tracheal deviation), percussion (tympani or dullness) and finally auscultation
( presence of breathing sounds and lateralisation) [20]. Clinically, PTX is characterised by
mild to severe signs and symptoms of chest pain (due to rib fractures), dyspnoea,
tachypnoea, cyanosis, tachycardia, hypotension, contralateral tracheal deviation and
ipsilateral lung hyperresonance with diminished or absent breathing sounds (figure 5) [7].
To palpate for s.c. emphysema, crepitation from rib fractures, pain and thoracic cage
instability combined with measurements of pulse rate, blood pressure and arterial oxygen
saturation measurements are helpful [6, 21]. In particular, s.c. emphysema is a strong
clinical predictor for concurrent PTX, although this sign is often absent despite injury (i.e.
not found in 85% of patients with an actual PTX [22]). Various percussion techniques have
also been used to diagnose PTX in mechanically ventilated patients in the intensive care
unit [23]. The most reliable part of the physical examination is auscultation of the lungs,
because clinical suspicion of PTX is reinforced by diminished or absent breath sounds on
the affected side [21, 24]. The diagnostic accuracy improves further if the patient complains
of respiratory distress and presents an increased respiratory rate [20]; however, auscultation
is often difficult due to environmental noise (e.g. during air transport or in the emergency
department [25]) and because unequal breath sounds can be caused by either air (PTX) or
blood (haemothorax) within the pleural cavity. Moreover, the physical examination can be
misleading, and diagnoses based solely on auscultation fail to detect up to 20–30% of PTX
[4, 26]. Although a large PTX can sometimes be identified [26], others may be overlooked
but can become clinically relevant [12, 27]. Furthermore, the fact that a high incidence of
extrathoracic injuries is associated with blunt trauma makes the diagnosis of PTX even
Respiratory distress
Cyanosis
Tracheal deviation
Chest pain
Hyperresonance
Figure 5. Clinical manifestations of pneumothorax. Reproduced and modified from [1] with kind permission
from N.P. Oveland.
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more challenging. Therefore, diagnostic adjuncts are needed as an extension of the physical
examination.
Release of air
In some trauma patients, the expedited insertion of a chest tube is necessary. If there is
release of air, a characteristic hiss can be heard and used to confirm the correct diagnosis
of PTX. However, this invasive procedure is only to be used in physiologically nonpermissive
patients who are too unstable to await further diagnostic imaging.
Chest radiography
The portable anteroposterior CXR is routinely obtained as the first radiograph in most
trauma patients, and through the use of modern digital machines, these pictures are readily
available for the medical team [28]. However, both lung fields must be examined carefully
for the presence of PTX signs, which include a readily apparent visceral pleural line,
depressed diaphragm and the deep sulcus sign (i.e. enlargement of the costophrenic angle)
[29]. Furthermore, s.c. air in the soft tissue should not be overlooked, because this is a
pathognomonic sign of lung and airway leakage [22]. Injured patients are often confined to
the supine position (strapped to backboards) for neuroaxial protection, and the location of
a PTX within the chest is directly associated with the force of gravity, the elastic recoil of
the lung and the attachment of the lung to the hilar structures. The intrapleural air
therefore collects anteromedially in the least-dependent pleural space [30–32]. Air trapped
anteriorly and medially to the lung is particularly difficult to detect and quantify on supine
CXRs, and even large air pockets may be overlooked at hospitalisation (figure 3) [33]. In
one large prospective observational study of multiply injured patients, the incidence of
occult PTX was 76% when the supine CXR was interpreted by the trauma team in the
emergency department [22]. Most studies refer to board-certified radiologist dictations
when reporting the proportions of PTX that are occult (30–55%) [27, 32, 34–37], although
the time required to request and obtain the result of a CXR can be as long as 20 min [37].
Therefore, it is the initial interpretations made by the trauma team, and not the delayed
dictations by the radiologist, that result in treatment decisions. The conventional supine
anteroposterior CXR remains the most available but least sensitive of all plain radiographic
techniques for diagnosing PTX [33] and evaluating its extension [38].
Computed tomography
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an emergent CT scan of the chest after obtaining a negative CXR should not be performed
routinely, because this type of examination comes with a substantial cost. The radiation
hazard is eminent [42–44], and the need for patient transportation to the radiology
department and the time required to obtain such images can result in delayed diagnosis
[37]. Indeed, timing is often critical for physiologically nonpermissive trauma patients,
because CT scanning prolongs the time to lifesaving resuscitation (hence, the expression
“tunnel of death”).
An accurate method for diagnosing PTXs is needed. Over the last two decades, PoCUS has
evolved from a modality used by only a select group of medical specialities to its current
position encompassing a wide range of operator backgrounds and rapidly expanding
clinical applications [45]. This has in large part been due to the increasing portability and
image quality of machines combined with decreased cost [46]. Physicians from different
specialities have shown that they can quickly become skilled in US for diagnostic and
procedural applications relevant to their medical field. TUS is a true point-of-care
diagnostic test that can be performed in almost any clinical setting. It is noninvasive,
radiation free, rapid and repeatable at the bedside, and has been shown to be more sensitive
than, and equally specific as, supine CXR to detect PTX [36, 37, 47–52].
Equipment
The current generation of machines are impressively lightweight and utilise sophisticated
processors and imaging software to provide high-quality images, including multiple modes
(e.g. brightness or B-mode, motion or M-mode, Doppler). They are often laptop sized (∼3–
5 kg) or even truly pocket sized (∼0.1–0.5 kg), and importantly are designed for PoCUS use
[46]. Sonographic diagnosis of PTX can be done using different machines with a variety of
probes. The preferred transducers for imaging superficial structures (e.g. ribs, pleura) are
linear (∼5–14 MHz), but microconvex or convex transducers (∼4–8 MHz) working at lower
frequencies may also be used for imaging both superficial and deep structures [9, 53]. Both
transducers fit between the ribs and can be “pushed” under the back of the supine patient
to examine the posterior chest. Even a larger, low-frequency, curvilinear (∼2–5 MHz) probe
may be used to look between multiple ribs. The conventional B-mode is adequate, but
occasionally the M-mode setting can be helpful to distinguish movement and standstill at
the pleural line [53].
The paradox is that US imaging poorly visualises the lung parenchyma. Therefore, the
conceptual basis for the US diagnosis of PTX is dynamic signs that originate from the
pleural line (i.e. the adjacent two visceral and parietal pleural layers) [9, 54]. It is sufficient
to combine movements and sonographic artefacts from the pleural line and study them in
B-mode and M-mode to rapidly rule out or confirm PTX. The primary dynamic features
are the lung sliding sign [55], B-line reverberation artefacts [56] and the pathognomonic
lung point sign [57], all of which are synchronous with respiration, and finally lung
pulsation transmitted from heartbeats [58].
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Lung sliding
In B-mode, lung sliding is a dynamic sign that is visible as a slight and bright sparkling/
twinkling/glittering/shimmering “to-and-fro” horizontal movement at the pleural line. The
relative movement is between the lung’s surface covered by the visceral pleura towards the
chest wall covered on the inside by the motionless parietal pleura. Lung sliding is more
evident during active ventilation; it can be difficult to see with small tidal volumes, and
may even be absent in apnoea.
B-lines
In the normal lung, air inside the alveolar spaces hinders visualisation of the lung
parenchyma, but if the interlobular septa start to fill up with fluid, this traps the US beam
between elements with opposite acoustic impedance. Using B-mode, this creates a multiple
reflection artefact call B-lines (i.e. a reverberation artefact) that has the visual appearance of
echogenic lines or rays extending from the parietal pleura to the end of the screen without
fading. The B-line artefact is dynamic, as it moves synchronously with respiration.
Lung point
In B-mode, this pathognomonic US sign of PTX is found by placing the US probe over the
area where the collapsed lung is still in contact with the inside of the chest wall, as shown
in figure 2. This location is called the lung point and is visible as two distinct patterns on
the US screen: one suggestive of no lung sliding and/or B-lines where the parietal layers are
separated by air (i.e. PTX), and one with normal lung sliding and/or B-lines where the
pleural layers are still in contact. The lung point sign is dynamic, as lung sliding and/or
B-lines intermittently replace motionless pleura during respiration.
In M-mode, the lung point appears as an interchanging seashore pattern and stratosphere
pattern.
Lung pulse
In the absence of lung sliding, the heart may push the motionless lung and transmit
vertical movements to the pleural line. In B-mode, these movements can be seen as small
lung pulses synchronous with the cardiac rhythm. The heart beats transmitted through the
lung can also be seen in M-mode as pulsatile seashore patterns on a motionless
stratosphere background.
TUS detection of PTX may appear complex due to the need to recognise or exclude these
four signs, but the use of a step-by-step approach (figure 6) and a flow chart for decision
making (figure 7) makes the procedure straightforward. Another simplifying factor is that
intrapleural air tends to accumulate in the least-dependent parts of the chest due to gravity,
and with the patient in the supine position this corresponds to the anterior and lateral
parts of the chest on both sides [33, 59]. These anatomical locations are almost always
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accessible and easy to scan in both pre- and in-hospital patients, regardless of clinical
condition and body habitus.
Several intercostal spaces are often scanned on each side of the chest by repeating the
procedure (i.e. figure 6, steps a–c) to confirm the diagnosis of PTX. Different methodical
approaches with scanning zones [9, 54] or key anatomical points [53] have been suggested,
all with the common feature of covering both the anterior and lateral lung surfaces. A
simple approach is to divide each lung into anterior and lateral zones demarcated by the
parasternal border and anterior axillary line (i.e. anterior zone) and by the anterior axillary
line and posterior axillary line (i.e. lateral zone). Furthermore, the zones can be split into
upper (i.e. towards the apex/axilla) and lower (i.e. towards the diaphragm) scanning areas
[54, 60].
Discussion
Whether TUS is a better diagnostic test than supine CXR in injured patients with a
suspected PTX is debated [61]. The British Thoracic Society (BTS) maintains their caution
regarding the use of US for the detection and management of PTX because there is no
evidence of improved patient outcomes [62]. The World Interactive Network Focused On
Critical UltraSound (WINFOCUS) organisation argues that US is more sensitive for
diagnosing PTX and is therefore an improvement on the current standard practice [60].
However, there must be a continuous focus on appropriate use and correct interpretations
of US images [63]. Regardless of opinion, the use of TUS is expanding followed by growing
evidence of its clinical usefulness for diagnosing PTX. The latter statement is based on the
numerous publications on this diagnostic technique and recent prospective studies and
reviews comparing TUS with supine CXR and CT.
Spontaneous PTX
The presence of spontaneous PTX can be inferred sonographically using the same key steps
as described in the section “TUS to detect PTX”, including absence of lung sliding and
reverberation artefacts. These patients often present with less severe symptoms and can
endure the extra time required to take a CXR in the hospital. Based on the availability of a
standard erect CXR, which has increased sensitivity and specificity compared with supine
CXR, the main value of TUS to date has been in the diagnosis and management of supine
trauma patients [64].
Occult PTX
The body of literature that supports the use of TUS for the diagnosis of PTX is increasing,
and an illustrative selection is presented in table 2.
Due to competing concerns, such as spinal injury, haemodynamic compromise and the
need for clinical interventions, patients most often lie on their backs. In this supine
position, the intrapleural air collects anteromedially to the lung parenchyma where it is
particularly difficult to detect and quantify in anteroposterior CXR [32, 33, 59]. This is the
first lung area to be examined in the extended Focused Assessment with Sonography for
Trauma (eFAST) protocol, which may explain the increased sensitivity of US to diagnose
PTXs that are otherwise undetected on CXRs (i.e. occult PTX) [70]. Three reviews and
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a)
Rib
w
Ba
ing
do
tw
sha
tw
ha
bs
ing
Ba
dow
Ri
b)
Depth
Time
c) Skin
Rib shadow
Depth
Time
Figure 6. Step-by-step diagnostic approach for the US detection of pneumothorax (PTX). Thick arrows
indicate the pleural line, thin arrows indicate B-lines and crosses indicate the lung points. a) When
examining a supine patient, the US scan should always start in the anterior–inferior chest area (i.e. at the
third to forth intercostal space) between the parasternal and the midclavicle line (i.e. an area close to the
mammilla) (left image). If PTX is present, the intrapleural air will move and reside in front of the lung and
can easily be detected by an US probe placed adjacent. The initial plane of the probe is longitudinal to
visualise two ribs and identify the echogenic pleural line passing between and under the ribs (middle
image). The image of two rib shadows connected by this pleural line resembles the wingspread of a bat,
hence the term “bat sign” (right image). Beginning each LUS procedure by identifying the “bat sign” is
important because doing so immediately targets the parietal and visceral pleura, where all the dynamic
movements and artefacts originate. b) The next step is to slightly rotate the probe so that it is aligned with
the intercostal space (left image). This is an oblique plane that gives an extended view of the pleural line
without interfering rib shadows, because the axis is alongside the intercostals (middle image). In doing so,
remember not to place the probe on top of a rib, as this will reflect a hyperechoic motionless white line (i.e.
the cortex of the bone) on the US screen that resembles the pleural line. The scanning then follows the
curve of the lateral and inferior chest (i.e. the direction indicated by the arrow drawn on the chest), and at
any level, the US operator carefully evaluates the images for signs of horizontal lung sliding and vertical
echogenic B-lines that extend from the parietal pleura to the end of the screen (middle and right image).
Lung sliding and/or B-lines rule out PTX, whereas both signs are absent if the pleural layers are separated
by air. Sometimes it is necessary to use M-mode scanning to make the correct diagnosis (right images in b
and c). The seashore pattern rules out PTX, while the stratosphere pattern suggests PTX. c) When lung
sliding is absent in the anterior chest, the progressive movement of the probe towards the lateral-inferior
chest is useful to look for the area where the collapsed lung is still in contact with the inside of the chest
wall. This location is called the lung point (middle and right images) and corresponds to the place where
lung sliding and/or B-lines intermittently appear during respiration (best illustrated in video clips). The
detection of the lung point is 100% pathognomonic for PTX, and is useful to evaluate the size of a PTX as it
marks the lateral extension of intrapleural air inside the chest. The cutaneous projections of the observed
lung points (middle image, white double-ended arrow) can be marked by a pen cross on the chest to make
a topographical map of the lateral extension of the PTX (left image). The more lateral the lung points are,
the more extensive the intrapleural air volume (i.e. PTX size). Reproduced and modified from [1] with kind
permission from N.P. Oveland.
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1) Lung sliding?
Seashore
Yes
2D M-mode B-lines
2) B-line(s)
2D
No PTX Yes No
Stratosphere
Lung point
Seashore
3) Lung point? Yes
No PTX M-mode
Lung pulse
4) Lung pulse? No
2D
Yes
Figure 7. Diagnostic decision making using a flow chart to distinguish pneumothorax (PTX) and normal
lungs. 1) The first sign to be checked is lung sliding, which excludes PTX, but a lack of sliding may be due
to other medical conditions involving pleural adhesions that result in motionless pleura (e.g. pleurisy,
massive pneumonia, complete atelectasis, fibrosis, severe asthma, emphysema, one-lung intubation,
oesophageal intubation, apnoea). In chest trauma cases, the absence of lung sliding is more likely to
indicate PTX. 2) The visualisation of even one isolated B-line demonstrates the adjoining of the visceral
pleura to the parietal pleura and rules out PTX. In the presence of PTX, the US image lacks B-lines but can
have horizontal echogenic A-lines that run parallel to the pleural line (i.e. artefacts that appear under the
pleural line at a depth exactly corresponding to the distance from the skin to the parietal pleural layer).
A-lines have less diagnostic value because they are found both in normal lungs and with PTX, and only
indicate air inside the chest (i.e. they do not distinguish air inside the lungs from intrapleural air). The
absence of B-lines has 100% sensitivity but only 60% specificity (in itself not enough for PTX to safely be
ruled in). 3) In contrast to the other US signs, the lung point confirms the diagnosis of PTX and is
pathognomonic for the presence of air within the pleural cavity. Unfortunately, not all patients present this
sign. One explanation for this absence with a large PTX is the complete retraction of the lung with
elimination of lung sliding in the anterior, lateral and posterior locations on the chest, and thus no lung
point can be visualised. Pleural adhesions may also cause motionless pleura and thereby limit the
likelihood of obtaining this sign. However, detection of the lung point is important to confirm PTX and
evaluate its size. 4) A lung pulse is useful in the absence of lung sliding and is often observed in patients
with consolidated motionless lungs, apnoea syndromes and main bronchus endotracheal intubation. The
transmission of heartbeats through the lung parenchyma generates a lung pulse sign, which, similar to
lung sliding, rules out PTX. Reproduced and modified from [1] with kind permission from N.P. Oveland.
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56
First author [ref.] Study design/ Details of patients or included studies US sign(s) Reference Sensitivity Specificity
publication type test % %
LICHTENSTEIN [55] Not reported ICU patients: 43 lungs with PTX, 68 normal lungs LS CXR, CT 95.3 91.1
LICHTENSTEIN [56] Prospective ICU patients: 41 lungs with PTX, 146 normal lungs LS, B-lines CXR, CT 100.0 96.5
observational study
LICHTENSTEIN [57] Prospective ICU patients: 66 lungs with PTX, 233 normal lungs LP CXR, CT 66.0 100.0
observational study
DULCHAVSKY [65] Prospective 382 trauma patients: 39 lungs with PTX LS, B-lines CXR 94.9 100.0
observational study
ROWAN [50] Prospective 27 trauma patients: 11 lungs with PTX LS, B-lines CT 100.0 94.0
observational study
BLAIVAS [48] Prospective 176 trauma patients: 53 lungs with PTX LS CT, ROA 98.1 99.2
observational study
SOLDATI [66] Prospective 186 trauma patients: 56 lungs with PTX LS, B-lines, LP CXR, CT 98.2 100.0
observational study
ZHANG [37] Prospective 135 trauma patients: 29 lungs with PTX LS, B-lines, LP CT, ROA 86.2 97.2
observational study
SOLDATI [36] Prospective 109 trauma patients: 25 lungs with PTX LS, B-lines, LP CT 92.0 99.4
https://doi.org/10.1183/2312508X.10006317
observational study
WILKERSON [67] Evidence-based Four prospective observational studies LS, B-lines, LP CT, ROA NA NA
review
DING [68] Meta-analysis 20 English-language studies: 15 prospective, four LS, B-lines, LP CT, ROA 88.0 99.0
not reported and one retrospective
ALRAJHI [69] Systematic review Eight English-language prospective studies LS, B-lines CT, ROA 90.9 98.2
and meta-analysis
VOLPICELLI [60] Conference reports Consensus meetings of 28 experts; NA NA NA NA
and expert panel evidence-based guidelines for LUS extracted from
320 references
ICU: intensive care unit; LS: lung sliding; LP: lung point; ROA: release of air; NA: not applicable. Reproduced and modified from [1] with kind
permission from N.P. Oveland.
PNEUMOTHORAX | N.P. OVELAND
undetectable on CXR, then it is unlikely to require intervention and use of US will not have
changed the management [71]. This may be valid for spontaneously breathing patients but
not in patients receiving positive-pressure ventilation. Detecting even small amounts of air
in the latter is highly relevant, as mechanical ventilation triples the risk of observation
failure and the need for a chest tube [12]. Moreover, even if a small PTX is left undrained,
prognosis, follow-up and observational strategy in the emergency department, operation
room or intensive care unit change when PTX is recognised (e.g. as seen in the first clinical
scenario).
Another remaining question is how best to manage and monitor occult PTX. The
hypothesis is that an identifiable cohort of positive-pressure ventilated patients can safely
be observed without the insertion of a chest tube [72]. Although it may seem reasonable
to consider the size of the PTX before making treatment decisions, a large prospective
observational study found PTX size not to be an independent predictor of observation
failure with the subsequent need for chest-drain insertion. However, other factors that do
predict failure have been identified. Positive-pressure ventilated patients have a tripled
risk, and those with respiratory distress are six times more likely to fail observation. In
addition, the patients with a progression of their PTX (i.e. occult PTX found on
follow-up CXR) are 70 times more likely to undergo a tube thoracostomy [14]. Thus, the
assessment of PTX extension and any subsequent change in size is particularly important
in these patients. In standard clinical practice, the methods to do this have been CT
imaging or CXR. While CT has proved to be highly accurate in quantifying the volume of
a PTX [34, 73, 74], CXR readings are equivalently low [38]. The conceptual basis for
using bedside TUS in occult PTX patients is that any PTX size progression should be
detected early and treated promptly, without the need for patient transport or radiation
exposure. The US lung point sign marks the lateral edge of the intrapleural air layer, as
demonstrated through comparison with CT and CXR images (figure 6) [10, 36, 48, 75].
Thus, the more lateral the lung point is on the chest wall, the greater the extension of the
air layer [9]. However, the lung point will not be found if the lung is completely
retracted. A possible contribution of bedside TUS is that it can be used to follow the
progression of a PTX during positive-pressure ventilation [10, 75]. This strategy of
repeated chest US examinations should be adopted if a decision is made to observe
mechanically ventilated trauma patients with occult PTX without placing a chest tube (e.g.
the PTX followed in the second clinical scenario). Although the ongoing OPTICC (Occult
Pneumothoraces in Critical Care) trial is set to determine the treatment strategy of an
occult PTX in general [72], future research should try to find any relationship between
the cutaneous projections of the lung points on the chest, marked with US, and the best
treatment options. More knowledge is definitely important, as the level of evidence for US
evaluation of PTX size is still too subtle and the accuracy of the method has been
questioned and debated [48, 76, 77].
Haemodynamic instability
Trauma is a leading cause of morbidity and mortality [2], where patients with additional
chest injuries have an increased haemodynamic instability [6]. In some extremities,
patients may die from causes that are preventable if promptly diagnosed and aggressive
lifesaving therapeutic procedures initiated. In a setting when other image tests are not
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applicable, the introduction of eFAST has revolutionised trauma care through improved
diagnostic accuracy, increased clinical confidence and tailored resuscitation manoeuvres
[70, 78]. Of the eight treatable causes of cardiac arrest (i.e. the 4Ts and 4Hs), PoCUS
can help in the diagnosis of cardiac tamponade, hypovolaemia, pulmonary embolism
and PTX [79]. In the extreme emergency of cardiac arrest, more of the US diagnosis
should rely on simple signs and protocols (e.g. the SESAME (Sequential Emergency
Scanning Assessing Mechanism or Origin of Shock of Indistinct Cause) protocol [80]).
Thus, to rule in or rule out PTX in an arrested patient, one should rely strictly on lung
sliding, B-lines and a lung pulse, without the need to look for the lung point at the
lateral chest (the lung is most probably totally collapsed). Furthermore, only scan the
anterior chest in one location per side. Any absence of lung sliding, B-lines and a lung
pulse of unstable patients should induce the clinician to insert a needle or chest tube
immediately [9].
In recent years, PoCUS has developed rapidly due to miniaturisation of US machines. The
attributes of increasing portability, image quality and power durability of these machines
have made them ideal working tools that can be cart mounted or hand carried to the
patient’s bedside in or out of the hospital environment. In fact, US scans can be performed
in almost any clinical setting and are low risk, rapid and repeatable [45, 78]. These features
make TUS suitable in remote and extreme environments, where radiographic evaluation is
delayed or impossible, such as wilderness sports events, military conflicts, rural medicine
and space aviation [46, 81, 82]. In pre-hospital critical care, the encounter with emergency
medical service (EMS) staff and helicopter EMS (HEMS) staff is the first step of triage for
ill patients (figure 8).
This setting naturally requires the capacity to make a quick diagnosis to tailor the level of
care and treatment strategies. These rapid diagnoses are often made with limited
information and time, and it is paramount to remain “goal directed” based on predefined,
often binary, clinical questions to identify life-threatening conditions and hasten correct
treatment (e.g. is there a PTX: yes/no) [70]. Furthermore, technology allowing real-time
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videoconference assistance for interpreting PoCUS images may prove important for some
(H)EMS systems (i.e. remote telementored US) [83]. Real-time transmission of a video
showing the placement of the probe on the patient’s body as well as the corresponding
PoCUS image has been tested in a North Sea offshore oil installation, and the study
produced clinically useful information in 96.4% of cardiac cases and 87.8% of abdominal
cases in all (100%) of the LUS images (N.P. Oveland, unpublished data). This remote
telementored US modality is limited only by network availability, as other necessary
videoconference and PoCUS equipment is readily available “off the shelf”. Finally, the
increasing costs of hi-tech diagnostic hardware, such as angiographic radiography, CT and
MRI machines, limit their availability in developing countries. In fact, the World Health
Organization (WHO) has stated that two-thirds of the world’s population has no access to
these imaging technologies. The paradox is that 80–90% of all diagnostic problems could
potentially be solved by basic radiography and US examinations [84]. The low cost and
increasing availability of machines makes this a tool of choice in developing countries [85].
Pitfalls
Several conditions could mislead the operator or hinder the TUS examination when applied
to detect signs of PTX. Some of these are medical conditions with motionless pleura, as
explained in figure 7. An important condition common in trauma patients and iatrogenic
PTX is s.c. emphysema (i.e. air that has leaked into the s.c. tissue). This may give artefacts
on the US screen often described as “false lung sliding” based on movement of echogenic
muscular layers resembling the pleural line, and US images with “false B-lines” as air
within the s.c. tissue gives echogenic lines that spread like vertical rays, reaching the lower
How to scan? The sonographic signs of PTX include the following (strong/level A):
Presence of lung point(s)
Absence of lung sliding
Absence of B-lines
Absence of lung pulse
In the supine patients, first scan the anterior chest and progress more
laterally (strong/level A)
Adjuncts such as M-mode or colour mode may be used (strong/level A)
Microconvex transducers are preferred in adults, but others such as
linear probes can also be used based on preference and clinical setting
(strong/level B)
When to scan? TUS should be used in all clinical settings when PTX is a possible
diagnosis
What does TUS add? TUS more accurately rules in PTX than supine anteroposterior CXR
(strong/level B)
TUS more accurately rules out PTX than supine anteroposterior CXR
(strong/level A)
TUS may be a better initial diagnostic test for PTX than CXR, and hence
lead to a better outcome (no consensus/level C)
TUS is a useful tool to differentiate small and large PTXs, using detection
of the lung point (no consensus/level C)
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ERS MONOGRAPH | THORACIC ULTRASOUND
edge of the screen without fading [9]. These linear artefacts are called emphysema or
E-lines and differ from true B-lines as they do not arise from the pleural line [53].
Furthermore, foreign bodies such as bullets and shrapnel within the s.c. tissue will generate
similar vertical artefacts that are not true B-lines. Another phenomenon is the “double lung
point” where an air bubble is trapped between two areas of adherent pleural layers. In this
case, the laterality of the lung point fails to indicate the real extension of the PTX, while
two lung points surrounding the air bubble may be visualised [86, 87]. Similar although
rare, septated and complex PTXs with posterior locations are difficult to diagnose [53].
Finally, external factors such as voluminous clothing and chest dressings, limited workspace
inside ambulances and helicopters, and ambient lighting outside of hospitals make the
diagnosis of PTX more challenging.
Further reading
This Monograph highlights the endless possibilities of TUS for diagnosis of multiple clinical
conditions of the chest. In the last 5 years, numerous publications have been published for
TUS detection of PTX alone. Many are written by pioneers of TUS, such as Giovanni
Volpicelli and Daniel A. Lichtenstein, but it is beyond the scope of this chapter to give a
complete review of this literature. For some suggested books, reviews and guideline articles,
see [53, 88–93].
Conclusion
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| Chapter 5
Pleural effusion
Christopher Merrick1, Rachelle Asciak2,3,4, Anthony Edey5,
Fabien Maldonado1 and Ioannis Psallidas2,3,4
Pleural effusions represent a significant disease burden globally. TUS, performed by both
radiologists and physicians, has increasingly become an essential tool in the evaluation and
management of pleural effusions. It detects pleural effusions with higher sensitivity and
specificity than CXR, and provides valuable information about the size and depth of the
pleural effusion, the echogenicity of the fluid, the presence of septated or loculated fluid,
pleural thickening and nodularity, and the presence of any contralateral pleural effusion.
TUS can provide information on diaphragm position and movement with respiration, and
can assess the presence of lung sliding and the accessibility of pockets of fluid in loculated
pleural effusions, thereby improving the success rate and safety of pleural procedures. Given
the added detail that US provides and its increasing availability, it is no surprise that its use
is increasingly expanding in clinical practice.
Cite as: Merrick C, Asciak R, Edey A, et al. Pleural effusion. In: Laursen CB, Rahman NM, Volpicelli G, eds.
Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 64–74 [https://
doi.org/10.1183/2312508X.10014817].
Physician competency
With the growing use of bedside US by treating clinicians, there is an increasing awareness
that US practice need no longer be isolated to the radiology department. Bedside TUS has
been shown to decrease expense, as well as time in hospital [2]. Optimal management of
pleural effusion from a healthcare cost and patient wellness perspective is best initiated by
1
Vanderbilt University Medical Center, Tennessee, Nashville, TN, USA. 2Oxford Centre for Respiratory Medicine, Churchill Hospital,
Oxford University Hospitals NHS Foundation Trust, Oxford, UK. 3Oxford Respiratory Trials Unit, Nuffield Dept of Medicine,
University of Oxford, UK. 4Laboratory of Pleural and Lung Cancer Translational Research, Nuffield Dept of Medicine, University of
Oxford, UK. 5Dept of Radiology, Southmead Hospital, North Bristol NHS Trust, Bristol, UK.
Correspondence: Ioannis Psallidas, Oxford University NHS Foundation Trust, Old Road, Churchill site, Oxford, OX3 7LE, UK.
E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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the chest physician through skilled TUS analysis and TUS-guided procedures at the
bedside. However, patient safety requires that bedside physicians have received appropriate
training and hands-on experience with TUS prior to independent use for management of
patients. Multiple studies have demonstrated a decreased incidence of iatrogenic
thoracentesis complications following initiation of formalised TUS training and regular use
of US for percutaneous procedures [3, 4]. An increasing number of respiratory medicine
training programmes internationally are creating formal US training programmes to
promote physician competency. Competence in pleural US is now a compulsory part of
respiratory medicine training programmes in the UK [5]. The Royal College of Radiologists
stipulates that obtaining a certificate of basic TUS competence (level 1) includes keeping a
logbook of US examinations by the trainee and an assessment of competence by an
experienced trainer. Required competencies include the performance of safe and accurate
examinations, recognition of anatomy and pathology, recognition of when to appropriately
refer for a second opinion, and an understanding of the relationship between US imaging
and other imaging techniques. With more practice and experience, including the
performance of noncomplex US-guided procedures, and with conductance of research in
US, the trainee can then be certified as level 2 competent. Level 3 is an advanced level of
practice, which in the UK would usually equate to a consultant radiologist with a
subspecialty practice [6].
At all stages, respiratory physicians should collaborate with radiologists, and TUS findings
should be correlated and combined with other imaging techniques, such as CT scanning, in
order to deliver the best care for patients with pleural effusions.
With the growing use of US in various specialties, there is also a move to integrate US
training into medical school curricula [7].
Pleural effusion
The pleural space is a tightly regulated virtual space that contains a small amount of pleural
fluid in physiological conditions, governed by a balance of plasma ultrafiltration and
venous and lymphatic drainage. This delicate balance can be disturbed in a variety of
situations, such as in the setting of pleural tumour, infection, and lymphatic obstruction or
disruption, resulting in a net accumulation of pleural fluid.
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ERS MONOGRAPH | THORACIC ULTRASOUND
urinothorax, respectively) or chyle (chylothorax) [9, 10]. Invariably, any given case of
pleural effusion may be multifactorial and can incorporate a combination of the above
mechanisms.
Epidemiology
Pleural effusions represent the end result of a variety of clinical conditions, which vary
based on patient characteristics and local disease patterns. There are an estimated 1.4
million cases of pleural effusions annually in the United States, with an estimated incidence
of pleural effusion in the developed world of 320 cases per 100 000 persons per year [11].
There are no obvious gender predilections, and men and women seem to be affected
equally. Pleural effusions are much less common in children, where they are primarily due
to infectious aetiologies [12].
Diagnosis
Basic principles
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Simple effusion
Complex effusion
Complex effusions are characterised by loculations (collections of fluid that do not follow
gravity) and septations (fibrin strands) and are typically not free flowing. On US, the
appearance of complex effusions is characterised by heterogeneous fluid collections with
interspersed hyperechoic tissue strands. These effusions are typically composed of cellular
material, which can organise into fibrinous or proteinaceous strands of cellular debris
called septations (figure 2). These septations can ultimately result in the
compartmentalisation of the pleural effusion into several smaller locules, which may or
may not communicate with one another. Effusion complexity is variable, and can range
from relatively mild with only a few loculations to severe complexity with a substantial
loculation burden and intense heterogeneity of the fluid collection on US. Exudative
effusions, such as those due to malignancy and infection, are often complex. Effusion
chronicity also appears to be important in terms of development of a complex effusion.
A simple effusion, if left untreated for a substantial period of time, may develop
loculations [20].
Figure 1 . A simple pleural effusion with echogenic contents, in this case a transudate. Note that atelectasis
(arrow) has a texture similar to liver (*).
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Figure 2. A complex, septated effusion with dense, organising fibrinous material. Note the pleural margin
deep to the collection (arrow) with noisy, disorganised echoes distally in place of the aerated lung.
Lung consolidation/hepatisation
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Malignant pleural effusion (MPE) is the most common cause of massive unilateral pleural
effusion (defined as occupying more than two-thirds of the hemithorax) in the Western
world and affects over 150 000 people annually in the United States alone [14, 29].
Diagnosis of MPE is based on fluid cytology and often requires additional diagnostic
procedures such as pleural biopsy and pleuroscopy. In patients presenting with pleural
Figure 3. Pleural effusion with a single prominent septation centrally and another at both the top and
bottom of the screen. This patient would be expected to experience less dyspnoeic improvement following
drainage than an individual with more than five septations.
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disease suggestive of MPE, TUS has been found to have a diagnostic sensitivity of 73% and
a specificity of 100%. Pleural thickening of >1 cm is highly suggestive of MPE (figure 4). As
such, TUS can be highly beneficial in the diagnostic evaluation of suspected MPE but is
not sufficient to confirm the diagnosis [30].
Pleural infection is a significant cause of pleural disease and appears to be on the rise
globally due to improved clinical recognition and diagnostics, in addition to a hypothesised
replacement phenomenon attributable to increasing use of multivalent pneumococcal
vaccines [31, 32]. Complicated pleural space infections are defined by ongoing signs of
sepsis in spite of adequate antibiotic treatment, and these effusions require drainage.
Thoracic catheter size is an area of frequent debate informed by regional practices and
individual experience. Prospective post hoc analysis of randomised controlled trial data has
demonstrated no significant difference in clinical outcomes or referral for surgery among
patients receiving either small-bore, wire-guided thoracic catheters or traditional large-bore
chest tubes [33]. Prior to publication of these data, one study evaluated the accuracy of
TUS in determining sonographic effusion characteristics that predict successful drainage by
small-bore catheters (12–16 French gauge). Complex septated effusions were more likely to
fail treatment if drained by small-bore catheters than complex unseptated effusions [34].
However, it deserves mentioning that standard medical treatment at the time of this study
primarily comprised the use of antibiotics. These data need to be interpreted in light of the
advent of intrapleural fibrinolytic–nuclease therapy for the management of complicated
pleural space infections [35].
Rib
Parietal
Visceral
Figure 4. Longitudinal US image showing gross pleural thickening (1.4 cm; indicated by crosses). Note the
pleura is hyperechoic; the echogenicity of malignant pleural thickening is variable and ranges from low
through intermediate to hyperechoic.
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The technique required patients to lie in a supine position and perform a maximum
breath-hold while US images were obtained over the laterodorsal chest wall just superior to
the margin of the diaphragm. An effusion depth of 20 mm was found to correlate with a
mean volume of 380 mL, and 40 mm with 1000 mL. TUS was found to far outperform
lateral decubitus chest radiography in terms of effusion volume estimation [36]. For the
mechanically ventilated patient, a basic formula has been proposed to determine effusion
volume [37]. TUS was performed with the patient supine at 15° and the probe was placed
in the posterior axillary line. Based on a single series of observational data, the pleural fluid
volume could be estimated by multiplying the maximal distance (in millimetres) between
the visceral and parietal pleura by a factor of 20 [37]. It should be noted that multiple
different formulae have been proposed, but none has been independently validated or
demonstrated to be superior to any other at predicting effusion volume.
Special considerations
Pleural effusion is common in the intensive care unit setting, given the multitude of
comorbid illnesses such as sepsis, malnourishment, cardiac dysfunction and iatrogenic
volume overload. Evaluation of such effusions is paramount, especially in situations of
concern for complicated parapneumonic effusions or malignancy. There are multiple
imaging modalities available to the clinician in this setting including, primarily, CXR.
Frequent, or sometimes daily, CXRs are obtained in the intensive care unit setting and
often provide the first insight to incidentally diagnosed pleural effusions. In multiple
prospective cohorts, the performance of TUS versus CXR in detecting pleural effusion in
mechanically ventilated patients was examined [15]. TUS was found to far outperform CXR
in both its sensitivity and specificity for pleural effusion detection. The sensitivity and
specificity of TUS to detect pleural effusion in a mechanically ventilated patient have been
demonstrated to be 93% and 97%, respectively [38]. As one would imagine, the diagnostic
accuracy of TUS also far surpassed that of auscultation in the mechanically ventilated
patient [17].
Future directions
TUS is an actively growing field of research, given its immense clinical utility. In recent
years, its usefulness has flourished from an occasional novelty in bedside assessment to a
cornerstone of evaluation and management of pleural effusion. A major area of
investigation in TUS is in evaluating its ability to predict procedural success in terms of
patient-oriented outcomes.
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Following the results from the previously mentioned septation analysis study [26], detection
of septations on TUS has the potential to predict the symptomatic outcome of subsequent
pleural procedures, and a larger multicentre study is needed to confirm these results and to
study the septation score in more detail.
Imaging enhancement
Finally, the use of contrast-enhanced TUS is an area of interest that may hold benefit for
evaluation of patients with MPE. It can be difficult to differentiate pleural thickening in the
setting of effusion due to similar sonographic characteristics (figure 5). There is a small
body of data and experience using hexafluoride-based contrast for enhancement of
pleural-based nodules. Contrast can be beneficial in enhancing nodule visibility and may be
helpful in forming a differential diagnosis based on the US qualities of the nodules [40].
Currently, CEUS remains a niche technique due to the technical limitations of appropriate
training and equipment, and further investigation and clinical experience is needed with
this modality.
Conclusion
TUS is rapidly becoming a cornerstone as a management modality for the chest physician
caring for patients with pleural effusion. TUS is sensitive for detection of pleural effusion
and is useful in further evaluation and categorisation of effusion type based on fluid
sonographic characteristics. As such, it is pivotal in guiding therapy directed towards
effusion, and is even beneficial in elucidating which patients will benefit most from effusion
drainage. TUS has increased the safety of bedside procedures and simplified patient care,
thus providing the potential to decrease costs and hospital length of stay for those
Figure 5. Pleural nodularity, seen prominently on the diaphragmatic pleura. The pleural effusion is
echogenic and confirmed as an exudate in this case of pleural malignancy. Contrast-enhanced TUS may
have a role in improving visualisation of pleural nodularity in the setting of pleural effusion.
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hospitalised with pleural effusion-related disease. Bedside TUS carried out by a physician
should serve a foundational role in the management of both ambulatory and hospitalised
patients suffering from pleural effusion.
References
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2. Bateman K, Downey DG, Teare T. Thoracic ultrasound for pleural effusion: delays and cost associated with
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3. Duncan DR, Morgenthaler TI, Ryu JH, et al. Reducing iatrogenic risk in thoracentesis. Chest 135: 1315–1320.
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6. Royal College of Radiologists. Ultrasound Training Recommendations for Medical and Surgical Specialties. 3rd
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7. Patel SG, Benninger B, Mirjalili SA. Integrating ultrasound into modern medical curricula. Clin Anat 2017; 30:
452–460.
8. Light RW, Macgregor M, Luchsinger PC, et al. Pleural effusions: the diagnostic separation of transudates and
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9. Psallidas I, Kalomenidis I, Porcel JM, et al. Malignant pleural effusion: from bench to bedside. Eur Respir Rev
2016; 25: 189–198.
10. Light RW. Pleural Diseases. 6th Edn. Philadelphia, Lippincott Williams & Wilkins, 2013.
11. Marel M, Zrůtová M, Štasny B, et al. The incidence of pleural effusion in a well-defined region. Chest 1993; 104:
1486–1489.
12. Efrati O, Barak A. Pleural effusions in the pediatric population. Pediatr Rev 2002; 23: 417–426.
13. Campbell EJM, Howell JBL. The sensation of breathlessness. Br Med Bull 1963; 19: 36–40.
14. Porcel JM. Etiology of pleural effusions: analysis of more than 3,000 consecutive thoracenteses. Arch Bronconeumol
2014; 50: 161–165.
15. Kalantri S, Joshi R, Lokhande T, et al. Accuracy and reliability of physical signs in the diagnosis of pleural effusion.
Respir Med 2007; 101: 431–438.
16. Rocco M, Carbone I, Morelli A, et al. Diagnostic accuracy of bedside ultrasonography in the ICU: feasibility of
detecting pulmonary effusion and lung contusion in patients on respiratory support after severe blunt thoracic
trauma. Acta Anaesthesiol Scand 2008; 52: 776–784.
17. Lichtenstein D, Goldstein I, Mourgeon E, et al. Comparative diagnostic performances of auscultation, chest
radiography, and lung ultrasonography in acute respiratory distress syndrome. Anesthesiology 2004; 100: 9–15.
18. Soni NJ, Franco R, Velez MI, et al. Ultrasound in the diagnosis and management of pleural effusions. J Hosp Med
2015; 10: 811–816.
19. Yang PC, Luh KT, Chang DB, et al. Value of sonography in determining the nature of pleural effusion: analysis of
320 cases. Am J Roentgenol 1992; 159: 29–33.
20. Havelock T, Teoh R, Laws D, et al. Pleural procedures and thoracic ultrasound: British Thoracic Society pleural
disease guideline 2010. Thorax 2010; 65: Suppl. 2, i61–i76.
21. Lichtenstein DA. BLUE-protocol and FALLS-protocol: two applications of lung ultrasound in the critically ill.
Chest 2015; 147: 1659–1670.
22. Villena V, Lopez-Encuentra A, Pozo F, et al. Measurement of pleural pressure during therapeutic thoracentesis.
Am J Respir Crit Care Med 2000; 162: 1534–1538.
23. Pereyra M, Ferreiro L, Valdés L. Unexpandable lung. Arch Bronconeumol 2013; 49: 63–69.
24. Salamonsen MR, Lo AKC, Ng ACT, et al. Novel use of pleural ultrasound can identify malignant entrapped lung
prior to effusion drainage. Chest 146: 1286–1293.
25. Corcoran JP, Tazi-Mezalek R, Maldonado F, et al. State of the art thoracic ultrasound: intervention and
therapeutics. Thorax 2017; 72: 840–849.
26. Psallidas I, Yousuf A, Talwar A, et al. Assessment of patient-reported outcome measures in pleural interventions.
BMJ Open Resp Res 2017; 4: e000171.
27. Mulvey RB. The effect of pleural fluid on the diaphragm. Radiology 1965; 84: 1080–1086.
28. Wang LM, Cherng JM, Wang JS. Improved lung function after thoracocentesis in patients with paradoxical
movement of a hemidiaphragm secondary to a large pleural effusion. Respirology 2007; 12: 719–723.
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29. American Thoracic Society. Management of malignant pleural effusions. Am J Respir Crit Care Med 2000; 162:
1987–2001.
30. Qureshi NR, Rahman NM, Gleeson FV. Thoracic ultrasound in the diagnosis of malignant pleural effusion. Thorax
2009; 64: 139–143.
31. Muñoz-Almagro C, Jordan I, Gene A, et al. Emergence of invasive pneumococcal disease caused by nonvaccine
serotypes in the era of 7-valent conjugate vaccine. Clin Infect Dis 2008; 46: 174–182.
32. Grijalva CG, Zhu Y, Nuorti JP, et al. Emergence of parapneumonic empyema in the USA. Thorax 2011; 66:
663–668.
33. Rahman NM, Maskell NA, Davies CWH, et al. The relationship between chest tube size and clinical outcome in
pleural infection. Chest 2010; 137: 536–543.
34. Chen CH, Chen W, Chen HJ, et al. Transthoracic ultrasonography in predicting the outcome of small-bore
catheter drainage in empyemas or complicated parapneumonic effusions. Ultrasound Med Biol 2009; 35: 1468–
1474.
35. Rahman NM, Maskell NA, West A, et al. Intrapleural use of tissue plasminogen activator and DNase in pleural
infection. N Engl J Med 2011; 365: 518–526.
36. Eibenberger KL, Dock WI, Ammann ME, et al. Quantification of pleural effusions: sonography versus radiography.
Radiology 1994; 191: 681–684.
37. Balik M, Plasil P, Waldauf P, et al. Ultrasound estimation of volume of pleural fluid in mechanically ventilated
patients. Intensive Care Med 2006; 32: 318.
38. Lichtenstein DA. Lung ultrasound in the critically ill. Ann Intensive Care 2014; 4: 1.
39. Thomas R, Azzopardi M, Muruganandan S, et al. Protocol of the PLeural Effusion And Symptom Evaluation
(PLEASE) study on the pathophysiology of breathlessness in patients with symptomatic pleural effusions. BMJ
Open 2016; 6: e013213.
40. Görg C. Transcutaneous contrast-enhanced sonography of pleural-based pulmonary lesions. Eur J Radiol 2007; 64:
213–221.
Disclosures: F. Maldonado has received a grant from Centurion, outside the submitted work. I. Psallidas has
worked part-time as Medical Science Director at AstraZeneca, but his work was on a different disease area
and was not linked with pleural effusion.
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| Chapter 6
Interstitial syndrome
Luna Gargani
B-lines are probably the most “revolutionary” sign of LUS and can be used for the
evaluation of interstitial syndrome. They indirectly visualise different degrees of partial
deaeration of the pulmonary parenchyma, and therefore can be seen in the presence of both
hydrostatic and inflammatory pulmonary oedema, as well as in pulmonary fibrosis.
Assessment of B-lines can thus be applied to many different diseases, such as heart failure,
end-stage renal disease, acute lung injury, interstitial lung disease and pre-eclampsia. To
differentiate these conditions, a thorough integration with the clinical picture is absolutely
necessary, but some LUS characteristics can also significantly improve B-line specificity and
overall LUS diagnostic accuracy ( pattern of distribution over the thorax, response to therapy
and association with other LUS signs, such as pleural line alterations, small and large
consolidations, and pleural effusion). The clinical usefulness of B-lines has been
demonstrated not only for diagnosis but also for monitoring and prognosis.
Cite as: Gargani L. Interstitial syndrome. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic
Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 75–86 [https://doi.org/10.
1183/2312508X.10006517].
P ulmonary interstitial syndrome comprises a group of lung disease affecting the lung
interstitium. Although sonography cannot be used to evaluate the lung because the
pulmonary air represents an insurmountable obstacle to the US beam, it is possible to
recognise sonographic patterns, including “artefactual” B-lines, which can be used
effectively in many settings. These can aid in the differential diagnosis of dyspnoea, and
can be used to monitor the response to therapy.
B-lines
Definition
In recent years, B-lines have been described as the sonographic sign of pulmonary
interstitial syndrome. It is difficult to define sonographic interstitial syndrome, as this is a
term derived from radiology, where it refers to a pattern that can be applied both to CXR
and to chest CT, including linear, reticular, nodular and pseudonodular alterations.
Correspondence: Luna Gargani, Institute of Clinical Physiology, National Research Council, via Moruzzi 1 – 56124, Pisa, Italy.
E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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B-lines have officially been defined as “discrete laser-like vertical hyperechoic reverberation
artefacts that arise from the pleural line, extend to the bottom of the screen without fading,
and move synchronously with lung sliding” [1]. B-lines are indeed sonographic artefacts,
which do not depict real anatomical structures but rather are the result of the peculiar
acoustic properties of the lung. The physical genesis of B-lines is not yet fully understood,
although some sound hypotheses have been proposed [2].
To understand what B-lines represent in the context of LUS basic semiotics, we have to
refer strictly to the physical interaction between the US beam and the pulmonary
parenchyma. When the pulmonary parenchyma is normally or over-aerated, the US beam
is usually unable to penetrate below the pleural line; the resulting image thus shows all of
the structures above the pleura (e.g. adipose tissue, muscles, fascia) and the pleura itself as a
hyperechoic horizontal line moving synchronously with respiration. The structures above
the pleural line are sonographically portrayed as corresponding to real anatomical
entities. This is not true for what is depicted below the pleural line, unless the lung is
consolidated. Whether the sonographic pleural line fully corresponds to the anatomical
pleura is still debated.
A reduction in pulmonary aeration changes the physical acoustic interaction between the
US beam and the lung, allowing the US beam to partially penetrate the lung parenchyma,
and resulting in the appearance of B-lines. A complete or almost complete pulmonary
deaeration would generate the sonographic display of a consolidation, with direct imaging
of the anatomical consolidated parenchyma. Milder degrees of deaeration do not allow
direct imaging of the lung parenchyma but generate B-lines, which are more numerous as
long as the air diminishes. It follows that B-lines are visible in the presence of a partial
deaeration of the lung, which is, however, not consolidated. This condition is not
necessarily linked only to alterations of the pulmonary interstitial space, making the term
“interstitial syndrome” somewhat of an oversimplification, although very figurative.
Referring to a condition of “partial deaeration”, which characterises the pre-consolidated
lung, seems more appropriate [2, 3]. However, the term interstitial syndrome is suitable for
most pathology, and it is true that those conditions that do not purely affect the interstitial
space usually show additional signs to B-lines.
Characteristics
There are some typical features of B-lines that help in the differentiation from other
artefacts. Table 1 presents the main B-line characteristics. These elements are especially
useful to differentiate B-lines from Z-lines. Z-lines are vertical hyperechoic artefacts
that, similar to B-lines, arise from the pleural line, although the pleural origin is better
defined for B-lines. Moreover, Z-lines do not reach the edge of the screen and do not
clearly move with lung sliding [4]. Z-lines are usually less hyperechoic than the relative
pleural line. Z-lines do not seem to have pathological meaning. Figure 1 shows a Z-line
and B-lines.
Pleural line
The pleural line is a cornerstone of LUS. It is the first structure that should be searched for,
and its movement, referred to as lung sliding, should always be identified before moving on
to further evaluations. When lung sliding is not apparent, the different potential causes of
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Characteristic Comments
absent lung sliding should be taken into account, and the LUS examination should
continue to exclude or confirm the main clinical suspicion.
The normal pleura is visualised by LUS as a hyperechoic horizontal thin line, representing
the apposition of the parietal with the visceral pleura layers (figure 1). The pleural line may
appear abnormal in some pathological conditions, such as acute lung injury/acute
respiratory distress syndrome (ALI/ARDS) or interstitial lung disease (ILD). The
appearance of the pleural line can be helpful in contributing to the differential diagnosis of
the aetiology of B-lines [5–7], as detailed in the following section.
a) b)
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The mere presence of B-lines is not enough to characterise a lung from the sonographic
point of view. A few B-lines, especially at the lung bases, can be present in healthy subjects
and do not have a specific pathological meaning. A positive examination for B-lines needs
the presence of multiple, diffuse, bilateral B-lines. Multiple B-lines means at least three
B-lines between two ribs when applying the probe longitudinally, or at least three close
B-lines along the intercostal space when applying the probe obliquely or transversally.
Diffuse B-lines means that multiple B-lines should be seen in at least two regions of the
lung and bilaterally (i.e. in both hemithoraxes) [1]. As thoracic regions, the eight-region
scanning scheme proposed by Volpicelli et al. [1] is usually accepted. Another scanning
scheme that is accepted and has been used in many studies is the 28-scanning-site scheme
[8], which is more time consuming but allows a type of quantification of B-lines that,
although imprecise, has been shown to correlate with clinical [9, 10], biochemical [11],
radiological [12, 13], echocardiographic [9], gravimetric [14] and invasive [15] parameters
related to the interstitial involvement of the lung. Moreover, it has shown clear prognostic
value in both acute and chronic patients [16–20].
The definition of multiple B-lines as at least three B-lines between two ribs can be in part
subjective and does not take into account different thoracic dimensions. In acute
conditions, this is usually not so relevant, because the US patterns tend to be clear and
straightforward. However, clinical reasoning is mandatory, and a blind adherence to the US
picture, unrelated to the patient’s characteristics, should be avoided.
Clinical applications
In recent years, many studies have confirmed that B-lines can be useful in the detection,
monitoring and prognosis of patients with cardiogenic pulmonary oedema [6, 21, 22]. The
first published data were about the differential diagnosis of patients with acute dyspnoea. In
this setting, a positive LUS scanning for B-lines can help differentiate from other causes of
acute dyspnoea, in particular from exacerbation of COPD [11, 23–25]. Again, it is
important not to refer to the mere presence of B-lines but to assess multiple, diffuse,
bilateral B-lines, as patients with COPD, as well as healthy subjects, may show a few
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B-lines. In a large multicentric prospective study on >1000 patients with acute dyspnoea,
adding LUS to the standard clinical evaluation in the emergency department improved the
accuracy of acute heart failure (AHF) diagnosis (sensitivity and specificity 97%), with a net
reclassification index of the LUS-implemented approach compared with the standard
work-up of 19.1% [25]. This study addressed the diagnostic performance of LUS, whereas
an improvement in outcomes was not evaluated in the LUS-implemented group. LUS
evaluation of B-lines for the differential diagnosis of AHF compared with other causes of
acute dyspnoea also seemed a more effective method of implementation of PoCUS in a
large cohort of consecutive adult patients presenting with dyspnoea and admitted after
emergency department evaluation [26]. The presence of multiple bilateral B-lines increased
the sensitivity of the diagnosis of AHF from 77% (standard evaluation) to 88% ( p<0.001),
with a slight reduction in specificity (98% versus 96%; p<0.001) [26].
B-lines can also be used effectively for monitoring decongestion in heart failure [16, 27–29],
with a potential additional impact on accelerating discharge [30]. Indeed, LUS is particularly
suitable for monitoring, being a noninvasive, bedside, user-friendly imaging tool; it is
therefore promising for checking day-to-day changes in extravascular lung water with high
versatility, although no clear data are available about the use of B-lines to guide therapy as
yet [31]. The advantage of using LUS for monitoring pulmonary congestion in AHF is also
linked to the possibility of reducing ionising radiation exposure due to serial CXR, although
the dose of a single CXR is relatively small (∼0.02 mSv for a single posteroanterior
film) [32].
Encouraging data have been published on the prognostic value of B-lines. Persistent B-lines
at discharge after hospitalisation for AHF predict readmission for decompensated heart
failure at 3 and 6 months [16, 17, 19]. Similar results have been published for outpatients:
patients with a higher number of B-lines during a routine ambulatory office visit were more
prone to be readmitted for decompensated heart failure in the following months [18, 33].
LUS signs are quite different in cardiogenic compared with noncardiogenic pulmonary
oedema. When the pathophysiology of extravascular lung water accumulation is an increase
in the alveolar–capillary membrane permeability instead of an increase in hydrostatic
pressure, not only is the pulmonary interstitium affected but also the alveoli. From a
sonographic point of view, this translates into the presence of multiple, diffuse, bilateral
B-lines, as in AHF, but also into alveolar consolidations of different sizes. Very small,
subpleural consolidations are thought to be the reason why the pleural line in ALI/ARDS
looks so different from the pleural line in AHF. The latter condition is characterised by a
rather thin and regular hyperechoic horizontal line, whereas in ALI/ARDS the pleural line
looks irregular with hypo/anechoic spaces just below it, which are likely to be the
sonographic imaging of small peripheral consolidations (figure 2) [5]. This is not the only
sonographic difference, although it is probably the most striking and easy to detect: the
geographical distribution of B-lines is also different, because cardiogenic pulmonary
oedema tends to follow a gravity-related gradient with B-lines appearing before and more
frequently in the dependent zones, and later and less frequently in the most anteroapical
regions of the chest [6]. This typical distribution also slightly affects the sensitivity of LUS
in diagnosing pulmonary oedema when evaluating only the anteroapical regions [34].
Moreover, ALI/ARDS US alterations show a jeopardised distribution, with highly damaged
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a) b)
Figure 2. a) B-lines (arrow) with a regular, thin pleural line in a patient with acute heart failure. b) B-lines
with an irregular, fragmented pleural line (arrow) in a patient with acute lung injury.
areas close to completely spared areas [5]. B-lines in ALI/ARDS are correlated with lung
weight and density, determined by gravimetry in an experimental model in pigs [14, 35], as
well in humans, determined by CT [36].
LUS has also been used to monitor changes after therapy in ALI/ARDS. In this condition,
B-lines alone are not enough for appropriate monitoring, which should also include the
presence of larger and smaller consolidations [37–39]. When considering LUS as a kind of
“densitometer” (i.e. a tool that depicts images that correspond to different levels of
pulmonary deaeration), it is possible to create a deaeration score, taking into account all of
the sonographic patterns. These patterns are represented by the so-called A-profile [4], by
separated B-lines, by coalescent B-lines with and without subpleural consolidations, and by
consolidated lung. Recruiting the pulmonary parenchyma will thus imply moving from one
less aerated pattern to a more aerated one, which can be scored with a number. Such scores
can help not only for monitoring but also to predict post-extubation distress [39] and to
titrate positive end-expiratory pressure, avoiding overdistension [40].
Overall, these results underline the ubiquitous presence of LUS B-lines as an early sign of
extravascular lung water in many different conditions. B-lines are especially appealing in
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resource-limited settings, thanks to the versatile nature of the US technique, which can now
easily be performed on the spot using a portable or even a hand-held device [44], with
good accuracy and relatively low cost, and without the need for ionising radiation.
However, it must be noted that no data at the moment clearly demonstrate an
improvement in either the diagnosis or the outcome of these conditions as a result of the
addition of LUS to standard management.
Dialysis
The dynamic behaviour of B-lines has also attracted the nephrology community. The
number of B-lines significantly decreases after haemodialysis [45], is correlated with some
echocardiography parameters including left atrial volume, pulmonary artery systolic
pressure and E/e′ ratio as an index of diastolic function and ejection fraction [46], and is
correlated with bioelectric impedance analysis, especially with segmental thoracic bioelectric
impedance analysis [47]. In line with other studies in different settings, even if B-lines were
more numerous in patients with New York Heart Association (NYHA) functional classes
III–IV, the vast majority of asymptomatic patients had moderate to severe B-lines [46].
Extravascular lung water measured by B-lines is common not only in haemodialysis but
also in peritoneal dialysis, where it is present even more often in asymptomatic patients
[48, 49]. The correlation between LUS and lung auscultation is poor. Lung auscultation to
detect crackles is the cornerstone for diagnosing and monitoring congestion in patients
with heart failure and chronic kidney disease, but its reliability to detect interstitial oedema
is known to be low and, not surprisingly, LUS B-lines seem to be much more sensitive for
the detection of interstitial pulmonary oedema [50]. In addition, a linear correlation
between B-lines and fluid overload has been demonstrated in children with acute kidney
injury and end-stage renal disease [51]; the nonionising nature of LUS makes it even more
appealing to be widely employed in the paediatric population.
B-lines can be found not only in the presence of extravascular lung water (for both a
transudate and an exudate) but also in patients with ILD [3]. The partial deaeration of these
conditions is thought to be the physical basis for the appearance of B-lines. Preliminary data
were published >15 years ago, and multiple B-lines (called “comet-tail artefacts”) distributed
over the entire lung in combination with a thickened and irregular fragmented pleural line
were reported as strongly suggestive of the presence of diffuse parenchymal lung disease [56].
Since then, LUS has been compared with chest CT in patients with ILD, and mostly in
systemic sclerosis-related ILD. A good correlation has been found between the number of
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B-lines at LUS and some specific scores, such as the Warrick score, which takes into account
the typical radiological signs of ILD [13]. More interestingly, in this specific subset of patients
who are at high risk of developing ILD during the natural course of the disease, B-lines could
have a role as a screening tool [57]. This is due to the high negative predictive value (NPV) of
B-lines that, although not very specific, is extremely sensitive. Indeed, data suggest that some
false-positive LUS cases can be identified (patients with some B-lines at LUS but without
signs of systemic sclerosis-related ILD on chest CT), but no false-negative cases have been
observed (patients with abnormal chest CT but no B-lines at LUS). This highlights the very
high NPV of LUS B-lines, which makes them especially attractive and suitable for screening
patients who are at known risk of developing ILD, such as in connective tissue disease and
especially in systemic sclerosis. The imaging information of LUS could be coupled to
pulmonary function tests and diffusion capacity for carbon monoxide, reducing the need for
the serial radiological tests that are often requested in this fragile population [32].
LUS characteristics of B-lines derived from collagen tissue accumulation are different from
B-lines derived from water accumulation, at least in the more advanced phases. In patients
with ILD and multiple diffuse B-lines, the pleural line usually appears irregular and
fragmented, depicting a thickened fibrotic pleura. However, the exact physical genesis of these
imaging patterns has not yet been fully elucidated. It is also true that the subpleural alterations
visible in ALI/ARDS are very similar, from an imaging point of view, to the irregular
fragmented pleural line visible in significant pulmonary fibrosis. This further underlines the
fact that the clinical context should always lead the interpretation of the imaging data.
Despite these encouraging data, currently there are no clear indications to implement LUS
in the diagnostic or follow-up algorithm of patients with ILD. As for other clinical
conditions, understanding the real added value of LUS in terms of morbidity, mortality or
at least cost reductions represents a stimulating research area.
Other applications
There are some emerging applications of B-lines, such as in patients with pre-eclampsia,
where B-lines seem promising to detect and then monitor extravascular lung water, without
the need for ionising radiation [58]. In a recent study on 21 women with severe
pre-eclampsia, the number of B-lines was significantly higher than in healthy pregnant
women, both before delivery and 1 day post-delivery, whereas there was no significant
difference at 4 days post-delivery [59]. As in patients with cardiac conditions [9], B-lines
tend to be related to echocardiographic signs of increased left ventricular filling pressure
(E/e′ ratio) [58, 59]. Application of LUS in gravid women with dyspnoea or chest pain
seems particularly appealing, because it could reduce the issues related to the use of
radiological imaging tests during pregnancy.
B-lines in isolation or as part of a more complete LUS examination have been assessed in
perioperative settings, in both adults [60] and children [61], or effectively used as a screen
for pulmonary oedema following subarachnoid haemorrhage [62].
B-lines in PoCUS
When using B-lines in our clinical practice, as well as for other LUS features, we should take
into account that the best use we can make of these signs is integrating them into a
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point-of-care “clinical echography” [63]. This means that the LUS examination should be done
by the physician who is taking care of the patient, as well as this physician auscultating the
patient’s chest. LUS allows a kind of “enhanced” physical examination with higher accuracy to
detect signs of partial or total deaeration, although it cannot usually differentiate a normally
aerated versus an overaerated lung [64]. When patients are frankly symptomatic, if the cause of
dyspnoea is a condition where B-lines are present (i.e. hydrostatic and inflammatory
pulmonary oedema, or pulmonary fibrosis), B-lines are multiple, diffuse and usually bilateral,
and therefore easily detected. Implementing LUS in a PoCUS approach in the emergency
department allows reaching the correct diagnosis in a faster way compared with standard
diagnostic tests alone. This was nicely shown in a randomised trial of patients admitted to the
emergency department with respiratory symptoms: the addition of PoCUS (for the heart, lungs
and deep veins) to the standard initial diagnostic tests led to an absolute increase of 24% of
patients who were correctly diagnosed 4 h after admission, although no reduction in length of
hospital stay, or in-hospital or 30-day mortality was seen [65].
The learning curve for performing and interpreting B-lines is short and is significantly
different from the high level of expertise and skills needed to interpret CXR [63, 64].
Detection of B-lines can be repeated many times at the bedside, allowing close monitoring
of pharmacological and nonpharmacological treatment. This versatility makes B-lines, and
LUS in general, the new “visual auscultation”, which is likely to decrease the time needed
for a correct diagnosis in patients with respiratory symptoms [26, 65].
In the last decade, LUS has moved from a research tool to its use in the clinical arena. It is
especially in emergency departments and intensive care units that the technique is now
largely being used, although there are still significant geographical and cultural differences
that mean that US assessment of the lungs is not yet universally accepted, and is still
unknown in some environments.
The setting where the use of B-lines is supported by the most robust data is the differential
diagnosis of acute dyspnoea and, in particular, the added value in ruling in or ruling out
cardiogenic pulmonary oedema. B-lines are even mentioned in the 2016 European Society of
Cardiology (ESC) guidelines for heart failure, where it is stated that bedside LUS for B-lines
and pleural effusion “may be useful in detecting AHF if the expertise is available” [66], as
well as in the recommendations of the European Association of Cardiovascular Imaging and
Acute Cardiovascular Care Association [67, 68]. For other applications in heart-failure
patients, such as monitoring congestion to guide therapy in chronic and/or acute patients
and deciding the optimal timing to discharge a patient, there are promising data, but no
clear indications can be made until a randomised trial has demonstrated that a strategy
implementing LUS provides better outcomes or helps reduce costs compared with standard
management. Similarly, the use of B-lines for the diagnosis and follow-up of noncardiogenic
pulmonary oedema is encouraging but not officially included in routine clinical practice.
Applying LUS to ILD patients poses different issues, since ILD is a chronic condition, and
LUS is usually implemented in a PoCUS approach in acutely symptomatic patients. The very
high NPV of B-lines in excluding ILD could be extremely useful in patients at risk of
developing ILD, such as in connective tissue disease, where a clinically oriented use of LUS
together with pulmonary function tests (possibly with CXR, if needed) could be integrated in
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the diagnostic work-up of these patients in order to increase the appropriateness of chest CT
prescription. However, this hypothesis has yet to be fully demonstrated. The use of B-lines for
the follow-up of ILD is less supported but represents an interesting field of research.
The versatility of B-lines opens other potential applications that need to be explored in the
future, such as individualised and automatic detection of pulmonary interstitial oedema by
operator-independent, computer-based systems that could be implemented in a portable
device for individualised remote monitoring [69]. The use of B-lines and LUS in
resource-limited settings, as well as in neonates and children, are two other broad fields
that have only partially been explored and that could have a tremendous impact on the
healthcare system.
It is likely that, in the next few years, PoCUS will be officially included in standard
academic medical education [70].
Conclusion
The clinical use of the sonographic B-line artefacts represents a sort of revolution in the
imaging field. B-lines are easy to detect and evaluate, and a significant amount of data from
many different research groups underlines the usefulness of this simple LUS sign in patients
with both acute and chronic conditions. The versatility of this examination, which can be
implemented and repeated at the patient’s bedside, makes B-lines the visual translation of
some pulmonary sounds and therefore a suitable completion of a physical examination,
which reduces the time needed for a correct diagnosis in many different diseases.
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Disclosures: L. Gargani reports receiving personal fees from GE Healthcare and GlaxoSmithKline, outside the
submitted work.
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| Chapter 7
Pneumonia
Gebhard Mathis
Several studies suggest that LUS could be useful for the diagnosis of pneumonia. It also has a
more favourable safety profile and a lower cost than chest radiography or CT. The
characteristic sonographic signs of pneumonia are a hypoechoic liver- or tissue-like subpleural
consolidation and a marked dynamic bronchoaerogram. The borders are blurred and serrated,
often accompanied by comet tail artefacts. A parapneumonic effusion can be detected in 55%
of cases. Abscess formations are better seen in LUS than in CXR. They can be treated under
US guidance. LUS cannot rule out pneumonia. However, accuracy is >90%. These patients
should therefore be treated immediately according to clinical presentation and laboratory
findings, without further imaging procedures. In cases of tuberculosis and diseases of the
frame of the lung, sonography is the optimum method of visualising small pleural effusions
and subpleural consolidations.
Cite as: Mathis G. Pneumonia. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS
Monograph). Sheffield, European Respiratory Society, 2018; pp. 87–101 [https://doi.org/10.1183/2312508X.
10006617].
P neumonia has been documented as a forgotten killer [1]. According to the data
released by the World Health Organization (WHO), lower respiratory tract infection is
the leading cause of infectious disease-related mortality worldwide and refers to the
top-ranking cause of death in low-income countries. Pneumonia accounts for 16% of all
deaths in children <5 years of age and is thought to be the highest cause of mortality in
children around the globe [1]. Pneumonia is also a serious disease in adults, with high rates
of mortality and hospitalisation [2]. One-year all-cause mortality rates range 1% (age 18–49
years, low risk) to 36% (age ⩾65 years, high risk) [3].
The aim of this chapter is to familiarise the reader with sonomorphology of pneumonia
including LUS-differential diagnoses. The accuracy of LUS in diagnosing pneumonia will
also be discussed, and a comparison with standard imaging modalities, such as CT and
CXR, will be considered.
Parts of this chapter are reproduced and modified from the following, with the kind permission of Springer Nature. Mathis G, ed. Chest
Sonography. 4th Edn. Berlin, Springer, 2017.
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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Sonomorphology of pneumonia
Pathophysiological prerequisites
In cases of lobular and segmental pneumonia, large amounts of air are displaced from
the lung as a result of extensive fibrinous exudation. Affected lobes or segments are
depleted of air and sink in water. The phase of engorgement and hepatisation, i.e. the first
week of the disease, offers good conditions for pathological echo transmission. In this
phase, pneumonia is well imaged on the sonogram. In the phase of lysis, the inflamed
portion of the lung is ventilated to an increasing extent. Air reflexes superimpose deeper
infiltrations. The image on sonography at this time may underestimate the actual extent of
disease [4].
Focal pneumonias and interstitial pneumonias barely extend up to the pleura and are
therefore poorly accessible to sonographic imaging. However, bronchial pneumonias are
often accompanied by involvement of the pleura and are therefore partly visualised by
sonography [4].
Phase of engorgement
In the initial phase of disease, i.e. in the phase of engorgement, the pneumonic lesion is
hypoechoic, relatively homogeneous, and hepatoid or tissue-like in echotexture. Its
configuration is bizarre. It is rarely explicitly segmental like the pulmonary infarction or
rounded like carcinomas and metastases. Its margins are irregular, serrated and somewhat
blurred (figure 1) [5].
Bronchoaerogram
Figure 1. A 68-year-old severely ill man with clinical signs of acute pneumonia. In the upper lobe of the
lung on the left side, there is a liver-like consolidation with a bronchoaerogram. Reproduced and modified
from [4] with permission.
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PNEUMONIA | G. MATHIS
of the parenchyma. In all stages of the disease the bronchoaerogram is more pronounced
than in cases of pulmonary embolism. Quite often one finds a small number of, and in
most cases numerous, lenticular internal echoes just a few millimetres in size (figures 1 and 2).
These echoes indicate the presence of air in the small bronchi [6–15]. The
bronchoaerogram visualised by LUS cannot be equated with that seen on a radiograph [4].
In patients with lung consolidation in whom air bronchograms are displayed on US, the
dynamic air bronchogram indicates pneumonia, differentiating it from resorptive
atelectasis. Static air bronchograms have been found in most resorptive atelectases cases
and in one-third of pneumonia cases [16].
Viral and fungal pneumonias are often less ventilated and/or reveal less pronounced
bronchoaerograms. They are smaller and more compact than bacterial pneumonia and may
resemble large pulmonary infarctions. In contrast to pulmonary infarctions, they are
strongly perfused with blood (figure 3). The latter conclusions have been drawn from
personal experience and have been confirmed in expert meetings [4].
Fluid bronchogram
Figure 2. A 28-year-old woman with H1N1 influenza. She had a high fever, a moderate cough and mild
pleuritic pain. LUS shows a consolidation with air inlets. At the border of the consolidation are some B-
lines, a sign of a focal interstitial syndrome. Reproduced and modified from [4] with permission.
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a) b) c)
Figure 3. A 52-year-old woman with pain on inspiration, fever and haemoptysis. a) Sonography revealed a
consolidation measuring 5×3.5 cm in size, with less bronchoaerogram. b) Colour Doppler showed regular
perfusion: viral pneumonia. c) The corresponding CT showed a deeper infiltration. Reproduced and modified
from [4] with permission.
Vascularisation
In comparison with other contrast-enhanced imaging procedures, CEUS has the following
inherent advantages: the possibility of assessing the extent of enhancement in real-time
PE
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examination during the arterial and parenchymal phases; the ability to differentiate
pulmonary arterial vascularity from bronchial arterial vascularity by measuring the time to
enhancement; and the ability to perform repeated examinations.
With CEUS, pneumonias are rapidly enriched with contrast medium and achieve intensive
saturation after just 8–10 s. In patients with pleurisy and subpleural lesions of unknown
cause that were found in LUS, CEUS allows the diagnosis or exclusion of pleuropneumonia
and differentiation from pulmonary embolism [19–21].
The European Federation of Societies for Ultrasound in Medicine and Biology has
recommended the following uses and applications for CEUS. CEUS is useful in
differentiating inflammatory from embolic lung consolidation, especially in patients with
equivocal CT findings. CEUS may be used in equivocal cases to diagnose lung
abscesses within pneumonia, as CEUS appears better than conventional B-mode US or
CXR [22].
Abscess formation
Bacterial pneumonias tend to develop colliquations and form abscesses. This is seen in
approximately 6% of lobar pneumonia patients (figure refers to radiographic investigations).
Sonography more commonly reveals microabscess [23, 24].
If antibiotic therapy does not yield the desired result, LUS examination and US-guided
transthoracic aspiration are useful and safe diagnostic procedures for the collection of
specimens that enable the accurate diagnosis of lung abscesses [23–28].
Figure 5. Colliquated abscess with persistent fever after pleuropneumonia. Sonography-guided needle
aspiration was successful. The patient went into complete remission.
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Small abscesses measuring ⩽2 cm in size can be punctured and emptied with ordinary
aspiration. Lung drainage and lavage of large abscesses is rarely necessary. Drainage may be
performed under sonographic guidance. The catheter is seen as a two-layered reflex. The
investigator should use the shortest access and puncture through consolidated lung tissue to
minimise the risk of pneumothorax and to avoid bronchopleural fistula. The results are
equally as good as in CT-guided drainage. However, the position of the catheter can be
supervised using LUS at bedside (table 1) [4].
In the healing phase of pneumonia, the consolidated lung is reventilated. The size of the
infiltration is reduced. More and more air inlets are reflecting and show reverberation
artefacts. The typical dynamic airbronchogram is lost. The resolution of these
consolidations in LUS correlates well with the patient’s clinical progress, better than with
CXR (figure 6) [15, 16, 29].
Primary diagnosis of pneumonia is usually performed on the basis of clinical signs and
radiological imaging, initially CXR and/or CT. Several studies in adults [10, 13, 29, 30–33]
and children [34–40] suggest that LUS could be useful for diagnosing pneumonia.
The time needed to formulate an US diagnosis was significantly less than that required for
an ED diagnosis. The average time needed to formulate the US diagnosis was 24 min,
whereas the formulation of the ED diagnosis required a significantly longer time (187 min)
[41]. The baseline symptoms in a series of 229 patients with ambulant
community-acquired pneumonia (CAP) were: fever 78%, cough 91%, purulent
expectoration 52%, dyspnoea 70%, thoracic pain 54% and auscultation typical for CAP 73%
[29]. Immediately after considering the patient’s history and physical examination, LUS can
confirm the diagnosis by imaging the pneumonia [4].
In eight meta-analyses of LUS in CAP, overall sensitivity (85–97%) and specificity (80–
96%) were very high and had an accuracy of >90% (table 2) [42–49]. LUS may therefore be
able to rule in pneumonia but not rule it out [43].
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b)
a)
c)
e)
d)
f)
Figure 6. Follow-up in a patient with pneumonia. LUS shows the regression better than CXR. Day 1: a) CXR,
b) LUS with brochoaerograph, and c) LUS with regular vascularisation. Day 6: d) CXR with rest shadowing,
and e and f ) LUS with reventilation according to the clinical course.
The scope of the results is based on different inclusion criteria and various populations.
Overall, pooled positive and negative likelihood ratios (LR) were 20 and 0.06, respectively
[40, 42, 45]. A combination of auscultation and LUS increased the positive LR to 42.9 and
decreased the negative LR to 0.04 [29].
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First author Year Studies Patients Sensitivity Specificity DOR AUC Reference
[ref.] n n method
DOR: diagnostic odds ratio; AUC: area under the curve; ?: unknown.
One of the studies evaluated critically ill patients in intensive care (n=3) and found a
pooled sensitivity of 72% and a pooled specificity of 86% [46]. LUS can therefore help
accurately diagnose pneumonia and may be promising as an alternative resource to
traditional approaches.
Indications for the use of sonography where pneumonia is suspected or present are as
follows: 1) dyspnoea and fever, pleuritic pain; 2) to confirm a diagnosis of pneumonia; 3) a
pleural/basal shadow on CXR; 4) visualisation of abscesses; 5) isolation of pathogens; 6)
abscess drainage; and 7) follow-up of consolidation and pleural effusion.
Currently, international guidelines recommend CXR as the routine evaluation method for
suspected pneumonia. However, CT is now the gold standard for detecting lung
consolidation. In six studies that used chest CT as the sole criteria, LUS exhibited a pooled
sensitivity of 91% and a pooled specificity of 90% [29, 34, 40, 42, 45, 47]. Recent studies
show that ⩽25% more cases of pneumonia can be visualised with LUS than with CXR
when CT is used as the reference method.
In 112 patients with CAP correctly diagnosed with LUS and radiograph at baseline, both
examinations were repeated between days 13 and 16. Concordant results were observed in
85 (75.6%) patients (35 negative, 48 positive, two equivocal). 11 cases of CAP were
diagnosed with LUS but not radiograph. Conversely, nine cases of CAP were detected with
radiography but were missed with LUS, controlled by CT, as is the gold standard [29].
LUS is a reliable tool for bedside diagnosis of ventilator-associated pneumonia. LUS was
effective in reducing the number of CXRs, the relative medical costs and the radiation
exposure in the intensive care unit (ICU), without affecting patient outcome [15, 50–54].
LUS has a sufficiently high interrater reliability for the detection of lung consolidation [40].
In a feasibility and safety trial for the substitution of LUS for CXR when diagnosing
pneumonia in children, there was a 38.8% reduction in CXR among subjects with
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Figure 7. Persistent pleural effusion in a 32-year-old woman. Note the nodular and large thickening below
the visceral pleura, seen through the 15 mm-wide pleural effusion. The diagnosis of tuberculosis was
confirmed with sonography-guided biopsy.
pneumonia compared with no reduction in the control group. Novice and experienced
physician-sonologists achieved 30.0% and 60.6% reductions, respectively, in CXR use. There
were no cases of missed pneumonia among the study participants [55].
In conclusion, some authors propose that LUS should be used as the first-line examination
instead of CXR, and that chest CT should be reserved for complicated cases. Therefore, the
investigator should use LUS after performing a stethoscope-based investigation in patients
with fever and dyspnoea, particularly in the ED and the ICU [56–58].
Lung tuberculosis (TB) offers very different findings in every imaging modality. LUS is very
limited because it does not provide a complete overview of the chest. However, in some fields,
LUS can provide information additional to that of other radiographic techniques, with better
resolution, as follows: narrow pleural effusions; small subpleural nodules; small fluid collections
in a consolidated lung; and finally, better visualisation of the lymph nodes (figure 7).
Post-tuberculous nodular scars look like neoplasms and can be differentiated with
US-guided core biopsy, in doubt through labour testing by PCR [4, 59, 60].
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Figure 8. Aspergillosis in a 38-year old woman. The consolidation is inhomogeneus with large air inlets, not
a typical tree-like bronchoaerogram.
Figure 9. Chronic organising pneumonia after fungal sepsis and 11 days in intensive care with ventilation.
5 weeks later, the patient had cachexia and dyspnoea. Subpleural consolidations with air inlets and
irregular borders were noted. Diagnosis was confirmed using US-guided biopsy.
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Figure 10. Rheuma nodule in a 63-year-old patient with rheumatoid arthritis in remission. Metastasis was
initially suspected and this was constantly seen in follow-up.
The pleura is involved in many interstitial lung diseases. Pleural changes are better
demonstrated with sonography than with other imaging modalities. In patients with
dyspnoea or pleuritic pain, a diffuse interstitial syndrome, point-of-care LUS can lead to
the next efficient diagnostic steps.
Sonographic signs of interstitial lung disease are as follows: 1) multiple B-lines in irregular
distribution; 2) fragmented pleura with pleura thickening 3) subpleural consolidations
(figure 9b); and 4) minimal pleural effusions (figure 9a). The primary sonographic sign to
be identified is the presence of multiple B-lines in a diffuse and nonhomogeneous
distribution. B-lines are defined as discrete laser-like vertical hyperechoic reverberation
artefacts that arise from the pleural line ( previously described as “comet tails”), extend to
the bottom of the screen without fading, and move synchronously with lung sliding [45].
Patients with diffuse parenchymal lung disease (e.g. exogen allergic alveolitis, pulmonary
fibrosis) often have pleural line abnormalities; the distribution of B-lines correlates with
signs of fibrosis on CT [13, 42, 47, 48, 61–63].
The value of the method lies in the detection of a serious condition and in steering the
diagnostician’s attention towards a specific target (figures 10 and 11).
Therapy controls are highly efficient in cases of minimal pleural effusions and subpleural
infiltrations; no method is superior to sonography in this regard.
The US image does not provide a complete overview of the chest. However, it does show a
certain portion of the lung surface and thus provides diagnostic information about a variety
of problems. LUS cannot see the depth of the healthy lung. Only alterations reaching up to
the pleura, pathological artefacts and consolidations can be visualised.
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a) b)
c)
Figure 11. Sarcoidosis. A 26-year-old male with “a cold”: dyspnoea, moderate pleuritic pain. a) Minimal
basal pleural effusion. Fragmented pleura line with B-lines. b) Subpleural consolidations. c) Corresponding
CT showing intrapulmonal alterations.
A lot of studies and eight meta-analyses have considered CAP. There is less research is on
hospital-acquired pneumonia and lung consolidations in ICU.
High-frequency and positive end expiratory pressure ventilated patients show less or no
dynamic bronchoaerograms in consolidations. It is therefore difficult to differentiate
obstructive atelectasis from pneumonia.
Expectations based on clinical history and the patient’s physical presentation could be a
further bias to the imaging examination. The examiner’s education and experience, and bad
documentation could be further limitations.
Conclusion
Based on the literature, LUS has a high accuracy of >90% in the diagnosis of
community-acquired pneumonia. LUS cannot rule out pneumonia. The sonographer
should strictly exercise the signs and sonomorphologic criteria. LUS has advantages beyond
those of CXR when used in certain situations, such as for bedridden patients, in the
emergency room, in pregnant patients, in children and so on. LUS lacks ionising exposure
and can be performed at the bedside as well as in follow-up, especially in cases with
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parapneumonic effusion. Beyond CAP, other inflammatory lung diseases are less frequently
studied. In these conditions, the value auf LUS is limited but it can help to plan further
diagnostic strategies and imaging procedures.
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ventilator-associated pneumonia. Crit Care Med 2010; 38: 84–92.
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compared to chest computed tomography. Am J Emerg Med 2015; 33: 620–255.
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55. Jones BP, Tay ET, Elikashvili I, et al. Feasibility and safety of substituting lung ultrasonography for chest
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59. Yuan A, Yang PC, Chang DB, et al. Ultrasound guided aspiration biopsy for pulmonary tuberculosis with unusual
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| Chapter 8
Pulmonary embolism
Giovanni Volpicelli
The diagnosis of pulmonary embolism is often a complex process that starts from clinical
suspicion and is guided by risk stratification in selected populations. LUS may have a role in
this process, as it is a valid technique that is highly specific for diagnosing typical peripheral
lung infarctions and highly sensitive in ruling out alternative pulmonary diagnoses to
pulmonary embolism. Either alone, or in particular in combination with cardiac and venous
US, sonographic examination of the lung represents a valid alternative to a multidetector CT
scan when the latter is unavailable or contraindicated. Moreover, when integrated in the
pre-test clinical risk score assessment of pulmonary embolism, a multiorgan US based on
evaluation of pulmonary peripheral infarctions and deep vein thrombosis is useful to
improve the performance of the Wells score. Integration of US in the process to assess the
risk score for pulmonary embolism may significantly reduce the number of unnecessary CT
scans. Finally, LUS is also useful in all undifferentiated emergency situations, such as cardiac
arrest, shock and respiratory failure, to orientate the diagnosis and include the possibility of
unexpected pulmonary embolism.
Cite as: Volpicelli G. Pulmonary embolism. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic
Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 102–114 [https://doi.org/
10.1183/2312508X.10006717].
In the context of patients with suspected pulmonary embolism, LUS should be evaluated as
a diagnostic method. More than simply finalising the diagnosis of pulmonary diseases and
injuries, very often it may contribute to expedite the process, to guide further diagnostic
steps and to help restrict the differential possibilities. The main principle of the efficacy of
US in examination of the lung is based on the fact that changes in the condition of
Dept of Emergency Medicine, San Luigi Gonzaga University Hospital, Torino, Italy.
Correspondence: Giovanni Volpicelli, Dept of Emergency Medicine, San Luigi Gonzaga University Hospital, Torino, Italy.
E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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To optimise the diagnostic process and favour the safest and quickest decision making, the
modern clinician is required to orient their mind between accredited rules on a daily basis.
We currently live in the era of Bayesian medicine, which is the best-known approach for
complex problem solving. According to Bayes’ theorem, the diagnostic process depends on
consideration of the specific population being examined and the level of risk of having the
disease in these patients [3]. Moreover, a complex evaluation of costs, benefits and
invasiveness of the investigating tools must be considered to orientate the diagnostic
work-up. Thus, the clinician cannot rely only on the calculated absolute accuracy of a
positive or negative test to evaluate sufficiently the probability of disease; consideration
about the prevalence of the disease in the tested population, as well as evaluation of the
availability and opportunity to submit the patient to a specific test, are issues that may have
a significant influence on the process.
Thus, the three main steps that characterise the diagnostic work-up for pulmonary
embolism are: 1) a suspicion of pulmonary embolism, 2) assessing the pre-test probability
and 3) deciding the most appropriate test to finalise the diagnosis. This is a diagnostic
cascade that cannot be interrupted. For instance, the diagnostic process for pulmonary
embolism cannot perform correctly in a population without clinical symptoms or signs that
support the suspicion. In addition, without stratifying the probability risk, the accuracy of
the applied diagnostic tests will remain undefined.
The European Society of Cardiology (ESC) has produced specific guidelines for the
diagnostic process of pulmonary embolism [4], which start from the consideration of
suspected pulmonary embolism. However, in the real practice of the emergency setting,
suspicion of pulmonary embolism is not always the first step to initiate the diagnostic
process. Sometimes, pulmonary embolism is a hidden or unlikely possibility, inside a more
complex diagnostic process for undifferentiated respiratory failure, shock and hypotension,
pleuritic pain or syncope, often in complex multipathological elderly patients. In these
situations, pulmonary embolism may represent an even harder diagnostic challenge. The
diagnostic process is also challenged by the difficult conditions that may be encountered,
for example, in the case of unstable patients who cannot be moved in the radiology unit, or
when the high risks linked to irradiation, allergies and renal failure contraindicate a
contrast-enhanced CT scan.
In general, the main diagnostic possibilities for demonstrating pulmonary embolism are: 1)
detecting the presence of a thrombus in the main pulmonary artery tree, 2) detecting the
presence of a source thrombus in the deep venous system or in the right heart, 3)
observing the upstream effect of the artery occlusion (i.e. the haemodynamic consequence
visible in the right cardiac function) and 4) visualising the downstream effect of the artery
occlusion in the form of peripheral pulmonary infarcts. The last condition is potentially
detected by LUS. Indeed, peripheral infarctions are due to a cascade of events following the
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The usefulness of LUS for pulmonary embolism has been investigated in the literature over
the last 15–20 years, and it is clear that US represents a new and efficient tool in the
armamentarium of physicians facing clinical conditions where pulmonary embolism is
included in the differential diagnosis. The specific properties of the modern PoCUS make this
tool particularly suitable at the bedside for guiding complex diagnostic processes [5]. US is a
powerful, noninvasive diagnostic tool that may be repeated at the bedside to monitor changes
in time, and may reduce costs and time, and is even more efficient when used by clinicians.
In the existing literature, the validation of LUS for pulmonary embolism followed three
sequential steps. The use of LUS alone was the first step, demonstrating that US had the
potential to visualise lung infarcts and that it was a valid alternative to CT scans in the
diagnostic work-up of pulmonary embolism. Next, multiorgan US was used to show that a
combination of LUS with cardiac and venous US could improve the performance of each
organ examination considered alone, particularly considering the potential of LUS to detect
alternative pulmonary diagnoses. This multiorgan and multitask examination is even more
valid as an alternative to CT scans, not only to confirm but especially to rule out the disease.
Finally, the US-enhanced prediction rule was used to demonstrate that LUS, in combination
with venous US, may be useful to improve the performance of the pre-test prediction rule in
the diagnostic process for pulmonary embolism. Thus, LUS contributes to the definition of
the pre-test clinical probability of disease and guides further diagnostic steps in patients with
suspected pulmonary embolism. These three steps are discussed further.
Several studies explored the accuracy of LUS for pulmonary embolism by investigating its
potential in visualising the peripheral infarctions. The most significant was a multicentre
study performed on 352 patients with suspected pulmonary embolism and admitted to
internal medicine and pulmonology wards [6]. LUS was performed at the bedside and
targeted to the visualisation of typical triangular or rounded pleural-based lesions. The
main hypothesis was that at least two of these lesions were pathognomonic of the disease.
The US technique consisted of scanning the whole chest in the anterior, lateral and
posterior areas by longitudinal and oblique intercostal scans. The typical US lesions
indicating peripheral lung infarctions appeared as small, well-defined consolidations with
sharp margins, usually of triangular or rounded shape, with interruption of the pleural line
and the absence of air bronchogram and vascularisation. These infarcts are considered
significant when the diameter at the pleural surface is >5 mm (figure 1). In the study, the
authors investigated four US patterns, assigning to each of them different diagnostic criteria
in terms of probability of the disease: 1) confirmation of pulmonary embolism when at
least two of these typical lung infarctions were detected, 2) probable pulmonary embolism
when one typical lesion was detected combined with a corresponding low-grade pleural
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Figure 1. Two examples of typical infarcts detected by LUS in two cases of confirmed pulmonary embolism.
The typical consolidations are hypoechoic images of size >5 mm, wedge or round shaped, pleural based and
without air bronchogram or vascularisation.
effusion, 3) possible pulmonary embolism when small (<5 mm) nonspecific subpleural
lesions were detected or pleural effusion alone and 4) pulmonary embolism ruled out when
US showed a normal lung pattern (i.e. a regular pleural line with sliding and A-lines, or
other patterns sometimes indicative of alternative conditions, in the absence of typical
consolidations) [6]. In most cases, the gold standard used was single-row CT. To
compensate for the low sensitivity of this radiological tool, a combination of at least two of
the following adjunctive criteria confirmed the diagnosis in the case of a negative CT scan:
1) high clinical suspicion, 2) a positive D-dimer result in the case of outpatients, 3) positive
leg-vein thrombosis, 4) characteristic changes in echocardiography, 5) a high-probability
V/Q scan, 6) angiography of the pulmonary artery or 7) necropsy. The study demonstrated
that the combination of the two US criteria, confirmed pulmonary embolism and probable
pulmonary embolism, yielded the best sensitivity (74%) and specificity (95%), whereas the
criteria of confirmation alone showed an even better specificity (99%) at the expense of a
much lower sensitivity (43%) [6]. Notably, in this study, only 352 patients were definitively
enrolled out of a projected number of 710 with suspected pulmonary embolism during the
study period. The authors reported different reasons to explain this high rate of exclusion.
Two of the main reasons, accounting for 77% of the exclusion rate, were the impossibility
of performing CT (the patient could not be transported or had a contrast medium allergy
or severe renal failure, or the unavailability of CT at the time of admission; total 44%) and
unavailability of an expert in US (33%) [6]. Thus, often a CT scan cannot be performed,
and implementing US education will be fundamental to improve the standard of care.
A recent meta-analysis by SQUIZZATO et al. [7] analysed the results of studies on LUS for
pulmonary embolism. Ten studies were evaluated for a total of 887 patients investigated.
Overall, LUS showed a sensitivity of 87% and a specificity of 82% for the diagnosis of
pulmonary embolism. The analysed studies covered a period of 20 years, which is quite
long considering the progress in medical imaging technology and the rapid changes in the
consideration of LUS signs of pulmonary embolism. For instance, the performance of the
old single- or two-row detector CT is much inferior to the modern multidetector CT
(MDCT) devices. Notably, the accuracy of LUS changed significantly when more advanced
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CT devices were used as the gold standard in pulmonary embolism studies. Pooled data
from the meta-analysis demonstrated higher sensitivity (98%) and specificity (94%) when
LUS was compared with MDCT [7]. Another major limitation of this meta-analysis was
that in some studies the authors did not explain in detail the US criteria for the diagnosis
of pulmonary embolism. Of course, the standardisation of these criteria is fundamental.
Modern literature is more focused on US standardisation than the older studies. The study
of MATHIS et al. [6] responds better than others to this need. The main criteria introduced
in the study to support the diagnosis (i.e. typical peripheral consolidation of >5 mm) is
currently widely accepted among experts.
Lungs are wide organs. Thus, exploring the lung surface by US to look for consolidations
should be extended to the whole chest, including the anterior, lateral and posterior walls.
A whole-chest examination may be complex to perform in some patients and in some
specific settings, particularly in an emergency setting and in the critically ill. There are
some situations where LUS may reveal infarctions more reliably if guided in a restricted
area by the patient’s symptoms. This is typically the case for pleuritic pain. The usefulness
of US to reveal pulmonary radio-occult conditions causing pleuritic pain has been clearly
demonstrated [8, 9]. In these cases, US is very efficient simply because pain reveals the
involvement of the parietal pleura. Thus, when the pain is due to a pulmonary disease, it is
peripheral and potentially visible by LUS. Pleuritic pain is also a common and frequent
symptom in pulmonary embolism. Unpublished data obtained by analysing three databases
from multicentre studies on LUS for pulmonary embolism have shown that LUS performed
better in terms of sensitivity and specificity in the subgroup of patients complaining of
pleuritic pain (table 1) [10–12].
The first international consensus conference on point-of-care LUS discussed the evidence
on the usefulness of LUS for pulmonary embolism [13]. The results confirmed the
usefulness of LUS as a valid alternative to CT when the latter cannot be used. This
validated technique is based on whole-chest examination for the detection of typical images
corresponding to pulmonary infarctions. The sonographic signs are small (1–3 cm, range
0.5–7 cm), pleural-based, echo-poor consolidations with sharp margins and without central
vascularisation. These signs have a good specificity, but the studies analysed by the
consensus process did not show an optimal sensitivity (80%). In practice, in suspected
pulmonary embolism with a level of probability of disease that indicates further testing, and
Table 1. Diagnostic performance of LUS for the diagnosis of pulmonary embolism in unselected
patients, and in patients without and with pleuritic chest pain
The meta-analysis was performed on the databases of three multicentre studies [10–12]. Data
represent work in progress and are unpublished. PPV: positive predictive value; NPV: negative
predictive value; PLR: positive likelihood ratio; NLR: negative likelihood ratio.
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when a CT scan cannot be undertaken, the caring physician should consider LUS.
Detection of typical US signs allows diagnosis with good specificity, but the absence of
typical infarctions does not rule this out with certainty, and further testing would be
necessary when the probability of disease remains high. The consensus conference also
recommended the use of LUS in pleuritic pain, as this technique is highly reliable in the
detection of pulmonary conditions not visible by chest radiography, including lung
peripheral infarctions due to pulmonary embolism [13].
In the diagnostic process for pulmonary embolism, organs other than the lung may also be
the object of an US examination and may provide indirect signs of the disease.
Cardiac US
Cardiac US is targeted to the demonstration of the haemodynamic effect of pulmonary
embolism (i.e. dysfunction of the right ventricle) [10, 14, 15]. The most used sign is dilation
of the ventricle, which is assessed semi-quantitatively by comparing the end-diastole
measures of the diameters of the two ventricles [10]. The normal dimension of the right
ventricle, when compared with the left ventricle, is fixed in terms of percentage at a cut-off
that is slightly variable depending on the window used, between the apical, subcostal and
parasternal windows [10, 14, 16]. In the apical four chambers (i.e. the optimal view for
assessing the right dilation), the diameters of the two ventricles are assessed close to the
valve level, and a ratio of 0.9 represents the cut-off value to define dilation. Evidence of
right-ventricle dilation is a sign of acute strain in haemodynamically unstable patients with
suspected pulmonary embolism, and should confirm the diagnosis when CT cannot be
performed [4]. However, dilation of the right ventricle has two main limitations in the
diagnostic process for pulmonary embolism. First, it is not sensitive enough to also be used
in stable patients [4]. In cases of pulmonary embolism with stable haemodynamics, it is quite
common to observe a normal right ventricle. Second, in patients with chronic diseases,
right-ventricle dilation may exist prior to the acute event, thus inducing a misdiagnosis. The
ESC guidelines recommend considering additional US signs indicating chronic dilation, and
do not recommend the use of echocardiography as part of the diagnostic work-up in
haemodynamically stable, normotensive patients and in patients who are not high risk [4].
Additional dynamic echocardiography signs, such as depressed contractility or a disturbed
ejection pattern of the right ventricle, may be considered, but these signs are more complex
to assess in an emergency situation. Assessment of the thickness of the free walls of the right
ventricle is more practical and may help in differentiating chronic situations.
Venous US
Compressive venous US has an important role in the diagnostic work-up of pulmonary
embolism. Lack of compressibility of the deep veins of the legs at two points,
corresponding to the common femoral and the popliteal veins, with some extension to the
proximal main tributary veins, is the validated US sign allowing direct confirmation of a
source of thrombosis [17–19]. The technique consists of pressing the probe on the veins
visualised on the screen in the short axis. Lack of total occlusion of the pressured vein is a
highly specific sign, which authorises the caring physician to finalise the diagnosis in
patients with suspected pulmonary embolism, independent from CT scan confirmation [4].
However, as for right-ventricle dilation in echocardiography, evidence of a thrombus during
venous US is also of low sensitivity, as ∼50% of patients with confirmed pulmonary
embolism have no more thrombotic material deposited in the peripheral deep veins. In
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Multiorgan US
Echocardiography for right-ventricle dilation and venous compressive US for signs of
thrombosis are currently considered part of the bedside point-of-care examination. This is due
to the widespread use of new portable machines and growing evidence on the reliability of
bedside US in the hands of the clinician. In the diagnostic work-up of pulmonary embolism,
echocardiography, venous US and LUS all have the potential to be of use. However, in the
existing literature, these three techniques considered alone have demonstrated good specificity
but low sensitivity [6, 14, 19]. When negative, none of the three examinations considered
alone is enough to rule out the disease in an unselected population with an open diagnostic
dilemma for pulmonary embolism. Thus, the question was raised as to whether a combination
of the three techniques might improve this insufficient sensitivity.
The answer to this question was provided by a multicentre trial that demonstrated, in 357
patients, the high feasibility and reliability of a multiorgan US evaluation in suspected
pulmonary embolism, targeted to visualisation of lung infarcts, dilation of the right ventricle
and lack of compressibility of the deep leg veins [10]. In this study, the negative predictive
value of the multiorgan approach was increased to 95%, compared with 84.6% for LUS, 74.8%
for echocardiography and 82.2% for venous US alone. The study also showed that LUS and
echocardiography may be useful to diagnose alternative conditions to pulmonary embolism,
such as pneumonia, pneumothorax, pleural effusion, pericardial effusion and cardiogenic
pulmonary oedema [10]. Using this potential, the combination of negative multiorgan US
coupled with a positive alternative diagnosis raised the negative predictive value to 100%. This
combination was observed in 37% of cases in the population showing positive D-dimer result
or a high-probability Wells score. Considering also the positive diagnosis of deep vein
thrombosis obtained in the same population (17.9% of patients), there was a high percentage
of patients (55%) who might avoid an MDCT scan, which would still be considered necessary
if based on the conventional rules [10].
Another study tested the multiorgan approach for pulmonary embolism. This study was
focused mainly on the hypothesis that integrating US of the lung, heart and leg veins may
be useful to reduce the number of CT scans in cases of suspected pulmonary embolism [21].
Again, the results of the study were encouraging, as the authors found 56% of cases where
the sonographic alternative diagnosis to pulmonary embolism or the direct visualisation of
the venous peripheral thrombi might allow the avoidance of CT scans, with 100% sensitivity
in a population of 96 patients. Indeed, the conclusion of the study was that a multiorgan US
approach safely reduces the number of unnecessary CT scans ordered to rule out pulmonary
embolism. In this study, the authors applied LUS only for diagnosing alternative pulmonary
conditions and did not consider the potential of a direct visualisation of pulmonary
infarctions [21]. The same authors concluded that incorporating this adjunctive LUS
technique would allow an even greater reduction in the use of unnecessary CT scans. My
personal comment is that, rather than just confirming pulmonary embolism, LUS for
infarctions may allow a safe exclusion of the disease when the multiorgan test is negative, as
was demonstrated by the study of NAZERIAN et al. [10]. Indeed, KOENIG et al. [21] observed
30% of cases where pulmonary embolism was confirmed although cardiac and venous US
examinations were negative, but in the absence of alternative diagnoses. Thus, the question
remains unanswered as to whether integrating the US investigation for infarctions might
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have improved the results for this 30%, using not only the confirmation of an alternative
disease but also the negativity of the three tests to rule out the disease.
These experiences from multiorgan US further confirm the usefulness of LUS for
pulmonary embolism. When LUS is integrated in a multiorgan approach, it represents a
better alternative to CT when the latter is unavailable or contraindicated.
Following the Bayesian methodology, the diagnostic work-up for pulmonary embolism is
guided by standardised prediction rules to define the probability of disease and orientate
the process. Once the validity of LUS as an alternative to CT scans in the diagnostic
work-up of pulmonary embolism had been explored, there was one further question that
remained unanswered: is it useful to integrate US into the clinical prediction rule that is
applied in the suspicion of pulmonary embolism?
For assessing the probability of disease, the ESC guidelines recommend the combination of
D-dimer tests with clinical scores, such as the Wells score, which optimises the diagnostic
process, and the use of a CT scan for final confirmation [4]. The clinical score is based on
evaluation of a list of items, of which the most weighted are the probability of pulmonary
embolism and clinical signs of deep vein thrombosis [23]. These two items are based on
considerations that are strictly subjective and remain highly variable when decided by
physicians with different skills and experience. Both the alternative pulmonary diagnosis
and the venous thrombosis are two conditions that PoCUS can objectively confirm at the
bedside during the first examination of patients with suspected pulmonary embolism. Thus,
the hypothesis that integration of the clinical evaluation with US of the lung and leg veins
might improve the efficiency of the pre-test clinical scoring needs to be investigated.
A recent multicentre study responded to this question by investigating 446 patients with
suspected pulmonary embolism in the emergency department of four academic institutions
[10]. LUS for the evaluation of typical pulmonary infarctions or alternative pulmonary
conditions, and compression US of the leg veins for peripheral thrombi were performed
during the first evaluation in all patients. The objective results of the bedside US
examination were used to adjudicate the first two items of the Wells score, replacing the
clinical subjective judgements. After finalisation of the diagnosis, based on a combination
of MDCT scan and clinical follow-up, the performances of the traditional clinical Wells
score and the US-enhanced Wells score were compared. The results of the study
demonstrated a better performance of the US-enhanced Wells score in terms of both
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sensitivity (12% increase) and specificity (22% increase) [11]. The conclusion of the study
was that a diagnostic strategy that integrates clinical information, lung and venous US, and
D-dimer results may increase the performance of risk stratification and may reduce the use
of CT scans in the diagnostic approach to pulmonary embolism, while still maintaining an
acceptable safety profile. Figure 2 shows a newly proposed diagnostic algorithm for
suspected pulmonary embolism, based on venous US, US Wells scores and D-dimer results.
The application of this revolutionary US/clinical scoring would hypothetically have allowed
the avoidance of 50.5% of CT scans in the population of the study.
These data pave the way for a new consideration of the usefulness of PoCUS for pulmonary
embolism, which includes the significant potential of LUS. Rather than just serving to
confirm the diagnosis when CT is contraindicated or unavailable, a systematic application
to the whole unselected population with suspected pulmonary embolism may allow further
optimisation of the diagnostic work-up and reduce the need for confirmatory CT.
In the daily practice of crowded and busy emergency departments and in critically ill
patients, physicians face challenging and complex diagnostic situations where pulmonary
embolism may be unlikely but should still be included as a possibility. In these situations,
Suspected
pulmonary embolism
Venous Diagnosis
US of DVT
DVT
excluded
US Wells
score ≤4 LUS
Figure 2. Proposed flow chart for the diagnostic work-up in suspected pulmonary embolism, based on the
integration of venous US and LUS with clinical scoring and D-dimer results. This new strategy allows the
avoidance of unnecessary multidetector CT scans in a higher percentage of patients than the traditional
combination of clinical scoring/D-dimer results. DVT: deep vein thrombosis; CTPA: CT pulmonary
angiogram.
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The role of LUS in the diagnostic work-up for pulmonary embolism is highly variable
when considering the characteristics of the population, the haemodynamic condition of the
patient, the probability of the disease and the availability of alternative tools, as well as the
related biological risks and costs.
There is already good evidence that LUS may be extremely useful in the diagnostic
work-up of pulmonary embolism at the bedside. PoCUS is a relatively low-cost technology,
is free from irradiation, is noninvasive, and is easily performed and repeatable at the
bedside in the hands of trained clinicians. In contrast, a CT scan is costly, invasive and
difficult to perform in emergency situations. We should never forget that the advanced and
wealthy health systems of western countries serve only a small minority of humankind.
Most of the world’s population have no access to advanced and costly technology. In
resource-scarce areas, US may be the only available imaging tool. Moreover, the
invasiveness of CT with the possible side-effects of irradiation and contrast medium
injection, together with the inability to move unstable patients to the radiology area,
sometimes mean that this technology is contraindicated. In cases where it is not possible to
perform CT scans, LUS targeted to visualisation of peripheral lung infarctions may be a
valid alternative. Once the typical infarcts are detected, the diagnosis becomes highly
probable. If no typical infarcts are detected, the sensitivity is not enough to conclude a
diagnosis of exclusion. A multiorgan approach that includes lung, cardiac and venous US,
which also considers the possibility of evaluating alternative cardiac and pulmonary
diagnoses to pulmonary embolism, increases the sensitivity and may be considered safe to
rule the condition in or out in the unselected population with suspected pulmonary
embolism. Table 2 summarises the efficacy of each individual US pattern in ruling the
condition in or out in patients with suspected pulmonary embolism. Further studies are
needed to compare US with pulmonary scintigraphy (V/Q scan), which to date represents
the accredited alternative to CT scans in the ESC guidelines [4]. The PIOPED (Prospective
investigation of pulmonary embolism diagnosis) II trial showed that the sensitivity of a
high-probability V/Q scan was 77.4%, while the specificity of a very low probability or
normal V/Q scan was 97.7% [26]. However, the occurrence of a nondiagnostic intermediate
V/Q scan represents the main criticism of this method. In the same study, only 73.5% of
patients had a conclusive V/Q scan, but this percentage may be far lower in common daily
practice. A V/Q scan is an invasive procedure, although the irradiation for an average-sized
adult (1.1 mSv) is lower than that for CT angiography (2–6 mSv) but still significant [27].
Thus, for ethical reasons, LUS and lung scintigraphy cannot be compared by simple
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observational protocols using CT angiography as the gold standard. Rather, more expensive
randomised controlled trials would be indicated, based on a comparison of two different
populations and using complex follow-up strategies to confirm the diagnosis.
Further efforts should also be made to better standardise the US criteria for the diagnosis
of typical infarctions. Indeed, the sonographic appearance of the peripheral infarctions
changes with time ( personal observations). This change may represent a limitation of the
technique if there is no consideration of the difference in time between the onset of
symptoms and the LUS examination.
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Another suggestive potential of LUS is its integration in the clinical prediction rule for risk
assessment. Integrating lung and venous US with the Wells score and D-dimer results in
the first examination of a patient with suspected pulmonary embolism improves the
performance of the process for clinical risk assessment, thus contributing to a reduction in the
number of unnecessary CT scans. Further studies are needed to test, in sufficient numbers of
patients, a new diagnostic strategy based on steps in succession, starting with venous US, and
followed by LUS, integrated US Wells scores and D-dimer results (figure 2).
References
1. Wells PS, Anderson DR, Rodger M, et al. Excluding pulmonary embolism at the bedside without diagnostic
imaging: management of patients with suspected pulmonary embolism presenting to the emergency department by
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17. Bernardi E, Camporese G, Buller HR, et al. Serial 2-point ultrasonography plus D-dimer vs whole-leg color-coded
Doppler ultrasonography for diagnosing suspected symptomatic deep vein thrombosis: a randomized controlled
trial. JAMA 2008; 300: 1653–1659.
18. Elias A, Colombier D, Victor G, et al. Diagnostic performance of complete lower limb venous ultrasound in
patients with clinically suspected acute pulmonary embolism. Thromb Haemost 2004; 91: 187–195.
19. Le Gal G, Righini M, Sanchez O, et al. A positive compression ultrasonography of the lower limb veins is highly
predictive of pulmonary embolism on computed tomography in suspected patients. Thromb Haemost 2006; 95:
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20. Nazerian P, Volpicelli G, Gigli C, et al. Diagnostic accuracy of focused cardiac and venous ultrasound examinations
in patients with shock and suspected pulmonary embolism. Intern Emerg Med 2017; in press [DOI: https://doi.org.
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22. Lichtenstein DA, Mezière GA. Relevance of lung ultrasound in the diagnosis of acute respiratory failure: the BLUE
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24. Shokoohi H, Boniface KS, Pourmand A, et al. Bedside ultrasound reduces diagnostic uncertainty and guides
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undifferentiated hypotension in the emergency department. Intensive Care Med 2013; 39: 1290–1298.
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| Chapter 9
Lung tumours
Christian Görg1, Corinna Trenker1 and Andreas Schuler2
The diagnostic value of TUS of lung tumours, especially bronchial carcinomas, is limited
and dependent on the localisation of the tumour. Focused clinical use is to be distinguished
in the context of primary diagnosis, staging, therapy response and tumour growth.
Symptom-oriented practice is important at the bedside for palliative patients, in
point-of-care sonography, in the emergency room and in intensive care units. Different
US-based procedures, such as transcutaneous US, EUS and EBUS are used for distinct
approaches to lung tumours. B-mode imaging, colour Doppler sonography, CEUS and
US-controlled interventions are the sonographic modalities used in daily clinical practice and
for special clinical questions. In special clinical indications, US is the primary guideline
diagnostic procedure. Transthoracic LUS is limited by physical factors such as absorption and
reflection and, in principle, by a high interobserver variability, as well as differences in device
and examining competence.
Cite as: Görg C, Trenker C, Schuler A. Lung tumours. In: Laursen CB, Rahman NM, Volpicelli G, eds.
Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 115–128 [https://
doi.org/10.1183/2312508X.10006817].
L ung tumours are amongst the most frequently seen malignant tumours in the world
and are one of the most common causes of cancer death [1]. Smoking is a major risk
factor. Clinical symptoms are uncharacteristic and include cough, dyspnoea, haemoptysis,
weight loss and occasional chest pain. Diagnostic procedures, therapy and follow-up are
presented in the current guidelines [2]. A whole-body PET (PET-CT) in combination with
an all-body CT, a radiographic thorax examination and EBUS, is part of the standard
diagnostic procedure [3]. Transoesophageal US (EUS), angiography, MRI, mediastinoscopy
and ultimately transcutaneous sonography are additional methods. The aims of the
diagnostic procedures are correct tumour diagnosis and characterisation of the cancer,
including TNM (tumour, node, metastases) classification [4–7]. In the context of diagnosis
and therapy of lung tumours, transcutaneous LUS is used for primary tumour diagnosis
and differential diagnosis, histological confirmation, staging, therapy response, aftercare and
detection of tumour- or therapy-associated complications [8, 9]. The following modalities
are used: B-mode imaging [10–12], colour Doppler sonography (CDS) [13, 14], CEUS [15–
18] and US-guided biopsy [19, 20]. The benefits of US examination are: high spatial
resolution, real-time conditions, the absence of radiation exposure [21], arbitrary
repeatability, and the possibility of bedside examination. Last but not least, ultrasound
1
Universitatsklinikum Giessen und Marburg, Marburg, Germany. 2Alb Fils Kliniken, Zentrum Innere Medizin, Helfenstein Klinik
Geislingen, Geislingen, Germany.
Correspondence: Christian Görg, Universitatsklinikum Giessen und Marburg – Standort Marburg. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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ERS MONOGRAPH | THORACIC ULTRASOUND
2) Visualisation and characterisation of the peripheral collar [4, 34, 35] and mediastinal
lymph nodes with percutaneous and endosonographic US, and possibly US-guided biopsy
(N-Stage).
In the diagnosis and differential diagnosis of bronchial carcinoma, CT of the thorax is the
standard procedure for T-classification, and where possible, should be taken as the basis of
US examination. An indication for transthoracic LUS does not exist in general, but can be
deployed in a focused manner, according to the clinical questions. First, basic and
sonographic criteria of lung tumour assessment will be presented. Subsequently,
sonographic findings will be presented with regard to the clinical questions.
Lung sonography where a lung tumour is suspected is limited and depends on the
presentation of the primary tumour. In general, peripheral lung tumours can be
differentiated from central tumours. While peripheral tumours can be visualised due to
contact with the pleural/thoracic wall, central lung tumours can only be detected with
associated obstructive atelectasis or pleural effusion with compression-induced atelectasis
(figure 1) [37, 38].
In B-mode imaging, pulmonary consolidations are characterised by their size, margins and
echogenicity, and the homogeneity of the lung tissue. In CDS, vascularisation is evaluated
by the extent of the CDS (missing, reduced, marked flow signals) and the vascular patterns
(regular, disordered vessels) [39]. With spectral curve analysis (SCA), high-impedance can
be differentiated from low-impedance flow signals in the consolidated lung;
high-impedance flow signals can be assigned to the pulmonary arteries and low-impedance
flow signals to the bronchial arteries [40–42]. Tumour neoangiogenic capacity is attributed
to the bronchial arteries [43–46].
CEUS of the thorax is possible and has to be performed according to the guidelines of the
European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) [15].
The first evaluation criterion is the “time to enhancement”. Pulmonary artery supply of a
pulmonary lesion can be determined by early arterial enhancement before systemic vascular
enhancement. Bronchial artery supply is characterised by delayed arterial enhancement at
the same time as systemic vascular presentation. Further CEUS evaluation criteria are the
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a) b) c) d)
e) f) g)
Another procedure is US-guided biopsy of thoracic tumours [19, 20, 47]. Differentiation is
made between the size of the biopsies (core needle: >1 mm needle diameter; fine needle:
<1 mm needle diameter). Depending on clinical indication, pleural effusion-paracentesis
(diagnostic, therapeutic) and catheter drainages ( pig-tail catheter, subtunneled continuous
drainage) can be differentiated.
The following clinical questions have to be answered through focused LUS examination.
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Thorax wall infiltration classifies a lung tumour as T3 [2]. This does not limit surgical
treatment but is important for operation planning. B-mode US represents the imaging
method of choice here due to the high spatial resolution of US but mainly because it
allows the possibility of the real-time examination [25, 26]. Criteria for thoracic wall
infiltration are: absent pulmonary sliding to the thoracic wall (“fixed lung”);
a) b)
c) d)
Figure 2. Patient with lung consolidation and histologically proven nonsmall cell lung cancer. a) CXR shows
a left-sided central lung consolidation. b) CT shows a left-sided central tumour with suspected obstructive
atelectasis. c) B-mode US shows a homogeneous hypoechoic lung consolidation without airbronchogram.
The central tumour cannot be distinguished from the atelectatic tissue. d) CEUS shows reduced
enhancement of the central tumour in the parenchymal phase, in comparison to atelectasis.
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interruption of the pleural line; detection of continuous tumour infiltration into the
thoracic wall; tumour vascularisation of the lesion via bronchial artery tumour
neoangiogenesis [54]; and additional systemic tumour vascularisation from the
intercostal arteries [42]. Tumour localisation in the apex of the lung is known as a
Pancoast tumour (figure 3).
a) b)
c) d)
e)
Figure 3. Patient with pain in the left shoulder and histologically proven nonsmall cell lung cancer
(Pancoast tumour). a) CXR shows a left-sided apical opafication suggestive of Pancoast tumour. b) CT shows
a left-sided apical tumour which infiltrates the thoracic wall (arrow). c) B-mode US shows a left-sided
apical echoic consolidation which infiltrates and destroys the rib (arrow). d) CEUS shows an inhomogeneous
enhancement of the tumour with areas of no enhancement due to necrosis (arrow). e) US-guided tumour
biopsy was performed using vital tissue. The arrow indicates needle reflexion.
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Supraclavicular lymph nodes are an important component of the lymphatic drainage of the
chest. Sonographic access is excellent due to their superficial location. Whenever a CT scan
of the neck shows the suspicion of or a proven bronchial carcinoma and/or suspicious
lymph nodes, sonography should be performed immediately prior to therapeutic or
invasive diagnostic procedures. The aim of is to prove or exclude enlarged or suspicious
supraclavicular lymph nodes and, if positive, to perform an US-guided biopsy in the same
session [35]. CT scans and MRI are less sensitive than US of the neck (83% CT/MRI versus
>90% US) [69]. Specificity is lower with all imaging modalities to exclude malignancy.
Lymph node metastasis in the neck are mostly hypoechoic, with a transversal diameter of
⩾5 mm. Transcutaneous lymph node core needle biopsy for histological purposes is highly
recommended in such patients. Patients with mediastinal lymph node metastasis in N3
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a) b)
c) d)
Figure 4. Patient with histologically proven nonsmall cell lung cancer and pleural effusion. a) CXR shows a
left-sided basal opafication suggestive of pleural effusion. b) CT shows a left-sided pleural effusion with
pleural nodules. c) B-mode US shows a left-sided echofree pleural effusion with echoic nodular pleural
lesions. d) CEUS shows an enhancement of the pleural lesions suggestive of pleural carcinosis. Cytological
examination of the pleural fluid shows tumour cells.
position have ⩽51% enlarged supraclavicular lymph nodes which are not palpable. Positive
histology findings in lymph nodes of the neck lead to a complete change in therapeutic
management due to inoperability at stage IIIB lung cancer [4, 34]). Particularly in patients
with negative cyto-histology for primary tumours or mediastinal lymph nodes seen in other
biopsy procedures (such as transbronchial biopsy), EUS or transcutaneous ultrasound
provide histological proof of malignancy in the supraclavicular lymph nodes and avoid
other more invasive procedures (such as mediastinoscopy and thoracoscopy).
Are there distinct sonographic patterns of lymph node metastasis in the neck?
It is well known that there are specific signs of malignancy in sonographic patterns of
supraclavicular lymph node metastasis. Malignancy is strongly suspected if there is loss of the
central hyperechoic hilum within the lymph node, as well as a round-shaped mostly hypoechoic
lymph node with a transversal diameter of ⩾5 mm. Sometimes borders are not sharp, and in
aggressively growing lymph node metastasis there might be signs of infiltration in the muscles,
vessels or soft tissue. Vascularisation criteria for malignancy are peripheral vessels, an irregular
vascular pattern and a chaotic spreading of vessels with different flow directions [70].
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Various head and neck malignoma of several primary origins can lead to lymph node
metastasis: thyroid, parathyroid, pharyngeal and laryngeal tumours, salivary gland
carcinoma, skin tumours and others. Chest tumours (lung cancer, breast cancer) and
sometimes other cancers can lead to lymph node metastasis in the neck. Biopsy of
suspicious lymph nodes is therefore highly recommended.
Enlarged or suspicious lymph nodes in the neck found using sonography can almost always
be easily punctured with ( permanent) US-controlled histology (core needle biopsy)
(figure 5). This is the most common and safest way to obtain histological specimens with
only a minimal rate of complication [72]. Punctures should only be performed if there is
any (diagnostic and/or therapeutic) consequence of the histological result. A colour
Doppler should be performed to avoid accidental vessel injuries. The nerve bundle should
be demonstrated if there is any doubt about its location in relation to the lymph nodes or
other tumour presentation [69]. In a lymph node with a transversal diameter of ⩾5mm, a
sufficient histological specimen can be achieved in nearly 100% of cases with an
experienced examiner and an 18-G (1.2-mm) core needle. Cytology is less sensitive and
specific for definite diagnosis; this is due to smaller specimen size and relatively less
experience amongst pathologists. It is also increasingly necessary to perform
immunohistological examinations with the acquired specimen to prove or exclude
molecular mimicry and mutation. Clinically speaking, a proven supraclavicular lymph node
metastasis refers to lung cancer stage N3 (figure 5).
The mediastinum, EBUS and EUS are covered elsewhere in this Monograph [73].
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a) b)
AMI
ST
TU
c) d)
+
+ +
+
Figure 5. Supraclavicular lymph node metastasis in a patient with nonsmall cell lung cancer (Pancoast
tumour). a) Location of the primary tumour (TU) in the right upper lung near to the pleura, beside the
sternum (ST). Real-time US did not demonstrate an infiltration of the parietal pleura. Fine-needle aspiration
of the primary lesions was not performed due to the location dorsal to the Arteria Mammaria interna (AMI).
b) EBUS-FNA was performed for cytology of the mediastinal lymph node in position 3 (pretracheal). c)
Suspicious supraclavicular lymph nodes on the left side (contralateral): hypoechoic, round shaped, >0.5 cm
in short transversal axis. d) US-guided transcutaneous core-needle biopsy demonstrated histologically proven
N3 stage (metastasis of nonsmall cell lung cancer). Two lymph nodes were punctured in one session.
If there are any suspicious positive lesions (in the lymph nodes, soft tissue/small part,
bones, abdomen, chest) on PET-CT that could potentially be seen with transcutaneous US,
then go for it! This means the supraclavicular lymph node positions as well as the
supra-aortal and upper mediastinal positions could be seen transcutaneously. And by
extension, this means all other previously mentioned lesions wherever they are. If there is
any possibility of/necessity to achieve histology this should be done using real-time US
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a) b)
c) d)
Figure 6. Patient with swollen head and mediastinal tumour primarily suspected for lung cancer. a) CXR
shows a mediastinal opafication suggestive of lung cancer. b and c) B-mode US of the left-sided jugular
vein shows in the longitudinal and transversal scan, an echoic dilated venous vessel suggestive of vena cava
superior syndrome. d) B-mode US shows a left-sided apical echoic lung consolidation. Histology revealed
large cell lymphoma.
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| Chapter 10
The diaphragm
Giovanni Ferrari1, Søren Helbo Skaarup2, Francesco Panero3 and
John M. Wrightson4
This chapter covers US evaluation of diaphragm function, and describes the methods and
US techniques used to measure movement and thickening of the diaphragm. Current
validated techniques that assess diaphragm function are often invasive or expose the patient
to ionising radiation. US is a noninvasive, easily repeatable bedside tool allowing direct
visualisation of the muscle. There are a number of applications of DUS, from assessment
and emergency medicine to respiratory medicine. DUS has become a useful tool in
evaluating diaphragm dysfunction, suggesting its use to predict discontinuation from
mechanical ventilation and to evaluate muscle atrophy during mechanical ventilation. It also
has an important role in assessing respiratory effort, and in evaluating diaphragm paralysis
and the mechanical consequences of pleural effusion. Thus, DUS is a fast, easy procedure
that can identify diaphragm dysfunction, monitor muscle activity over time and provide
useful information during invasive procedures such as thoracentesis.
Cite as: Ferrari G, Helbo Skaarup S, Panero F, et al. The diaphragm. In: Laursen CB, Rahman NM,
Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018;
pp. 129–147 [https://doi.org/10.1183/2312508X.10006917].
T he diaphragm represents the main respiratory muscle but prior to the widespread use
of US remained challenging to assess. This is of relevance given that diaphragm
dysfunction is frequent in the critically ill, with patients developing a degree of muscular
atrophy and weakness secondary to mechanical ventilation [1].
1
Pulmonary Medicine, Ospedale Mauriziano Umberto I, Torino, Italy. 2Dept of Pulmonary Medicine and Allergy, Aarhus University
Hospital, Aarhus, Denmark. 3High Dependency Unit, San Giovanni Bosco Hospital, Torino, Italy. 4Oxford Centre for Respiratory
Medicine, Churchill Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK.
Correspondence: Giovanni Ferrari, Pneumologia, Ospedale Mauriziano Umberto I, Largo Turati 62, 10128 Torino, Italy. E-mail:
[email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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of probable pleural malignancy. A number of studies have demonstrated its easy learning,
high reproducibility and good correlation with other validated measures.
This chapter provides a summary of the pathology affecting the diaphragm and proposes
methods for assessing diaphragm function and structure using DUS. We highlight specific
examples of DUS use, particularly where there is an evidence base.
Many disorders affect the structure and function of the diaphragm, including those
affecting its innervation (central and peripheral nervous system and neuromuscular
junction) and the muscular and tendinous diaphragm itself, and other disorders causing
mechanical disruption of the diaphragm (including pleural and pulmonary causes)
(table 1). Identification and quantification of the effects of these disorders on the
diaphragm is of relevance to physicians from a wide range of specialities, including
pulmonologists, intensivists, neurologists, spinal physicians, radiologists and surgeons.
Table 1. Disorders that affect the diaphragm and their site of effect
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DUS technique
The diaphragm is the most important muscle in breathing. Contraction of the diaphragm
causes it to move in a craniocaudal direction, thereby increasing intrathoracic volume and
decreasing intrathoracic pressure. This results in inspiratory airflow into the lungs. The
intercostal and pectoral musculature also contributes to inspiration but to a lesser extent
during tidal breathing. Sufficient diaphragmatic function is considered vital [5]. During
exhalation, the diaphragm relaxes and, due to elastic recoil of the lungs, the diaphragm is
passively drawn cranially to its resting position. In a forced exhalation manoeuvre, the
diaphragm is relaxed, and contraction of internal intercostal and abdominal muscles leads
to rapid exhalatory airflow.
Assessment of both diaphragm excursion and diaphragm thickening may be used as tools
for functional assessment.
M-mode
The time motion mode (M-mode) may be used to measure the excursion of the
diaphragm. While there is no consensus on how the M-mode should be performed, most
authors suggest the use of a curvilinear low-frequency transducer placed in the
midclavicular line and angled in a cranial direction (figure 1). The M-mode line is placed
at the posterior part of the diaphragm where there is maximal movement and excursion.
On the right side, the liver acts as an acoustic window, and the diaphragm is easily
identified as a hyperechoic curved line abutting the liver (figure 2). Left hemidiaphragm
imaging is more difficult due to the poor acoustic window of the spleen and the gas
content of the stomach.
Many studies describing the M-mode technique only assess the right hemidiaphragm [10,
11], while others note a lower success evaluating the left [12]. The probe should be placed
in the subcostal area, between the midclavicular and the anterior axillary line, directing the
US beam medially, dorsally and cranially [12]. The angle of incidence of the US beam
should be perpendicular to the direction of the muscle movement [13]. As the patient
inhales, the abdominal wall is pushed forward, potentially displacing the transducer, and
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Figure 1. US evaluation of diaphragm movement with a curvilinear transducer in the sagittal plane in the
midclavicular line (red line). The transducer is angled cranially and uses the liver as an acoustic window.
B-mode
Another method of quantifying diaphragm excursion is to use brightness mode (B-mode)
to measure craniocaudal movement during breathing. This method is simple and can be
used at both hemidiaphragms [15–17]. A curvilinear low-frequency transducer is placed
perpendicularly in a lower intercostal space (ICS) between the mid- and posterior axillary
Figure 2. The right hemidiaphragm is identified as a curved hyperechoic structure posterior to the liver. The
M-mode line (white line) is placed to measure maximal excursion (bottom panel).
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line using the liver or spleen as an acoustic window. Other authors have proposed that the
craniocaudal movement of the portal vein can also be measured as a surrogate for
diaphragm excursion [18].
Other methods
New methods to assess diaphragm movement, such as speckle tracking, are under
investigation but require further validation [19–21]. The rate of diaphragm excursion has
also been studied [22].
During US, the diaphragm appears as a hypoechoic structure superior to the liver or
spleen, flanked by two thin hyperechoic lines, which are the diaphragmatic pleura
(superficially) and the peritoneum (deeper) (figure 4). The minimal thickness in the resting
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1+
Figure 4. The diaphragm identified as a three-layered structure superficial to the liver or spleen.
Hyperechoic layers of the diaphragmatic pleura (thoracic side) and the peritoneum (abdominal side)
surround the hypoechoic diaphragm. Thickness is measured with the calliper function in maximal inhalation
and exhalation (indicated by crosses and a dotted line). “1” indicates the diaphragmatic pleura.
diaphragm is 12–15 mm [24, 25]. Accurate assessment of thickness requires that the US
beam is perpendicular to the diaphragm, rather than oblique [26].
Thickness
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to one-third of healthy people show no increase in thickening during tidal breathing [25].
Intra- and inter-rater agreement is high [30], including during mechanical ventilation
(although more so on the right than on the left) [31].
Excursion
Evaluation of excursion during breathing has mostly been undertaken using M-mode in a
subcostal midclavicular view. There is a linear relationship between M-mode excursion and
exhaled lung volume measured by spirometry [10, 11, 17]. A linear relationship has also
been found using other US methods that measure craniocaudal movement of the
diaphragm or the portal vein [18]. Movement is correlated to sex and weight [16]. Normal
values for men and women have been proposed as 1.0 and 0.9 cm during quiet breathing,
1.8 and 1.6 cm during a sniff manoeuvre, and 4.7 and 3.6 cm during deep breathing [12].
Another study reported similar findings [32].
When comparing DUS with chest radiography, US can detect poor diaphragm movement
even with a normal radiographic diaphragm position, and, conversely, the finding of an
elevated hemidiaphragm does not always correspond to decreased movement at US
examination [33].
DUS can therefore be seen to provide rapid and reproducible information about diaphragm
function that cannot be obtained as easily and safely by other diagnostic modalities.
Despite the lack of consensus-based standardised methodology, it seems likely that DUS is
set to become the primary tool for evaluation of diaphragm function.
Assuming that mechanical ventilation has an unloading effect on respiratory muscles that
leads to diaphragm atrophy and dysfunction, GROSU et al. [40] measured muscle thickness
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in seven intubated patients from the first day of intubation until extubation, tracheostomy
or death. They found a daily average of 6% decrease in diaphragm thickness and that
thinning of the diaphragm occurred within 48 h of intubation.
SCHEPENS et al. [41] studied right hemidiaphragm thickness in 53 patients ventilated for at
least 72 h. The mean baseline value was 1.9 cm; compared with baseline, diaphragm
thickness decreased >10% in 77% of the patients studied, remained stable in 19% and
increased in 4%. The daily rate of thickness reduction was 10.9%. The main variable
associated with diaphragm thinning was length of ventilation, while disease severity
(assessed by the Simplified Acute Physiology Score II), steroid use, muscle relaxants or
sepsis on admission were not associated with a decrease in thickness.
In a small study of eight patients receiving either pressure support ventilation (PSV) or
assist-control ventilation (ACV), a decline in diaphragm thickness was observed only in
patients receiving ACV, while subjects receiving PSV showed an increase in thickness [42].
Similarly, EL-MORSY et al. [43] studied diaphragm thickness in 67 mechanically ventilated
patients, stratified by ventilatory modalities (CMV, ACV and spontaneous ventilation).
CMV and ACV were associated with significantly higher rates of diaphragmatic atrophy
than spontaneous modes. A daily decrease in thickness was observed in patients treated
with CMV and ACV, while in spontaneous modalities a daily increase in thickness was
observed [43].
ZAMBON et al. [44] measured daily atrophy rates in critically ill mechanically ventilated
patients, categorising the subjects into four classes: 1) spontaneous breathing or continuous
positive airway pressure, 2) PSV of 5–12 cmH2O (low PSV), 3) PSV of >12 cmH2O (high
PSV) and 4) CMV. The authors reported, for the first time, that the degree of diaphragm
atrophy was associated with different ventilation settings and observed a linear relationship
between ventilation support and Dtf.
GOLIGHER et al. [45] described the evolution of diaphragm thickness over time in patients
during mechanical ventilation. A total of 128 mechanically ventilated patients and 10
control patients were enrolled. Thickness and Dtf were measured daily. Diaphragm
thickness remained unchanged in 47 subjects (44%), decreased by >10% in 47 subjects
(44%) and increased by >10% in 13 subjects (12%). Changes in thickness occurred early.
Thickness was stable over time in nonventilated control subjects and in patients following
extubation [45].
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mechanical ventilation, while subjects with lower or higher values of Dtf had a longer
duration of mechanical ventilation and a higher risk of ventilation [46].
In conclusion, the findings of these studies suggest that changes in diaphragm thickness are
common in mechanically ventilated patients, occur early and may be modulated by the
intensity of respiratory muscle work performed by the patient [45]. The degree of atrophy
may be associated with the duration of mechanical ventilation and not with other risk
factors for muscle atrophy, such as sepsis.
The role of DUS in predicting weaning success has been investigated by studies measuring
either excursion [39, 49, 50] or thickness and Dtf [50–52]. Both diaphragm excursion and
Dtf measurements performed during a spontaneous breathing trial (SBT) in intubated/
tracheotomised patients have shown utility in predicting weaning success.
KIM et al. [39] evaluated diaphragm dysfunction in 82 patients during a SBT by assessing
vertical excursion or paradoxical movements of the diaphragm. A cut-off value of 1.0 cm
was found, and patients with diaphragm dysfunction according to this criterion had longer
weaning times and a higher frequency of re-intubation [39].
In a recent study, FARGHALY and HASAN [50] observed that a threshold value of
diaphragmatic excursion of ⩾10.5 mm was associated with successful extubation with a
sensitivity and specificity of 87% and 71%, respectively.
Another recent study by SPADARO et al. [53] compared the role of a new index, the
diaphragmatic-RSBI (D-RSBI), as opposed to RSBI, to predict weaning failure. Diaphragm
displacement and D-RSBI performed better than traditional RSBI at predicting weaning
outcome, and D-RSBI had the best diagnostic accuracy with a cut-off value of >1.3 breaths
min−1 mm−1, giving a sensitivity of 94%, specificity of 65%, PPV of 57% and NPV of 96%.
Excursion as a weaning index should be assessed only during a SBT and not in patients
receiving mechanical ventilation (which would give a false assessment of contractile
activity). Moreover, variables such as abdominal or thoracic compliance, tidal volume, rib
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cage or abdominal muscle activity, and the presence of ascites may affect diaphragm
motion and excursion assessment.
Several studies have evaluated the role of Dtf in predicting extubation success. DININO et al.
[51] studied 63 patients weaned either by a SBT (27 patients) or a pressure support trial
(36 patients). A Dtf cut-off value of 30% was associated with a PPV of 91% and NPV of
63% for successful extubation with a sensitivity and specificity of 88% and 71%,
respectively. FERRARI et al. [52] evaluated Dtf in 46 tracheotomised patients during a SBT. A
threshold Dtf of >36% was associated with a successful SBT with a sensitivity of 82%,
specificity of 88%, PPV of 92% and NPV of 75%. Moreover, a significant difference
between diaphragm thickness at TLC and residual volume was observed between patients
who succeeded and those who failed the SBT. Finally, FARGHALY and HASAN [50] assessed
Dtf percentage in 54 patients with a cut-of value of 34.2%, giving a sensitivity and
specificity of 90% and 64%, respectively. In these three studies, the assessment of Dtf
performed similarly to other weaning indexes, such as RBSI or MIP measurement.
Thus, according to these preliminary studies, the optimal threshold values for predicting
weaning success are 1 cm for diaphragm excursion and 30–36% for Dtf. DUS provides
important information for the weaning process. In particular, Dtf performs comparably to
other weaning indexes, such as RSBI or MIP. Further randomised controlled studies are
warranted to validate the role of DUS in the weaning process.
DUS has been studied as a proxy of respiratory effort and work of breathing in healthy
volunteers [17, 55] and in people suffering from neuromuscular diseases [56, 57]. DUS
offers many advantages over other measures, being a noninvasive, repeatable bedside
technique allowing direct visualisation of the diaphragm and discrimination of the
dysfunctional side. Few studies have compared DUS with other methods in mechanically
ventilated patients in terms of either movement of one hemidiaphragm or thickness change
[31, 58–60].
LEROLLE et al. [59] compared the best diaphragmatic excursion on maximal inspiratory
effort from FRC with both PTD and the derived Gilbert index (GI). GI evaluates the
contribution of the diaphragm to respiratory pressure swing during quiet tidal breathing: a
GI value of >0.30 is normal, while a GI value of ⩽0 indicates severe diaphragmatic
dysfunction [61]. The authors evaluated a cohort of 28 post-cardiac surgery patients
requiring prolonged invasive mechanical ventilation, who were then at risk of
diaphragmatic dysfunction [59]. All but one patient exhibited an abnormal PTD. The best
diaphragmatic excursion and GI value correlated significantly (Spearman’s ρ=0.64;
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p=0.001), with lower values of excursion among those with severe muscle dysfunction (GI
>0 versus GI ⩽0, 30 versus 19 mm; p=0.007). Discrimination capability (assessed with a
receiver operating characteristic curve) for the best diaphragmatic excursion with respect to
a severe impairment (GI ⩽0) was 93%, with an optimal cut-off point of 25 mm, showing a
sensitivity and specificity of 100% and 85%, respectively. When applied to a different
cohort of patients with an uncomplicated post-operative course, none of them showed a
best diaphragmatic excursion of <25 mm.
More recently, GOLIGHER et al. [31] evaluated 66 patients receiving mechanical ventilation
and nine healthy volunteers. Overall diaphragmatic function, estimated by Dtf, was
considerably lower among the former than among the latter (p<0.0001), and was almost
negligible in the subgroup undergoing neuromuscular blockage [31].
In 2011, UMBRELLO et al. [60] recruited 25 intubated patients after a major elective surgical
intervention, who were deemed suitable for a weaning trial. Sedation and muscular
blockage were withheld and PSV commenced. Dtf and the best excursion of the right
hemidiaphragm, PTPdi and the respective oesophageal pressure–time product (PTPoes) for
the Poes were collected. Unsurprisingly, they found that increasing levels of support were
significantly associated with decreasing patient respiratory drive (P0.1) and effort. As in the
study by VIVIER et al. [58], Dtf was significantly lower for rising levels of pressure support,
being highest when breathing spontaneously (52.7% versus 13.0%; p<0.001). Dtf was
significantly correlated with PTPoes (Pearson’s r=0.801; p<0.001) and PTPdi (Pearson’s
r=0.701; p<0.001). In the same way, Dtf was positively and strongly associated with P0.1,
PTPoes and PTPdi in a linear mixed model of regression analysis ( p<0.001 for all). No
correlation was found for the best diaphragmatic excursion and other measures.
To conclude, a few studies have investigated the role of DUS as an index of respiratory effort
among critically ill patients. Some evidence supports the use of Dtf (rather than peak excursion)
when compared with other measures of the work of breathing. Further studies should
overcome the limit of small and highly selected cohorts, elucidate the differences between
invasive and noninvasive ventilation (NIV), and narrow the wide variability of the data.
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Proposed M-mode reference ranges, from a large study of normal patients [12], are
provided in table 2. It is apparent from these data that assessment of the right
hemidiaphragm is more frequently possible than the left. The fifth percentile provided is of
most use in defining a lower limit of normal: 1.0 cm (women) and 1.1 cm (men) during
Figure 5. B-mode (two-dimensional; left) and M-mode (right) analysis of a normally moving right
hemidiaphragm.
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Figure 6. B-mode (two-dimensional; left) and M-mode (right) analysis of a poorly moving left
hemidiaphragm in association with pleural fluid and thickening, in the same patient as in figure 5.
quiet respiration, 1.6 cm (women) and 1.8 cm (men) during sniffing, and 3.6 cm (women)
and 4.7 cm (men) during deep respiration.
Diaphragm thickening
Various studies have proposed criteria for diaphragm paralysis based on thickness at FRC
(tdiFRC). GOTTESMAN and MCCOOL [64] carried out a study of 30 subjects and suggested
that diaphragmatic paralysis occurs when tdiFRC is <2 mm, while BOON et al. [24], in a
study of 150 subjects, taking the 5th percentile as the lower limit of normal, suggested that
Data are presented as 5th to 95th percentile values. Reproduced and modified from [12] with
permission.
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Despite these proposed criteria for paralysis, absolute values of tdiFRC are affected by a
number of variables including sex, body weight, height and nutritional status [65, 66], and
therefore it has been suggested that measurement of Dtf is more reliable.
A Dtf value of <0.2 (representing a <20% increase in diaphragmatic thickness from FRC to
TLC) suggests diaphragmatic paralysis [24, 64]. In a study of 131 hemidiaphragms, the
combined criteria of Dtf of <0.2 and tdiFRC of >1.4 mm were associated with a sensitivity of
93% and specificity of 100% for diagnosis of neuromuscular diaphragmatic paralysis [7].
Anomalies/controversies
Despite the evidence presented above advocating both excursion and thickening for
assessment of paralysis, it should be noted that there is only a weak correlation between
such measurements [20]. Correlation between diaphragmatic excursion and lung volumes
has been suggested in several studies [11, 12, 17] but not confirmed in others [22].
Therefore, there remains uncertainty as to the optimal sonographic method for assessment
of paralysis.
These two studies are small and somewhat underpowered but do suggest that an initial
US-based triage might supplement standard clinical evaluation of patients with acute
dyspnoea, particularly those having an acute exacerbation of COPD. DUS may predict the
prognosis and risk of failure of NIV, but larger studies are required to clarify a role.
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Primary malignant pleural disease, such as pleural mesothelioma, and metastatic pleural
malignancy cause (often nodular) pleural thickening. Such nodularity frequently affects the
parietal pleura but can be hard to discern using CT and US. Given the predilection of
malignant pleural disease for a posteroinferior location, these sites of malignancy frequently
affect the diaphragm, and careful evaluation of the diaphragm by US may therefore
increase the sensitivity of malignancy detection [8]. In addition to assessing diaphragm
nodularity, thickening and disruption of the usual three to five smooth alternating
hypoechoic (muscular) and hyperechoic (fibroadipose septae) layers are reported in
malignancy.
US criteria for pleural malignancy involving the diaphragm compare favourably with classic
CT criteria: diaphragmatic thickening of >7 mm, failure to resolve the layers of the
diaphragm and the presence of diaphragmatic nodules each have a high specificity (95%,
95% and 100%, respectively) but a low sensitivity (42%, 30% and 30%, respectively) for
cancer. However, the sensitivity rises to 79% (specificity 100%) when combining these
features with three further US features of pleural malignancy. Such test characteristics
compare favourably with CT criteria of malignancy (sensitivity 72%, specificity 83%) [8].
Mimics of malignancy do exist, and care should be taken to ensure that apparent nodules
do not represent anatomical variations, including diaphragmatic herniae, eventration or
slips (a fold of muscle protruding from the diaphragm) [2, 3]. Figure 7 demonstrates
diaphragmatic nodularity associated with malignancy and a large echogenic pleural effusion
causing diaphragm flattening.
In addition to helping predict malignancy, DUS adds to the safety of pleural procedures
such as thoracentesis and thoracoscopy. Knowledge of diaphragmatic position using TUS is
particularly useful in minimising potential harm from injudiciously selected pleural
puncture sites, particularly given that some constricting malignant pleural diseases may
cause substantial hemidiaphragm elevation such that nonguided pleural puncture may
actually be subdiaphragmatic [71].
Figure 7. Large echogenic effusion, diaphragm flattening and malignant diaphragmatic nodularity.
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Pleural effusions are a common cause of dyspnoea but cause relatively small alterations in
lung volumes, despite significant symptoms. Studies, including those using US, have
revealed that this substantial dyspnoea is caused by alterations in diaphragmatic mechanics
caused by pleural fluid.
Experimental studies have demonstrated that artificial instillation of fluid into the pleural
cavities of anaesthetised dogs only reduces FRC by one-third of the volume instilled.
Two-thirds of the volume was accommodated by an increase in the thoracic cage size,
mostly secondary to hemidiaphragm flattening [72, 73]. Caudal displacement of
the diaphragm causes it to operate at a disadvantageous point in its length–tension curve
[72, 74]. A shortened diaphragm has a reduction in capacity to develop tension and PTD,
requiring higher neural activation [75–77]. This state of “neuromechanical uncoupling”,
whereby a given neural drive does not produce the expected ventilatory output, creates
significant breathlessness.
Larger effusions, often caused by malignancy, may cause diaphragmatic inversion (figure 8)
[9, 78]. Such positional changes of the diaphragm in its relaxed position may,
paradoxically, cause upward (rather than downward) displacement during contraction,
readily seen using DUS. This paradoxical motion mimics diaphragm paralysis (so-called
“pseudoparalysis”). Differentiation from genuine paralysis is possible by noting a large
effusion, lack of diaphragmatic elevation and because contraction of the muscular parts of
the diaphragm is still evident.
Patients with paradoxical diaphragmatic movements are more breathless than those
without, and are more likely to improve in their breathlessness after thoracentesis [9]. DUS
may therefore have a role in predicting the response to thoracentesis and can also ensure
that sufficient fluid is removed to correct an inverted diaphragm to ensure that
symptomatic benefits are realised. Despite the improvement in diaphragmatic
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A recent study by UMBRELLO et al. [80] investigated the effect of unilateral pleural drainage
on diaphragmatic function. Pleural drainage was associated with a significant increase in
diaphragmatic displacement and in Dtf. Moreover, a significant correlation between the
volume of the fluid removed and the increase in diaphragm thickening was observed [80].
Conclusion
This chapter has highlighted the diverse applications of DUS in functional and structural
assessment of the diaphragm in many settings within the hospital. While studies suggest
significant agreement with other diagnostic modalities and good inter- and intra-observer
agreement with DUS, further investigation is required to clarify patient end-points
associated with DUS use.
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27. Cohn D, Benditt JO, Eveloff S, et al. Diaphragm thickening during inspiration. J Appl Physiol 1997; 83: 291–296.
28. Carrillo-Esper R, Perez-Calatayud AA, Arch-Tirado E, et al. Standardization of sonographic diaphragm thickness
evaluations in healthy volunteers. Respir Care 2016; 61: 920–924.
29. Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects.
Thorax 1995; 50: 1157–1161.
30. Baldwin CE, Paratz JD, Bersten AD. Diaphragm and peripheral muscle thickness on ultrasound: intra-rater reliability
and variability of a methodology using non-standard recumbent positions. Respirology 2011; 16: 1136–1143.
31. Goligher EC, Laghi F, Detsky ME, et al. Measuring diaphragm thickness with ultrasound in mechanically
ventilated patients: feasibility, reproducibility and validity. Intensive Care Med 2015; 41: 642–649.
32. Gerscovich EO, Cronan M, McGahan JP, et al. Ultrasonographic evaluation of diaphragmatic motion. J Ultrasound
Med 2001; 20: 597–604.
33. Fedullo A, Lerner RM, Gibson J, et al. Sonographic measurement of diaphragmatic motion after coronary artery
bypass surgery. Chest 1992; 102: 1683–1686.
34. Jubran A. Critical illness and mechanical ventilation: effects on the diaphragm. Respir Care 2006; 51: 1054–1061.
35. Powers SK, Kavazis AN, Levine S. Prolonged mechanical ventilation alters diaphragmatic structure and function.
Crit Care Med 2009; 37: S347–S353.
36. Esteban A, Frutos F, Tobin MJ, et al. A comparison of four methods of weaning patients from mechanical
ventilation. N Engl J Med 1995; 332: 345–350.
37. Capdevila X, Lopez S, Bernard N, et al. Experimental effects of controlled mechanical ventilation on respiratory
muscle contractile properties in rabbits. Intensive Care Med 2003; 29: 103–110.
38. Anzueto A, Peters JI, Tobin MJ, et al. Effects of prolonged controlled mechanical ventilation on diaphragmatic
function in healthy adult baboons. Crit Care Med 1997; 25: 1187–1190.
39. Kim WY, Suh HJ, Hong SB, et al. Diaphragm dysfunction assessed by ultrasonography: influence on weaning from
mechanical ventilation. Crit Care Med 2011; 39: 2627–2630.
40. Grosu HB, Lee YI, Lee J, et al. Diaphragm muscle thinning in patients who are mechanically ventilated. Chest
2012; 142: 1455–1460.
41. Schepens T, Verbrugghe W, Dams K, et al. The course of diaphragm atrophy in ventilated patients assessed with
ultrasound: a longitudinal cohort study. Crit Care 2015; 19: 422.
42. Francis CA, Andres HJ, Reynolds S. Ultrasonographic evaluation of diaphragm thickness during mechanical
ventilation in intensive care patients. Am J Crit Care 2016; 25: e1–e8.
43. El Morsy AA, Ibrahim MR, Sakr MMA. Serial ultrasonographic evaluation of diaphragm thickness during
mechanical ventilation in ICU patients. Biolife 2015; 3: 922–936.
44. Zambon M, Beccaria P, Matsuno J, et al. Mechanical ventilation and diaphragmatic atrophy in critically ill patients.
Crit Care Med 2016; 44: 1347–1352.
45. Goligher EC, Fan E, Herridge MS, et al. Evolution of diaphragm thickness during mechanical ventilation: impact
of inspiratory effort. Am J Respir Crit Care Med 2015; 192: 1080–1088.
46. Goligher EC, Dres M, Fan E. Mechanical ventilation-induced diaphragm atrophy strongly impacts clinical
outcomes. Am J Respir Crit Care Med 2017; in press [DOI: https://doi.org/10.1164/rccm.201703-0536OC].
47. Vassilakopoulos T, Petrof BJ. Ventilator-induced diaphragmatic dysfunction. Am J Respir Crit Care Med 2004; 169:
336–341.
48. Doorduin J, van Hees HWH, van der Hoeven JG, et al. Monitoring of the respiratory muscles in the critically ill.
Am J Respir Crit Care Med 2013; 187: 20–27.
49. Jiang J, Tsai T, Jerng J. Ultrasonographic evaluation of liver/spleen movements and extubation outcome. Chest
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50. Farghaly S, Hasan AA. Diaphragm ultrasound as a new method to predict extubation outcome in mechanically
ventilated patients. Aust Crit Care 2017; 30: 37–43.
51. DiNino E, Gartman EJ, Sethi JM, et al. Diaphragm ultrasound as a predictor of successful extubation from
mechanical ventilation. Thorax 2014; 69: 431–435.
52. Ferrari G, De Filippi G, Elia F, et al. Diaphragm ultrasound as a new index of discontinuation from mechanical
ventilation. Crit Ultrasound J 2014; 6: 8.
53. Spadaro S, Grasso S, Mauri T, et al. Can diaphragmatic ultrasonography performed during the T-tube trial predict
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54. Bellani G, Pesenti A. Assessing effort and work of breathing. Curr Opin Crit Care 2014; 20: 352–358.
55. Wait J, Nahormek P, Yost W, et al. Diaphragmatic thickness–lung volume relationship in vivo. J Appl Physiol 1985;
67: 1560–1568.
56. Noda Y, Sekiguchi K, Kohara N, et al. Ultrasonographic diaphragm thickness correlates with compound muscle
action potential amplitude and forced vital capacity. Muscle Nerve 2016; 53: 522–527.
57. Pinto S, Alves P, Pimentel B, et al. Ultrasound for assessment of diaphragm in ALS. Clin Neurophysiol 2016; 127:
892–897.
58. Vivier E, Mekontso-Dessap A, Dimassi S, et al. Diaphragm ultrasonography to estimate the work of breathing
during non-invasive ventilation. Intensive Care Med 2012; 38: 796–803.
59. Lerolle N, Guerot E, Dimassi S, et al. Ultrasonographic diagnostic criterion for severe diaphragmatic dysfunction
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60. Umbrello M, Formenti P, Longhi D, et al. Diaphragm ultrasound as indicator of respiratory effort in critically ill
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62. Alexander C. Diaphragm movements and the diagnosis of diaphragmatic paralysis. Clin Radiol 1966; 17: 79–83.
63. Houston JG, Morris AD, Howie CA, et al. Technical report: quantitative assessment of diaphragmatic movement –
a reproducible method using ultrasound. Clin Radiol 1992; 46: 405–407.
64. Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med 1997;
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Respir Crit Care Med 1997; 155: 1323–1328.
66. Arora NS, Rochester DF. COPD and human diaphragm muscle dimensions. Chest 1987; 91: 719–724.
67. Fantini R, Mandrioli J, Zona S, et al. Ultrasound assessment of diaphragmatic function in patients with
amyotrophic lateral sclerosis. Respirology 2016; 21: 932–938.
68. Carrié C, Bonnardel E, Vally R, et al. Vital capacity impairment due to neuromuscular disease and its correlation
with diaphragmatic ultrasound: a preliminary study. Ultrasound Med Biol 2016; 42: 143–149.
69. Bobbia X, Clement A, Claret PG, et al. Diaphragmatic excursion measurement in emergency patients with acute
dyspnea: toward a new diagnostic tool? Am J Emerg Med 2016; 34: 1653–1657.
70. Antenora F, Fantini R, Iattoni A, et al. Prevalence and outcomes of diaphragmatic dysfunction assessed by
ultrasound technology during acute exacerbation of COPD: a pilot study. Respirology 2017; 22: 338–344.
71. Diacon AH, Brutsche MH, Solèr M. Accuracy of pleural puncture sites: a prospective comparison of clinical
examination with ultrasound. Chest 2003; 123: 436–441.
72. De Troyer A, Leduc D, Cappello M, et al. Mechanics of the canine diaphragm in pleural effusion. J Appl Physiol
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76. Finucane KE. Efficiency of the normal human diaphragm with hyperinflation. J Appl Physiol 2005; 99: 1402–1411.
77. De Troyer A. Effect of hyperinflation on the diaphragm. Eur Respir J 1997; 10: 708–713.
78. Wang JS, Tseng CH. Changes in pulmonary mechanics and gas exchange after thoracentesis on patients with
inversion of a hemidiaphragm secondary to large pleural effusion. Chest 1995; 107: 1610–1614.
79. Michaelides SA, Bablekos GD, Analitis A, et al. Temporal evolution of thoracocentesis-induced changes in
spirometry and respiratory muscle pressures. Postgrad Med J 2017; 93: 460–464.
80. Umbrello M, Mistraletti G, Galimberti A, et al. Drainage of pleural effusion improves diaphragmatic function in
mechanically ventilated patients. Crit Care Resusc 2017; 19: 64–70.
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| Chapter 11
The upper abdomen
Stefan Posth1 and Ole Graumann2,3,4
When carrying out an US scan of the thorax, the examiner will also detect structures in the
upper abdomen. Incidental abdominal pathologies may be detected with varying frequency
during TUS. In this chapter, we provide an overview of the most common pathologies.
Clinicians should be aware of the technical challenges when interpreting abnormal US
patterns. Examiners who normally only examine the thorax may not be familiar with the
abdominal organs. It is therefore essential that a specialist opinion is requested when a
possible pathology is detected.
Cite as: Posth S, Graumann O. The upper abdomen. In: Laursen CB, Rahman NM, Volpicelli G, eds.
Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 148–160 [https://
doi.org/10.1183/2312508X.10007417].
W hen performing US of the lungs, anatomical structures in the upper abdomen will
inevitably also be visualised.
Although the focus of this Monograph is US pathologies in the thorax, it is important for
the examiner to be familiar with the most common pathological findings in the upper
abdomen. It is not the purpose of this chapter to go through all possible pathologies but
rather to draw attention to pathologies that require transferral to another specialist, for
example a radiologist, for further examination. We will review pathologies in the right
upper abdominal quadrant, the epigastrium and the left upper abdominal quadrant.
A number of studies have considered the question of which pathologies would be expected
in an unselected group of patients, many of whom do not present with obvious abdominal
problems. Table 1 summarises the pathological findings of these studies.
When performing US of the thorax, organs in the upper abdomen will also be visualised.
Table 2 offers an overview of abdominal organs that can be seen while scanning sections of
the thorax. This is discussed further in another chapter in this Monograph [8]. If incidental
1
Dept of Emergency Medicine, Odense University Hospital, Odense, Denmark. 2Dept of Radiology, Odense University Hospital, Odense,
Denmark. 3Dept of Clinical Medicine, Odense University, Odense, Denmark. 4Dept of Clinical Medicine, Aarhus University, Aarhus,
Denmark.
Correspondence: Stefan Posth, Kløvervænget 25, 5000 Odense C, Denmark. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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The PubMed search keywords used to search for studies were: abdominal US, incidental findings, incidence, frequency of abnormalities.
149
ERS MONOGRAPH | THORACIC ULTRASOUND
R2 Liver, gallbladder, bile ducts, inferior vena cava, abdominal aorta, pancreas
R3 Liver, gallbladder, bile ducts, kidney
R5 Liver, bile ducts, kidney
L2 Inferior vena cava, abdominal aorta, pancreas, bile ducts, stomach
L3 Spleen, kidney, stomach
L5 Spleen, kidney
relevant or undefinable pathology is detected in the upper abdomen, the patient should be
referred to a specialist, such as a radiologist or gastroenterologist.
The US anatomy of the right upper abdominal quadrant of a healthy subject is shown in
figure 1a and b. Pathologies in this section can occur in the liver, gallbladder, bile ducts or
right kidney.
Liver pathologies
The most common liver pathologies are steatosis, cysts and focal lesions [9].
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a) b)
Liver
Liver Gallbladder
na
Kidney m
lu
Co
Di
ap
hr
ag
c) d)
Stomach Stomach
Pancreas
Vertebra
Vertebra
e) f)
Liver
Liver
Inf
er
ior
ve
nac Right
av atrium
Aorta a
Liver
Columna
g) h)
Spleen
Spleen
Kidney Diaphragm
Figure 1. a and b) Normal anatomy of the right upper abdominal quadrant; c–f ) normal anatomy of the
epigastrium; g and h) normal anatomy of the left upper abdominal quadrant.
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ERS MONOGRAPH | THORACIC ULTRASOUND
a) b)
Ascites
Liver
Liver
Kidney
c)
Ascites
r
Liver de
lad
llb
Ga
Hepatocellular adenoma
A hepatocellular adenoma is usually isoechogenic with the surrounding liver tissue.
Therefore, it can be very difficult to differentiate an adenoma from the surrounding liver
tissue. In a fatty liver, adenomas may be poorly echogenic.
Liver metastases
Liver metastases have a wide variety of B-mode appearances, from isoechogenic with the
surrounding liver tissue, and therefore impossible to detect, to hyperechoic or hypoechoic
(figure 3e–g). They may be confused with any kind of liver lesion.
The most frequent pathology of the bile ducts is cholestasis [10]. The major sonographic
feature of cholestasis, which can be caused by multiple diseases, is dilation of the intra- and
extrahepatic biliary ducts (figure 4a and b). In intrahepatic cholestasis, two anechoic tubes
are seen side by side, or the dilated bile ducts and adjacent portal vein branch are seen as
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a) b)
Liver
Cyst
Kidney
Calcification
Liver
c) d)
*
*
Liver
Liver
e) f)
*
*
Metastasis
* *
ey
dn
*
Ki
Metastasis
g)
* *
* *
* *
*
*
*
*
* *
*
Figure 3. a) Liver cyst; b) liver calcification; c) hepatic haemangioma (*); d) focal nodular hyperplasia (*);
e and f) hypoechoic liver metastasis (*); g) hyperechoic liver metastasis and cholestasis (*).
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ERS MONOGRAPH | THORACIC ULTRASOUND
a) b)
Liver
Liver
c) d)
r
dde
Liver la
Gallbladder llb
Ga ge
Stones ud
Sl
Liver
e) f)
er
Liver
add Gallbladder
l l bl Liver
*
Ga
Figure 4. a) Intrahepatic cholestasis; b) intra- and extrahepatic cholestasis (crosses and dotted line indicate
measurement of the common bile duct); c) cholecystolithiasis; d) biliary sludge; e) cholecystitis;
f) gallbladder polyp (*).
two adjacent anechoic circles. This phenomenon, which is also called “double tracking” or
“multiple tubes”, can occur in part of the liver or, if the cause of cholestasis is extrahepatic,
in the whole liver.
Extrahepatic obstruction is diagnosed by measuring the common bile duct, running parallel
to the portal vein, as >6 mm in diameter (figure 4b).
Gallbladder pathologies
The most common pathologies of the gall bladder are cholecystolithiasis, cholecystitis and
polyps (figure 4c, e and f ) [11]. The healthy gallbladder sometimes cannot be visualised by
US if the patient just has eaten. When filled with bile, it appears anechoic.
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Cholecystolithiasis
The classic US appearance of a gallbladder stone is a hyperechoic/echogenic structure
located within the gallbladder lumen with posterior acoustic shadowing (figure 4c). Stones
typically lie on the dependent wall of the gallbladder under the influence of gravity, and are
mobile. Occasionally, stones become impacted in the gallbladder infundibulum, which
creates a hydrops.
Cholecystitis
The sonographic appearance of cholecystitis is an enlarged gallbladder with a thickened,
multiple layered wall (figure 4e). The layering is caused by oedema, haemorrhage, ulcers
and pus, and the wall is usually >3 mm in diameter. There is often oedema around the
gallbladder.
During examination, most patients will feel pain when the gallbladder is visualised. This is
called a positive US Murphy’s sign. Thickening of the gallbladder wall can be seen in a
variety of medical conditions. Therefore, cholecystitis is a clinical diagnosis that should be
supplemented with US and blood samples.
Gallbladder polyps
Gallbladder polyps are usually hyper- or isoechoic in comparison with the gallbladder wall
(figure 4f ).
Kidney pathologies
Healthy kidneys measure approximately 6×9×12 cm, depending on the size of the patient.
The renal cortex appears hyperechoic, often slightly darker than the liver or spleen. The
renal pelvis appears hyperechoic in comparison with the cortex and is located centrally in
the kidney. The most common pathologies of the kidneys are cysts, stones and
hydronephrosis [12].
Nephrolithiasis
Kidney stones can have many different compositions and therefore vary in appearance. The
US appearance of kidney stones can, independent of size, vary from not being seen to
hyperechoic foci in the pelvis, often with acoustic shadowing (figure 5d). Small kidney
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ERS MONOGRAPH | THORACIC ULTRASOUND
a) b)
Cyst
Cyst Kidney
Kidney
c) d)
Kidney
Kidney
e) f)
Kidney
Kidney
phrosis
Hydronephrosis
Hydrone
g)
Kidney
is
os
hr
ep
on
dr
Hy
Figure 5. a and b) Renal cyst; c) multiple renal cysts; d) multiple kidney stones; e) hydronephrosis stage 1;
f) hydronephrosis stage 2; g) hydronephrosis stage 4.
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stones (<3 mm) are rarely seen on plain B-mode US. They can vary greatly in number and
size. Pelvis fatty tissue can imitate kidney stones.
Hydronephrosis
Normally, the renal pelvis is more hyperechoic than the cortex due to fatty tissue. The
calyx system is fluid filled and therefore hypoechoic. With hydronephrosis present, the
pelvis appears dilated and anechoic, often with characteristic “Mickey Mouse ears” as the
calyx minor and major enlarge.
Frequent liver and bile duct pathologies are described in the previous section.
The most common pathologies of the IVC are signs of hypo- or hypervolaemia [13]. The
diameter of the IVC can be examined 2 cm from the diaphragm where it enters the right
atrium. The largest diameter and the degree of collapse during respiration should be
measured.
In patients with hypovolaemia, the diameter of the IVC is often decreased to <15 mm, and
the vein collapses by >50% during respiration (figure 6a). In patients with hypervolaemia,
the diameter is often enlarged to >25 mm, and no or minimal collapse can be seen during
inspiration (figure 6b and c).
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ERS MONOGRAPH | THORACIC ULTRASOUND
a) b)
V
Liver
Liver
Inf
eri
or Right atrium
ven
ac
ava Right atrium
Inferior vena cava
c) d)
Live
r ve
in
Liver
e) f)
Aorta Aorta
Thrombus
Pancreas pathologies
The most frequent pathologies of the pancreas are pseudocysts [14]. It is often difficult to
visualise the pancreas, especially when the patient is not fasting. When pseudocysts are
present, they are often easier to detect than the organ itself.
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a) b)
Ascites
Retention
Liver
c)
Ascites
Spleen
Stomach pathologies
The most common stomach pathology that can be detected by US is retention [15]. In
upper gastrointestinal obstruction, of whatever origin, the stomach appears dilated, with
ingested food and fluid–fluid levels. Stomach retention can imitate the appearance of a
large tumour, located in the epigastrium or below the left diaphragm (figure 7a).
The US anatomy of the left upper abdominal quadrant of a healthy subject is shown in figure
1g and h. Pathologies in this section may be located in the spleen, left kidney or stomach.
Spleen pathologies
Ascites
Ascites can be detected in all of the areas described in previous sections [17]. Ascites
is often found adjacent to the diaphragm or the anterior margin of the liver. It often
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ERS MONOGRAPH | THORACIC ULTRASOUND
occurs between the liver and right kidney, or between the spleen and left kidney (figure 7b
and c). Sometimes, smaller amounts of ascites can be found between the diaphragm and
liver or spleen.
Free abdominal fluid may appear anechoic but can also contain floating debris and show
signs of septation. The gallbladder wall is often thickened when ascites is present.
References
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| Chapter 12
The mediastinum
Felix J.F. Herth
The number of patients suffering from lung diseases is increasing worldwide. Lung cancer,
for example, is now one of the most common cancers. Many of these diseases having
mediastinal lymph node involvement. Accurate diagnosis or possible staging of the
mediastinum is important not only to determine the prognosis but to decide the most
suitable treatment plan. CT, MRI, PET and PET-CT are used for noninvasive imaging of the
mediastinum. If a cytological or histological conformation is required, EBUS-TBNA is the
preferred test. This chapter will focus on technique, procedures and limitations.
Cite as: Herth FJF. The mediastinum. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound
(ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 161–171 [https://doi.org/10.1183/
2312508X.10007017].
T he need to access the mediastinum has increased over the last two decades. Almost
100 years ago, lung cancer was a rare disease. Over time, diagnosis has increased and
lung cancer is now the leading cause of cancer death worldwide [1, 2]. To treat the disease,
proper staging is required and lymph node staging of the mediastinum is particularly
important. Adequate lung cancer staging will also improve: research into the disease;
accurate data comparison; and quality control. Mediastinal lymph node staging can be
performed with radiological imaging, endoscopically or surgically [3]. CT scans, MRI [4],
PET and PET-CT are useful noninvasive imaging techniques for staging lung cancer;
however, they are neither sufficiently sensitive nor specific for the determination of
mediastinal lymph node involvement [5].
In 1959, CARLENS [6] published his first report about mediastinoscopy. Following the report,
the technique became and remained the gold standard for the mediastinum for several years.
The surgical option remained undiscussed, even after the implementation of improved
imaging techniques, such as CT and PET. Not all lymph node stations were accessible with
this invasive procedure (only 2, 4 and anterior 7); access to the posterior and inferior
mediastinum was limited and required extended cervical mediastinoscopy or thoracoscopy.
This invasive procedure also required general anaesthesia and clinical admission [7].
Dept of Pneumology and Critical Care Medicine, Thoraxklinik University of Heidelberg, Heidelberg, Germany.
Correspondence: Felix J.F. Herth, Dept of Pneumology and Critical Care Medicine, Thoraxklinik University of Heidelberg, Röntgenstr. 1,
D-69126 Heidelberg, Germany. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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Nowadays, EBUS is routinely used and allows visualisation and sampling of mediastinal
lymph nodes or masses adjacent to the tracheobronchial system. It is used in the diagnosis
of benign diseases (such as sarcoidosis and tuberculosis) and in the inflammatory processes
of malignant diseases. Initially used for diagnosing and staging lung cancer, the technology
is now the preferred technique in the diagnosis of mediastinal diseases [9].
Equipment
Currently, several companies offer EBUS equipment. The difference in scope size, and the
size of the working channels, is minimal. There have been no head-to-head trials and it
seems that all scopes can be used with comparable results.
Since 2009, Pentax has offered a quite similar EBUS scope (EBUSpro; Pentax, Tokyo,
Japan). The CCD chip of the EBUSpro is integrated directly into the endoscope’s distal
end, the scope is 6.3 mm wide and has a 2 mm instrument channel, and a slightly degreed
side-viewing optic. Later, Fujifilm launched their EBUS scope with a distal end outer
diameter of 6.7 mm (EB-530US; Fujifilm, Tokyo, Japan).
Depending on the scope used, US scanning is performed with frequencies of 5–12.5 MHz
and a tissue penetration of 20–50 mm. To see the parabronchial structure via US, the scope
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Figure 2. A lymph node in position 10 r (light grey). Directly below, the primary is visible (darker grey).
Regarding evidence, it must be stated that most of the literature published up to this point
was obtained using the Olympus scope.
TBNA is performed by direct contact of the transducer with the wall of the trachea or
bronchus [10]. When a lesion is visible with US (figure 2), a needle can be moved through
the working channel into the lymph nodes under real-time US visualisation (figure 3).
While the procedure is taking place, the time colour Doppler can be used to identify the
surrounding vascular structures (figure 4). After insertion of the needle into the lesion,
suction is applied with a syringe, and the needle is moved back and forth though the node.
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Figure 4. The vessel (in orange) within the lymph node in the Doppler mode.
Normally, physicians stab the target 10–15 times. Prior to retracting the needle into the
needle sheath, suction must be removed to minimise sample loss into the syringe.
After collection, there are several possible ways to handle the material. The most frequently
used method is air flushing the material on a glass slide or sending the material for
cell-block analysis [11]. The local handling should be discussed with the pathologist in
order to provide the tissue-reader with the material in his preferred way.
Several needle sizes are available ranging 19–25 gauge. Most of the published data have used
the 21 or 22 gauge needle [12–16]. Larger and smaller needles have benefits for different
special indications, but a real evidence regarding this question does not, as yet, exist.
Results
The success story of EBUS-TBNA began in 2003 in a Thorax article by KRASNIK et al. [12].
The article provided the first description of the principle of EBUS-TBNA. 3 years later, in
the same journal, HERTH et al. [13] presented their study of 502 patients showing that
EBUS-TBNA resulted in a 93% diagnostic yield, a sensitivity of 94%, a specificity of 100%
and an accuracy of 94%, with a positive predictive value (PPV) of 100% and a negative
predictive value (NPV) of 11%. A further interesting outcome of the study was that no
significant difference between US diagnosis under local and general anaesthesia was
identified. Since then, several studies have been published that show comparable data
relating to the staging and diagnosis of lung cancer with the help of EBUS-TBNA [13].
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In 2010, ANNEMA et al. [16] presented the results of ASTER (Assessment of Surgical Staging
versus Endosonographic Ultrasound in Lung Cancer: a Randomized Clinical Trial) in
JAMA. This large randomised controlled multicentre trial conducted between February
2007 and April 2009 enrolled 241 patients with resectable, suspected nonsmall cell lung
cancer. Where the need for mediastinal staging was indicated via CT or PET, patients were
randomised to either surgical staging or endosonography followed by surgical staging in
cases were no nodal metastases were found at endosonography. The group were able to
show that nodal metastases were found in 41 patients via surgical staging and 56 patients
via endosonography, with sensitivities of 79% versus 85%. Thoracotomy was unnecessary in
21 patients in the mediastinoscopy group versus nine in the endosonography group. The
complication rate was similar in both groups.
All of this data changed the gold standard for staging the mediastinum. In the lung cancer
guidelines of the American College of Chest Physicians (ACCP), EBUS-TBNA was for the
first time clearly recommended as the initial method for examining the mediastinum [5],
superseding classical mediastinoscopy. Several other international societies then followed
this recommendation [17, 18].
Beyond its use for staging and diagnosing lung cancer, Dr Yasufuku’s group are dedicated
to evaluating the benefits of EBUS-TBNA samples for immunohistochemical analysis and
have reported encouraging results with cell cycle-related proteins in chemotherapy patients
[19]. A year earlier, the same group presented a study that showed that epidermal growth
factor receptor mutation can be easily detected in metastatic lymph node samples using
EBUS-TBNA [20]. The group had also previously reported chemosensitivity-related
aberrant methylation profiling in samples obtained using EBUS-TBNA [21]. In short, the
group proved that samples obtained using EBUS-TBNA allowed genetic evaluation of
tumour cells from lymph nodes, e.g. in EML4-ALK testing [22]. Recently, the first studies
have been published that show that the material obtained with EBUS-TBNA can also be
used to confirm the PDL-1 situation of the patients [23, 24].
In 2007, WONG et al. [25] presented the first study that evaluated EBUS-TBNA use beyond
mediastinal staging. This large-scale case study included 65 patients. EBUS-TBNA was
shown to be a safe method that allowed a high diagnostic yield for sarcoidosis.
EBUS-TBNA was diagnostic in 85–91.8% of patients with a final diagnosis of sarcoidosis.
ANNEMA et al. [26] also conducted a prospective randomised trial that compared the use of
EBUS-TBNA with transbronchial biopsies in patients with suspected sarcoidosis. They
found a diagnostic yield for the detection of granulomas of 80% with EBUS-TBNA and
only 53% with transbronchial biopsies. As a result, EBUS-TBNA is now the recommended
technique in these patients and should be used instead of mediastinoscopy.
The use of EBUS-TBNA in suspected tuberculosis (TB) is less well established. However,
one multicentre case series describing 156 patients with a diagnosis of TB-associated
lymphadenopathy reported a sensitivity and accuracy of 94% [27].
Several studies have evaluated the usefulness of EBUS-TBNA in the diagnosis of lymphoma
[28, 29]. In a retrospective analysis that included 25 patients with mediastinal adenopathies
and suspected lymphomas [28], EBUS-TBNA enabled a sample of lymph tissue to be
obtained in 96% of the patients (24 out of 25). The sensitivity, specificity, PPV and NPV
observed were 90%, 100%, 100% and 92.6%, respectively. Larger specimens are often
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required to identify the exact subtype and grading when diagnosing lymphoma. A study by
STEINFORT et al. [29] evaluated EBUS-TBNA in lymphoma and found a diagnostic
sensitivity of 76%; however, some of these patients required further biopsy reducing the
sensitivity to 57%. EBUS-TBNA should not be considered the first diagnostic approach in
suspected lymphoma but can identify a proportion of patients with the disease. This may
change in the future with use of better and, in particular, larger needles.
If additional tissue specimens are required for histological analysis, it is possible to insert
1.15-mm mini-forceps through the EBUS scope and past the airway wall via a needle
puncture. This method allows the pulmonologist to obtain real-time guided forceps
biopsies of mediastinal lymph nodes [30]. EBUS-TBNA has also been used to successfully
obtain biopsy specimens in centrally located paratracheal and peribronchial tumours with a
diagnostic sensitivity of 82–94% [31, 32]. Furthermore, real-time guided EBUS-TBNA has
been used therapeutically to drain mediastinal, as well as bronchogenic cysts and
consequently relieve central airway obstruction [33, 34].
Complications
Reading the available literature and the reviews, it is undisputable that EBUS-TBNA is a
very safe procedure and that complications are very rare. In a meta-analysis by GU et al.
[35], an overall complication rate of 0.15% was reported. Infectious complications were
found when puncturing cysts. As with regular bronchoscopy, other complications
(including infection, transient fever and haemoptysis) can also occur [36].
Damage to the bronchoscope caused by untrained use of the needle and other handling
mistakes can be a very expensive complication. It is recommended that the whole team
involved with handling this device receives regular training from the bronchoscope
provider. In a Japanese survey, damage to the working channel was found to be the most
frequent complication [37, 38].
Learning curve
EBUS-TBNA takes time to learn under experienced guidance in order to fully understand
the ultrasonographic pictures not seen in regular bronchoscopy. There is currently no
consensus in the national and international guidelines regarding how best to train
physicians in this technique. Learning curves have been examined and one Australian study
reported that the diagnostic yield improved significantly by 20 procedures but that 50
procedures was required to reach the peak diagnostic yield [38, 39]. Another trial
recommended performing 13 procedures under supervision in order to be able to perform
the procedure safely and obtain an adequate yield [40]. Different learning models have been
proposed and KONGE and co-workers [39, 40] published data on the use of virtual reality
bronchoscopy simulators to assess performance in order to set a standard for training prior
to “real-life” bronchoscopy. Skills learned on simulators appear to be transferrable to a
clinical setting. Larger trials are necessary here but more training opportunities need to be
implemented since the technique is becoming ubiquitous.
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EUS and EBUS provide access to different areas of the mediastinum. By combining these
techniques, most lymph node stations, as well as the left adrenal gland, can be reached
(with the exception of stations 5 and 6). In a meta-analysis, the accuracy of EUS-FNA and
EBUS-TBNA used in combination for the diagnosis of mediastinal cancer was 95% [42].
The use of EBUS and EUS-B have also been examined. HWANGBO et al. [43] and HERTH
et al. [44] showed similar results compared to those seen with the use of EBUS and EUS.
Therefore, combining oesophageal and bronchoscopic endoscopic staging with a single
linear US bronchoscope is effective when performed by an experienced endoscopist.
An almost complete evaluation of the mediastinal and hilar nodes can be achieved in a
single staging procedure by inserting the EBUS scope into the oesophagus (EUS-B)
following an endobronchial evaluation [45]. Following an EBUS procedure via the airways,
the EBUS scope is retracted from the trachea and positioned into the oesophagus while the
patient remains in a supine position. Para-oesophageal nodes should be investigated
systematically, particularly those located in the lower mediastinum, and the subcarinal and
paratracheal space. The advantages and results of this procedure are presented in a
systematic review by J.T. Annema’s group [42].
Future developments
The next generation of EBUS scopes are now entering the market. The newest model of
Olympus scope (prototype TCP-EBUS, BF-Y0046; Olympus Medical Systems Corp.) has
been tested and will be launched in 2018. The scope is slimmer, has a thinner tip (5.9 mm),
and has a larger bending angle (170 degrees upward) than the current convex EBUS probe
(6.9-mm tip, 120 degrees upwards, and 35 degrees downwards). Accessibility, operability
and TBNA capability of the slim EBUS scope were examined by K. Yasufukus’ group [46,
47]. They were able to show that both the endoscopic visibility range (14.7 mm) and the
maximum reach (16.0 mm) were greater than in the current EBUS scope. The TCP-EBUS
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was able to visualise 1–3 distal bifurcations further. Adequate sampling from the lobar and
segmental lymph nodes was possible using the aspiration needle.
New needle options have also been launched. With the current 21- and 22-gauge needles,
the procedure can be limited by the degree of flexibility in the needle and the size of the
lumen in tissue acquisition. A new flexible 19-guage EBUS-TBNA (Flex 19G; Olympus
Respiratory America, Redmond, WA, USA) needle has therefore been developed, and has
been evaluated at three centres [48]. In 47 patients with enlarged hilar and/or mediastinal
lymphadenopathy, the diagnostic yield of the Flex 19G needle was 89% (42 out of 47
patients). The diagnostic yield with the 19G needle was: malignancy in 24 (89%) out of 27
patients, sarcoidosis in 13 (93%) out of 14 patients and reactive lymph node hyperplasia in
five (83%) out of six patients. There were no complications. All 13 patients diagnosed with
adenocarcinoma using the 19G needle had sufficient tissue for genetic testing. It seems the
19G needle can be feasibly and safely used, with promising diagnostic yield, while
providing a greater degree of flexion with the EBUS scope. As always, further clinical
evaluation is required.
From a technical perspective, the additional features are also under investigation.
Elastography in particular seems to be helpful (figure 5). Elastography is an ultrasonic
method in which the stiffness of tissues can be seen in real-time as a colour map. This
technology has been used in the EUS field for several years; the European Federation of
Societies for Ultrasound in Medicine and Biology (EFSUMB) has published guidelines
and recommendations describing the technology [49, 50]. Several groups have also used
it in EBUS [51–53]. Up to now, the largest published trial was performed by SUN et al.
[54]. The group used the technology in 68 lymph nodes (33 benign and 35 malignant)
from 56 patients, in order to examine the ability of EBUS elastography to differentiate
between benign and malignant lymph nodes. The EBUS characteristics on B-mode,
vascular patterns and elastography were recorded in all patients. The elastographic
patterns and the mean grey value inside the region of interest were also analysed. All
methods were compared with the definitive diagnosis of the lymph nodes. SUN et al.
[54] were able to show that elastography is able to differentiate between benign and
malignant lymph nodes with high sensitivity, specificity, PPV and NPV, and accuracy. It
seems that EBUS elastography is potentially capable of further differentiating between
benign and malignant lymph nodes. Elastography therefore seems to support
Figure 5. Elastography of the lymph node (in green) as well as of part of the primary tumour (in blue).
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nonmalignant needle puncture results and help the bronchoscopist believe in those
results. Again, however, additional evidence is required here.
Conclusion
EBUS-TBNA is a minimally invasive technique that has been shown to be effective in the
mediastinal staging of patients with nonsmall cell lung cancer and can also be used in the
diagnosis of mediastinal and pulmonary masses. Successful implementation of
EBUS-TBNA will decrease the number of invasive staging or diagnosis procedures required
for mediastinal lesions.
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Disclosures: F.J.F. Herth has received lecture fees and personal fees for participation on the boards of
Pulmonx, BTG, Uptake and Olympus.
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| Chapter 13
Ultrasound of the neck for airway
management
Michael S. Kristensen1 and Wendy H. Teoh2
US is an important tool in the provision of safer airway management for patients. Using a
high-frequency linear probe affixed to conventional bedside portable US machines, the
patient’s upper airways from the mandible to the jugular notch can be depicted with US
such that when the US beam penetrates to the luminal surface of the airway, as for example
in the trachea, a strong echo arises yielding a distinct hyperechoic white line on the screen,
the “tissue–air border”, and everything beyond that visualised on the screen is mere artefact.
There are numerous indications for the use of US for airway management; only the most
clinically valuable will be described in detail in this chapter. These include: US identification
of the cricothyroid membrane in preparation for management of a difficult airway where
emergency airway access via the anterior neck might become necessary, identification of the
ideal interspace between tracheal rings for tracheostomy, and simultaneous scanning
of the trachea and oesophagus just cranial to the jugular notch to observe whether a tube
enters the airway or the oesophagus.
Cite as: Kristensen MS, Teoh WH. Ultrasound of the neck for airway management. In: Laursen CB,
Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory
Society, 2018; pp. 172–183 [https://doi.org/10.1183/2312508X.10007517].
A strong echo (i.e. a strong white line) will appear when the US beam reaches air [1]. This
is the tissue–air border, and everything beyond this line is an artefact. This means that we
can depict the tissue from the skin to the anterior luminal surface of the upper airway from
the mouth to the midtrachea [2]. US for airway management should be performed at the
1
Dept of Anaesthesia, Rigshospitalet, University Hospital of Copenhagen, Copenhagen, Denmark. 2Private Anaesthesia Practice, Wendy
Teoh Pte. Ltd, Singapore.
Correspondence: Michael S. Kristensen, Dept of Anaesthesia, Center of Head and Orthopaedics, Section 3071, Rigshospitalet, University
Hospital of Copenhagen, Blegdamsvej 9, DK-2100 Copenhagen, Denmark. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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point of care by the airway manager as an adjunct to the desired procedures. A standard
linear high-frequency transducer is sufficient to scan the structures of the upper airway.
The basic US appearance of the upper airways is shown in figures 1–4.
US has a wide range of applications for safer airway management. The most important of
the published indications are: 1) intrauterine (pre-natal) US to identify fetal airway
abnormalities (e.g. lymphatic malformations or cervical teratoma) allowing planning of
optimal airway management in the case of fetal airway obstruction [2], 2) scanning of the
upper airway from the mandible to the trachea to screen for prediction of a difficult direct
laryngoscopy [3, 4] and for evaluating pathology that can influence airway management
[1], 3) scanning of the hyoid bone and thyrohyoid space to facilitate superior laryngeal
nerve blocks [5], 4) scanning of the vocal cords for investigation of vocal cord palsy and
other pathology and for verification of tracheal intubation, 5) identification of the
cricothyroid membrane for pre-anaesthetic airway evaluation in preparation for elective or
emergency front-of-neck airway access [1, 6–9], 6) identification and examination of the
trachea for better planning of an elective or emergency tracheostomy [10], 7) scanning of
the trachea/oesophagus/pleura for evaluation of the placement of a breathing tube and to
determine whether it is in the trachea, in a main-stem bronchus or in the oesophagus [11],
8) scanning of the diaphragm/adjacent organs for evaluation of hemidiaphragmatic
paralysis [12] and for evaluation of force of breathing before extubation [13], 9) scanning of
the pleura to diagnose or rule out pneumothorax and to differentiate between different
causes of hypoxia [2], 10) scanning of the gastric antrum to determine stomach content
and aspiration risk [14, 15] and 11) scanning of the oesophagus and stomach to determine
the correct placement of a gastric tube.
The authors consider indications (5)–(7) the most important and clinically useful, and
these are covered in this chapter. Indication (9) is also important for airway management,
and the technique is described in another chapter of the Monograph [16]. For detailed
Anterior
Figure 1. A curved low-frequency transducer and the area covered by the scan (left; blue line), with the
resulting US image (middle). The following are indicated on the scan on the right: the shadow from the
mentum of the mandible (green), the muscles in the floor of the mouth ( purple), the shadow from the hyoid
bone (orange) and the dorsal surface of the tongue (red). Reproduced and modified from [1] with
permission.
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Anterior
Figure 2. A transverse midline scan over the thyroid cartilage in an 8-year-old boy (left) and the resulting
US scan (middle). The following are indicated on the scan on the right: the thyroid cartilage (green), the
vocal cords (orange), the anterior commisure (red) and the arytenoid cartilages (yellow). Reproduced and
modified from [1] with permission.
descriptions of the other indications, the reader is referred to [2] and the accompanying
video links [17].
Figure 3. A linear high-frequency transducer placed in the midsagittal plane and the scanning area (left;
blue line), with the resulting US scan (middle). The following are indicated on the scan on the right: the
thyroid cartilage (green), the cricoid cartilage (dark blue), the tracheal rings (light blue), the cricothyroid
membrane (red), the tissue–air border (orange) and the isthmus of the thyroid gland (brown); below the
orange line, only artefacts are seen. Reproduced and modified from [1] with permission.
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Figure 4. The position of the transducer for a transverse scan just cranial to the suprasternal notch and on
the left side of the patient’s trachea (left) and the resulting US scan (middle). The following are indicated on
the scan on the right: the anterior part of the tracheal cartilage (light blue), the oesophagus (purple) and
the carotid artery (red). Reproduced and modified from [1] with permission.
Two techniques have been described for systematic, stepwise identification of the
cricothyroid membrane: 1) the longitudinal “string-of-pearls” (SOP) technique [1], and
2) the transverse thyroid–airline–cricoid–airline (TACA) technique [28].
The SOP technique is the most well published and has proven its superiority over palpation
in a cadaveric study that demonstrated its ability to heighten success and limit tube
misplacement in cricothyrotomy [8, 27]. This technique can also be used to identify the
optimal interspace between tracheal rings for placement of a tracheostomy tube. We
recommend this technique as the first to learn and as the default technique, so that every
anaesthesia department dealing with difficult airways on a regular basis should have the
expertise available to apply this method. On occasions where one encounters patients with
a very short neck, or with flexion deformity of the neck that leaves no space to place the
US transducer in the longitudinal position, we recommend the transverse TACA technique
to identify the cricothyroid membrane, as in these subsets of patients this may be the only
successful technique [28]. Achieving a 100% success rate of identifying the cricothyroid
membrane was possible when the longitudinal SOP technique was applied in tandem with
the transverse TACA technique [28].
Thus, US-guided localisation of the cricothyroid membrane fills the void of very poor
results caused by inaccurate localisation by visualisation or palpation; it is easily learned
and should be considered if not routinely, then at least before embarking on the
management of anticipated difficult airway situations.
The longitudinal SOP technique is carried out as follows [29]. The sternal bone is
identified and the transducer is placed transversely on the patient’s neck, just cephalad to
the suprasternal notch to visualise the trachea (a horseshoe-shaped dark structure with a
posterior white line) (figure 5a). The transducer is then slid towards the patient’s right side
(towards the operator), so that the right border of the transducer is positioned in the
midline of the trachea, and the US image of the tracheal ring is thus truncated in half on
the screen (figure 5b). The right end of the transducer is maintained over the midline of
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a)
b)
c)
d)
Figure 5. a–d) The longitudinal “string-of-pearls” technique for identifying the cricothyroid membrane and
the interspaces between the tracheal rings (see text for details). Images on the left show the position of the
transducer, with the resulting scans in the middle. Images on the right show the positions of the following:
the tracheal ring (red), the tissue–air border (light blue), the cricoid cartilage (green) and the distal end of
the thyroid cartilage ( purple). The shadow from the needle slid in between the transducer and the skin is
shown in yellow in (d). Reproduced from the Airway Management for Anaesthesiologists 2018 course
available at www.airwaymanagement.dk, with permission.
the trachea, while the left end is rotated 90° into the sagittal plane, resulting in a
longitudinal scan of the midline of the trachea. A number of dark (hypoechoic) rings will
be seen anterior to the white hyperechoic line (air–tissue border), akin to a string of pearls.
The dark hypoechoic “pearls” are the anterior part of the tracheal rings (figure 5c). The
transducer is kept longitudinally in the midline and slid cephalad until the cricoid cartilage
comes into view (seen as a larger, more elongated and anteriorly placed dark “pearl”
compared with the other tracheal rings. Further cephalad, the distal part of the thyroid
cartilage can also be seen (figure 5d). The longitudinal course of the midline of the airway
can be marked with a pen. While still holding the transducer, the other hand is used to
slide a needle (as a marker, for its ability to cast a shadow in the US image) between the
transducer and the patient’s skin until the needle’s shadow is seen midway between the
caudal border of the thyroid cartilage and the cephalad border of the cricoid cartilage
(figure 5d). The transducer is then removed, and the needle marks the centre of the
cricothyroid membrane in the transverse plane, which can be marked on the skin with a
pen. For a video demonstration of this technique, see [30].
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To perform the transverse TACA technique, the following steps are carried out [28]. First,
an estimate is made of where the level of the thyroid cartilage is on the neck and the US
transducer is placed transversely over it, scanning to identify the thyroid cartilage as a
hyperechoic triangular structure (figure 6a). The transducer is moved caudally until the
a)
b)
c)
d)
Figure 6. a–d) The transverse thyroid–airline–cricoid–airline (TACA) method for identifying the cricothyroid
membrane (see text for details). Images on the left show the position of the transducer, with the resulting
scans in the middle. Images on the right show the positions of the following: the thyroid cartilage (blue
lines in a), the airline or cricothyroid membrane (horizontal blue line in b and d) and the anterior part of the
cricoid cartilage (curved blue line in c). Reproduced from the Airway Management for Anaesthesiologists
2018 course available at www.airwaymanagement.dk, with permission.
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US for tracheostomy
The addition of US for both dilational and surgical tracheostomy may increase the success
rate by helping to identify the trachea and the optimal interspace between tracheal rings, to
determine the depth to the tracheal lumen, and to identify overlying blood vessels or other
pathology prior to the procedure. US can be applied before the tracheostomy itself to guide
the decision as to whether the best approach is a surgical technique or a dilational
technique. The surgical technique would typically be chosen in cases of large overlying
blood vessels, an inability to identify an appropriate interspace between tracheal rings and
s.c. emphysema. US may also be used before a tracheostomy in order to determine the ideal
interspace between the tracheal rings and the depth to the trachea [10, 32]. US may also be
used before and during the procedure instead of guidance by a flexible bronchoscope,
and/or in combination with a flexible bronchoscope.
Identification of the trachea can be challenging in obese patients, in those with a short
thick neck or with a neck mass, or in those who have had previous surgery or radiotherapy
to the neck, or who have thoracic pathology or another condition resulting in tracheal
deviation [33]. Even the addition of CXR and techniques of needle aspiration to locate
the trachea may be futile [34]. Under such circumstances, pre-operative US for localisation
of the trachea and the tracheal structures is extremely useful [34]. Pre-procedural US
often leads to a change in technique from a dilational technique to a surgical technique or
vice versa [10], and to a change in the selection of the best interspace between tracheal
rings [35].
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rate of puncture of the orotracheal tube in the US group versus 1.7% in the bronchoscopy
group (p=0.619) but RUDAS et al. [37] concluded that, overall, US guidance is an acceptable
alternative to bronchoscopy guidance.
These findings lead us to recommend that real-time US guidance alone should be reserved
for the highly experienced, and that combination with bronchoscopy is the ideal approach.
If the ultrasonographer is highly experienced, the needle insertion can be performed under
real-time US guidance only; otherwise, we recommend the combination of pre-procedural
US and procedural flexible bronchoscopy, as this combination adds the possibility of
observing the needle entry into the tracheal lumen to avoid penetration of the posterior
wall, as a supplement to the advantages obtained with US.
When attempting endotracheal intubation, confirmation of whether the tube enters the
trachea or the oesophagus can be obtained either by using direct US scans of the anterior
neck during or immediately after intubation, by indirectly looking for ventilation at the
pleural or diaphragmatic level, or by combining these techniques [11].
The direct scan of the anterior neck can be performed as follows: 1) transversely high on
the neck at the level of the vocal cords/cricothyroid membrane (as a dynamic process in
real time), 2) transversely a little lower at the level of the suprasternal notch (here, both
dynamic and static scanning are effective) [41] or 3) by a longitudinal scan covering the
visible length of the trachea.
We recommend the following approach [1, 2, 11]. Place a linear high-frequency transducer
transversely on the neck immediately cranial to the suprasternal notch in the midline.
Identify the trachea as a horseshoe-shaped dark structure with a strong white line (the
tissue–air border [1]) immediately posterior to it. Identify the oesophagus, seen as a “bull’s
eye” appearance due to its concentric layers, most often visible posterolateral to the trachea
on the patient’s left side. Asking the patient to swallow will make the oesophagus compress
and expand, and will help with its identification.
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Intubation should then be performed. If the tube enters the trachea, this may be seen as a
brief “snowstorm” when part of the tube touches the anterior tracheal wall from the inside,
or nothing may be seen if there is air between the tube and the tracheal wall precluding the
US beam from reaching the tube. If the tube enters the oesophagus, it will create a tissue–
air border in the otherwise collapsed oesophagus; this is seen as a strong white horizontal
line that may repeat itself several times (like a flutter) due to a “comet-tail”-like artefact.
This means that if the tube has entered the oesophagus, it will give the oesophagus an
appearance that resembles the trachea, called the “double-trachea” sign. This test has a high
sensitivity of 86–100% of detecting oesophageal intubation in emergency and cardiac arrest
patients [41–43]. If the tube is seen passing into the oesophagus, it should be removed
without ventilating the patient and subsequently another intubation attempt made, by an
optimised intubation technique. However, if the tube is not seen in either the trachea or
the oesophagus, or if it is seen in the trachea, ventilation of the patient should be started
via the tube.
Subsequently, move the transducer to the midaxillary line on both sides, identify the
“pleural line” posterior to the rib shadows and look for “lung sliding” bilaterally [2]. Lung
sliding appears as a to-and-fro movement synchronous with ventilation, a movement that is
striking because the surrounding tissue is motionless. Lung sliding is best seen dynamically
or on a video [17]. Detection of lung sliding can be enhanced by applying motion mode or
M-mode scanning, which produces a clear distinction between a wave-like pattern located
above the pleural line and a sandy-like pattern below; this is called the “seashore” or the
“sandy beach” sign.
If there is bilateral lung sliding, this confirms that the tube is in the airway, but intubation
of a main-stem bronchus cannot be ruled out. If there is one-sided lung sliding and on the
other side there is a “lung pulse” (a sign that arises from the transmitted heartbeat that
pushes the lung and the pleura slightly with every heartbeat, seen as an artefact
synchronous with the pulse [1]), then main-stem bronchial intubation is likely, and the
tube should be withdrawn gradually until bilateral lung sliding is present. If there is no
lung sliding on either side, but there is a lung pulse bilaterally, there is a risk of the tube
having entered the oesophagus, and re-intubation should be performed. If there is neither a
lung pulse nor lung sliding, then pneumothorax should be suspected.
The correct position of a double lumen can be checked by TUS. The US approach reaches
the same sensitivity and specificity as fibreoptic bronchoscopy but is more rapid and less
expensive.
Other methods for determining the location of the tube include: direct observation of the
tube going through the glottis, symmetric chest movements during ventilation via the tube,
the presence of vapour in the tube, auscultation of breath sounds, epigastric auscultation,
capnometry, quantitative waveform capnography, use of an oesophageal detector device,
CXR and CT, and bronchoscopic visualisation of tracheal or bronchial rings. Each has their
advantages and disadvantages.
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The clinician performing tracheal intubation should have multiple confirmation methods
that allow the practitioner to adapt to a variety of clinical situations.
Both direct and indirect confirmation methods have advantages compared with
capnography as they can be applied in very low cardiac output situations or in
bronchoconstriction, and they can replace auscultation in noisy environments, such as
helicopter retrievals.
Conclusion
US is an essential adjunct in the management of the difficult upper airway that allows
identification of essential airway structures. The cricothyroid membrane is an essential
structure for emergency access to the airway and is identified with much higher success
with US than with palpation. Ideally, all physicians, or at least all departments, who are
responsible for managing patients with difficult or compromised airways should be able to
apply US for identification of the trachea and of the cricothyroid membrane.
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| Chapter 14
Focused cardiac ultrasound
Gabriele Via1, Anthony Dean2,3, Gabriele Casso1, Brian Bridal Løgstrup4
and Guido Tavazzi5
Cite as: Via G, Dean A, Casso G, et al. Focused cardiac ultrasound. In: Laursen CB, Rahman NM, Volpicelli G,
eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 184–205
[https://doi.org/10.1183/2312508X.10007117].
T he use of FoCUS is becoming widely accepted as a tool to aid clinical decision making,
especially in critical care, emergency medicine, anaesthesia and acute cardiac care. In
these settings where cardiovascular/respiratory compromise may be challenging and rapidly
evolving, FoCUS has the potential to provide crucial pathophysiological information. In
this chapter, the concept, aims, technique and clinical applications of FoCUS are described,
with an emphasis on its technique, how it relates to formal comprehensive
echocardiography and its limitations.
1
Cardiac Anesthesia and Intensive Care, Cardiocentro Ticino, Lugano, Switzerland. 2Division of Emergency Ultrasonography, Dept of
Emergency Medicine, University of Pennsylvania Medical Center, Philadelphia, PA, USA. 3Universidad de San Carlos de Guatemala,
Guatemala City, Guatemala. 4Dept of Cardiology, Aarhus University Hospital, Aarhus, Denmark. 5University of Pavia, Anesthesia,
Intensive Care and Pain Therapy, Anesthesia and Intensive Care, Emergency Dept, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
Correspondence: Gabriele Via, Cardiac Anesthesia and Intensive Care, Cardiocentro Ticino, Via Tesserete 48, 6900 Lugano, Switzerland.
E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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time-sensitive clinical decision making [1, 2]. The primary goals of FoCUS are an
understanding of the cardiovascular physiology/pathophysiology of the patient and the
mitigation of diagnostic uncertainty. Furthermore, when FoCUS findings are sufficiently
conclusive, they may allow a definitive diagnosis. If they do not, they may narrow the
differential diagnosis, thereby accelerating the diagnostic/therapeutic process with potential
savings in time, clinical resources and costs.
Although most commonly conducted at the bedside by noncardiologists using highly mobile
or even portable US machines, FoCUS can be performed by any appropriately trained
clinician regardless of his or her specialty, with any US machine capable of obtaining the
necessary information [1, 2]. It can be performed within the hospital, as well as in any
out-of-hospital setting in which unstable or emergently ill patients are being cared for. Such
settings include hospital wards, emergency departments, operative theatres, intensive care
units, pre-hospital and inter-hospital transport, and remote and austere environments.
FoCUS is targeted based on the clinical evaluation; it is informed by the clinical evaluation,
and seeks to complement and augment it. Examples of typical questions to be addressed by
FoCUS include: Why is this patient hypotensive/dyspnoeic? Might this patient benefit from
volume resuscitation? Is major right ventricle (RV) systolic dysfunction responsible for the
shock state of this patient? Another important distinction between FoCUS and the traditional
echocardiographic examination is that many critical care and emergency sonologists are
trained in LUS, allowing them to integrate this skill with their cardiac US evaluation.
Currently, LUS is not a component of most echocardiology protocols, and the majority of
echocardiologists are not trained or experienced in its use. Indeed, FoCUS represents the
cardiac US application within a broader critical US praxis, which includes (as indicated by
the patient’s clinical condition) evaluation of the lungs, pleural spaces, abdominal cavity and
vascular system, and is frequently augmented by the use of US to guide invasive procedures
[3]. Outside the emergency/critical care context, evidence also suggests an emerging role for
FoCUS in the screening of cardiac disease in specific high-risk populations [1, 4].
Table 1 provides a detailed summary of how FoCUS differs from traditional comprehensive
echocardiography.
There is clear evidence that noncardiology clinicians can be proficient in the skills required
for FoCUS [1, 9–14]. The learning curve for FoCUS is shorter (and steeper) than that of
comprehensive echocardiography, so that training programmes can be relatively short
compared with those required for expertise in comprehensive echocardiography [1, 15].
However, given the heterogeneity of FoCUS literature in the training protocols, there are no
data that precisely define and quantify the training and experience needed for competence
in FoCUS, and the recommendations vary. The core components of a FoCUS training
programme should be a theoretical part, hands-on training and image-interpretation
training. According to several scientific bodies, there is general agreement that a brief
introductory course, followed by the execution of at least 50–60 examinations performed
under appropriate proctorship represents an adequate training for competency in the most
basic FoCUS examination (evaluation for pericardial effusion, tamponade, acute
intravascular volume depletion, acute RV failure, left ventricle (LV) systolic dysfunction and
gross valvular abnormalities) [1, 2, 16–19].
It is important that clinicians are mindful that the test characteristics of FoCUS are
different from those of comprehensive echocardiography, in the same way that portable
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Performed at the point of care FoCUS is performed at the point of care by the
clinician attending the patient.
Focused FoCUS is not an exhaustive cardiac investigation,
nor does it aim necessarily at a definitive
diagnosis. It provides pathophysiological insight
on relevant clinical issues that require a rapid
response. Even in situations in which a diagnosis
is not made, FoCUS frequently narrows the
differential diagnosis, embodying the concept of
“mitigation of diagnostic uncertainty”.
Problem-based, goal-directed FoCUS is problem oriented and targeted, based on
the clinical condition of the patient. For this
reason, it is frequently referred to as
goal-directed.
Time sensitive FoCUS is time sensitive, consistent with the short
time frame of the patient’s illness. For example,
in a patient with sudden cardiovascular instability,
the time frame for evaluating the cause of shock
might be a matter of seconds, whereas in the
same patient with gradual decompensation, the
evaluation of evidence of left ventricular failure
might occur over a longer period.
Generally follows a specific protocol Parts or all of the FoCUS examination may be
defined by protocol. While every FoCUS
examination is individualised to the patient’s
clinical condition and may vary based on the
training and experience of the sonologist, in
managing time-sensitive critical conditions (such
as cardiopulmonary arrest) it is frequently useful
to follow scientifically established protocols [5–8].
As such the FoCUS examination can easily be
integrated with other resuscitation protocols, such
as the Advanced Cardiac Life Support (ACLS)
protocol, although there are currently no data to
demonstrate that use of FoCUS in this setting
improves survival.
Provides mainly qualitative/ FoCUS collects a series of mainly qualitative/
semi-quantitative data semi-quantitative findings that are interpreted in
light of the clinical context.
Limited in scope, number of views and FoCUS is often limited in scope in that it frequently
echocardiographic modalities used uses a limited number of transthoracic views and
US modalities (two-dimensional and M-mode),
and addresses an evidence-based restricted list
of targets.
Examination in which there should be a With its defined and limited focus, and as a single
low threshold for further testing component of the ongoing diagnostic/therapeutic
evaluation of the critically ill, it is appropriate that
FoCUS frequently triggers additional testing,
mostly comprehensive echocardiography. In
contrast to FoCUS performed as a screening tool
for cardiac disease in asymptomatic populations,
FoCUS performed in the critically ill generally has
Continued
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Table 1. Continued
and nonportable chest radiographs, chest CT and pulmonary CT angiograms all have
different test characteristics. In particular, the training and experience of a clinical
sonologist are often limited in comparison with those of imaging specialists, and the
limitations of FoCUS in the context of the management of critically ill patients mean that it
yields more limited information. For these reasons, the FoCUS practitioner in the critical
care setting should have a low threshold for obtaining a comprehensive echocardiogram (as
well as other diagnostic tests) in cases where findings are ambiguous or unclear, or where
the clinical context suggests that the patient’s condition may be due to cardiac pathology
that is not obtainable from the FoCUS examination (e.g. chronic heart disease, valvular
disease). Recognition of specific limitations (e.g. frequently mechanical ventilation, or the
immediate post-cardiac surgery setting) and of technical limitations of the US equipment is
a component of FoCUS expertise. A clear definition of the FoCUS goals, purview and
limitations is an important part of any FoCUS training curriculum. Conversely, traditional
imaging specialists should be aware that the intensivist’s familiarity with the patient’s
clinical condition, the integration of US evaluation of the lungs and other organ systems
with the FoCUS examination, and the ability to perform the examination in real-time,
concurrent with changes in the patient’s condition, may confer advantages on FoCUS over
a comprehensive echocardiographic evaluation.
A final limitation that should be noted is that FoCUS is widely used in clinical settings outside
those of traditional echocardiography (e.g. trauma, resuscitation and intensive care in general),
and is frequently integrated into the US examination of other body areas. Discussion of the
extensive uses of FoCUS in these settings is beyond the scope of this chapter.
A FoCUS examination does not require the execution of all the views of a comprehensive
echocardiographic examination. A limited number of views (figure 1 and table 2) usually
suffices to allow confirmation of findings [1]. Those most commonly used in the FoCUS
examination are the subcostal long-axis (SLAX, also named subcostal four-chamber
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1. SLAX/S4CH
RV
5 RA
4 LV
LA
3
1
2
RV
RA LV
LA
2. SIVC 3. A4CH
RV LV
IVC RA
RA
LA
Liver
IVC LV
RA RV
RA LA
4. PLAX 5. PSAX
RV Asc Ao RV
LV LA LV
RV IVS
Asc Ao RV
LV LV
LA
Figure 1. Suggested standard set of views for FoCUS, with corresponding anatomical sections and planes. If
compatible with the clinical scenario, a systematic approach going through all of these views is
recommended. The upper left panel depicts where the probe is located on the patient’s chest in order to
obtain the FoCUS views. For each of the five FoCUS views, the remaining panels provide a schematic
description of: probe orientation (indicated on the torso image in each part), US cross-section through the
heart (upper right on each part), anatomical plane (left on each part) and corresponding cardiac US view
obtained (lower right on each part). The five views are: 1) subcostal long axis (SLAX, also named subcostal
four-chamber (S4CH)), 2) subcostal inferior vena cava (SIVC), 3) apical four-chamber (A4CH), 4) parasternal
long axis (PLAX) and 5) parasternal short axis (PSAX) (in this image, the midpapillary level is shown, but the
left ventricle (LV) from apex to base can be scanned). For a better understanding of the US images of the
heart obtained with each view, the arrow on the torso pictures indicates the orientation of the marker on the
probe (yellow dot in the picture), while the yellow line on the margin of the US sector cutting the heart and
of the anatomical plane picture indicates the side corresponding to the probe’s indicator, e.g. for A4CH, the
probe indicator (yellow dot) is oriented on the left side of the patient, and the left-sided structures of the
heart (LV and left atrium (LA)) are represented in the anatomical plane and in the US image on the side of
the sector highlighted by the yellow line. RV: right ventricle; RA: right atrium; IVC: inferior vena cava;
AscAo: ascending aorta; IVS: interventricular septum.
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Table 2. Suggested FoCUS views standard set, representing the minimum data set for a complete
FoCUS examination
(S4CH)), subcostal inferior vena cava (SIVC), parasternal long-axis (PLAX), parasternal
midpapillary short-axis (PSAX) and apical four-chamber (A4CH). The SLAX view is
particularly useful in patients with chronic lung disease, or in mechanically ventilated
patients. Whenever possible, a combination of views should be obtained, although this may
not be possible in the critical setting. Ideally, each target structure as well as abnormal
findings should be visualised in at least two different planes or views, provided the patient’s
clinical status allows it.
Recommendations regarding the most useful cardiac views in FoCUS are contradictory. In
the critically ill nonventilated patient, the PLAX view seems to be the most easily obtained
[20]. However, the SLAX and A4CH views offer several advantages: 1) they allow
simultaneous visualisation of all cardiac chambers, providing the information required to
screen for chronic cardiac disease (the advised preliminary target of each FoCUS
examination; see later section), 2) especially in cardiac arrest scenario, the SLAX view is the
most easily accessible one, and in the challenging mechanically ventilated patients it can be
the only viable one, and 3) the SLAX view, with minimal probe manipulation, also quickly
provides sonographic access to the inferior vena cava (IVC) (i.e. through the SIVC view).
In extreme situations with the greatest time sensitivity, the two combined subcostal views
may provide sufficient initial minimal information (although the FoCUS examination
should be completed as soon as the clinical picture permits).
FoCUS can be performed with any US machine capable of 2D cardiac imaging, from a full
functionality platform to pocket-sized and hand-carried devices. The latter use a simpler
technology and thus present relevant technical and diagnostic limitations in comparison
with high-end US machines. When cardiac US was performed comparing experienced
operators with high-end machines and with portable devices, results varied according to
the targets of the examination considered, ranging from a good agreement [21, 22] to
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Unresponsive?
Open airway,
look for signs of life
CPR 30:2
Defibrillator/monitor
Assess rhythm
Shockable Nonshockable
(VF/pulseless VT) PEA/asystole
Figure 2. The Focused Echocardiography Evaluation in Life support (FEEL) protocol. This is a widely used
protocol-based FoCUS approach that is designed to be integrated within the Advanced Cardiac Life Support
(ACLS) protocols in cardiac arrest. FoCUS is performed if nonshockable rhythms are detected, and in an
ACLS-conforming manner: only after five cardiopulmonary resuscitation (CPR) cycles, during the 10-s
interval of the pulse check, and without interfering with resuscitation manoeuvres. VF: ventricular
fibrillation; VT: ventricular tachycardia; PEA: pulseless electrical activity; EMD: electromechanical
dissociation; ETCO2: end-tidal CO2.
significant superiority of stationary high-end machines [23]. Several factors may potentially
affect the quality and interpretation of the FoCUS information obtained with such highly
portable devices, especially in situations in which suboptimal patient echogenicity poses a
challenge: smaller and lower resolution of the screen, an intrinsic lack of complex image
enhancement and artefact reduction capabilities, and the possibility of limited acquisition
modifications [24]. Awareness of portable US machine limitations by FoCUS practitioners
is extremely important: the ability to undertake a careful assessment of image quality and
reliability should be part of any FoCUS competency-based training [1, 24].
FoCUS includes the assessment of a narrow list of evidence-based detectable targets [1, 19]
(table 3). While there are numerous modalities used in comprehensive echocardiographic
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Each FoCUS examination should systematically search for these pathological cardiac US signs
(see text for details). The screening for signs of chronic cardiac disease is an essential
preliminary step, as it allows interpretation of subsequent findings in the correct light.
examinations to measure cardiac function and anatomy, many of these are time consuming
and require training beyond that of the usual critical care or emergency sonologist.
However, there are a few metrics that are relatively easy to assess, and with a trained eye
these can often be rapidly evaluated by visual estimation with a degree of accuracy that is
sufficient for critical clinical decision making [1, 9].
With appropriate training, visual pattern recognition of these findings (either in isolation
or combination) can be learned relatively rapidly [1, 9–11]. Development of adequate visual
pattern recognition skills usually requires review of large numbers of normal and
pathological video clips, which is an important component of a training programme. The
goal is to identify distinctive sonographic features that are associated with common and
significant cardiocirculatory disease. This process is facilitated by the fact that, in many
cases, “the sicker the patient, the grosser the FoCUS findings”. A description of these
patterns is provided in table 4. Figure 3 provides examples of common FoCUS patterns in
shock, some of which are also found as reversible causes of PEA.
Dilation of the left atrium (LA) and LV and pronounced LV hypertrophy usually suggest
pre-existing myocardial and/or valvular disease [25]. Right atrium (RA) dilation may
suggest pre-existing right heart disease, and RV hypertrophy may indicate long-standing
pulmonary hypertension. All of these can cause acute illness and critical instability when
they decompensate (often in the setting of another precipitating stress or illness). The
normal range of LV end-diastolic diameter (LVEDD) is 40–60 mm, with the size related to
the height of the patient. LVEDD of >60 mm (especially in smaller patients) suggests a
dilated LV. LVEDD of <40 mm (especially in larger patients) suggests either ventricular
hypertrophy or intravascular volume depletion. These dimensions are not applicable in
aerobically conditioned athletes who in health have enlarged ventricular volumes. Another
useful parameter for visual assessment is LV wall thickness, which is also assessed at
end-diastole. In normal health, all the walls of the LV have a similar thickness of <11 mm.
LV walls that are significantly thicker than this should prompt consideration of the
possibility of LV hypertrophy and diastolic dysfunction, or, if accompanied by a contracted
LV cavity and hyperdynamic function, the presence of severe hypovolaemia (see later
section). The maximum thickness of the RV free wall in diastole is 5 mm. If it is dilated
with a thickness greater than this, chronic RV failure should be suspected.
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Common FoCUS patterns in adult cardiac arrest and shock scenarios are shown. Common
patterns in shock are represented by acute left ventricle (LV) systolic dysfunction, acute right
ventricle (RV) systolic dysfunction, biventricular failure, severe hypovolaemia and tamponade
(patterns 1–4 and 6). Common cardiac arrest findings when electromechanical dissociation
occurs are also represented by dramatic acute LV systolic dysfunction, acute RV systolic
dysfunction, severe hypovolaemia and tamponade (patterns 1–3 and 6). Cardiac standstill is
another typical finding in cardiac arrest pulseless electrical activity/asystole rhythms. Patterns 8–
12 (suspected pre-existing chronic heart disease, suspected valvular disease) should trigger
comprehensive echocardiography referral within an appropriate time frame, as their evaluation
may go beyond FoCUS competency. TAPSE: tricuspid annular plane systolic excursion; IVC:
inferior vena cava; RA: right atrium; LA: left atrium; AV: aortic valve; MV: mitral valve.
Reproduced and modified from [1] with permission.
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a) b)
2D
M-mode
LV
RV
LA
EDD ESD RA
c) d)
RV
RV
RA
PE
RA
LV LV
LA
e) f)
LV
RV
LV
LA
RV
RA
LA
RA
Figure 3. Common FoCUS findings in shock. a) Parasternal long-axis view (two-dimensional (2D) and
M-mode evaluation) showing severely reduced left ventricular (LV) systolic function as testified by a small
variation between end-diastolic diameter (EDD) and end-systolic diameter (ESD) (double-headed arrows).
The patient had cardiogenic shock due to acute myocardial infarction (AMI). b) Apical four-chamber view
showing a markedly dilated right ventricle (RV), a leftward shift of the interventricular septum and LV
compression. The patient was submitted to abdominal surgery 4 days previously and suddenly developed
syncope and shock. Massive pulmonary embolism was suspected based on this pattern of acute cor
pulmonale. The patient was stabilised with vasopressor infusion and then taken for an angio-CT scan,
where diagnosis was confirmed. c) Subcostal four-chamber view showing small RV and LV cavities at
end-diastole (a corresponding video clip also showed a hyperdynamic pattern). This was an intensive care
unit patient with community-acquired pneumonia, who suddenly manifested severe hypotension. Severe
hypovolaemia was diagnosed and treated with aggressive volume repletion. Septic shock was later
confirmed as the cause. d) Subcostal long-axis view showing circumferential large pericardial effusion and
compression of the RV (arrow) in mid-diastole. This patient with acute lymphatic leukaemia and increasing
dyspnoea over recent weeks presented in acute shock. The patient had relief of symptoms with echo-guided
pericardiocentesis. e) Apical four-chamber view showing a floating mass attached to the mitral valve and
moving into the left atrium (LA) during systole (arrow). The patient developed acute pulmonary oedema and
shock on day 3 of an inferior AMI. The diagnosis of a ruptured papillary muscle and severe mitral
regurgitation was confirmed with transoesophageal echocardiography. f ) Apical four-chamber view showing
a dilated LV and LA in a patient with acute pulmonary oedema and an apparently unremarkable past
medical history. The patient was confirmed to have dilated cardiomyopathy upon a comprehensive
echocardiographic examination. RA: right atrium; PE: pericardial effusion.
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The presence of chronic cardiac disease calls for caution in interpreting the FoCUS
examination as it signals the presence of potentially confounding cardiac findings [1].
Failure to identify underlying cardiac conditions may result in erroneously attributing an
acute problem to a chronic derangement (e.g. diagnosing acute pulmonary embolus in the
patient with chronic cor pulmonale when the problem is actually acute pneumonia) or,
conversely, failing to identify an acute problem because it is masked by a chronic
abnormality (e.g. failing to identify hypovolaemia because of the absence of hyperdynamic
function in a patient with chronic dilated cardiomyopathy).
LV systolic dysfunction
Many studies have demonstrated that visual estimation of LV ejection fraction (EF) is as
accurate as sonographically derived measurements among both imaging specialists and
clinician sonologists [26–28]. An estimation of LV EF is obtained qualitatively by gauging the
change in size of the LV cavity from end-diastole to end-systole (either of its midcavity
diameter or short-axis area, or of its “visually estimated volume”, i.e. also considering its
long-axis size change). An end-systolic reduction in LV diameter or area of more than
one-third of its end-diastolic size corresponds to a normal EF (>60%). Evaluation of the
motion of the anterior leaflet of the mitral valve is also useful. With a healthy ventricle and
normal intravascular volume, this leaflet should almost touch the ventricular septum in early
diastole (referred to as E-point septal separation). While exaggerated motion suggests
intravascular volume depletion, attenuated movement implies elevated cardiac filling pressures,
often due to diastolic failure, with or without accompanying forward (systolic) failure due to
any number of causes (correlated clinically and sonographically). A cut-off of <7 mm for
E-point septal separation is often used to detect severe LV systolic dysfunction (EF <30%) [29].
RV systolic dysfunction
The primary means of assessment of the RV by FoCUS is by comparison with the LV. In
normal health, the RV area in a four-chamber view is approximately <0.6 times the LV
area. A larger RV size is the hallmark of RV failure, which is defined as severe when the
ratio is ⩾1/1 [30]. Visual estimation of EF is more difficult in the RV than in the LV due to
its more complex shape. Longitudinal base-to-apex excursion of the tricuspid annular plane
(either visually estimated or measured using M-mode) serves as a good surrogate to assess
RV global systolic function in most cases [31].
Severe hypovolaemia
A small end-diastolic size of both LV and RV, and a small IVC (⩽1 cm diameter) [33] are
the hallmarks of hypovolaemia in the spontaneously breathing patient. In mechanically
ventilated patients, such findings become less sensitive, although they remain sufficiently
specific. IVC inspiratory collapse in the spontaneously breathing patient (>40% of the
end-expiratory size) [34] and IVC inspiratory distensibility in the mechanically passively
ventilated patient (>20%) predict fluid responsiveness [35]. Nevertheless many confounders
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in IVC size and respiratory variation interpretation exist [36]. For example, in patients with
tamponade and haemodynamically significant pulmonary embolus, as well as in those with
many forms of chronic cardiac disease, these findings may be absent, despite moderate or
severe intravascular volume depletion.
The target findings include flail (untethered) valve cusps/leaflets with exaggerated motion,
evident disruption of the valvular apparatus, any mass attached to a valve (especially if
>5 mm in diameter), and grossly thickened, calcified and immobile aortic cusps or mitral
leaflets. As in all aspects of the FoCUS examination, the sonologist will correlate the
findings with all other clinical information available.
There is extensive literature support for the use of FoCUS in the management of the
critically ill and its impact on clinical decision making, although currently there are limited
data on its impact on patient outcomes [1, 37, 38].
Shock
The use of FoCUS in undifferentiated nontraumatic shock states reduces the number of viable
diagnoses [39, 40]. FoCUS allows the categorisation of patients into one of the main shock
pathophysiological subsets (hypovolaemic, cardiogenic, obstructive or distributive) by detecting
either the specific cardiac dysfunction involved (e.g. LV or RV failure, cardiac tamponade,
severe valvular dysfunction) or the consequences of disturbances in volume status/peripheral
circulation at the level of the heart (e.g. hypovolaemia, vasodilation) [41]. FoCUS identifies
global LV systolic dysfunction and accurately estimates its degree [28]. Once the aetiology of
the haemodynamic instability is established, management can be tailored and directed to the
patient’s specific derangements. Detection of RV dilation and hypokinesia in a shock patient
may suggest, in the appropriate clinical context, massive pulmonary embolism, RV acute
myocardial infarction (AMI) or decompensation of chronic RV failure. As it specifically
concerns the diagnosis of pulmonary embolism, it is worth highlighting that FoCUS has
sufficient sensitivity only for haemodynamically significant pulmonary embolism [42].
Echocardiography is, in fact, recommended in some current guidelines for investigation of
suspected pulmonary embolism only in a patient too unstable for transfer for a CT scan [42].
Nevertheless, the absence of FoCUS signs of RV failure in a patient in shock allows exclusion
of pulmonary embolism as the cause. This begs the question of why FoCUS should not be
used to investigate pulmonary embolism while other reversible causes are also being
sonographically investigated. With this approach, it might be said that, in haemodynamically
unstable patients suspected for pulmonary embolism, FoCUS functions in the same way as the
D-dimer test in the stable patient diagnostic algorithm [42]. FoCUS provides vital information
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concerning the presence and amount of free (nonloculated) pericardial effusions and their
haemodynamic relevance. Although beyond the scope of this chapter, if tamponade is
identified, the sonologist will use the US machine for guidance in pericardiocentesis,
minimising procedure-related complications and increasing the success rate [43, 44].
Current evidence suggests a role for FoCUS in identifying patients who may benefit from fluid
loading, especially in pronounced states of hypovolaemia. A typical “hyperdynamic pattern”
characterised by small, hyperkinetic ventricles, especially if accompanied by a flat or highly
collapsible IVC, should prompt a diagnosis of severe hypovolaemia, whatever the cause
[45, 46]. This pattern has indeed been validated as a strong predictor of sepsis in emergency
department patients with nontraumatic undifferentiated hypotension [47]. In ventilated
patients, the IVC can appear relatively distended, even in the presence of significant
intravascular volume depletion; indeed, patients on positive pressure ventilation require
abnormally high central venous pressures to attain normal cardiac filling. Thus, while a
well-filled IVC (a negative test) does not exclude fluid responsiveness in ventilated patients, the
presence of a collapsed IVC (a positive test) is an even stronger sign of volume depletion in this
group than in spontaneously breathing patients [33, 46, 48, 49]. Although popular and
frequently observed, conflicting results exist concerning the reliability of IVC respiratory
variations in spontaneous respiration (“IVC collapsibility index”) as diagnostic of hypovolaemia
or fluid responsiveness, especially if values in the grey zone of its accuracy (20–40%
collapsibility) are found [34, 50]. However, as the IVC collapsibility index approaches the
extremes (complete collapse or plethora with complete absence of respiratory variation), the
clinician can be increasingly confident in these findings. In the context of the management of
the critically ill, this is a useful quality in a test: in haemodynamically unstable patients, extreme
derangements are ones that need to be addressed first and most quickly. In passive
mechanically ventilated patients, there is some evidence that there is a correlation between an
IVC distensibility index value of >18% (with inspiration) and fluid responsiveness [51–53]. In
septic shock, some empirical criteria may suggest a low peripheral vascular tone as the
prevailing pathophysiology: persistence of hypotension despite adequate pre-load and preserved
(or pharmacologically normalised) biventricular systolic function, and small LV end-systolic
dimensions with normal end-diastolic size (meaning ejection against low resistances) [54].
Indeed, the addition of LUS and deep venous US to FoCUS in the approach to the patient
presenting with an undifferentiated shock state has proven to simplify and accelerate the
diagnostic process [56].
Cardiac arrest
Recent international recommendations advocate that FoCUS should become the standard
of care in the management of cardiac arrest [1]. Although not yet fully acknowledged by
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current resuscitation guidelines, several observational trials have shown that the use of
FoCUS in cardiac arrest identifies the presence or absence of organised myocardial
mechanical activity [57, 58], rapidly detects a potentially treatable cause [5, 8], changes
management [8] and predicts outcome [59]. FoCUS goals in cardiac arrest resuscitation
include the following three steps [60].
The first step is to determine whether the patient’s arrest is due to a dysrhythmia. If this is
the case, it is necessary to establish whether it is a shockable or nonshockable rhythm. This
can usually be done on the basis of the electrocardiac monitor (although in some cases
FoCUS has been reported as useful in differentiating asystole from fine ventricular
fibrillation) [61]. If the patient has organised cardiac electrical activity and no pulses,
FoCUS is then used to determine whether there is coordinated mechanical cardiac activity
associated with the rhythm. If there is not, the diagnosis is electromechanical dissociation
(frequently erroneously referred to as “true” pulseless electrical activity (PEA)). The
presence of ventricular contraction in a pulseless patient identifies the important finding of
PEA with organised myocardial mechanical activity, i.e. profound hypotension with an
impalpable pulse (sometimes mistakenly referred to as “false” PEA).
Third, FoCUS allows earlier detection of recovery of cardiac activity than simple pulse
palpation. In addition, immediately following the return of spontaneous circulation, FoCUS
can be used to monitor cardiac function and volume status, to guide resuscitative measures
and to evaluate their impact. As such, it is currently recommended as an integral part of
post-resuscitation care [63].
As noted, FoCUS should not delay electrical treatment of ventricular arrhythmias. FoCUS
should be performed in cardiac arrest in an ACLS-conforming manner (figure 3) by a
FoCUS-trained sonologist as part of a team using rehearsed protocols that integrate FoCUS
within the ACLS algorithms and coordinate cardiac US examinations with pulse checks [1, 5].
Trauma
Since early studies in 1992 showing decreased mortality with the use of FoCUS in
penetrating cardiac injury [64], a large body of literature has accumulated, making FoCUS
an integral part of the evaluation of trauma patients. FoCUS for the screening of
haemopericardium in penetrating and blunt chest injury is a component of the Advanced
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Trauma Life Support (ATLS) training and practice, as part of the Focused Assessment with
Sonography in Trauma (FAST) examination [65]. FoCUS can also be used to identify
blood-loss-associated hypovolaemia [49]. Even with a negative FAST examination,
identification of a “flat IVC” and small hyperdynamic ventricles is strongly predictive of
haemorrhagic shock that will respond to volume replacement [66] and has been associated
with better fluid management of trauma patients in shock [67]. It should be remembered
that the IVC evaluation may be normal (along with the absence of clinical signs) in milder
degrees of haemorrhage [68]. Finally, the detection of depressed myocardial contractility in
a patient without evidence of chronic cardiac disease may suggest the presence of
myocardial contusion, prompting testing for serum markers, monitoring for arrhythmias
and comprehensive echocardiography. In contrast, the presence of signs of pre-existing
cardiac disease may add information relevant for patient management.
Dyspnoea/respiratory failure
FoCUS also provides useful information in patients presenting with acute respiratory
symptoms, often by triggering a comprehensive echocardiographic assessment. The cardiac
sonologist should beware of ruling out a cardiogenic origin of pulmonary oedema based on
the finding of normal LV contractility, since a significant proportion of cases of cardiogenic
pulmonary oedema are due to diastolic dysfunction and/or acute valvular disease. Readily
identifiable sonographic findings that might suggest acute valvular disease (and occasionally
diastolic dysfunction) have been described in a previous section. The identification by
FoCUS of significant cardiac derangements that could be responsible for a patient’s acute
dyspnoea/respiratory failure should prompt consideration of a comprehensive assessment of
cardiac haemodynamics beyond the scope of the FoCUS examination.
Dyspnoea is a class I indication for comprehensive echocardiography [69, 70]. FoCUS should
aim to identify: 1) signs of pre-existing cardiac disease (including findings suggestive of
major valvular abnormalities) that might indicate decompensation of chronic heart failure,
2) global LV systolic dysfunction, potentially associated with acute pulmonary oedema,
3) acute cor pulmonale, suggesting a potential pulmonary embolism or decompensated
pulmonary hypertension, and 4) pericardial effusion and tamponade. For most clinician
sonologists in this clinical setting, FoCUS will be complemented by focused sonography of
the lungs and peripheral deep venous system, allowing rapid identification of pleural
effusions, pulmonary oedema, pulmonary consolidations and infiltrates, and proximal deep
venous thrombi with probable greater accuracy than FoCUS used in isolation [71].
Chest pain
FoCUS has a limited role in the assessment of life-threatening chest pain syndromes in
comparison with comprehensive echocardiography [19]. As noted earlier, FoCUS can rule
out haemodynamically significant pulmonary embolism in the absence of acute core
pulmonale [42]. Conversely, if acute cor pulmonale is identified, pulmonary embolism is
significantly more likely but needs to be confirmed by the demonstration of right heart
thrombi or by carrying out a pulmonary CT angiogram. The circumstances where the
contribution of FoCUS to the diagnosis of thromboembolic disease is significant are
therefore those where the presentation symptom is shock, rather than chest pain. Acute
pulmonary embolism in the stable patient may be diagnosed in the presence of symptoms
and signs and by identification of proximal deep vein thrombosis [72]. An angio-CT scan
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FOCUSED CARDIAC ULTRASOUND | G. VIA ET AL.
remains the diagnostic tool for suspected pulmonary thromboembolism, and specific
treatment for this should be started based on a FoCUS finding of acute cor pulmonale only
in patients who are too unstable to be transferred for a CT scan.
Likewise, the role of FoCUS in the diagnosis of myocardial ischaemia is negligible: accurate
segmental wall motion and thickening analysis is a highly technically demanding skill,
beyond the scope of FoCUS [1]. Finally, in patients with suspected thoracic aorta
dissection, FoCUS may identify a mobile flap within the aorta (high PLAX view), or raise
the clinical suspicion for the disease by detecting pericardial and/or pleural effusion, and/or
a dilated aortic root (>4 cm) [73]. Neither FoCUS nor comprehensive transthoracic
echocardiography is sufficiently sensitive to exclude aortic dissection, for which CT
angiography or transoesophageal echocardiography is needed.
This can occur when patients receive inotropic pharmacological or mechanical support
(including positive end-expiratory pressure for the LV).
Assessment of volume status with FoCUS (based purely on the 2D modality) provides only
a good rule-in criterion for hypovolaemia: the hyperdynamic pattern with small ventricles
is specific to severe hypovolaemia but is poorly sensitive [74].
IVC respiratory variability is determined not only by central volume status but also by the
magnitude of the patient’s inspiratory efforts. In patients with respiratory distress, this may
be misleading. For example, pronounced IVC inspiratory size reductions (“IVC collapse”)
may coexist with systemic venous congestion and may be related to vigorous inspiratory
efforts rather than volume responsiveness; thus, end-expiratory IVC size (large in this case)
should never be disregarded [75].
A dilated, failing RV with signs of pressure overload should not be equated with massive
pulmonary embolism. FoCUS allows diagnosis only of acute cor pulmonale and not of
embolic disease, unless in-transit thrombi are detected in the right heart cavities. Chronic
cor pulmonale should always be ruled out.
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A large pericardial effusion does not necessarily have haemodynamic effects if the fluid
accumulates gradually. Tamponade is related to pericardial pressure (evidenced by clinical
signs associated with US signs of cardiac compression), rather than to the size of the
effusion.
In a trauma patient, it should not be assumed that free pericardial fluid is blood.
Pericardial fluid of nontraumatic origin may coexist.
The cardiogenic origin of a pulmonary oedema should not be ruled out based on the
finding of normal LV contractility. A relevant proportion of cardiogenic pulmonary
oedemas in fact develop in the absence of systolic LV dysfunction (e.g. diastolic
dysfunction, acute valvular disease).
Recording and storage of the results of FoCUS studies should be carried out for subsequent
analysis, review and comparison of findings [1, 2]. Digital image and video archiving serves
multiple objectives relevant to quality assurance of FoCUS: information sharing among
clinicians, documentation of changes in condition, specialist case review, clinician feedback,
medico-legal documentation, quality improvement and education. Video archiving is preferred
for almost all examinations in which measurements and analysis of still images (e.g. by
M-mode) are needed. Practitioners should be encouraged to scan through all relevant planes
during their video recordings (e.g. from the apex to the base on PSAX views).
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Figure 4. Example of a simplified FoCUS report. FoCUS reports should ideally be organised in different
sections, including demographics data, minimal clinical data, findings, summary, date and signature. The
description of findings and the summary should be consistent with the goals and targets of FoCUS.
Documentation of decision making based on FoCUS, including further diagnostic testing and therapy, may
be included in the report or in the body of the patient’s record. PEA: pulseless electrical activity; MV:
mechanical ventilation; CPAP: continuous positive airway pressure; PEEP: positive end-expiratory pressure;
Vt: tidal volume; FEEL: Focused Echocardiography Evaluation in Life support; SLAX: subcostal long-axis;
SSAX: suprascapular and axillary nerve; SIVC: subcostal inferior vena cava; PLAX: parasternal long-axis;
PSAX: parasternal midpapillary short-axis; A4CH: apical four-chamber; A2CH: apical two-chamber; ALAX:
apical long axis; LA: left atrium; RWMA: regional wall motion abnormalities; LV: left ventricle; RA: right
atrium; IVC: inferior vena cava; RV: right ventricle. Reproduced from [1] with permission.
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Conclusion
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| Chapter 15
Newborns, infants and children
Francesco Raimondi1, Fiorella Migliaro1, Antonietta Giannattasio1,
Letizia Capasso1, Claudia Lucia Piccolo2, Margherita Trinci3,
Vittorio Miele4 and Stefania Ianniello3
Chest US is a rapidly growing field in the imaging of the developing human, and is based on
the same images and artefacts employed by adult emergency physicians. Solid evidence has
recently been published about the US features of respiratory distress syndrome, transient
tachypnea of the neonate and meconium aspiration syndrome. Tension pneumothorax can
be accurately diagnosed with US and rapidly treated. Research into endotracheal tube
positioning and chronic lung disease is ongoing. Semiquantification of the US signal has
generated an intriguing comparison with the conventional radiogram with regard to the role
of the first-line technique in several respiratory diagnoses. In the infant and the child, LUS
can be applied in the work up of lung consolidations and several groups have investigated its
accuracy in diagnosing pneumonia and bronchiolitis. Further paediatric applications include
the study of chest wall masses and pleural effusions; focused assessment with sonography for
trauma protocol remains an important area of current investigation.
Cite as: Raimondi F, Migliaro F, Giannattasio A, et al. Newborns, infants and children. In: Laursen CB,
Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory
Society, 2018; pp. 206–225 [https://doi.org/10.1183/2312508X.10007217].
Adult emergency medicine physicians first applied LUS to the clinical field. As LUS
semiology is almost the same in patients of any age, neonatologists and paediatricians have
quickly learned how to apply it and are now using it with remarkable success. It is a novel
point-of-care, easy-to-learn imaging technique with the significant advantage of sparing the
developing human from exposure to ionising radiation. ESCOURROU and DE LUCA [1]
provided a convincing demonstration of this in an elegant report. By instituting a LUS
protocol in their French neonatal intensive care unit (NICU), the number of CXR per baby
in 2014 was roughly half that in 2012 and the mean radiation dose per baby decreased
from 180 to 60 EGy.
1
Division of Neonatology, Dept of Translational Medical Sciences, Università “Federico II”, Naples, Italy. 2Dept of Medicine and Health
Sciences, University of Molise, Campobasso, Italy. 3Emergency Radiology Unit, Dept of Diagnostic Imaging, S.Camillo-Forlanini
Hospital, Rome, Italy. 4Dept of Emergency Radiology, Azienda Ospedaliero Universitaria Careggi, Florence, Italy.
Correspondence: Francesco Raimondi, Dept of Translational Medical Sciences, Università “Federico II” di Napoli, via Sergio Pansini 5,
I-80131 Naples, Italy. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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This chapter provides a concise review of current applications in neonatal and paediatric
respiratory medicine, with emphasis on the strength of the evidence and areas of future
investigation. The fact that around half of the studies discussed were published in the last
4–5 years shows how rapidly interest is growing around the diagnostic potential of LUS in
the newborn infant.
The normal lung transitions at birth from fluid to air content. A recent study by BLANK
et al. [2] used LUS to document the rapid liquid clearance from the lungs in a cohort of
mostly term infants. All infants had an established pleural line at the first examination
(median 2 (range 1–4) min). Only 14% of infants had substantial liquid retention 10 min
after birth. 49%, 78% and 100% of infants had completed airway liquid clearance at 2, 4
and 24 h, respectively. In a smaller, single-centre study, MARTELIUS et al. [3] showed a
significant difference in postnatal liquid absorption attributable to the mode of delivery; in
particular, there was a significantly higher fluid retention at 3 h in term infants born by
caesarean section compared with vaginal delivery. The potential of LUS as a noninvasive
technique to anticipate the need of respiratory support after birth was assessed by RAIMONDI
et al. [4] in a cohort of 154 late preterm and term babies who underwent sequential LUS.
Images were classified as type 1 (white lung image), type 2 ( prevalence of comet-tail
artefacts or B-lines) and type 3 ( prevalence of horizontal or A lines) profiles. Shortly after
birth, 14 neonates were assigned to the type 1, 46 to the type 2 and 94 to the type 3
profiles. Within 36 h there was a gradual shift from types 1 and 2 to type 3. LUS had a
high accuracy in predicting NICU admission, with a sensitivity of 77.7% and a specificity of
100%. This information may be particularly valuable to healthcare workers at level 1 birth
centres with difficult access to intensive care.
In the NICU
LUS can also be useful in the diagnosis of RDS complications. A prospective study
conducted by LOVRENSKI [11] included 120 preterm infants with clinical and radiographic
signs of RDS. Within the first 24 h of life, LUS was performed using both a transthoracic
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and a transabdominal approach; sequential scans were then performed. In the 47 detected
pulmonary complications of RDS (including haemorrhage, pneumothorax (PTX),
pneumonia, atelectasis, bronchopulmonary dysplasia), comparisons between LUS and CXR
were made. In 45 instances, the same complication was diagnosed with LUS as with CXR,
indicating that this method has a high reliability in premature infants with RDS.
CATTAROSSI et al. [12] made the interesting observation that, unlike conventional CXR, the
LUS scan is not modified shortly after surfactant administration. However, in a subsequent
small study of 12 preterm infants, LOVRENSKI et al. [13] proposed a grading system for RDS
evolution after surfactant replacement.
Investigating LUS as a monitoring tool for RDS course is an ambitious yet achievable goal
and there is a considerable amount of work still to be done. For instance, no solid
longitudinal data is currently available showing the long-term evolution of neonatal RDS,
and we do not know whether stratification by gestational age of LUS scan might yield
useful information.
Tension pneumothorax
Although individual case reports and single-centre series were already available [16, 17], in
2016, RAIMONDI et al. [18] led the first international, prospective study on tension PTX in
the neonate. Taking the conventional chest radiogram as a reference standard in a series of
42 infants presenting with significant sudden desaturation and bradycardia, RAIMONDI et al.
[18] showed that LUS has an absolute diagnostic accuracy for tension PTX, outperforming
the clinical diagnosis. After sudden decompensation, a LUS scan was performed in a mean
±SD time of 5.3±5.6 min, in comparison with the 19±11.7 min required for a chest
radiography. Emergency drainage was performed after US but before radiography in
nine cases.
Neonatal pneumonia
In infectious pneumonia, LUS findings include large areas of lung consolidation with
irregular margins and air bronchograms, pleural line abnormalities, and interstitial
syndrome. These features assured absolute diagnostic accuracy for LUS in the study by LIU
et al. [19]. Investigating 40 neonates with symptomatic pneumonia and 40 healthy controls,
the authors failed to provide precise masking details. A different approach has been
adopted in studies investigating the aetiology of neonatal respiratory distress with LUS.
This was the case in a study of 63 symptomatic infants performed by RACHURI et al. [10],
which found six pneumonia cases. In a large cohort of 3405 Chinese neonates (2658 of
whom were symptomatic) screened with LUS, 1016 received an US diagnosis of pneumonia
[20]. In addition, 1692 cases were examined using LUS and chest radiography for the first
time within 48 h of admission. Among 81 cases who underwent CXR and who did not
receive a diagnosis of lung disease, 32 had clinical and US evidence of pneumonia. The fact
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Functional LUS
As previously mentioned, LUS has been used to provide detailed nosographic description.
However, a functional approach may be adopted by linking a specific LUS profile to a
clinical decision.
RAIMONDI et al. [24] investigated a cohort of 54 preterm neonates admitted to the NICU
with moderate respiratory distress who were stabilised on nasal continuous positive airway
pressure for 120 min. LUS was performed and blind classification to types 1 (white lung), 2
( prevalence of B-lines) or 3 ( prevalence of A-lines) was carried out. An experienced
radiologist blinded to the infant’s clinical condition examined and graded the chest
radiograph. The study’s primary outcome was the accuracy of bilateral type 1 in predicting
intubation within 24 h of scanning. A secondary outcome was the performance of the
highest radiographic grade within the same time interval. Type 1 lung profile showed a
high diagnostic accuracy with a sensitivity of 88.9% and a specificity of 100%, while CXR
had a sensitivity of 38.9% and a specificity of 77.8%
The advantages of LUS in predicting the failure of noninvasive respiratory support were
later confirmed by two other clinical research teams.
BRAT et al. [25] correlated a LUS score with several oxygenation parameters (transcutaneous
partial pressure of oxygen to fraction of inspired oxygen ratio, alveolar–arterial gradient,
oxygenation index, arterial to alveolar ratio) and with the administration of exogenous
porcine surfactant. Among the 130 neonates included in this study, the LUS score was
significantly correlated with all indices of oxygenation, independent of gestational age. The
LUS score was a better predictor of the need for surfactant in preterm babies with a
gestational age of <34 weeks (area under the curve (AUC) 0.93; 95% CI 0.86–0.99; p<0.001)
than in term and late preterm neonates with a gestational age of ⩾34 weeks (AUC 0.71;
95% CI 0.54–0.90; p=0.02); the AUC for these two gestational age subgroups are
significantly different ( p=0.02). In babies with a gestational age of <34 weeks, a LUS score
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cut-off of 4 predicted surfactant administration with 100% sensitivity and 61% specificity,
yielding a post-test probability of 72%.
The research from these three groups of investigators demonstrates LUS to be a rapid,
repeatable, radiation-free tool that supports the neonatologist in the difficult decision of
whether to intubate a patient.
Miscellaneous
Preliminary reports on possible LUS applications range from rare conditions, such as
localised interstitial emphysema [28], to common diseases, such as bronchiolitis [29, 30]
and atelectasis [31, 32].
Some adult cardiologists and emergency medicine physicians have integrated LUS data into
their cardiac and haemodynamic US evaluation [33]. Neonatologists are following in this
direction. RODRÍGUEZ-FANJUL et al. [34] investigated the accuracy of LUS in assessing
pulmonary overflow in 51 infants with congenital heart disease. Neonates were classified into
two groups depending on their predisposition to developing pulmonary overflow as evaluated
by the abundance of B-lines. The results were compared with physical examination, CXR and
echocardiography. No differences in the abundance of B-lines were present between the
groups; however, those with a cardiac defect with a tendency to develop pulmonary overflow
had a higher B-line score after 72 h (p<0.05), and showed a good correlation with
echocardiography findings and a better sensibility than physical examination and CXR.
Research perspectives
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evidence has been published, the search for a common language is mandatory. Large clinical
studies from China have shown that no US sign is typical of a neonatal respiratory disease
[7, 20]. It is also difficult to trace a combination of US features that univocally depict a
respiratory condition across all published studies. Part of the problem stems from the
different tools (e.g. the types of probes and machines) and examination techniques
(transthoracic versus transabdominal approach; number and type of US views) in use. Most
of the available evidence comes from single-centre studies, often with poor consideration for
masking and sample power procedures. There is great need for sufficient methodological
stringency to overcome the still widespread clinical and forensic concerns about LUS.
To provide a better understanding about the influence of these variables and to promote
collaborative studies, we have founded NeoLUS (Neonatal LUS for the neonate and the
small infant; https://www.facebook.com/groups/1493243264284547/), a dedicated research
network currently counting 140 members around the world.
In the near future, both standardisation and accurate quantification may become possible
with the help of computer-assisted image analysis techniques supporting LUS. This has
already been attempted in adults using the grayscale analysis techniques [36].
A different and more refined strategy of computer-aided analysis has recently been
proposed by VEERAMANI and MUTHUSAMY [37] using machine learning image classification.
This sophisticated technology has already been shown to be very effective when analysing
foetal lung to predict neonatal respiratory morbidity [38].
Conclusion
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For a long time, US has been performed solely to recognise pleural effusion in the thorax.
This is because the physical limitations of the normal aerated lung and thoracic cage
strongly affected the application of US in the diagnosis of thoracic disease [39]. In recent
years, lung evaluation has become feasible owing to advances in technology; the use of
multifrequency probes, together with the application of tissue-harmonic imaging, lead to
improved spatial resolution and tissue penetration, as well as a specific focus on decreasing
ionising radiation [40–42]. Children are at least four times more sensitive to ionising
radiation than adults because of a longer life expectancy and a faster cell rate division, thus
increasing the risk of the development of radiation-induced cancer. LUS, which lacks
ionising radiation, plays an essential role in the implementation of the ALARA (as low as
reasonably achievable) principle, which aims to reduce exposure to ionising radiation using
the imaging technique with little to no radiation [43–45].
In infants and children, TUS becomes useful in a variety of settings, especially in situations
of clinical and radiographic concern, as well as superficial lumps and bumps, the
characterisation of structures such as the thymus, and diaphragmatic motion, because of
the superior acoustic window and the relative paucity of adipose tissue compared with
adults [46, 47]. Its application in the paediatric lung assists children with a small thoracic
width and lung mass, allowing easier detection of lung anomalies with LUS because of a
more rapid involvement of the pleura [48].
Technique
In the typical clinical setting, LUS is usually preceded by a chest radiograph that may raise
several clinical questions relating to lung opacification, driving the examination to the
appropriate anatomical region.
The transducer is chosen according to patient size and the depth of penetration; infants
are usually studied with high-frequency probes, whereas older children are studied
with lower-frequency probes. The classic acoustic windows are the supraclavicular,
suprasternal, parasternal, intercostal, subxiphoid and transdiaphragmatic windows in
longitudinal and transversal sections. The young patient is usually studied in the supine,
lateral decubitus or sitting position, depending on their clinical condition and the clinical
question [49].
The anterior chest wall and mediastinum are well depicted through sternal and
costochondral cartilages because of the low ossification of the thoracic cage and the
relatively large thymus [41, 42].
As regards LUS physics and semeiotics, we refer to what is explained elsewhere in this text.
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Lung evaluation
LUS is mandatory in this setting because it can characterise pleural effusion, and
discriminate between lung consolidation and cancer by identifying air bronchograms and
pulmonary vessels not seen in tumours or pleural effusion.
The most common neoplastic causes of white hemithorax at this age are teratomas and
lymphomas, with the latter being the most common cause of neoplastic pleural effusion in
children. Pleural effusion can also be caused by pleural metastases from neuroblastoma,
rhabdomyosarcoma and Wilms’ tumours. In the presence of a white hemithorax with a
neoplastic cause, it is always is useful to explore the chest wall, as rib involvement is
extremely common (in Ewing tumours, for example). Soft tissue neoplasms can appear
with a large white hemithorax, such as rhabdoid tumours and lung metastases [57, 58].
According to the guidelines of the World Health Organization (WHO) [63] and other
societies, CAP diagnosis and classification is clinical and chest radiography is only
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a) b)
c)
Figure 1. A 9-year-old boy presenting with a) a left white hemithorax without mediastinal displacement. b) A
CT scan with contrast media injection shows a complicated pneumonia, characterised by thickening of
visceral and parietal pleura, which enhanced after contrast media injection, with fluid in between, and
collapse of the adjacent parenchyma. c) LUS shows a corpuscolated echogenic pleural effusion along with
atelectasis of the adjacent lung.
recommended in complicated and severe cases [59]. Nevertheless, many physicians depend
on it for a definitive diagnosis, leading to rising concerns about its application. Exposure to
ionising radiation increases carcinogenic risk; moreover it is characterised by lack of patient
collaboration, a low ability to reproduce and a high interobserver and intra-observer
variability, owing to consolidations affecting hidden areas (such as the retrocardiac region
and lung bases) and to interstitial disease. Therefore, in recent years, doubts have been
raised about its application as a routine technique in children with suspected CAP and its
follow-up [64, 65].
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a) b) c)
f)
d) e)
Figure 2. A 13-year-old boy presenting with fever and cough. a) CXR performed at admission in anterior–
posterior projection shows an extensive upper right lobe opacification. b and c) LUS performed
simultaneously with CXR shows a well-defined round consolidation with an “air bronchogram”. d–f ) A CT
scan performed the day after confirmed LUS findings, enhancing the inner features of the disease, as well
as the presence of the air bronchogram. This was a case of Haemophilus influenzae pneumonia.
methods but that LUS classified more cases as alveolar disease compared with chest
radiography [73]. A more recent study performed by IANNIELLO et al. [74] on 84 consecutive
children with clinical signs of pneumonia who underwent both LUS and CXR,
demonstrated that LUS was superior in the recognition of pulmonary consolidations,
especially for CXR-occult findings and for early diagnosis of pleural effusion. Furthermore,
in follow-up, LUS allowed early recognition of complications and avoided additional
radiation exposure.
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a) b) c)
d) e) f)
Figure 3. The patient discussed in figure 2 underwent serial imaging follow-up. a) LUS and b) CEUS show
the parenchymal disease associated with the air bronchogram. With CEUS (b) it is possible to observe
normal lung enhancement. c) CXR shows substantial resolution of the disease, while d) at LUS it is possible
to recognise a significant reduction in the size of the lung consolidation, with a persistent “parallel”
bronchogram suggesting a residual minimal atelectasis component. Both e) CXR and f ) LUS confirm
resolution of the disease.
LUS can detect the interstitial involvement of a flogistic condition as multiple B-lines,
without any consolidation, as IANNIELLO et al. [74] demonstrated.
Pleural evaluation
Pleural effusion
US has always been widely accepted as an effective tool for the detection and
characterisation of pleural effusion. CXR cannot recognise pleural effusions <200 mL in the
lateral sulcus on a frontal radiograph, and <50 mL in the posterior sulcus on a lateral
radiograph, whereas LUS can detect pleural effusions of 3–5 mL (figures 6 and 7). LUS can
also define its inner features, such as the presence of echoes which suggests an exudative
process, whereas an anechoic collection can be either exudative or transudative [81–83].
The presence of pleural thickening or nodularity may suggest inflammation or a neoplastic
cause. The presence of loculations within the pleural fluid may help to decide between
drain placement, with or without fibrinolytic agents, or video-assisted thoracoscopy
[84, 85].
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a) b)
c) d)
2
1
Figure 4. An 8-year old boy presenting with cough, fever and thoracic pain. a and b) LUS shows a
well-defined wide pneumonic consolidation. c) LUS follow-up after therapy shows a significant reduction in
size of the pneumonic consolidation, though it is still present. d) A further LUS follow-up (14 days later)
shows the pneumonic consolidation’s disappearance, with regular A-lines.
Pneumothorax
Several authors investigated the accuracy of US in the detection of PTX in trauma patients
and in those undergoing interventional procedures, such as lung biopsy [86–89]. A
meta-analysis by DING et al. [90] compared the use of antero-posterior chest radiograph
with transthoracic US for the diagnosis of PTX; pooled sensitivity and specificity were 88%
and 99%, respectively, for US, and 52% and 100% for chest radiograph.
In patients with major trauma, first-line examination is generally performed with a FAST
(focused assessment with sonography for trauma) protocol able to depict intraperitoneal
collections of free fluid and indirect signs of solid organ injury that require urgent surgical
exploration [88]. After the initial FAST survey, the US examination may be extended to the
thorax to rule out haemothorax and PTX; when extended to the thorax, this examination is
known as extended-FAST (e-FAST). In a trauma setting, the FAST examination is usually
performed in hypotensive and haemodynamically unstable patients because it helps to
determine whether immediate surgery is needed; in the presence of intrabdominal free
fluid, the probability of death increases by ∼1% for every 3 min that elapses before surgical
exploration [89]. In all unstable patients, in addition to the FAST acquisition, a right and
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a) b)
c) d) e)
LOBO MEDIO
LOBO MEDIO
LOBO MEDIO
Figure 5. A 5-year-old girl presenting with fever and cough. a and b) CXR shows a medium lobe
consolidation. c–e) LUS shows c) multiple B-lines, expression of interstitial involvement, and d and e) a
wide medium lobe consolidation with a fluid bronchogram, appearing as an echo-poor tubular structure,
with hyperechoic walls, along the airways.
left longitudinal anterior thoracic view can be quickly obtained to rule out pleural effusion
and PTX. LUS has proved to be a feasible technique that can rapidly detect occult PTX in
adults, avoiding serious potential consequences such as tension PTX, especially in
mechanically ventilated patients. By applying harmonic imaging, which reduces artefacts
and enhances resolution, some useful features may be amplified, such as comet tail
artefacts, which are bands of reverberating echoes normally located at the junction between
the pleura and the aerated lung [91, 92]. Their absence can aid confirmation, with high
confidence, of PTX; the location of the lung point in the supine patient allows for
evaluation of the extent of PTX [66, 70, 93]. LUS application in the emergency setting is
rarely performed in children (only 15% of children’s hospitals in the USA) because of a
reported limited sensitivity [93].
Mediastinum evaluation
With LUS, the anterior and middle mediastinum can be easily studied; in particular, the
evaluation of normal thymus tissue is a typical indication for US. The thymus normally
appears as a homogeneous organ with echogenic strands, which does not press on adjacent
structures [39, 47]. In the presence of a large mediastinal mass in a healthy child, a
massively enlarged thymus, or thymus hyperplasia, should be considered [94]. US is usually
enough to reach a diagnosis, although a biopsy is sometimes required to exclude a
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a) b) c)
d) e) f)
Figure 6. Two cases showing the capability of LUS to estimate the size of the effusion, differentiate free
from loculated pleural fluid, and evaluate the echogenicity of the fluid. a) CXR shows a wide left hemithorax
opacification. b and c) LUS depicts a large amount of highly corpuscolated pleural effusion in a patient
affected by a Streptococcus pneumoniae-induced disease. d) CXR shows a large opacification of the right
hemithorax. e and f ) LUS depicts a well-organised pleural effusion associated with atelectasis of the lower
lobe (white arrow).
neoplastic cause. As previously mentioned, the most common causes of mediastinal masses
are lymphoma and leukaemia [41, 86, 95]. US performed with the child in an upright
position can confirm the mass, evaluate adjacent vascular structures and guide biopsy.
Typical signs of infiltrating thymic tumours might be suggested by the loss of the normal
internal architecture or adjacent confluent nodular soft tissue. Focal masses appear as
anechoic cysts seen incidentally or in the setting of HIV or Langerhans’ cell histiocytosis.
Solid masses, such as germ cell tumours, can be suspected by the presence of calcification
or fat; a CT or MRI is necessary for more definitive tissue characterisation [96]. Masses in
the middle mediastinum may appear as cystic lesions with or without internal debris,
suggesting foregut duplication cysts. Among this spectrum of diseases are: bronchogenic
cysts, which can be obscured in the subcarinal region but can be visualised if they are
located in the paratracheal region; and oesophageal duplication cysts, which can be
identified if they extend above the carina. Neuroenteric cysts, typically arising in the
posterior mediastinum, can extend anteriorly and become more visible; they are typically
associated with vertebral anomalies on a chest radiograph. Lymphatic malformations also
appear cystic and can invaginate into all compartments of the mediastinum. Solid lesions of
the middle mediastinum are secondary to nonspecific lymphadenopathy.
Diaphragmatic evaluation
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a) b)
c) d)
Figure 7. A 4-year-old girl with cough and fever. a) CXR shows an upper right lobar consolidation. b–d) LUS
reveals a small amount of pleural effusion, not detected by CXR, and some B-lines. It is important to
recognise even a small amount of pleural effusion, as it will be infected very frequently.
measure the diaphragmatic excursion, with normal excursion considered greater than 4 mm
and normal symmetric motion between the leaflets of the diaphragm demonstrating less
than a 50% difference [97–99]. The subcostal window is used to evaluate the motion of
each side in the coronal plane. Normal excursion will be toward the transducer with a
subxiphoid approach.
TUS is useful in the assessment of anterior chest wall masses, also characterised by
deformity of the ribs in the majority of cases, as SUPAKUL et al. demonstrated [100]. In
a cohort of 16 patients presenting with a firm anterior chest wall mass, having
undergone prior chest examinations, US showed an angular deformity of the costal
cartilage in the majority. However, rib tumours may occur, even if rare. Therefore,
recourse to second-line imaging techniques is mandatory. Imaging findings of these
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As with chest wall masses, US plays a primary role in the evaluation of chest wall infection
[102, 103]. In cases of cellulitis, one may see a diffuse increased echogenicity; tenderness
over a normal-appearing costal cartilage might represent costochondritis in the appropriate
clinical setting. Subperiosteal fluid collections or fluid adjacent to bone might be seen in
the setting of osteomyelitis. As for as vascular lesions, while the sonographic appearance of
haemangioma is quite heterogeneous and nonspecific, a vessel density greater than 5 vessels
per cm2 combined with a maximum systolic Doppler shift of greater than 2 kHz has a
specificity of 98%. In contrast, other vascular tumours, such as hemangioendotheliomas,
tufted angiomas and infantile myofibromatosis may have a similar appearance, requiring
other imaging modalities to be utilised. Venous malformations can present as sponge-like
diffuse masses with internal anechoic tubules demonstrating venous flow; arteriovenous
malformations appear as a tangle of arteries and veins without associated mass.
Mesenchymal hamartoma, desmoid tumours and lipomas or lipoblastoma might not be
easily diagnosed, requiring CT or MRI when in doubt.
In the presence of aggressive chest wall lesions, US may show abnormal thickening of ribs
and sternal cortex as well as destruction, with an adjacent soft tissue mass.
Rib fractures are easily detectable by means of US; in older children, sonography can detect
and diagnose superficial fractures in the setting of a previous trauma [104–106].
Research perspectives
Some studies have recently focusing on the capability of LUS to quantify fluid overload in
infants and children receiving dialysis. Optimising a target weight in paediatric patients in
dialysis is still an important clinical challenge since fluid overload is a well known
independent risk factor; such patients in dialysis often suffer with hypertension and left
ventricular hypertrophy [107]. In adults, quantification of B-lines by LUS correlates well
with extravascular lung water; they usually manifest before clinical signs and symptoms of
fluid overload. ALLINOVI et al. [108] found that the linear correlation of B-lines score with
fluid overload was stronger in patients with acute kidney injury than in those affected by
end-stage renal disease, perhaps because in patients with the latter condition it is more
difficult to find a gold standard dry weight as opposed to patients with acute kidney
disease, in whom baseline weight is determined following resolution of fluid overload. The
authors demonstrated a reduction in B-line scores during haemodialysis with ultrafiltration.
These findings corroborate the hypothesis that LUS can guide progressive reduction in
post-dialytic weight to assess patients’ baseline fluid status.
Conclusion
LUS can be considered a valuable imaging technique in a variety of clinical settings: it can
be performed in conjunction with chest radiography to investigate a white hemithorax,
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being able to delineate underlying causes in such situations, or guiding the diagnostic
work-up in those conditions requiring second-line examinations.
Several studies have demonstrated its capability to diagnose CAP in children with suspected
pneumonia, aiding reduction in exposure to radiation; its application in the emergency
setting, as the final stage of FAST examination, has found great consensus in adult
populations; further studies to assess the same effectiveness in children are needed.
LUS has proven to be very useful in the assessment of chest wall masses, at least to
understand the nature of a lesion; in the presence of any signs of malignancy, an additional
imaging modality (CT or MRI) is required.
Sonography is a very adaptable technique, with a wide range of application in the right
hands; the sonographer has to be skilled enough to take advantage of its many benefits,
taking into account that US applied on the thorax has a very fast learning curve with
respect to other US examination skills.
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| Chapter 16
Ultrasound-guided procedures
John P. Corcoran1,2, Mark Hew3, Fabien Maldonado4 and
Coenraad F.N. Koegelenberg5,6
Cite as: Corcoran JP, Hew M, Maldonado F, et al. Ultrasound-guided procedures. In: Laursen CB, Rahman
NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society,
2018; pp. 226–243 [https://doi.org/10.1183/2312508X.10007317].
A s the technology has become more portable and reliable over the past two decades,
TUS has become an indispensable tool for any physician managing patients with
respiratory disease. Nowhere is this more evident than in the field of interventional
pulmonology and pleural procedures, with post-graduate training documents increasingly
focused on competency in this area of clinical practice [1–5]. The increasing familiarity of
physicians with TUS means the range of pleural interventions being offered to patients has
grown rapidly in recent years [6, 7], and has allowed physicians to take control of
a diagnostic and therapeutic pathway that might previously have required the support of a
radiologist or thoracic surgeon [8]. As a result, procedures are now being performed in
a variety of settings around the hospital with increasing frequency, and on both an in- and
outpatient basis.
It could be argued that long-recognised concerns around patient safety in the context of
pleural intervention have been the single greatest driving force behind the widespread
uptake of TUS by physicians [9, 10]. At this point in time, the evidence that the
appropriate use of TUS reduces the risk of iatrogenic complications from pleural
1
Interventional Pulmonology Service, Dept of Respiratory Medicine, Plymouth Hospitals NHS Trust, Plymouth, UK. 2University of
Oxford Respiratory Trials Unit, Churchill Hospital, Oxford, UK. 3Dept of Respiratory Medicine, The Alfred Hospital, Melbourne,
Australia. 4Vanderbilt University Medical Center, Tennessee, Nashville, TN, USA. 5Division of Pulmonology, Dept of Medicine,
Stellenbosch University, Cape Town, South Africa. 6Tygerberg Academic Hospital, Cape Town, South Africa.
Correspondence: John P. Corcoran, Dept of Respiratory Medicine, Derriford Hospital, Plymouth, PL6 8DH, UK.
E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
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The use of TUS as a diagnostic tool for a variety of lung parenchymal and pleural
pathologies has been discussed at length in earlier chapters in this Monograph. The
primary goal of this chapter is to look at how the use of TUS can, when appropriate,
facilitate and enhance a diagnostic and/or therapeutic procedure in the context of different
respiratory conditions. The chapter will also consider some of the technical aspects of
performing an individual procedure and will, where necessary, direct readers to other
resources; it does not aim to provide a step-by-step guide on how a particular intervention
might or should be performed. In taking this approach, this chapter hopes to provide the
reader with an understanding of key concepts relating to the use of TUS for procedural
work including: 1) the practicalities of using TUS in a procedural setting (e.g. optimising
patient positioning and safety during procedures, and technical considerations including
probe choice, orientation and US modality), 2) the indications for and published data
supporting the use of TUS during basic interventions (e.g. thoracocentesis, tube
thoracostomy) for pleural fluid, 3) the indications for and published data supporting the
use of TUS guidance during more advanced interventions (e.g. pleural, lung parenchymal
and other related biopsies, and medical thoracoscopy), 4) the role of TUS as a predictor of
clinical outcomes before and after pleural intervention and 5) the potential implications for
training standards in TUS as an adjunct to procedural work.
Pre-procedural considerations
Patient factors
The decision to undertake any medical intervention involves balancing the risk of
complications against the indications for and benefits of the procedure. As a minimum, this
requires the operator to exercise due diligence with respect to those factors that might
complicate or increase the risk of any given procedure. These will include, for example,
clotting studies and/or use of anticoagulation [16], patient comorbidities including
cognitive function and body habitus, and acuity of illness. Unless a procedure is being
undertaken in the context of a life-threatening emergency, written informed consent should
be obtained as standard, with appropriate time provided to discuss any potential
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complications associated with the intervention (table 1). The advance provision to the
patient of an information leaflet outlining the benefits and risks of the procedure can
simplify this process.
Taking time to optimise the patient’s position for both TUS examination and the
subsequent planned intervention is critical, yet often underappreciated. This should be
considered in advance whenever possible, and guided by the area(s) of greatest interest as
determined from prior imaging (e.g. chest radiograph, CT). The posterior chest is most
easily examined with the patient in a seated upright position, resting their arms on a table
or other support placed in front of them. It is worth highlighting that if a patient is leant
too far forwards onto their support, it may be difficult to keep a needle perpendicular to
the chest wall and create a situation whereby the path of the needle heads superiorly in the
rib space towards the neurovascular bundle. The lateral and anterior chest can be examined
with the patient either semi-supine or in lateral decubitus, while the superior sulcus,
supraclavicular fossa and neck can be inspected in a seated, semi-supine or supine position.
Regardless of the position thought to be optimal from the operator’s perspective, the
patient must be able to tolerate remaining in that position throughout the TUS
examination and subsequent procedure.
Table 1. Common and important complications associated with thoracic interventions that
should be discussed with the patient when obtaining informed consent
Procedure Complications
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Available equipment
The operator should ensure they are familiar with all the equipment that might be required
during any intervention. This includes the procedural kit itself and the US machine being
used. Most US machines offer a variety of modalities, of which conventional brightness
(B)-mode will be sufficient for the majority of interventions; however, motion (M)-mode
and colour flow Doppler scanning may provide additional information to those
practitioners confident with their use and limitations.
If only one probe is available, this should be a low-frequency (2–5 MHz) curvilinear or phased
array transducer, which allows a balance to be struck between image quality and the tissue
penetration required for most thoracic work. A higher-frequency (6–12 MHz) linear probe
sacrifices depth of view but provides high-resolution detail that can be of benefit when evaluating
proximal chest wall structures (e.g. ribs, parietal pleura) and cervical or supraclavicular lymph
nodes [17, 25, 26]. Again, if default modes are provided by the machine, these should be selected
to suit the TUS examination being undertaken. “Abdominal” settings will suit work where more
distal structures (e.g. pleural fluid, lung, mediastinum) must be assessed, whereas “vascular”,
“musculoskeletal” or “thyroid” settings will favour proximal examinations.
The authors would encourage the reader to position the US probe parallel to the intercostal
spaces when preparing for and performing interventions. While many clinicians hold the
transducer in a longitudinal (vertical) plane across a number of rib spaces due to the
advantages this provides in point-of-care TUS diagnostics (e.g. potentially greater sensitivity for
detecting pneumothoraces), scanning in an individual rib space allows superior visualisation of
the pleura and peripheral lung tumours. This parallel approach is also necessary to facilitate
real-time (direct TUS) guidance of any transthoracic procedure. Regardless of the approach
taken, it is crucial that any examination is systematic and allows the operator to build a
three-dimensional model of the chest from images acquired in multiple sonographic planes
[17, 25, 26]. Operators should report their TUS examination and any subsequent procedure in a
structured fashion consistent with local recommendations and policy, as well as ensuring that a
suitable number of labelled TUS images and/or clips have been recorded as supporting material.
Interventional TUS and procedures will usually take place in a dedicated area (e.g. theatre,
clean room) with staff who are familiar with each other and the interventions being
performed. Standard operating procedures and bespoke safety checklists (figure 1) are likely
to be in use as part of a wider risk-management strategy. This is rarely the case in
emergency interventions undertaken on a ward and/or at the patient’s bedside; in these
circumstances, the lead operator must consider the impact that the available space,
monitoring facilities, sterility of the environment and expertise of support staff may have
on procedural outcomes. In certain cases, a swift judgement may have to be made as to
whether the risk posed by the immediate setting outweighs that of any delay incurred by
moving the patient to a more familiar working environment.
Procedural technique
Following appropriate site selection, the practitioner must decide whether to perform a
procedure using TUS in “real time” (i.e. under continuous direct sonographic vision,
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ERS MONOGRAPH | THORACIC ULTRASOUND
Figure 1. Example of a pleural procedural safety checklist based on the World Health Organization (WHO)
surgical safety checklist model. Figure provided by N.M. Rahman and J. Wrightson (Oxford University
Hospitals NHS Foundation Trust, Oxford, UK).
utilising either a bespoke needle guide mounted on the probe or a free-hand technique)
or as an “US-assisted” intervention (i.e. marking a safe site as identified by TUS
immediately prior to intervention). This choice is likely to depend on factors including
operator expertise with either technique, and the size or complexity of the pleural
collection being accessed. While there is no robust evidence that a “real-time” TUS
technique improves either patient safety or procedural success when compared with an
“US-assisted” approach, it does allow the operator to place their needle, guidewire and/
or drain into a specific location. This can be of particular benefit in more complex
septated collections where accessing the largest pocket of fluid possible is most desirable
(figure 2).
“Real-time” procedures can be undertaken either out of plane (short axis), where the needle
enters the skin away from the TUS probe and only the tip is aimed at and visualised within
the plane of the sonographic window, or in plane (long axis), where the needle enters the
skin at the side of the probe and traverses the sonographic plane, allowing the whole shaft
to be visualised as the needle approaches the target area (figure 3). Either approach can be
utilised by an experienced single operator holding the TUS probe in their nondominant
hand and the needle in the other; sterile probe sheaths are also available that can help
stabilise the needle’s position in relation to the probe during any intervention. The authors
would encourage the use of an in-plane approach if possible, since it provides a clearer
view throughout and therefore greater precision.
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a) b)
Chest wall
Septations
Pleural
Lung fluid
c) d)
Figure 2. a–d) Sonographic images demonstrating the use of real-time TUS guidance to access a septated
pleural collection. US guidance is used to sequentially place the introducer needle (solid arrows) (b), the
guidewire (dashed arrows) with J-tip (circled) (c) and the drain into the largest and most distal pocket. An
agitated saline flush (d) can then be used to confirm the drain position as hyperechoic bubbles of air
(circled) are seen entering and circulating within the pleural space. Figure reproduced with the kind
permission of N.M. Rahman (Oxford University Hospitals NHS Foundation Trust, Oxford, UK).
Basic interventions
For the purposes of this chapter, basic interventions are considered those that will be
performed by the vast majority of, if not all, TUS practitioners, i.e. thoracocentesis (pleural
aspiration) and tube thoracostomy (chest-drain insertion) for pleural fluid only. While
there are published data to support a diagnostic role for TUS with respect to pneumothorax
(PTX) (discussed in another chapter in this Monograph [29]), including as an iatrogenic
complication of transthoracic interventions [30–32], it remains a largely binary test that
cannot necessarily guide a clinician with respect to size or relative need for therapeutic
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a) b)
Figure 3. Demonstration of the relative positions of an US probe and needle during a) out-of-plane (short axis)
and b) in-plane (long axis) procedures under real-time TUS guidance (insets). Figure reproduced with the kind
permission of C.F.N. Koegelenberg (Tygerberg Academic Hospital, Cape Town, South Africa).
intervention. As widely accepted guidelines do not advocate the use of TUS prior to
intervention in the context of spontaneous PTX [17, 33–35], it is not felt to be appropriate
for consideration in this chapter.
There is a vast body of evidence demonstrating that the use of TUS prior to intervention for
suspected pleural fluid substantially reduces the risk of either a failed “dry tap” or iatrogenic
complications, including PTX or other visceral puncture; indeed, in expert hands, this risk
approaches almost zero [11, 13, 14, 36]. Practitioners should, however, be alert to the
possibility that TUS may instil false confidence and encourage them to stray outside the
anatomical safe triangle (bordered anteriorly by the lateral edge of the pectoralis major,
laterally by the lateral edge of the latissimus dorsi, inferiorly by the line of the fifth intercostal
space and superiorly by the base of the axilla). With a patient sitting upright, a posterior
intervention site may be considered more easily accessible due to the thoracic anatomy, which
allows a greater apparent depth of fluid to be visualised under TUS as it accumulates in the
costodiaphragmatic recess. However, this approach risks injuring the intercostal vessels, which
may become exposed in the middle of the rib space with increasing proximity to the spine
[37, 38]. There are published data to suggest that practitioners can sonographically screen for
vulnerable vessels within individual rib spaces using colour Doppler, thereby potentially
minimising the risk of causing an iatrogenic intrapleural bleed [39–41]; however, this work
has not been either replicated on a larger scale or proven to improve patient outcomes in the
context of what is already an infrequent complication. Neither does the use of US screening
obviate good practice and anatomical landmarks; a needle should always be introduced
immediately superior to the rib for safety reasons.
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depth of fluid and no obvious incursion by either the lung or diaphragm during
respiration. The distance between the skin surface and pleural space should be measured,
particularly in more obese or oedematous patients, so that appropriate measures can be put
in place where necessary. Whenever possible, thoracocentesis and tube thoracostomy should
be undertaken in the anatomical safe triangle, or otherwise as laterally as the
pleural collection will allow. If a more posterior approach is unavoidable, the patient’s consent
should be obtained for the additional risk of vascular injury associated with this, and
consideration given to the use of colour Doppler to screen for vulnerable intercostal vessels.
An aseptic (sterile) technique should be employed with the appropriate use of gowns,
drapes, gloves and cleaning materials. Local anaesthetic should be administered to the
chest wall, with particular attention paid to the skin and pleural surface where
innervation is greatest; the use of a “real-time” technique allows the operator to confirm
this visually on TUS as opposed to relying on informed guesswork. The point of entry to
the pleural space should then always be immediately superior to the rib to minimise the
risk of injury to the neurovascular bundle. Following any procedure, a further TUS
assessment should be performed as standard and the findings documented. This allows
the operator to exclude both iatrogenic PTX (identified as a loss of sonographic
visualisation due to free air in the pleural space, with the subsequent absence of normal
lung sliding or B-line artefacts) and intrapleural bleeding at the site of intervention
(figure 4) [30–32, 42].
Advanced interventions
For the purposes of this chapter, advanced interventions are considered those that will
usually only be performed by TUS practitioners with a specific subspecialty interest in
pleural disease and/or interventional pulmonology, and for whom these procedures would
be considered part of their everyday practice. It is worth noting that published training
curricula and guidelines regard these procedures as requiring additional training, expertise
and experience [1, 5, 17, 19], and should in the authors’ opinions therefore be subject to
additional scrutiny with respect to demonstration of initial and continuing competence.
These include lymph node sampling, closed pleural biopsy, lung aspiration and biopsy, and
medical thoracoscopy.
Figure 4. TUS diagnostic of intrapleural bleeding post-intervention, with evidence of a pulsatile colour
Doppler “plume” (solid arrow) from the parietal pleural surface and deposition of highly echogenic material
(dotted arrow) into a dependent area of the pleural space. Reproduced from [42] with permission.
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The assessment and sampling of cervical, supraclavicular and axillary lymph nodes using
TUS is a key skill for the interventional pulmonologist or lung cancer physician, and is
standard practice in many institutions. The simplicity of the procedure is such that it can
often be performed as part of an initial consultation, and it has the advantage of
streamlining the patient pathway by providing a cytological diagnosis and clinical staging
(N3) in one minimally invasive intervention [43–45].
As outlined above, a high-frequency (6–12 MHz) linear probe should be used for this type
of work since image quality will be better and the smaller footprint of the transducer allows
easier access to sites of interest [25]. The sonographic appearance of the lymph node can
determine the likelihood of pathological involvement. Benign nodes tend to be smaller,
ovoid or polygonal, with a central hyperechoic fatty hilum. Malignant nodes often appear
bulky (>1 cm diameter) and rounded, asymmetric or irregular, necrotic, homogenously
hypoechoic and/or hypervascularised. Suspicious nodes can be sampled under real-time
TUS guidance, either by fine-needle aspiration or by core-cutting needle biopsy. If
lymphoma is suspected clinically, the latter technique is strongly advised to ensure
adequate material is available to assess features with prognostic implications including
lymph-node architecture, immunohistochemistry and histological subtyping [46, 47].
The technique of closed pleural biopsy has been utilised by clinicians for over half a
century [48, 49]; the addition of image guidance, whether via CT or TUS, is a more recent
development but has already been shown beyond reasonable doubt to improve key
outcomes such as diagnostic yield and complication rates [24]. Increased access to and use
of TUS by physicians has meant that closed pleural biopsy has become more frequently
employed over the past decade, having previously been superseded by medical
thoracoscopy [50]. Closed pleural biopsy has obvious advantages over thoracoscopy: it is
less invasive and therefore more suited to elderly and/or frail individuals, and can easily be
performed in resource-poor settings on an outpatient basis.
Image guidance has been shown to increase the likelihood of obtaining sufficient diagnostic
pleural tissue, irrespective of the extent of thickening seen radiologically; furthermore, TUS
has the advantage over CT of being more mobile and avoiding any exposure to ionising
radiation [51]. From a practical perspective, TUS is also potentially more adaptable than CT in
allowing the operator to compensate for patient factors including respiratory movement in real
time. There is now a growing body of data demonstrating that outcomes from TUS-guided
pleural biopsy in the hands of appropriately qualified interventional pulmonologists are
comparable to those of specialised colleagues in radiology (figure 5) [52–54].
There are no robust published data to satisfactorily answer the question of whether the
traditional reverse bevel (e.g. Abrams) or newer core-cutting (e.g. Tru-Cut) needles are better
at obtaining diagnostic material from the parietal pleura; the difference in outcomes between
CT- and TUS-guided biopsies is similarly uncertain. The authors therefore suggest that
TUS-guided pleural biopsy can be considered equivalent to CT where there is adequate
expertise available in the former technique under real-time conditions. Operators should use
whichever sampling needle is available and/or most familiar to them from everyday practice.
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Initial cross-sectional imaging studies should be reviewed to decide which sampling technique
is most appropriate. Patients can then be divided into those with a distinct pleural-based
mass lesion (>1 cm diameter), those with diffuse pleural thickening (>1 cm diameter) and/or
irregular nodularity, and those with minimal or no identifiable thickening [50, 51].
As a general rule, the authors would advocate taking four to six biopsies in different planes
of orientation across the pleural surface to ensure adequate sampling. Mass lesions can be
sampled using TUS-guided fine-needle aspiration and/or core-cutting needle biopsy
depending on the volume of material required (e.g. for oncological receptor or mutation
analyses). Those patients with diffuse thickening should have biopsies taken from the areas
a) b)
c) d)
e) f)
Figure 5. Closed pleural biopsy. a) Example of a core biopsy cutting needle. b) Example of a procedural
room set-up with operator line of sight and in-plane real-time US guidance. c) US view of irregular parietal
pleural thickening with effusion. d) US view of irregular diaphragmatic and parietal pleural thickening with
effusion. e) High-frequency (10 mHz) real-time US-guided cutting needle biopsy of pleural and chest wall
mass. f) Low-frequency (3.5 mHz) real-time US-guided cutting needle biopsy of parietal pleural thickening.
Reproduced from [8] with permission.
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thought to be of most interest, usually where the thickening is markedly irregular or at its
greatest. In the absence of any identifiable thickening on CT or TUS assessment prior to
intervention, a low supradiaphragmatic biopsy is most likely to yield a diagnosis [55], with
the notable exception of suspected tuberculous pleuritis. In these circumstances, the diffuse
nature of the disease allows the operator to take samples in the safest possible location
(usually the midaxillary line away from the diaphragm and underlying viscera) with
confidence that the material will be diagnostic [51]. The utility of newer imaging
techniques, such as PET, to identify the best site to biopsy in pleural disease is uncertain,
and is the subject of a randomised controlled trial (ISRCTN trial number 14024829) that is
now in follow-up and due to report its initial findings in 2018.
Although CT-guided procedures have been and are likely to remain the more common
mode for sampling lung parenchymal lesions in the context of suspected malignancy, it is
worth remembering that TUS-guided intervention is an equally long-established technique
[56]. Lung parenchymal abnormalities can only be detected by TUS if there is contact
between the visceral and parietal pleura; however, these circumstances also allow TUS-guided
sampling to be safely undertaken since visibility of the abnormality intrinsically implies that
no aerated lung should be traversed [57]. The presence of rib shadows prevents TUS from
demonstrating the whole circumference of any individual mass lesion; however, it can still
provide an accurate assessment of depth, while the extent of pleural contact in any one rib
space where sampling is to be performed has direct implications for diagnostic yield [58].
While the majority of published data relate to the use of TUS-guided fine-needle aspiration
and core biopsy by radiologists [59], there is a small but growing body of evidence from
interventional pulmonologists reflecting once more the increasing use of TUS by this group
of clinicians (figure 6) [21, 22, 60, 61]. The diagnostic yield from TUS-guided lung biopsy
is comparable to that by CT but with a shorter procedural time and lower rate of iatrogenic
complications, notably PTX [21, 59, 62], the latter likely to be a reflection of the peripheral
nature of the lesions sampled by TUS.
Although malignancy remains the primary indication for lung parenchymal sampling
under image guidance, the growing use of TUS as a front-door test for diagnosing
pneumonia in hospital [63, 64] has highlighted the potential for ultrafine (⩾22-gauge)
needle lung aspiration (or a “lung tap”) to be used on a more frequent basis [65, 66]. This
would allow an increase in microbiological diagnosis, with implications for targeting of
antibiotic therapy and risk reduction for the emergence of bacterial resistance thereafter.
Further evaluation of this technique in larger-scale multicentre studies is needed to
ascertain diagnostic yield, complication rates and potential impact on outcomes that are of
relevance to patients and clinicians alike.
Medical thoracoscopy
Medical thoracoscopy has become the gold standard for the patient with an undiagnosed
unilateral pleural effusion and/or suspected malignancy [19, 67], and is performed at an
increasing number of centres as a result. TUS is an invaluable adjunct to thoracoscopy
since it allows the operator to assess the nature of the pleural space in real time with
potential implications for the likely success of the subsequent procedure [68–70] and, if
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a)
b) c)
Figure 6. TUS-guided lung biopsy. a) CT imaging demonstrating synchronous right-sided pleural (*) and
left-sided lung parenchymal (+) lesions. b and c) TUS images confirming the same abnormalities. Note how
the extent of pleural contact and parenchymal depth of the lung lesion has been documented. Sequential
TUS-guided core-cutting needle biopsies of pleural (b) and lung parenchymal lesions (arrows marking the
path of the needle) (c) confirmed the diagnoses of epithelioid malignant pleural mesothelioma and primary
lung adenocarcinoma, respectively. Figure reproduced with the kind permission of J.P. Corcoran (Plymouth
Hospitals NHS Trust, Plymouth, UK).
necessary, conversion to an alternative diagnostic intervention during the same visit [54].
While the majority of medical thoracoscopic procedures will be in cases with moderate to
large effusions that permit easy access to the pleural space, TUS can facilitate the same
intervention in patients with little or no fluid but with other abnormalities suspicious for
pleural disease. In suitable cases, an artificial PTX can be induced by a practitioner with
the required expertise using either blunt dissection [71] or Boutin needle introduction
[72] under real-time in-plane TUS guidance. This allows the operator to use TUS to
watch the passage of instruments through the chest wall and confirm the successful
development of a PTX without waiting for a lateral decubitus chest radiograph.
Outcome prediction
The ability of TUS to predict clinical and patient-related outcomes in the context of pleural
disease does not appear immediately relevant to a chapter describing US-guided procedures.
However, if the prospective use of TUS allows clinicians to decide which intervention is most
likely to benefit an individual patient, then it is arguably the most important application of all.
Nowhere is this more obvious than in the identification of nonexpandable lung (NEL), a
scenario where the lung is physically restricted by underlying pathology and therefore
incapable of complete expansion, leaving a void within the thoracic cavity where pleural
fluid can repeatedly accumulate with potential symptomatic consequences for the patient
[73]. Early identification of those patients with or without NEL would allow them to be
pre-selected for the most appropriate intervention, such as indwelling pleural catheter
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placement for those individuals with NEL as opposed to drainage and pleurodesis.
Pre-existing strategies to identify NEL have relied on draining some or all of the pleural
fluid, an invasive strategy that allows either pleural manometry [74, 75] or a post-drainage
chest radiograph demonstrating PTX ex vacuo to make the diagnosis. More recently
published data suggest that the novel use of more advanced sonographic techniques,
including speckle tracking imaging analysis and M-mode, to evaluate the underlying lung
within an effusion can identify NEL prior to any invasive procedure [76]. Further
observational work has shown that some of the same techniques can be used in everyday
clinical practice [77], although large-scale prospective studies across multiple centres are
required before the utility of TUS in this particular diagnostic sphere can be proven.
The use of TUS to demonstrate normal lung sliding as a safety measure prior to
thoracoscopy has been discussed earlier in this chapter [69, 70]. Applying these same
principles following chemical pleurodesis to treat, for example, recurrent PTX or malignant
pleural effusion may allow TUS to predict probable long-term success through the early
identification of adhesions and loss of normal lung sliding. This concept has been
addressed in small-animal and human studies with promising results [78–80], and is now
the subject of a multicentre randomised controlled trial (ISRCTN trial number 16441661).
If successful, this would allow TUS to streamline care for patients undergoing pleurodesis
for malignant pleural effusion, identifying those suitable for early discharge from hospital
and/or in need of a further definitive procedure (i.e. indwelling pleural catheter insertion)
due to probable pleurodesis success or failure.
There has been long-standing interest in how the presence of septations within a pleural
collection might influence patient outcomes, regardless of the underlying pathological
process. This is of particular relevance to the use of TUS by interventional practitioners,
since US has been shown to outperform other radiological tests including CT in the
identification of septated pleural collections [81, 82]. Recent data looking at patients with
pleural effusions presenting to and undergoing intervention for diagnostic and/or
therapeutic purposes at a single UK centre suggest that the use of a simple septation score
can predict symptomatic benefit following drainage [83]. In the specific context of pleural
infection, the presence of septations on TUS assessment has also been linked in a number
of studies with adverse patient outcomes, such as the failure of medical therapy and the
need for surgical intervention to adequately drain the infected pleural space [84–86].
However, in all these publications, the data have been obtained from single centres and are
potentially inconsistent [82], suggesting that larger prospective multicentre studies are
needed to address these important questions in greater detail [87].
Training standards
There are a number of pre-existing position statements and post-graduate training curricula
[1–5, 17, 88] that have attempted to define the competencies required by clinicians who utilise
TUS for procedural work. This chapter and the authors do not intend to offer an alternative
specification, since what is required of practitioners to ensure safe and adequate service
provision in any single centre is likely to vary enormously. However, it is worth highlighting
that the authors firmly believe that having simply performed a specified number of procedures
can and should not be used to define competency by default. This is a notable failing in a
number of prior publications, particularly with respect to more complex interventions such as
medical thoracoscopy [19, 89]. In a modern era where physicians have access to a range of
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learning and educational tools such as online teaching modules, observed assessments,
simulation facilities and interactive models, we have the opportunity to develop more refined
methods of defining true procedural competence [90]. There is a robust body of evidence
relating to both transthoracic and other types of procedural work including, for example, EBUS
that illustrates the wide variation in learning curves required by individual practitioners [91–
95]. Instead, the authors believe that future training standards should look to bespoke
assessment tools [96–98] and the use of simulation models [12, 91, 99–101] as a means of
facilitating and determining both initial and continuing procedural competence.
The fact that a misjudged or inappropriate pleural intervention can result in harm to the
patient puts a responsibility on the physician operator to demonstrate their initial and
continuing competence through a record of their practice that may be subject to
independent and/or external audit of key outcomes. This logbook should include key
information such as diagnostic yield and complication rates associated with various
interventions. This is likely to be of particular importance for more complex interventions
such as medical thoracoscopy where the consequences of inexperience, poor technique and
any subsequent complication are potentially that much greater. Individuals must be able to
recognise the limitations of their own knowledge, skills and working environment, and to
have a clear pathway for onward referral to expert colleagues in allied specialties and/or
other centres. This will vary widely according to local circumstances (e.g. population size or
catchment area, availability or proximity to other specialist services such as thoracic
surgery, differences in clinical workload and service demands), and an individual
practitioner must make a reasoned judgement of what procedural competencies are
achievable and necessary for their everyday practice in light of these factors.
The authors suggest that an annual review of procedural activity could be incorporated into
usual and pre-existing appraisal processes. However, it is crucial that any evaluation is open
and constructive, such that those practitioners with negative outlying data compared with
their peers are able to seek support and engage in further training where necessary without
feeling devalued.
Conclusion
There is little doubt that the growing use of TUS since the turn of the century has
transformed the practice of healthcare professionals, and this is most clearly evident in the
field of interventional pulmonology where ways of working continue to evolve rapidly. TUS
has become indispensable not only from a patient safety perspective but as clinicians look
to undertake ever more complex procedures. Practitioners should be aware of both the
potential and the pitfalls of TUS as a tool to support procedural work, and should ensure
they practise in a safe and evidence-based manner at all times. It is likely that this area of
clinical work will continue to change as clinicians push the boundaries of what is
considered usual practice, and as front-line research with a focus on improving key
outcomes for patients informs new standards of care in turn.
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| Chapter 17
Future directions
Christian B. Laursen1,2,3, Najib M. Rahman4,5,6 and Giovanni Volpicelli7
Although the number of published studies describing the clinical use of TUS is steadily
increasing, several aspects are yet to be studied and assessed in clinical trials. Most
importantly, the use of TUS is yet to find its place in major guidelines describing some of
the conditions that can be assessed using US. It is hoped that future additional research will
help to provide an evidence-based approach that indicates how TUS should be incorporated
into the relevant guidelines.
Cite as: Laursen CB, Rahman NM, Volpicelli G. Future directions. In: Laursen CB, Rahman NM, Volpicelli
G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 244–252
[https://doi.org/10.1183/2312508X.10007617].
T his chapter focuses on some of the areas in which further knowledge is needed to
establish an evidence-based TUS approach and which may help incorporate TUS into
the relevant clinical guidelines.
Nomenclature
1
Dept of Respiratory Medicine, Odense University Hospital, Odense, Denmark. 2Centre for Thoracic Oncology, Odense University
Hospital, Odense, Denmark. 3Institute for Clinical Research, SDU, Odense, Denmark. 4Oxford Centre for Respiratory Medicine, Oxford
University Hospitals NHS Foundation Trust, Oxford, UK. 5Oxford Respiratory Trials Unit, Nuffield Dept of Medicine, University of
Oxford, Oxford, UK. 6Oxford NIHR Biomedical Research Centre, Oxford, UK. 7Dept of Emergency Medicine, San Luigi Gonzaga
University Hospital, Torino, Italy.
Correspondence: Christian B. Laursen, Dept of Respiratory Medicine, Odense University Hospital, Sdr. Boulevard 29, 5000 Odense C,
Denmark. E-mail: [email protected]
Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.
244 https://doi.org/10.1183/2312508X.10007617
FUTURE DIRECTIONS | C.B. LAURSEN ET AL.
Respiratory Society (ERS) will be able to provide the international network needed to help
facilitate further consensus on nomenclature and principles.
The extent to which the use of TUS has been implemented among respiratory physicians
varies significantly from country to country. This may be due to differences in the extent to
which the various specialities have taken ownership of the modality and whether US machines
are generally available. Based on current knowledge, use of TUS should be considered a core
skill for the vast majority of respiratory physicians and physicians from other specialities
handling emergencies and patients with respiratory symptoms. One of the future challenges
will therefore be to provide an evidence-based framework that may help achieve this.
The ERS is yet to describe recommendations for training and competency assessment in TUS.
Other national and international societies have previously provided such recommendations
[3–5]. The guidelines generally describe different competency levels and a minimum number of
supervised procedures to achieve competency. The major limitation is that there are not enough
studies that can provide the number of procedures required in order to obtain competancy in
TUS. The existing guidelines do not describe or use any validated tools for competency
assessment. As expertise increases within the respiratory community, it is likely that respiratory
societies themselves will define competence and training within TUS (as opposed to
radiologists), given that the majority of LUS/TUS is essentially delivered by non-radiologists.
Some published studies describe training in TUS but the majority provide low levels of evidence
and take the form of one-group pre- and post-tests studies [6–17]. This type of study design
does not provide any evidence showing how to build a training curriculum and is considered
obsolete [18–21]. The learning curves of novices in TUS have been described as being steep but
with good overall agreement with supervisor findings [16]. However, learning curves of focused
LUS- and US-guided transthoracic procedures indicate that even though most physicians can
obtain the skills quickly, there are some outliers who improve their skills at a slower rate, or do
not improve at all [22, 23]. Using a validated tool for competency assessment could
help to identify such outliers. Such a tool should encompass a range of aspects, including
understanding TUS, image acquisition and image interpretation. Two studies have gathered
validity evidence for such instruments [24, 25]. The developed tools have not yet been validated
elsewhere, but studies in abdominal US using similar principles found such an assessment tool
to be both valid and reliable [26]. Further studies are required in order to establish a test that
assesses theoretical competency and, ideally, randomised clinical trials that assess both the
optimal training programme and the effect on clinical outcome of patients when implemented.
In 2016, the ERS launched a structured training programme in EBUS [27]. Hopefully,
additional future studies in TUS education, training and competency assessment will be
able to provide the knowledge needed to establish a similar and evidence-based ERS
training programme in TUS.
Pleural diseases
The use of TUS in the diagnosis of pleural fluid, and for guidance in pleural procedures, is
well established. Early studies suggested using TUS in the diagnosis of pleural disease
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aetiology (including malignant pleural effusion) and pleural infection [28]. Exciting
potential future areas include the use of TUS in predicting outcomes in pleural disease; for
example, response to therapy in those with pleural infection according to septation
presence or fluid characteristics, and in malignant effusion where advanced M-mode
analysis may predict the presence of unexpandable lung [29]. There is also evidence that
US may reduce complications further through detection of the intercostal artery, potentially
preventing laceration during procedures [30]. All of these indications require further,
focussed prospective work.
Pneumothorax
Several studies have assessed the use of TUS for diagnosis of PTX and found the diagnostic
accuracy to be superior to conventional CXR [31–37]. Despite these studies, TUS is still not
integrated into clinical PTX guidelines [38]. This is mainly due to the fact that whether
TUS can accurately be used to estimate the size of a PTX is still an issue of debate [1].
Some studies have assessed this issue, but further studies are required that assess the
clinical impact when TUS is implemented either as an adjunct to or a complete
replacement of conventional CXR when diagnosing, managing and monitoring patients
with PTX in a variety of settings (e.g. spontaneous, traumatic, iatrogenic) [39–41].
However, the widespread use of conventional radiology that is recommended by the
existing societal guidelines should at least be questioned by the growing evidence of the
efficacy of LUS [33–37, 40, 41], which is in contrast with the absence of original trials
demonstrating the efficacy of CXR for confirmation and monitoring of PTX.
Several studies have discussed the use of TUS in the assessment of diseases affecting the
lung parenchyma (e.g. pneumonia, pulmonary embolism, contusion, malignancy,
acute respiratory distress syndrome, pulmonary oedema, interstitial lung diseases (ILD))
[1, 42–44]. However, the vast majority are feasibility studies or studies assessing diagnostic
accuracy, rather than clinical impact and safety when TUS is fully integrated into clinical
practice. A single randomised trial has assessed the safety of replacing CXR with TUS in
children with suspected community-acquired pneumonia; the study found it feasible and
safe to replace the standard CXR with TUS [45]. Similar studies are warranted in other
settings (e.g. adult, emergency department, intensive care unit, outpatient clinic) and for
the other diseases affecting the lung parenchyma.
It has been proposed that US is the visual stethoscope of the 21st century, and the
diagnostic accuracy of TUS is far better than lung auscultation for a wide range of
conditions [46, 47]. Even though some indirect signs may be present, TUS cannot be used
to diagnose obstructive pulmonary diseases such as COPD and asthma [48]. It has been
suggested that a focused TUS examination with no abnormal findings is consistent with a
COPD exacerbation in a patient with acute respiratory failure in an intensive care setting
[49]. This assumption does not seem to be applicable in the emergency department [50].
Stethoscope and lung auscultation may therefore still be of use in clinical practice and
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cannot be entirely replaced by TUS. Future studies will hopefully be able to clarify whether
TUS has a potential role in patients with obstructive pulmonary diseases.
Several studies have described the use of TUS in the assessment of various ILD [51–57]. It
does not seem to be possible to visualise rare cystic lung diseases with TUS, indicating that
it cannot be used as an efficient tool to rule out all types of ILD [58]. However, it does still
have a number of possible clinical applications: it can be used as a means of screening for
ILD subtypes in various populations and for monitoring purposes [57].
Acute respiratory failure may represent a complex diagnostic challenge, as this condition
could be the result of many different diseases. The physician has to consider a number of
possible differential diagnoses. Despite several milestone advances in diagnostic modalities
since Laennec invented the stethoscope, a significant proportion of patients with respiratory
failure are not diagnosed correctly and receives inappropriate treatment [59, 60]. Several
diagnostic accuracy studies have been published supporting the use of TUS when assessing
patients with respiratory failure [49, 50, 61–64]. The clinical impact of routine US
assessment has, however, only been assessed in one randomised single-centre clinical trial.
The study demonstrated that, when compared to routine diagnostics without the use of
focused US, the US group had a significantly higher proportion of patients who were
correctly diagnosed and treated within 4 h of admission to the emergency department.
There were no differences in outcome, such as mortality and length of hospital stay, but the
study was not powered to show such differences [65]. Larger studies focusing on outcome
and patient-reported outcomes are required.
Advanced TUS
A variety of different advanced US modalities are available and have been used by other
specialities for the assessment of other organs and anatomical structures. Some of these
modalities could also have a clinical use in the field of TUS.
As opposed to most other organs, the lungs have a dual blood supply, from both the
pulmonary and bronchial arteries. In benign conditions, the dominant blood supply will be
from the pulmonary arteries, whereas tumours are supplied from the bronchial arteries.
This difference can in theory be directly visualised using US contrast. It therefore might be
able to differentiate a benign from a malignant condition. The use of contrast may also
help identify metabolic-active areas (e.g. abundant blood supply) and thus increase the
diagnostic yield in patients undergoing US-guided biopsies. These aspects have been
assessed in studies performed in a variety of settings, but further studies are needed to
assess how contrast-enhanced TUS should be used in a clinical context [66–72]. US
elastography is used to assess the elastic properties of tissue and organs. In theory, this
allows for noninvasive differentiation between benign (soft) and malignant (hard) tissue
[73–75]. It may therefore be possible to use lung elastography as a noninvasive bedside tool
to assess whether lung parenchymal pathology is benign or malignant. Even though
elastography has been used extensively in other forms of clinical US, its use for lung
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assessment is new and current studies are limited to preliminary results [76, 77]. TUS is
generally based on the operator’s assessment of the generated two dimensional-mode
images and clips obtained. A new method has been proposed in which the results of several
US modes are incorporated into a so-called multiparametric US assessment [78]. There are
no studies published that develop and assess this multiparametric method in TUS; however,
such studies could provide a more objective assessment of the findings, thereby helping the
physician to increase the diagnostic accuracy of the examination.
The clinical practice of a respiratory physician is varied and may include a broad range of
patients, from those with very limited disease in an outpatient clinic, to those with
multi-organ failure in an intensive care unit. No matter the setting, patients may have
conditions involving the extrathoracic organs, and diseases that do not affect the lungs may
present with symptoms resembling respiratory disease. Several studies have demonstrated
the potential use and clinical impact of whole-body ultrasonography by respiratory
physicians with a basic knowledge of the technique; it allows the respiratory physician to
use US to assess relevant structures other than the lungs. Some examples are presented in
the following sections.
US can be used to diagnose diseases in the upper airways, to help predict “a difficult
airway” and to provide US guidance for airway management.
Respiratory disease may involve lymph nodes and other structures of the neck. Being able
to assess the neck using US and perform US-guided biopsies may therefore be a clinically
useful to the respiratory physician.
When performing TUS, the upper abdominal structures will inadvertently also be visualised
as part of the examination. Having basic knowledge of upper abdominal US may therefore
help the respiratory physician to identify clinically important incidental findings and
subsequently refer the patient to a diagnostic abdominal US. In addition to incidental
findings, abdominal US may also be actively integrated into a TUS examination. One
example is the Focused Assessment with Sonography for HIV-associated tuberculosis
(FASH) protocol. This protocol combines TUS, FoCUS and focused abdominal US to
assess whether a patient has signs of extrapulmonary tuberculosis [79–81].
FoCUS
In several settings, it can be a clinical challenge to differentiate between the different causes
of respiratory failure and shock [60, 82]. The use of cardiac US is recommended as part of
the clinical assessment of patients with shock [83]. Several studies have advocated that
cardiac assessment should be expanded into a whole-body approach that includes TUS [82,
84, 85]. In patients with respiratory failure, routine whole-body ultrasonography that
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includes TUS and FoCUS increases diagnostic accuracy and the proportion of patients
receiving the appropriate treatment [50, 65, 86, 87].
A combination of US assessment of the lungs, heart and deep veins has been described as a
method for the assessment of patients with suspected pulmonary embolism [88]. One study
indicated that this approach in combination with Wells score might be superior to the
Wells score alone [89]. When used in a population of unselected patients with respiratory
failure, the approach seems to be able to help the clinician identify patients with
thromboembolic disease who would otherwise have been missed [50, 65].
Future use
Conclusion
This is the first ERS Monograph dedicated to TUS. The process was warmly promoted by
ERS, which is a clear sign that TUS is now being considered an essential bedside tool for
the modern respiratory physician. We feel confident that current research progress will help
to significantly increase the implementation and, most importantly, the knowledge of how
to use TUS in an evidence-based approach. If, in the years to come, ERS decides to publish
an update of this Monograph, we hope that for each of the major areas, the authors will be
able to support their arguments by citing further relevant societal guidelines that have
finally included TUS.
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Disclosures: C.B. Laursen has received personal fees from GE Healthcare for giving lectures at an US course
organised by the company.
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