Perioperative Pulmonary Atelectasis - Part II. Clinical Implications Anesthesiology American Society of Anesthesiologists
Perioperative Pulmonary Atelectasis - Part II. Clinical Implications Anesthesiology American Society of Anesthesiologists
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Table 1.
Clinical Risk Factors for Perioperative Pulmonary Atelectasis
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Obesity
The increased weight of abdominal and thoracic adipose tissue exacerbates the
compressive forces transmitted by the chest wall to the lung and exaggerates the
cephalad displacement of the diaphragm.7 These produce a rightward shift of the
respiratory system pressure–volume curve,8 higher pleural pressure,9 lower
respiratory system compliance,8,10 and lower functional residual capacity (FRC)
before11 and after induction of general anesthesia.12 The combined effect of
compression of the dorso-caudal lung and the gas absorption in lung units exposed to
small airway closure results in greater risk of perioperative pulmonary atelectasis in
obese than nonobese patients.13,14 Postintubation atelectasis at positive end-
expiratory pressure (PEEP) 0 cm H2O assessed by computed tomography linearly
relates to body mass index (weight/square of the height) in the 18 to 30 range.15 Also,
during general anesthesia, transpulmonary pressure, i.e., the pressure directly acting to
expand the lungs, 16 decreases with body mass index up to 40, corroborating the
increased susceptibility to lung collapse with obesity. Indeed, mean PEEP estimates to
produce positive end-expiratory transpulmonary pressure during general anesthesia in
the overweight and obese were 9.1 cm H2O for body mass index 25 to 29.9; 11.2 cm
H2O for body mass index 30 to 34.9; 12.8 cm H2O for body mass index 35 to 39.9; and
16.8 cm H2O for body mass index 40 or greater.9 Also, after tracheal extubation and
during the first 24 postoperative hours, morbidly obese patients present larger
atelectasis than nonobese patients.17
Age.
The susceptibility for airway closure, as judged by the difference between FRC and
closing capacity, is minimal at young adulthood (20 yr old) and larger at younger and
older ages.18 Risk for intraoperative atelectasis would be expected to follow a similar
. .
pattern as airway closure promotes low ventilation/perfusion ratio (VA/Q) egions and
absorption atelectasis. An association between atelectasis area measured with
computed tomography immediately after induction of anesthesia and age has been
demonstrated. Atelectasis area increases with age from young adulthood to a peak at
about 50 yr old, and decreases after 50 yr old.15 Such reduction of atelectasis with age
greater than approximately 50 yr is presumably due to small airway closure delaying
denitrogenation and alveolar collapse during preoxygenation.15 In children,
anesthesia-induced atelectasis is relevant particularly before 3 yr old.19 The immature
chest wall muscles and incompletely developed supporting structures in the lung
parenchyma reduce outward tethering forces, while elastic recoil of the lung is fully
preserved,20 resulting in lower FRC and higher levels of required opening
pressures.18,21
Diaphragmatic Dysfunction
Intra-abdominal Hypertension
Pulmonary Conditions
Smoking
Active smoking has been associated with perioperative respiratory morbidity and
postoperative pulmonary complications (e.g., obstructive atelectasis, pneumonia, and
chest x-ray film findings of atelectasis or consolidation), 27–29 even if not consistently
related to anesthesia-induced intraoperative atelectasis.3,30 Increased airway
secretions in smokers leading to bronchial or bronchiolar obstruction, in addition to
bronchospasm, can contribute to lung collapse.31
.
in awake 32 and surgical33,34 patients, despite small airway closure and substantial VA/
disease has been associated with resistance to atelectasis, e.g., from oxygen absorption
.
Q mismatch.32,34,35 Such resistance to lung collapse is likely due to the effect of
hyperinflation and loss of lung elastic recoil. Perioperatively, the magnitude of
atelectasis is determined by the net effect of factors contributing to and preventing
lung collapse.
Sedative-hypnotics
Opioids
As respiratory depressants, opioids decrease the central neural drive to the respiratory
muscles and the sensitivity to carbon dioxide leading to respiratory depression and
cough inhibition. Accordingly, intraoperative systemic opioids have been dose-
dependently associated with postoperative atelectasis.47
Regional Anesthesia
While regional techniques are associated with less atelectasis than general
anesthesia,53,54 they may still produce respiratory muscle dysfunctions and facilitate
lung collapse.
Neuraxial anesthesia has been associated with a significant paresis of abdominal and
accessory respiratory muscles (e.g., intercostals) and deterioration of the exhalation
force, breathing pattern, or ability to cough. 55 Reduction of lung volumes has been
accordingly associated with neuraxial anesthesia, and depends mainly on the level and
extension of the blockade (i.e., impairment increases from lumbar to cervical). For
example, thoracic epidural anesthesia with T1–T5 sensory block decreases vital and
inspiratory capacity. 56,57 Spinal anesthesia similarly reduces vital capacity but
contributes to a higher reduction of the expiratory reserve volume (–48% with sensory
block at T2) than thoracic epidural anesthesia.58,59 Of note, reductions in
intraoperative lung volumes during spinal anesthesia are greater in the overweight53
or the obese60 patient. Due to the higher level of motor block and potential
compromise of the diaphragmatic innervation, cervical epidural anesthesia may further
deteriorate lung expansion as shown by a significant reduction in diaphragmatic
excursion, maximal inspiratory pressure, and tidal volume (VT).61 While such
respiratory muscle dysfunction associated with both epidural and spinal anesthesia
may compound to lung collapse in at-risk conditions,25 this risk does not appear to be
clinically relevant in patients without preexisting lung disease and might not surpass
the benefits of avoiding general anesthesia in patients at high respiratory risk.25,62
Peripheral nerve blocks can also facilitate lung collapse. The risk of ipsilateral
atelectasis due to phrenic nerve palsy and hemidiaphragmatic paresis may limit the use
of interscalene block or other injections of local anesthetic in the cervical region (e.g.,
supraclavicular, cervical plexus blocks) in patients presenting respiratory
conditions. 63,64 Importantly, this risk is substantially reduced by the use of ultrasound-
guided techniques and lowered volume of local anesthetic.64,65
Blood Transfusion
Body Position
The supine position is associated with a 27% decrease in FRC when compared to the
sitting position (90 degrees)68 as it facilitates the cephalad shift of the diaphragm
induced by the compression of intraabdominal organs. The Trendelenburg position
further increases compression of the dorso-caudal lung as shown by additional
reduction in FRC (approximately 12%) in anesthetized children.69 During robotic
surgery, steep Trendelenburg reduces end-expiratory transpulmonary pressure9
independently from patients’ body mass index and application of pneumoperitoneum.9
The reduction in regional ventilation70 and approximately 12% increase in silent spaces
(lung areas with little or no ventilation suggestive of atelectasis) in the dorsal
dependent lung have been confirmed by electrical impedance tomography.71 In
contrast, the 40-degree reverse Trendelenburg position relieves lung compression by
the abdomen with a marked benefit in obese patients, e.g., homogenization of regional
ventilation during bariatric laparoscopic surgery. 72
Prone Positioning
Normally, the prone position reduces FRC from the sitting posture in awake,
spontaneously breathing healthy humans.73 In the anesthetized surgical patient, the
prone position with free abdominal movements (upper chest and pelvic supports) can
markedly increase FRC by 53% when compared to supine posture,74 even more in
obese patients.75 Frequently, anterior chest and abdominal wall movements are
restricted in the prone position, and lung expansion is predominantly determined by
movement of the dorsal chest wall and diaphragm. The prone position reduces the mass
of dependent lung exposed to the effect of gravity, favorably modifies the matching of
lung and chest wall shapes, and reduces lung compression by cardiac and abdominal
structures. These result in spatial homogenization of lung aeration and less
deterioration of lung inflation and regional strain over time76 due to both gravitational
(dorsal greater than ventral expansion) and nongravitational (caudal greater than
. .
cranial expansion) mechanisms.77 Favorable effects on ventilation, VA/Q,78–80 and
oxygenation are also observed,81 while perfusion distribution is not significantly
affected.82
Lateral Decubitus
The dependent lung is exposed to compression from the weight of the nondependent
lung, mediastinum, and abdominal organs.83,84 Thus, atelectasis is almost exclusively
located in the dependent lung as detected by computed tomography in anesthetized
patients.83,85 Yet the global FRC is larger in the lateral than in the supine position both
before86 and after87 induction of general anesthesia due to the contribution of the
nondependent lung. This represents a larger nondependent lung volume exposed to
lower compression forces and larger transpulmonary pressures than that present in
supine conditions.88 Despite differences in lung size, the effect of lateral decubitus
appears similar if the patient is lying on the left or right side.68,88
Lithotomy
Lithotomy position has little differential effect on respiratory mechanics and the
amount of poorly aerated lung tissue when compared with the supine position.54,89
Pneumoperitoneum
Cardiac Surgery
Lung inflammation and ischemia–reperfusion injury from cardiopulmonary bypass are
associated with substantial pulmonary compromise characterized by alveolocapillary
membrane injury,96 surfactant impairment,97 and mucociliary dysfunction.98
Alterations of the chest wall function including the effect of sternotomy,99,100
diaphragmatic dysfunction,101 and pleural violation compound with those effects with
impairment of lung expansion in the intra- and postoperative periods. Accordingly,
atelectasis represents a frequent cause of hypoxemia both during and after
surgery.102–104 The predominance of retrocardiac lung collapse in the postoperative
period suggests an important contribution to atelectasis from compression by the
weight of the heart (fig. 1).105
Fig. 1.
Lung computed tomography: bilateral opacities of the dependent retrocardiac lung regions
(red lines) revealing the typical aspect of severe perioperative pulmonary atelectasis in an
obese patient requiring reintubation for postoperative respiratory failure 2 days after
coronary artery bypass graft surgery.
One-lung Ventilation
Atelectasis produced by lung isolation is remarkable for its extension to a lung volume
and its continuous character (i.e., no tidal recruitment). Depending on the preoperative
respiratory status and the effectiveness of hypoxic pulmonary vasoconstriction, one-
lung ventilation may be associated with critical impairment of intraoperative gas
exchange and cardiopulmonary function. 106 Lung isolation exposes the collapsed lung
to inflammatory,107,108 ischemic,109 and reexpansion110 insults, besides direct
surgical trauma. The ventilated dependent lung is also at risk in this setting not only due
to the potential systemic inflammatory response but also due to mechanical ventilation
injury and compressive atelectasis during lateral decubitus.111,112 This effect can be
exacerbated in the obese or if insufficient PEEP is associated with low VT.113 Such
intraoperative insults to the collapsed and the ventilated lungs likely contribute to the
large number of pulmonary complications, including postoperative atelectasis,
observed in the thoracic surgery population.114–116
Surgery Duration
Chest Radiography
Computed Tomography
Fig. 2.
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Sagittal cross-section magnetic resonance images showing the effect of general anesthesia and
paralysis in the supine position: dorsal cephalad shift of the diaphragm dome and atelectasis of
the dorso-caudal lung.
Pulmonary Ultrasound
Lung ultrasound has been recently extensively validated for bedside assessment of lung
collapse both in the operating room and in the intensive care unit (ICU).138 As air is a
strong ultrasound beam reflector, lung deaeration substantially increases the
echogenicity of lung parenchyma. Accordingly, pulmonary atelectasis, similar to other
causes of lung consolidation, is visualized as a “tissue-like” or “hepatized”
ultrasonographic structure (fig. 3A).139 Lung ultrasound is highly accurate to diagnose
pulmonary atelectasis in both children140 and adults,141 and performs better than
auscultation or bedside radiography to differentiate important causes of increased
density (e.g., pulmonary consolidation vs. pleural effusion). 142 Similar to computed
tomography, the differential diagnosis of pulmonary consolidation with ultrasound
(atelectasis vs. pneumonia) remains challenging. The visualization of dynamic air
bronchogram, revealed by a ventilation-synchronized, linear, or pinpoint hyperechoic
signal inside a lung consolidation, allows for high positive predictive value (86 to 97%)
but moderate sensitivity (61%) in the diagnosis of pneumonia. 143,144 Assessment of
atelectasis with ultrasound has been proposed for intraoperative individualization of
alveolar recruitment145–147 and postoperative prediction of pulmonary
complications.148 Transesophageal ultrasound may be used if transthoracic acoustic
windows are unavailable.149 Color Doppler interrogation of a lung consolidation can
help to evaluate local blood flow and the efficacy of hypoxic pulmonary
vasoconstriction (fig. 3B).150
Fig. 3.
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Pre- and postoperative regional distribution of the tidal impedance variation, assessed with
lung electrical impedance tomography, in a patient presenting postoperative respiratory
failure 2 days after coronary artery bypass graft surgery. Note that pulmonary atelectasis
observed on computed tomography is associated with a reduced impedance variation signal in
the dorsal hemithorax.
Fig. 5.
Fig. 6.
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Transpulmonary Pressure
Transpulmonary pressure is conceptualized as the pressure across the lungs, i.e., the
difference between airway opening pressure and pleural pressure. While airway
pressure is usually available, pleural pressure is not. Esophageal pressure measurement
has been used to estimate pleural pressure. 160 The obtained measurement has been
shown to correspond to the pleural pressure surrounding the region where the
pressure is assessed (i.e., dorso-caudal lung according to esophageal balloon
location). 161 Exposure to negative transpulmonary pressure, notably at the end of
expiration, increases the risk of lung collapse as shown by supine pig and human
cadaver imaging studies.161,162 Negative end-expiratory transpulmonary pressures
have also been consistently associated with hypoxemia and lung collapse during acute
lung injury163 and in surgical patients.95,159 Hence, the continuous monitoring of
esophageal pressure, targeting positive transpulmonary pressure,16 has been proposed
as a strategy to individualize airway pressure and maintain lung expansion during
mechanical ventilation (fig. 5).9,164
Blood Oxygenation
. .
Pulmonary atelectasis correlates with the presence of shunt or regions of low VA/Q and
contributes to intraoperative hypoxemia.52,120,165 The magnitude of the hypoxemia
will be determined by the degree of ventilation/perfusion mismatch, including the
volume of atelectatic lung and the adequacy of regional hypoxic pulmonary
vasoconstriction. Pulse oximetry is a simple and usually reliable continuous monitor of
oxygenation allowing for the early detection of possible perioperative atelectasis.166
Because absolute oxygen saturation measured by pulse oximetry (SpO2) can be
normalized by increasing FIO2, use of the SpO2/FIO2 ratio may help to diagnose impaired
blood oxygenation better than SpO2 alone. In injured lung patients, the range of
SpO2/FIO2 equaling 235 to 315 is associated with PaO2/FIO2 of 200 to 300 mmHg.167
Preoperative Period
Intraoperative Period
VT
Supraphysiological VT (10 to 15 ml/kg of predicted body weight) has been until recently
the decades-long cornerstone of intraoperative atelectasis treatment.1,179 Indeed,
lower VT implies the potential for poorly ventilated lung regions exposed, in the
absence of PEEP, to progressive deaeration. Yet while effective to prevent atelectasis,
large VT has been associated with higher risk of postoperative pulmonary complications
in meta-analyses,180,181 registry-based studies,182 and clinical trials in abdominal183
and thoracic184 surgery. The protective range of VT in surgical patients may be broader
than stricter lower tidal volume ranges utilized in critical care. A recent clinical trial
found that VT of 6 versus 10 ml/kg of predicted body weight with PEEP of 5 cm H 2O
resulted in similar outcomes after major surgery (table 2),185 in line with a previous
large registry-based study.157 The presence of PEEP of 5 cm H2O in these cases may be
essential for equivalent outcomes, as absence of PEEP in association with low VT may
be deleterious.5 Such a finding underscores a limitation of previous studies addressing
VT using bundle interventions of VT and PEEP settings,183,184 which prevent the
individual assessment of VT and PEEP to outcomes. Overall, current evidence supports
a VT range of 6 to 10 ml/kg of predicted body weight for two-lung ventilation of surgical
patients with noninflamed lungs.
Table 2.
Randomized Clinical Trials on Alveolar Expansion Strategies during General Anesthesia
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Of note, current data suggest that the protective effect may not derive from lower VT
by itself but from its role in limiting lung strain, defined as change in lung volume
divided by the initial lung volume, and clinically estimated from driving pressures.
Indeed, registry-based studies in surgical patients undergoing noncardiothoracic157
and cardiac surgery158 and studies in acute respiratory distress syndrome (ARDS)186
have indicated that improved outcomes are related primarily to driving pressures, not
to VT. While these two variables are related, driving pressure is more specifically
associated with lung strain, a possible explanation of those findings. That would lead
the clinician to consider ventilatory interventions when driving pressures increase,
rather than merely focusing on VT.16
Recruitment Maneuvers
PEEP
Besides those beneficial physiologic effects, PEEP can also prevent the mechanical and
biologic lung injuries associated with atelectasis26 and, consequently, improve
postoperative pulmonary outcomes. Such protection has been implied by the
observation of better postoperative pulmonary outcomes with moderate PEEP (5 to 8
cm H2O) than with lower to no or high PEEP in large registry-based studies in
noncardiothoracic surgery,157,198 and worse outcomes when PEEP of approximately 0
is associated with low VT.5 In multicenter randomized controlled trials, moderate PEEP
bundled with low VT leading to better outcomes than when no PEEP was combined with
high VT further supported its value (table 2).183,184
Application of PEEP higher than those moderate levels (i.e., 8 to 12 cm H 2O) has not
brought additional improvement of postoperative pulmonary outcomes, although it
reduces intraoperative atelectasis. Indeed, large randomized controlled trials using high
PEEP (12 cm H2O) strategies consistently enhanced intraoperative oxygenation and
respiratory mechanics, while they failed to improve postoperative pulmonary and
extrapulmonary outcomes (table 2).188,189,194 Importantly, high PEEP may expose
patients to excessive alveolar pressures, as suggested by the finding of biomarkers of
alveolar overdistension103,199 and the higher incidence of arterial hypotension,
bradycardia, and need for vasopressors in patients exposed to it.188,189,200
Consequently, recent expert recommendations propose the avoidance of PEEP of 0 cm
H2O while limiting intraoperative PEEP to fixed low levels (2 to 5 cm H2O) as the
standard intraoperative approach.168 High PEEP strategies would be restricted to
clinical scenarios strongly suggestive of significant atelectasis (e.g., oxygenation or
respiratory mechanics compromise) 156,201 or consistent with high risk for lung
collapse (e.g., body mass index greater than 50; obesity plus pneumoperitoneum or
Trendelenburg; abdominal hypertension; fig. 6).9,70,189,202
Spontaneous Ventilation
Of note, critically ill patients presenting uninjured lungs did not benefit from the
systematic use of low V T (6 ml/kg vs. 10 ml/kg of predicted body weight) 224 and PEEP
higher than 5 cm H2O.225 Accordingly, the ventilatory management of lung recruitment
in critically ill patients with normal lung function is consistent with the approach
described for the surgical patient.
In mostly nonobese patients undergoing emergence from anesthesia with FIO2 of 1.0 at
the end of noncardiothoracic surgery, neither weaning PEEP to 0 cm H2O236 nor
performing recruitment maneuvers and adding PEEP 10 cm H2O241 before extubation
significantly affected postoperative atelectasis formation or gas exchange.
Postoperative Period
Curative Use
In hypoxemic patients after major abdominal surgery (e.g., room air SpO2 96% or less for
5 min194 ), postoperative continuous positive airway pressure (5 to 10 cm H2O) was
effective in preventing postoperative pulmonary complications194 and
reintubation,252 and noninvasive ventilation (inspiratory pressure support 5 to 15 cm
H2O; PEEP 5 to 10 cm H2O) reduced 90-day mortality as compared to standard oxygen
therapy.253 Noninvasive ventilation prevented postoperative reintubation in patients
presenting acute respiratory failure after cardiothoracic surgery, also reducing ICU
length of stay,254–256 and after solid organ transplantation, also reducing ICU
mortality.257 In patients presenting with hypoxemia after cardiothoracic surgery
(approximately 32% with obesity), high-flow nasal oxygen therapy (flow 50 l/min; FIO2
50%) was noninferior to noninvasive ventilation to prevent reintubation.258
Preventive Use
High-risk patients, e.g., the obese, may particularly benefit from extended postoperative
noninvasive ventilatory support. 259 After bariatric surgery, preventive continuous
positive airway pressure or noninvasive ventilation improved blood oxygenation260
and postextubation lung volumes,261 while early application of high-flow nasal cannula
decreased postoperative hypoxemia and prevented postoperative pulmonary
atelectasis.262 Similarly, in mostly nonobese patients who had undergone elective
cardiac surgery, preventive nasal continuous positive airway pressure (10 cm H2O, 6 h
or greater) reduced the rate of postoperative complications and reintubation but had
no significant effect on ICU or hospital length of stay.263 Despite these results, recent
randomized clinical trials assessing the preventive use of postoperative noninvasive
ventilatory support did not demonstrate efficacy of continuous positive airway
pressure or high-flow nasal cannula after abdominal surgery in mostly nonobese
patients at intermediate-to-high pulmonary risk,194,264 noninvasive ventilation after
thoracic surgery in chronic obstructive pulmonary disease patients,265 or high-flow
nasal cannula after cardiac surgery in overweight to obese patients.266,267 These
results emphasize the need for better treatment stratification (e.g., super-obese,
significant intraoperative atelectasis) and identification of the optimal interface, time of
initiation, and dose of preventive ventilatory support.
Early Mobilization
Early mobilization, as part of enhanced recovery after surgery,268 has been suggested
to improve postoperative FRC.269 In clinical trials, early mobilization relieved lung
atelectasis after video-assisted thoracoscopic surgery270 and coronary artery bypass
graft surgery,271 but the effect on pulmonary complications was not significant after
colorectal surgery.272,273
Oxygen Therapy
Mucolytics
Along with lung expansion techniques, relieving severe extrinsic compression due to
pleural effusion (e.g., thoracocentesis) or abdominal hypertension (e.g., paracentesis,
medical treatment of ileus, laparostomy) as well as significant pneumothorax may be
necessary to improve lung aeration. Gastric decompression should be strictly selective
(e.g., severe postoperative gastric distension). Routine use of a nasogastric tube
significantly increased the incidence of postoperative atelectasis and pneumonia in a
meta-analysis of clinical trials. 291
Interventions described in this section compose most of the current clinical tools to
approach perioperative atelectasis. As can be derived from the presentation, the
evidence on interventions specifically addressing atelectasis is dispersed in sources
varying from clinical trials, in combination with other pulmonary outcomes, to
individual studies or meta-analyses addressing subsets of patients, single interventions,
and particular outcomes. Formal systematic analyses are needed to advance
quantitative and specific understanding in the field.
Conclusions
Acknowledgments
Research Support
This work was funded by National Institutes of Health–National Heart, Lung, and Blood
Institute (Bethesda, Maryland) grant Nos. R01 HL121228 to Dr. Vidal Melo and UH3
HL140177 to Drs. Vidal Melo and Fernandez-Bustamante. Dr. Lagier received research
grants from Societe Francaise d’Anesthesie Reanimation (Paris, France), European
Association of CardioThoracic Anaesthesiologists (Rome, Italy), and Fondation
Monahan (Paris, France).
Competing Interests
Dr. Fernandez-Bustamante reports financial relationships with Merck Sharp & Dohme
Corp. (Kenilworth, New Jersey) and the U.S. Department of Defense (Arlington,
Virginia). The other authors declare no competing interests.
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