J Ultrasound (2015) 18:101–107

DOI 10.1007/s40477-014-0085-6

REVIEW

Renal transplant vascular complications: the role of Doppler

ultrasound
Antonio Granata • Silvia Clementi • Francesco Londrino •

Giulia Romano • Massimiliano Veroux • Fulvio Fiorini •

Pasquale Fatuzzo

Received: 28 January 2014 / Accepted: 14 March 2014 / Published online: 11 April 2014
 Società Italiana di Ultrasonologia in Medicina e Biologia (SIUMB) 2014

Abstract Improvements in the care of kidney transplant undoubtedly increase the accuracy of ultrasonography in
recipients and advances in immunosuppressive therapy the diagnosis of vascular complications involving the
have reduced the incidence of graft rejection. As a result, transplanted kidney.
other types of kidney transplant complications, such as
surgical, urologic, parenchymal, and vascular complica- Keywords Ultrasonography
Doppler ultrasound
Renal
tions, have become more common. Although vascular transplant
Vascular complications
complications account for only 5–10 % of all post-trans-
plant complications, they are a frequent cause of graft loss. Riassunto La progressiva riduzione dell’incidenza del
Ultrasonography, both in B-mode and with Doppler ultra- rigetto ha reso più frequenti le complicanze urologiche,
sound, is a fundamental tool in the differential diagnosis of chirurgiche, parenchimali e vascolari. Queste ultime, pur
renal allograft dysfunction. Doppler ultrasound is highly rappresentando soltanto il 5–10 % di tutte le complicanze
specific in cases of transplanted renal artery stenosis, post-trapianto, sono frequente causa di perdita del graft.
pseudoaneurysms, arteriovenous fistulas, and thrombosis L’esame ultrasonografico, sia in B-mode che con l’ausilio
with complete or partial artery or vein occlusion. A single del color Doppler, è fondamentale nella diagnosi differen-
measurements of color Doppler indexes display high ziale delle cause che possono innescare una disfunzione del
diagnostic accuracy and in particular cases are more useful graft. Sebbene sia ormai indiscussa la sua utilità nella
during the post-transplantation follow-up period. More diagnosi di complicanze parenchimali, chirurgiche e uro-
recent techniques, such as contrast-enhanced ultrasound, logiche, non è ancora consolidato il suo ruolo in caso di

A. Granata M. Veroux
Nephrology and Dialysis Unit, ‘‘St. Giovanni di Dio’’ Hospital, Vascular Surgery and Organ Transplant Unit, University
Agrigento, Italy Hospital of Catania, Catania, Italy

A. Granata (&) F. Fiorini

Via F. Paradiso n78/a, 95024 Acireale (CT), Italy Nephrology and Dialysis Unit, ‘‘Santa Maria della
e-mail: [email protected] Consolazione’’ Hospital, Rovigo, Italy

S. Clementi P. Fatuzzo
Medical Oncology Unit, Humanitas, Centro Catanese di Cattedra di Nefrologia, Scuola di Specializzazione in Nefrologia,
Oncologia, Catania, Italy University Hospital of Catania, Catania, Italy

F. Londrino
Nephrology and Dialysis Unit, ‘‘St. Andrea’’ Hospital,
La Spezia, Italy

G. Romano
Internal Medicine Unit, AOU ‘‘Vittorio Emanuele, Policlinico’’,
Catania, Italy

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complicanze a carico dell’asse vascolare renale. L’eco- complications, which occur in 45–60 and 25–30 % of all
color-Doppler, in particolare, possiede una specificità tale cases, respectively [2]. Although vascular problems
da poter essere considerato uno strumento diagnostico nella account for only 5–10 % of all post-transplant complica-
maggior parte delle complicanze vascolari del rene tra- tions, they can be a frequent cause of graft loss [1]. The
piantato, sia acute (occlusione parziale o totale dei vasi principal vascular complications are stenosis and/or
renali) che croniche (stenosi dell’arteria renale, pseudo thrombosis of the renal artery and/or vein, segmental renal
aneurisma e fistola artero-venosa) Gli indici color-Doppler infarction, dissection of the iliac and/or renal artery, and
possiedono, infatti, una alta accuratezza diagnostica nella the development of arteriovenous fistulas (mainly after
loro singola determinazione, risultando in casi particolari biopsy) and pseudoaneurysms (Table 1).
più utili nel follow-up. L’utilizzo di tecniche più moderne,
come il mezzo di contrasto ecografico, consente indubbi-
amente di aumentare l’accuratezza diagnostica dell’esame Evaluation of the vascular axis of the transplanted
ultrasonografico nel caso delle complicanze vascolari del kidney: examination technique
rene trapiantato.
Color Doppler ultrasonography (CDUS) of the transplanted
renal artery and the rest of the graft’s vascular axis should
include full length of the vessels. To minimize the risk of
Introduction technical failures, the examination protocol should be
standardized. The examination should begin with a B-mode
Over the past 20 years, the availability of calcineurin assessment of the aorta, the aortoiliac axis, the external
inhibitors and other new classes of immunosuppressive iliac artery, and the origins of the transplanted vessels.
drugs has significantly reduced the incidence of rejection- Before starting, it is useful to read the operative report to
related loss of renal transplants and pushed other types of get a clear idea of the procedure used and the number of
complications to the forefront [1]. The latter consist mainly arteries transplanted [3]. For the color Doppler analysis, the
of surgical/urological events and parenchymal color box area should be restricted to the region to be
examined to improve the frame rate (FR). The clinician
should adjust the pulse repetition frequency (PRF)
Table 1 Complications of the transplanted kidney
(approximate range 1.5–3 kHz), the wall filter (100 Hz),
Early complications 50–60 % and the color gain to obtain an optimal image, i.e., a uni-
• Acute tubular necrosis (10–30 %) form red or blue map with no aliasing or color diffusion
• Acute rejection (20–40 %) effects into the perivascular tissues (color bleed) [4].
• Renal artery thrombosis (rare) Finally, the spectral analysis module is activated: the
• Renal vein thrombosis (rare) sample volume is positioned in the lumen of the renal
• Urinary obstruction artery and the velocity/time (V/t) curve recorded. The size
• Urinary hemorrhage and/or leak (6 %) of the sample volume (2–4 mm) should be adjusted to
• Fluid collections (abscess, hematoma, lymphocele, urinoma) allow homogeneous insonation of the vessel without pro-
• Cyclosporine and tacrolimus toxicity ducing oversampling/undersampling artifacts [4]. The V/
• Infections t curve should be recorded several times with optimal in-
• Disease relapse sonation angles (\60) because the diagnosis of renal
Late complications 10–20 % artery stenosis in the graft is based exclusively on absolute
• Transplanted renal artery stenosis (10–12 %) velocity values [measurement of the peak systolic velocity
• Renal infarction (PSV)] (Fig. 1).
• Cyclosporine and tacrolimus toxicity
• Infections
• Arteriovenous fistulas (10 %) Transplanted renal artery stenosis (TRAS)
• Obstruction
• Transplanted renal vein stenosis Transplanted renal artery stenosis accounts for 75 % of all
• Chronic allograft nephropathy vascular complications. It is generally observed
Long-term complications 1–2 % 3–24 months after the surgical procedure although it can
• De novo glomerulonephritis
really occur at any time [3].
• Recurrent disease
Transplanted renal artery stenosis is a relatively frequent
• Other complications (1 %)
complication, with a prevalence that ranges from 1.5 to
4 % [5] and an incidence between 1 and 23 % [6]. The

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Fig. 1 Renal artery stenosis. a Color Doppler study shows mosaic pattern at the site of the anastomosis and a significant increase in the peak
systolic velocity (460 cm/s). b Spectral analysis shows a ‘‘tardus-parvus’’ waveform at the level of the arcuate artery

wide variability of reported incidence rates reflects a lack Table 2 Diagnostic accuracy of CDUS in the diagnosis of TRAS
of consensus on the definition of hemodynamically sig- PSV C2.0 m/s C2.5 m/s C3.0 m/s
nificant TRAS. The definitions reported in the literature
vary from 50 to 80 %, and there are also differences in the Specificity 67 % 79 % 93 %
characteristics of the study population (presence/absence of (55–77 %) (65–82 %) (77–96 %)
chronic renal failure, arterial hypertension, etc.). Moreover, Sensitivity 100 % 100 % 80 %
(46–100 %) (46–100 %) (29–98 %)
in several cases angiographic documentation of the stenosis
Accuracy 68 % 81 % 92 %
is also lacking. One of the best-designed studies in terms of
the methods used revealed an incidence of 12.4 % [7].
Risk factors for TRAS include atherosclerotic disease in a imaging studies, such as computed tomography (CT) or
donor vessel, cytomegalovirus infection, delayed restoration magnetic resonance imaging (MRI) has led to an increase
of renal function, and transplantation of a pediatric kidney in in the incidence of asymptomatic cases of TRAS [10].
an adult recipient [7]. TRAS should be suspected when the
patient has poorly controlled blood pressure and/or a pro-
gressive decline in renal function that cannot be attributed to Color Doppler ultrasound criteria for the diagnosis
other obvious causes (rejection, obstruction, infection) or of TRAS
that follows the administration of ACE inhibitors or angio-
tensin receptor blockers [3]. Difficulties can arise during CDUS examination of the
In about half of all TRAS cases, the stenosis involves the transplanted renal artery. Marked tortuosity of the vessels
anastomosis site, and it is iatrogenic, i.e., caused by scarring can lead to erroneous insonation angles, reducing the
related to the explanation, clamping, and/or anastomosis of accuracy of PSV measurements; other sources of error are
the vessel with the iliac artery axis [8]. Less commonly renal artery stretching and/or kinking, which can cause
multiple segments of the artery (or even the entire vessel) false acceleration [11]. Renal blood flow is strongly
are stenotic. In these cases, the stenosis is generally the dependent on renal function, so defining a precise PSV
result of catheter-related trauma to the intima during the threshold for the diagnosis of TRAS (unlike stenosis of the
phase of cold ischemia, but it may also be caused by torsion native renal artery) is not possible. In the absence of
and/or kinking after surgical implantation [8]. hemodynamically significant stenosis, the PSV of the RA
Since TRAS is a major cause of graft dysfunction and/or in a hypertrophic, well-functioning transplanted kidney
loss, prompt diagnosis and treatment can significantly may exceed 250–300 cm/s along the full length of the
improve graft survival. Ultrasound studies, particularly artery. In contrast, in the presence of chronic graft dys-
color Doppler imaging, play important roles in the function with reduced organ volume, a focal PSV of
screening, diagnosis, and follow-up stages although angio- 180–200 cm/s may be suggestive of significant TRAS,
graphy is still the gold-standard in this setting [3, 9]. The particularly when the other segments of the artery exhibit
increased use of CDUS and/or other, more complex markedly lower PSVs (40–50 cm/s). Therefore, focal

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Table 3 Sensitivity of Doppler indexes in the diagnosis of severe Doppler exploration. Narrowing of arterial vessels within
TRAS the graft has been reported, but it is difficult to visualize
TRAS [ 80 % with CDUS or with angiography. CDUS is also particularly
useful during follow-up and in the diagnosis of recurrence
PSV ra/PSV ia [ 13 100 %
of TRAS after treatment [19].
PSV ra [ 300 cm/s 80 %
AT [ 0.06 s 93 %
RI \ 0.5 50 % Thrombosis of the transplanted renal artery
ra renal artery, ia interlobar artery, at acceleration time, ri resistance
index Frank occlusion of the renal artery is a very rare occurrence
with negative prognostic implications: it occurs very early
acceleration of flow that is 2.5 times higher than the pre- or during the postoperative period and leads inexorably to
post-stenotic velocity (e.g., PSV 250–270 vs. 80–120 cm/s) graft loss. The sensitivity and specificity of CDUS in the
represents a direct criterion for the diagnosis of TRAS. The diagnosis of renal artery thrombosis are close to 100 %.
PSV threshold for defining hemodynamically significant Occlusion of the main renal artery is reflected on CDUS by
stenosis varies somewhat from author to author [12, 13], the absence of arterial flow within the kidney (distal to the
but there is a reasonable level of consensus that a value of site of occlusion) along with the complete absence of
250 cm/s is still within the normal range, whereas higher venous flow [19]. Occlusion involving a segmental artery
velocities predict significant stenosis with high sensitivity leads to segmental infarction, which is reflected by the
and specificity (Table 2) [14, 15]. Some authors have absence of arteriovenous flow only in the affected segment.
pointed out that the PSV threshold for stenosis may vary Power Doppler imaging can be helpful in cases of this type
depending on the type of anastomosis (end-to-side vs. end- because of its excellent capacity for identifying low-flow
to-end) created between the renal artery and iliac vessels. vessels, but in certain cases, angiographic confirmation of
They also maintain that the best Doppler criterion for the diagnosis is still necessary [20].
diagnosis of TRAS, regardless of the type of anastomosis,
is a stenotic renal artery PSV that is [13 times higher than
that of an interlobar artery [16, 17] (Table 3). A limited Thrombosis and stenosis of the transplanted renal vein
number of studies have attempted to identify the presence
of TRAS using contrast-enhanced ultrasound, but the role Thrombosis of the transplanted renal vein (TTRV) is also a
of this technique is still unclear [18]. rare event: it occurs in approximately 4 % of cases, gene-
In contrast to the diagnosis of native renal artery ste- rally during the immediate postoperative period. It can be
nosis, indirect signs are of little use in the diagnosis of complete, in which case it leads to loss of the graft, or
TRAS because the transplanted artery can be directly partial [21, 22]. Surgical problems (complications, techni-
visualized in most cases, its tardus-parvus waveform can- cal errors), hypovolemia, thrombosis of the iliac axis, and
not be compared with that of the contralateral kidney, and compression caused by perinephric fluid collections (lym-
because the resistance to flow is influenced by numerous phocele, urinoma, etc.) are among the most common causes
variables [19] except in particular cases (Fig. 1). Accelera- (Fig. 3). TTRV should be suspected when there is a sudden
tion time is the only indirect index that displays high drop in urine output and enlargement of the graft with
sensitivity in the diagnosis of TRAS, but only when the tenderness, swelling, proteinuria, and deteriorating renal
degree of stenosis exceeds 80 % [19] (Table 3). Secondary function [19].
effects, such as turbulence, reverse flow, and spectral di- Color Doppler ultrasonography plays an important role
spersion, can be evaluated in the segment immediately in the diagnosis and follow-up of this complication. In the
downstream from the stenosis. presence of complete TTRV, the vessel is characterized by
In clinical practice, it can be very difficult to distinguish scarce or absent compressibility, and the B-mode exami-
between a true stenotic lesion and torsion/curving of the nation reveals renal enlargement, reduced parenchymal
renal artery, which also exerts hemodynamic effects on echogenicity, diminished/absent corticomedullary differen-
blood flow and the maximum PSV (Peak Systolic Velocity tiation, and disappearance of the renal sinus and collecting
max); Power Doppler imaging can be useful in these cases. system (all of which are nonspecific). The two most
The iliac arteries should also be examined to evaluate the important CDUS findings are the absence of the venous
preanastomotic PVSmax because iliac stenosis can lead to color signal (reflecting absence of vascularization) and
reduced renal function similar to that observed in the pre- reverse diastolic flow within the renal artery [22] (Fig. 2).
sence of TRAS. For this reason, the recipient’s iliac vessels In the presence of complete TTRV, it is also impossible to
must also be subjected thorough pretransplant color demonstrate the intrarenal veins at the level of the hilum,

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Fig. 2 Thrombosis of the transplanted renal vein. a Color Doppler ultrasound shows ‘‘reverse’’ diastolic flow (below the baseline); b color
imaging of the hilar region shows two segmental arteries (A) and no flow in the renal vein (V)

Fig. 3 Stenosis of the

transplanted renal vein. a Color
Doppler ultrasound shows
external compression of the
homolateral external iliac vein
and b a significantly increased
PSV (200 cm/s)

and the high resistance caused by the renal vein thrombosis hypoechoic. A 3–4-fold increase in the PSV between the
results in pathognomonic bidirectional flow in the intrare- stenotic and prestenotic segments is regarded as highly
nal arteries (the arterial waveform will be positive during suggestive of focal stenosis [19].
systole and negative during diastole [23]. The net flow Angiography should be used only to confirm or treat
across the kidney drops to zero, as does the mean flow stenosis in patients with positive CDUS findings or in cases
velocity for each cardiac cycle. This bidirectional flow is so in which there is a strong clinical suspicion of stenosis
specific for TTRV that it is regarded as an indication for despite the indeterminate or equivocal imaging findings.
immediate surgical revision of the graft without further
diagnostic confirmation.
Stenosis of the transplanted renal vein is rare. It may be Arteriovenous fistulas and pseudoaneurysms
the result of compression of the vein by a perinephric fluid
collection (Fig. 3) or perivascular fibrosis. The CDUS These two lesions are reported mainly as biopsy complications.
findings are not as conclusive as they are in cases of TTRV. Their incidence ranges from 1 to 2 %. Arteriovenous fistulas
Indeed, the parenchyma may appear normal or mildly (AVFs) develop as a result of damage to the walls of an artery

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Fig. 4 Color Doppler

ultrasound shows large-caliber
interlobar artery and vein. The
resistance index of the nutrient
artery is 0.50 (vs. approximately
0.80 in other regions of the
graft). The venous spectrum
reflects markedly pulsatile flow
that cannot be found in other
interlobar veins. Post-biopsy
arteriovenous fistula (arrow);
a Doppler shows alternating
flow

and a vein during needle biopsy of the kidney. In contrast, placement of the graft (which occurs during combined
pseudoaneurysms can develop when the damage is limited to renal–pancreatic transplants) [19]. Because of its
the arterial wall [19]. Both lesions are generally small, clini- increased mobility, the kidney may rotate around the
cally silent, and likely to resolve spontaneously [19, 24]. vascular pedicle, causing vascular occlusion that will lead
On ultrasound, pseudoaneurysms appear as small cyst- to parenchymal necrosis and graft loss if not identified
like anechoic areas containing finely hyperechoic material promptly. The clinical presentation varies: it may
representing internal thrombi. CDUS reveals turbulence resemble acute rejection or renal vein thrombosis.
and ‘‘to-and-fro’’ flow resembling to that seen in pseudo- Ultrasonography can facilitate the diagnosis by docu-
aneurysms involving the arterial extremities [24]. menting a change in the orientation of the kidney, so that
Arteriovenous fistulas can be visualized in B-mode only if the hilum is anterior rather than posterior [26]. Color
they are large. On CDUS, they appear as focal areas with both Doppler ultrasound findings are variable with low diag-
arterial and venous flow (color mosaic pattern) (Fig. 4): this nostic accuracy. Dissection of the iliac artery and renal
pattern can be differentiated from high flow patterns by artery are extremely rare events, which are caused by
increasing the PRF until only the area with anomalous, dissection of the aorta and present the same features on
accelerated flow inside the AVF is visualized. This maneuver CDUS.
almost always produces diagnostic results. Spectral analysis
may show increased systodiastolic flow in the area of interest
with resistive and pulsatility indexes that are often normal or
lower than those of nearby vessels, whereas venous flow may Conclusions
be normal or turbulent, and pulsatile acceleration is present in
around 33 % of all cases [25]. In rare cases, AVFs are large In expert hands, color Doppler ultrasound can be a valid
enough to reduce renal perfusion and cause graft ischemia; tool for the diagnosis and follow-up assessment of the
pseudoaneurysms can cause complications if they rupture. vascular complications of renal transplantation. However,
Patients with large AVFs, who undergo repeated renal biop- additional, well-designed studies are needed to further
sies are at increased risk for hemorrhagic complications. For validate its role in these settings, and the nephrologist
AVFs, the need for treatment is related to the size of the lesion. responsible for the transplant recipient must be well
With pseudoaneurysms, there is always the risk of rupture, and versed in both the theory and practice of
for this reason, they should always be treated. ultrasonography.

Conflict of interest Antonio Granata, Silvia Clementi, Francesco

Rare vascular complications Londrino, Giulia Romano, Massimiliano Veroux, Fulvio Fiorini,
Pasquale Fatuzzo declare that they have no conflict of interest.

Torsion of the vascular pedicle of the transplanted kidney Human and animal studies The study described in this article did
is extremely rare. It is caused by intraperitoneal not include any procedures involving humans or animals.

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