1285

Imaging of Vascular Complications

After Hepatic Transplantation

Kenneth Dalen1 Vascular complications after hepatic transplantation can compromise graft and patient
Deborah L. Day1 survival. Angiography defines the need for revascularization or retransplantation, but
Nancy L. Ascher the value of noninvasive imaging in this sethng is not clear. To assess the relative merit
of noninvasive imaging techniques (sonography, scintigraphy, CT, and MR), we retro-
David W. Hunter1
spectively reviewed 19 major vascular complications that occurred in 15 of 98 hepatic
Williarn M. Thompson1
recipients over a 3’/2-year period. Portal venous thrombosis was seen in seven patients,
Wilfrido R. Castaneda-Zuniga1 donor aortic or hepatic arterial thrombosis in seven, and inferior vena caval thrombosis
Janis Gissel Letourneau1 in five. Sonography provided the Initial diagnosis of portal venous thrombosis in three,
arterial compromise in five, and caval obstruction in four. CT was the first diagnostic
examination to identity portal occlusion in two, donor aortlc thrombosis in one, and
inferior vena caval thrombosis in one. Scintigraphy and MR imaging provided comple-
mentary data.
Both sonography and CT are useful in the evaluation of vascular complications that
occur after hepatic transplantation; however, neither is sufficiently sensitive to obviate
angiographic assessment

Hepatic transplantation has become an accepted therapeutic option for many

patients with irreversible liver failure [1 -3]. However, life-threatening complications
can arise in hepatic recipients, the most ominous being vascular thromboses, as
they frequently require immediate intervention. Clinical signs of arterial thrombosis
include fever, septicemia, elevated serum liver enzymes, and deteriorating coagu-
lation parameters [4, 5]. Arterial occlusion can lead to devastating complications,
such as biliary stricture and leaks and parenchymal ischemia or necrosis [4, 6].
Likewise, thromboses of the portal vein and inferior vena cava can lead to significant
problems, including fever, septicemia, impaired hepatic function, bleeding in the
upper gastrointestinal tract, ascites, and peripheral edema [7].
The diagnosis of vascular thrombosis after hepatic transplantation has relied on
angiography [8, 9]. The role of noninvasive imaging in this setting has not been
extensively evaluated [8, 1 0]. We reviewed our experience with vascular compli-
cations in hepatic recipients to determine the value of noninvasive imaging in these
Received December 2, 1987; accepted after re-
vision January 27, 1988. patients.
This work was supported by a research grant #
SMF-566-87 from the Minnesota Medical Founda- Materials and Methods
tion, Minneapolis, MN, 55455.
I Department of Radiology, University of Minne- Between April 1 1984, and September 15, 1987, 98 orthotopic liver transplants were
,

sets Hospital and Clinic, Box 292 UMHC, 420 Del- performed in 94 patients (41 adults, 53 children) at the University of Minnesota Hospitals.
aware St. SE., Minneapolis, MN 55455. Address The surgical techniques [1 1] and immunosuppressive regimens [1 2] used are described in
reprint requests to J. G. Letoumeau.
detail elsewhere. Nineteen postoperative vascular complications were seen in 1 5 patients
2 Department of Surgery, University of Minne-
(Table 1). Indications for transplantation in these 15 patients included extrahepatic biliary
sota Hospital and Clinic, Minneapolis, MN 55455.
atresia (seven), alpha-1-antitrypsin deficiency (three), Wilson disease (one), chronic active
Present address: Department of Surgery, University
of California, San Francisco, CA 94143. hepatitis (one), primary biliary cirrhosis (one), primary hepatoma (one), and sclerosing cholan-
gitis (one). The radiographic examinations (including scintigraphy, sonography, CT, MR
AJR 150:1285-1290, June 1988
0361 -803X/88/1 506-1285 imaging, and angiography) and hospital records of these patients were reviewed retrospec-
© American Roentgen Ray Society tively.
1286 DALEN ET AL. AJA:150, June 1988

Patients were referred for radiologic evaluation when vascular and angiography was not performed. In one pediatric patient,
occlusion was suspected because of persistent fever, deteriorating CT was falsely negative for thrombosis, and angiography was
liver function, and/or abnormal coagulation parameters. From the
used to make the initial diagnosis within 3 days. Five children
time of transplantation to the time of initial diagnosis of vascular
with arterial thrombosis have died; the mean interval from
thrombosis, a total of 105 examinations were performed (48 scinti-
transplantation to diagnosis was 4 weeks (range, 1 .5 weeks
grams, 33 sonograms, 21 CT scans, and three angiograms). Hepa-
to 2 months). The mean survival of these children was 73
tobiliary scintigraphy was performed with rapid-sequence; immediate;
1 0-, 20-, 30-, 40-, 50-, and 60-mm; and, if necessary, delayed imaging. days (range, 1 0-240). Of the two patients surviving arterial
Sonography was performed as described elsewhere; Doppler duplex occlusion, the interval from transplantation to diagnosis was
scanning techniques were used in the latter half of the study period much greater (51/2_38 months).
[1 3-i 5]. CT scanning was performed with IV contrast material by
using bolus and drip-infusion administration if possible. Our MR
techniques for definition of the upper abdominal vasculature have Portal Vein Thrombosis
also been reported [1 6, 17]. Angiographic techniques included ab-
Seven cases of portal venous thrombosis were identified
dominal aortography; hepatic, celiac, or mesenteric arteriography;
(Tables 2 and 3). Reduced uptake/delayed extraction on
splenoportography; inferior venacavography; wedged hepatic yen-
ography; and transhepatic portal venography. hepatobiliary scintigraphy was seen in three patients. The
Fifteen cases of vascular complications were confirmed by direct diagnosis of thrombosis was first identified by sonography in
examination, including angiography (seven), exploratory laparotomy three patients (Fig. 3), CT in two, angiography in one, and
(one), postmortem examination (four), or a combination of these laparotomy in one. Six of the seven patients had verification
examinations (three). Four patients merited a diagnosis of vascular of thrombosis by either angiography or postmortem exami-
thrombosis with noninvasive imaging techniques alone; inclusion in nation. One false-negative sonogram was identified after an-
this series required evidence for thrombosis on at least two nonin- giography later the same day showed portal vein occlusion.
vasive studios. The mean interval from transplantation to diagnosis was 2.3
weeks (range, 1-6 weeks). Three children have died, while
Results three children and one adult have survived.

Hepatic Artery/Donor Aorta Thrombosis

Inferior Vena Caval Thrombosis
Arterial thrombosis (hepatic artery in three cases and donor
aorta in four) was observed in six children and one adult. All Inferior vena caval thrombosis was seen in five patients
patients underwent hepatobiliary disofenin scintigraphy, (Tables 2 and 3); the diagnosis was first made by sonography
which showed focal areas of decreased uptake in two. Throm- in four (Fig. 4) and by CT in one. Surgical or postmortem
bosis was first diagnosed by sonography in three patients verification was available in three. Hepatobiliary scintigraphy
(Fig. 1), CT in one (Fig. 2), angiography in one, laparotomy in showed decreased excretion in all five patients. Three patients
one, and postmortem examination in one (Tables 2 and 3). (two adults, one child) experienced caval thrombosis within 2
Five cases of arterial occlusion were confirmed by angiogra- days of transplantation and death was imminent (mean sur-
phy, surgery, or postmortem examination. In one patient, CT, vival, 8 days after transplantation; range, 7-9). The diagnosis
sonography, and MR imaging were believed to be definitive of caval thrombosis was made later in the two survivors (1

TABLE 1: Hepatlc Transplant Vascular Complications

c::e Noninva:ive Diagnostic

Transplant Location of Thrombosis
(years)
1 40 Donor aorta NM, sonography, CT, MR
2 3V2 Donor aorta, inferior vena NM, sonography, CT
cava
3 5 Hepatic artery NM
4 3 Donor aorta NM, sonography, CT
5 4 Portal vein, hepatic artery NM
6 71/2 Donor aorta NM, sonography, CT
7 13 Portal vein NM, sonography, CT
8 1#{189} Portal vein NM, sonography, CT
9 37 Inferior vena cava NM, sonography, CT
10 2 Portal vein, inferior vena cava NM, sonography, CT
11 #{190} Portal vein NM, sonography, CT
12 1V2 Portal vein, hepatic artery NM, sonography, CT
13 49 Portal vein NM, sonography, CT
14 43 Inferior vena cava NM, sonography, CT
15 1 V2 Inferior vena cava NM, sonography

Note-NM = nuclear medacine (hepatobiliary scintigraphy).

AJA:150, June 1988 COMPLICATIONS AFTER HEPATIC TRANSPLANT 1287

A B C
Fig. 1.-case 12: 1’/2-year-old girl with sepsis and abnormal coagulation parameters immediately after transplantation. Hepatic necrosis was suspected
clinically.
A, Transverse duplex sonogram of liver reveals absence of hepatic arterial flow and inhomogeneous hepatic parenchyma.
B, Abdominal aortogram shows occlusion at anastomosis of native hepatic artery with donor celiac axis (arrow).
C, Percutaneous cholangiogram reveals numerous intrahepatic biliary strictures (long arrows) and multiple areas of extraductal contrast material (short
arrows) compatible with bile leak.

Fig. 2.-Case 1: 43-year-old woman with abdominal fullness and elevated liver enzymes 38 months after hepatic transplantation.
A, CT scan through mid abdomen shows low-attenuation thrombus in donor aortic graft (arrows).
B, Transverse 12-weighted MR scan at same level also shows high-signal-intensity aortic graft thrombus (arrows).
C, Coronal Ti-weighted MR image shows intermediate soft-tissue-density signal of thrombus in donor aorta near its anastomosis with iliac artery
(arrows).

and 6 months). One of these patients developed caval throm- malities. Therefore, differentiation of causes of graft dysfunc-
bosis 2 weeks after donor aorta thrombosis, and the other tion (ischemic injury, biliary obstruction, rejection, or infection)
developed caval thrombosis after portal thrombosis. is often difficult without radiologic evaluation [1 0, 1 8, 19].
Radiologic evaluation of the hepatic allograft frequently
involves the use of several techniques. Disofenin scintigraphy
Discussion
primarily assesses hepatocellular function and biliary excre-
Improved survival after hepatic transplantation is attribut- tion [1 0, 1 1 , 1 9]. Sonography can be used to evaluate the
able to more effective immunosuppression, surgical ad- hepatic parenchyma, and the addition of duplex scanning
vances, and meticulous postoperative care. Nevertheless, a capabilities permits differentiation between vascular and bili-
number of posttransplantation complications occur that often ary structures and reliably documents vascular integrity [10,
present with nonspecific symptoms and laboratory abnor- 1 3, 1 4, 20]. CT provides a means of determining the gross
1288 DALEN ET AL. AJA:150, June 1988

Fig. 3.-Case 13: 49-year-old man 10 days

after transplantation, with bleeding from gastro-
esophageal varices and increasing serum liver
enzymes.
A, Transverse sonogram with duplex scan-
ning shows no portal venous flow.
B, Dynamic abdominal CT scan shows
inhomogeneous density in portal vein (arrows),
confirming sonographic findings. Incomplete oc-
clusion of portal vein was substantiated angie-
graphically 3 weeks later when duplex sonogra-
phy also showed reconstitution of flow within
vessel.

TABLE 2: ConfIrmed Postoperative Vascular Complications After Liver Transplantation

Complication: Means of s b uent Confirmation Time after Status at

Case No. Diagnosis u Transplantation Follow-up
Hepatic artery/donor aorta thrombosis:
2 Sonography CT, angiography 5V2 months Alive
3 Autopsy None 1 1/2 weeks Died
4 Angiography Surgery, autopsy 2 months Died
5 Surgery Autopsy 2 weeks Died
6 Sonography Angiography, autopsy 2 weeks Died
12 Sonography Angiography 6 weeks Died
Portal vein thrombosis:
5 Surgery Autopsy 2 weeks Died
7 CT Sonography, angiography 3 weeks Died
8 Angiography Inferior venacavography 1 week Alive
10 Sonography CT, angiography 1 V2 weeks Alive
12 Sonography Angiography 6 weeks Died
13 Sonography CT, angiography 1 V2 weeks Alive
Inferior vena cava thrombosis:
9 Sonography Inferior venacavography 2 days Died
14 Sonography Surgery 2 days Died
15 Sonography Autopsy 1 day Died

TABLE 3: Vascular Complications After Liver Transplantation without Angiographic, Surgical, or Postmortem Confirmation

Case Means of Corroborative Time after Status at

Com p lcat’
I 10 n
No. Diagnosis Studies Transplantation Follow-up

1 Donor aorta thrombosis CT Sonography, MR 38 months Alive

2 Inferior vena cava thrombosis Sonography CT 6 months Alive
10 Inferior vena cava thrombosis CT 2D echocardiography 1 month Alive
11 Portal vein thrombosis CT Sonography 1 week Alive
Note.-2D = two-dimensional.

structural integrity of the hepatic allograft [1 0, 1 9-21] and the hepatic transplantation has not been defined precisely [8, 10,
patency of major vascular structures [21 , 22]. MR appears to 20].
be most valuable for documenting the patency of the graft Thrombotic phenomena are particularly critical to graft func-
vasculature [1 6, 1 7, 23]. However, the role of these nonin- tion because collateral circulation is not reconstructed and
vasive tests in the diagnosis of vascular complications after may take months or years to develop. The true rate of
AJR:150, June 1988 COMPLICATIONS AFTER HEPATIC TRANSPLANT 1289

Fig. 4.-Case 9: 37-year-old woman with 7.5-

kg weight gain 2 days after hepatic transplanta-
tion.
A, Longitudinal sonogram reveals area of in-
creased echogenicity at infrahepatic caval anas-
tomosis wIth obliteration of lumen (arrows).
B, Inferior venacavogram shows complete oc-
clusion of inferior vena cava at distal inferior
vena caval anastomosis (white arrows) with ccl-
lateral flow through hemlazygous system (black
arrows) and reflux into renal veins.

occurrence of arterial thrombosis is unknown, but rates of In summary, noninvasive imaging is valuable in diagnosing
3.4-1 2% in adults and 1 1 .8-42% in children have been vascular complications after hepatic transplantation. The high
reported [4, 20]. In our series, 2.3% of adult and 1 0.9% of fatality rate (60% in our series) associated with vascular
pediatric recipients (overall occurrence rate, 7.1 %) developed complications after hepatic transplantation emphasizes the
arterial compromise. If thrombosis occurs early in the post- importance of prompt and accurate diagnosis for determina-
transplantation period, the prognosis is grim and retransplan- tion of appropriate treatment. In our study, 1 4 (74%) of 19
tation may be indicated; if it develops later, survival is more instances of vascular thrombosis were initially diagnosed by
likely and possibly is enhanced by the development of collat- noninvasive techniques, 1 0 (53%) by sonography and four
eral circulatory pathways [4, 20]. In our study, arterial throm- (21 %) by CT. However, two examinations in our series were
bosis was first diagnosed by noninvasive imaging techniques falsely negative, and the diagnosis ultimately was made by
in four (57%) of seven patients. Because sonographic and CT angiography in both. Our data reinforce the roles cited by
examinations can be falsely negative, aggressive angio- several authors of scintigraphy, sonography, and CT as
graphic evaluation may be required. The sensitivity and spec- screening tools in determining which patients need more
ificity of each noninvasive imaging method cannot, unfortu- aggressive interventional evaluation [8, 1 0, 1 5, 21]. The use
nately, be determined from our series, because definitive of MR for evaluating upper abdominal vasculature has exciting
angiography, surgery, or autopsy was not performed in every implications in the evaluation of these patients; refinements
hepatic recipient during the study period. in MR may preclude angiography in certain cases.
Portal vein thrombosis is also associated with significant
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