AJR 2005; 184:1549-1555
© American Roentgen Ray Society
Hepatic Artery Pseudoaneurysms in Adult Living-Donor Liver Transplantation: Efficacy of CT and Doppler Sonography
Hyoung Jung Kim1,2,
Kyoung Won Kim1,
Ah Young Kim1,
Tae Kyoung Kim1,
Jae Ho Byun1,
Hyung Jin Won1,
Yong Moon Shin1,
Pyo Nyun Kim1,
Hyun Kwon Ha1,
Sung Gyu Lee3 and
Moon-Gyu Lee1
1 Department of Radiology, Asan Medical Center, University of Ulsan College of
Medicine, 388-1, Pungnap-dong, Songpa-ku, Seoul 138-736, Korea.
2 Department of Diagnostic Radiology, Kyung Hee University Hospital, Seoul,
Korea.
3 Department of Surgery, Asan Medical Center, University of Ulsan College of
Medicine, Seoul, Korea.
Received June 6, 2004;
accepted after revision September 13, 2004.
Address correspondence to K. W. Kim
(kimkw{at}amc.seoul.kr).
Abstract
OBJECTIVE. The purpose of this study was to evaluate the efficacy of
contrast-enhanced CT and Doppler sonography in the diagnosis of hepatic artery
pseudoaneurysm after adult living-donor liver transplantation (LDLT).
CONCLUSION. Because patients with hepatic artery pseudoaneurysm
after LDLT can have diverse clinical presentations, routine imaging follow-up
is important for early detection. Although Doppler sonography is limited in
showing the pseudoaneurysm, contrast-enhanced CT, especially MDCT with CT
arteriography, is effective in showing it in most patients.
Introduction
Living-donor liver transplantation (LDLT) has become a useful treatment
method for patients with end-stage liver disease. The recent evolution of LDLT
has led to its wide acceptance as the only realistic option to overcome the
organ shortage in many Asian countries where cadaveric organ harvesting is
limited
[1–5].
A comprehensive imaging strategy is required for the management of patients
after liver transplantation, as the diagnosis and management of complications
in the early postoperative period are important for graft and patient
survival. Doppler sonography and CT are commonly used for the detection and
diagnosis of complications in the hepatic vessels
[6,
7].
The development of hepatic artery pseudoaneurysm after liver
transplantation is rare but is associated with a high risk for early graft
loss and a high mortality rate in the recipients
[8–10].
The incidence, presenting features, and image findings of pseudoaneurysm have
been frequently reported
[8–13],
but most reports have a limited number of imaging evaluations. In addition,
recent advances in CT technology, such as MDCT and CT angiography, were not
incorporated into these previous reports. Thus, the efficacy of Doppler
sonography and CT for the diagnosis of hepatic artery pseudoaneurysm after
LDLT must be established. The purpose of this study was to evaluate the
efficacy of Doppler sonography and contrast-enhanced CT for the diagnosis of
hepatic artery pseudoaneurysm after LDLT.
Materials and Methods
Patients
Our study was a single-institution retrospective study. It was approved by
our institutional review board, but informed consent was not required for
retrospective review of patients' medical records and radiologic images.
We obtained from the LDLT database a list of 530 consecutive adult
recipients who underwent LDLT and routine postoperative Doppler sonography and
CT examinations at our institution between July 1999 and December 2003. After
a review of all radiologic reports and medical records, it was found that 15
patients had developed hepatic artery pseudoaneurysms. Among these patients,
those with procedure-related pseudoaneurysms, such as intrahepatic
pseudoaneurysms after liver biopsy (n = 1), percutaneous transhepatic
biliary drainage (n = 1), and anastomotic pseudoaneurysm after
balloon dilatation of the hepatic artery anastomosis (n = 1), were
excluded. In addition, a patient with hepatic artery pseudoaneurysm who had
not undergone a cross-sectional imaging study within 48 hr of diagnosis was
also excluded. The remaining 11 patients constituted the study population,
which included nine men and two women with a mean age of 53 years (range,
43–65 years). The underlying disease necessitating liver transplantation
was cirrhosis of the liver associated with hepatitis B virus (n = 6),
hepatocellular carcinoma and liver cirrhosis (n = 4), and biliary
cirrhosis (n = 1). LDLTs were performed using right-lobe (n
= 6), left-lobe (n = 4), or dual left-lobe grafts (n = 1).
Anastomosis of the hepatic artery was made in an end-to-end fashion to one of
the stumps of a main branch of the proper hepatic artery (n = 10) and
replaced left hepatic artery from left gastric artery (n = 1) of the
recipient. Verification of the hepatic artery pseudoaneurysm was made by
conventional hepatic arteriography (n = 8), surgery (n = 1),
or both (n = 2).
CT and Doppler Sonography Examinations
The routine imaging follow-up protocol using Doppler sonography and CT was
originally designed for the early detection of any vascular complication of
LDLT and did not focus on the detection of a pseudoaneurysm. Doppler
sonography examinations were performed on postoperative days 1, 2, 3, and 7,
and then every week to 1 month after LDLT. CT scans were obtained during
postoperative weeks 1, 2, and 4 after LDLT. MR 3D angiography partially
replaced postoperative 2- or 4-week follow-up CT to July 2000. Additional
Doppler sonography and CT scans were performed when clinically indicated.
Among the 11 patients with hepatic artery pseudoaneurysms after LDLT, six
underwent both Doppler sonography and CT and five underwent Doppler sonography
(n = 2) or CT (n = 3) within the 48 hr before verification
of the pseudoaneurysm.
Doppler sonography examinations were performed by experienced radiologists
using commercially available sonographic equipment such as HDI 3000 or 5000
units (Philips Medical Systems) (n = 4), a Logiq 700 unit (GE
Healthcare) (n = 1), or a Sequoia 512 unit (Acuson Solutions)
(n = 3), with a 2- to 4-MHz or 1- to 4-MHz curved array transducer.
The standard Doppler parameters were adjusted for maximal gain without
background noise, highest pulse-repetition frequency without aliasing
artifacts, a 2- to 5-mm Doppler sample gate, and a 125-Hz wall filter, for
optimal signal detection from the hepatic artery.
CT scans were obtained on helical CT scanners (Somatom Plus-4, Siemens
[n = 1] or 9800 Quick System, GE Healthcare [n = 2]) and
MDCT scanners (LightSpeed QX/I, GE Healthcare [n = 4] or Somatom
Sensation 16, Siemens [n = 2]). In all patients, 100–150 mL of
iopromide (Ultravist 370; Schering) was injected at a flow rate of 2.5–3
mL/sec using a mechanical injector. Contrast-enhanced CT scans were obtained
according to a single-phase protocol during the portal venous phase until July
2000 (n = 2) and thereafter with a dual-phase protocol during the
hepatic artery phase and the portal venous phase (n = 7). Continuous
5- or 7-mm-thick sections and 5- or 7-mm intervals were used with helical CT
scanners (n = 3). Variable detector-row configurations were used for
image acquisition on MDCT scanners (n = 6); 1.25 x 4 and 2.5
x 4 detector-row configurations were used for hepatic arterial phase
(HAP) and portal venous phase (PVP) in four patients and 0.75 x 16 in
two. HAP and PVP images were reconstructed at 2.5-mm and 5-mm intervals for
PACS (Radpia, Hyundai Information Technology). CT arteriography was
reconstructed using volume-rendering and maximum-intensity-projection
techniques on a workstation (Advantage Windows 3.0, GE Healthcare) in six
patients who underwent MDCT.
Image Analysis
Doppler sonography images were reviewed on a PACS monitor by two
experienced radiologists in consensus. The images were evaluated to determine
if a hepatic artery pseudoaneurysm was visualized; if it was visualized, its
size and location were recorded. Images were also evaluated for the presence
or absence of a fluid collection or hemorrhage around the liver transplant and
for abnormalities in the spectral waveform of the hepatic artery. CT scans
were reviewed on a PACS monitor by two experienced radiologists in consensus.
CT scans were also evaluated to determine if a hepatic artery pseudoaneurysm
was visualized; if it was visualized, its size and location were recorded. The
presence or absence of a fluid collection or hemorrhage around the liver
transplant and any abnormality in the graft parenchyma also were assessed. The
patients' medical records were reviewed for their clinical presentation by one
of the authors.
Results
The principal clinical findings, together with the Doppler sonography and
CT findings, are summarized in Table
1. Among the 11 hepatic artery pseudoaneurysms after LDLT, seven
were located in the arterial anastomosis while the other four were
preanastomosis: the common hepatic artery in two patients, right gastric
artery in one, and stump of hepatic artery in one. The patients with hepatic
artery pseudoaneurysms clinically presented with systemic hypotension caused
by intraabdominal bleeding (n = 5), incidental detection on routine
CT follow-up (n = 3), incidental detection on routine Doppler
sonography follow-up (n = 1), no detectable hepatic artery flow on
Doppler sonography (n = 1), or abnormal liver function tests
(n = 1). The median interval from LDLT to the diagnosis of
pseudoaneurysm was 10 days (range, 6–40 days).
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TABLE 1 Summary of the Patient Data and Radiologic Findings of Hepatic Artery
Pseudoaneurysm After Living-Donor Liver Transplantation
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Based on the results of Doppler sonography and CT examination, a
preangiographic or preoperative diagnosis of hepatic artery pseudoaneurysm was
possible in seven of the 11 patients. Of eight patients with hepatic artery
pseudoaneurysm who underwent Doppler sonography examinations within 48 hr
before angiography or surgery, pseudoaneurysm was detected in one patient
(13%); it was 1.5 cm in diameter and was located at the hepatic artery
anastomosis (Fig. 1A,
1B,
1C,
1D). Although pseudoaneurysms
were not seen in the other patients, Doppler sonography images showed no
Doppler-detectable intrahepatic arterial flow in two; a tardus-parvus pattern
of hepatic artery waveform in one; and fluid collection with internal echo
around the liver transplant, suggesting hematoma, in one patient,
respectively. Doppler sonography showed no abnormality in three patients.
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Fig. 1A. —63-year-old man with hepatic artery pseudoaneurysm detected
on Doppler sonography. Color Doppler sonogram at postoperative day 7 shows
periportal round structure with turbulent flow (white arrow).
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Fig. 1B. —63-year-old man with hepatic artery pseudoaneurysm detected
on Doppler sonography. Sudden hypotension developed next day. Hepatic artery
phase CT scan shows pseudoaneurysm (black arrow), extravasation of
contrast material (white arrow), and acute hematoma adjacent to
graft.
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Fig. 1C. —63-year-old man with hepatic artery pseudoaneurysm detected
on Doppler sonography. Maximum-intensity-projection image shows pseudoaneurysm
(white arrow) at hepatic artery anastomosis site.
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Of nine patients with hepatic artery pseudoaneurysms who underwent CT
within 48 hr before angiography or surgery, pseudoaneurysms were detected in
seven (78%); their mean diameter was 1.5 cm (range, 0.7–2.3 cm) and they
were located at the arterial anastomosis in three patients (Fig.
2A,
2B,
2C), the common hepatic artery
in two, right gastric artery in one, and stump of hepatic artery in one. MDCT
with CT arteriography was performed in six patients and showed pseudoaneurysm
in five (83%). Single-detector CT was performed in three patients and showed
pseudoaneurysm in two (67%). In two patients, CT scans could not show the
pseudoaneurysm. One patient (patient 5, Fig.
3A,
3B) was examined using MDCT
with CT arteriography; however, we could not show the pseudoaneurysm. The
other patient (patient 4) was examined using a single-detector CT scanner and
only portal venous phase images were acquired. Hematoma adjacent to the graft
was an associated finding in six of the nine CT examinations. Hepatic
infarction occurred in one patient. Partial thrombus of the common hepatic
artery near the pseudoaneurysm was found in two patients (Fig.
4A,
4B,
4C,
4D).
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Fig. 2B. —46-year-old man with mycotic pseudoaneurysm. Sudden
hypotension developed at postoperative day 19. Two consecutive hepatic artery
phase images show pseudoaneurysm (black arrow, C) and
extravasation of contrast material (white arrow, C). Emergency
surgery was performed to excise pseudoaneurysm and to reconstruct hepatic
artery.
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Fig. 2C. —46-year-old man with mycotic pseudoaneurysm. Sudden
hypotension developed at postoperative day 19. Two consecutive hepatic artery
phase images show pseudoaneurysm (black arrow, C) and
extravasation of contrast material (white arrow, C). Emergency
surgery was performed to excise pseudoaneurysm and to reconstruct hepatic
artery.
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Fig. 3A. —50-year-old woman with small hepatic artery pseudoaneurysm.
Hepatic artery phase CT scan at postoperative day 10 shows segmental
low-density lesion in left graft (white arrows). Hepatic artery
pseudoaneurysm is not seen.
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Fig. 3B. —50-year-old woman with small hepatic artery pseudoaneurysm.
Hepatic arteriogram shows small pseudoaneurysm (black arrow) and
narrowing of anastomosis site between hepatic artery of graft and left gastric
artery of recipient.
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Fig. 4A. —55-year-old man with hepatic artery pseudoaneurysm and
partial thrombosis. Serial hepatic artery phase CT scans at postoperative day
15 show hepatic artery pseudoaneurysm (black arrow, A) of
proximal common hepatic artery and partial thrombosis (white arrow,
B).
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Fig. 4B. —55-year-old man with hepatic artery pseudoaneurysm and
partial thrombosis. Serial hepatic artery phase CT scans at postoperative day
15 show hepatic artery pseudoaneurysm (black arrow, A) of
proximal common hepatic artery and partial thrombosis (white arrow,
B).
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Discussion
In liver transplantation, vascular complication is an important
consideration in patients with graft dysfunction, bile leak, intraabdominal
bleeding, or hemobilia. The relatively common complications are hepatic artery
thrombosis, stenosis, portal vein thrombosis, inferior vena caval thrombosis,
and bile duct stenosis [14].
Hepatic artery pseudoaneurysm is a rare complication and the diagnosis is
often delayed, but it is associated with a high mortality rate
[8].
Hepatic artery pseudoaneurysms can be classified as intrahepatic or
extrahepatic according to their location. Intrahepatic pseudoaneurysms are
mostly related to previous procedures such as liver biopsy and percutaneous
transhepatic biliary drainage
[15]. Extrahepatic
pseudoaneurysms have a different pathogenesis from intrahepatic
pseudoaneurysms. Reportedly, the most important risk factor was local sepsis
[8,
9,
16,
17], which is frequently
associated with the formation of a Roux-en-
hepaticojejunostomy that
creates the potential for colonization of the subhepatic space by enteric
organisms. Adhesion, fungal septicemia, pancreatitis, and technical
difficulties in the arterial anastomosis are other risk factors
[8]. We excluded three
procedure-related hepatic artery pseudoaneurysms from our study group because
of differences in pathogenesis and location.
In our study, the median interval between the LDLT and the diagnosis of
pseudoaneurysm was 10 days. Previous studies reported that most hepatic artery
pseudoaneurysms occurred within the 2 months after surgery
[8,
9]. Our study identified
mycotic pseudoaneurysm in one patient (Fig.
2A,
2B,
2C); this was a relatively low
incidence compared with previous reports
[8–10].
Our low incidence might have been due to the relatively low rate of surgical
confirmation of pseudoaneurysm and early detection of pseudoaneurysm before it
was infected.
In our series, clinical presentation of the pseudoaneurysms was diverse.
Five of 11 pseudoaneurysms presented with hypotension, a common presentation
in previous reports [8,
9]. However, the other six
presented as an incidental finding on routine follow-up examination
meticulously performed as a surveillance method for possible postoperative
vascular complications (n = 5) or laboratory abnormality (n
= 1). The results of our study suggest that routine imaging follow-up is
important in the detection of hepatic artery pseudoaneurysm.
Doppler sonography has been considered the primary imaging technique to
detect vascular complications after liver transplantation
[18]. The ability to perform
this examination at the patient's bedside and the absence of radiation hazards
make it an ideal first-line examination. However, in our study, only one
pseudoaneurysm (13%) was detected among eight Doppler sonography evaluations.
Although the vascular anastomosis site was included in the field of
examination, detection of pseudoaneurysm itself was difficult. The results of
our study are consistent with those of previous studies stating that the
sonographic detection rate of extrahepatic pseudoaneurysm is lower than that
of intrahepatic [8]. The
relatively poor sonic window of the extrahepatic portion and low suspicion of
the hepatic artery pseudoaneurysm during the sonographic evaluation may cause
a low detection rate. Nevertheless, in our series, Doppler sonography showed
abnormal hepatic artery flow spectrum (n = 3) and hematoma
(n = 1), and this led us to further evaluation, such as hepatic
arteriography or CT evaluation.
Among the nine CT evaluations, seven hepatic artery pseudoaneurysms were
detected (78%). It was a higher score than previous reports
[8,
9] and slightly lower than a
recent report [19] using CT
arteriography to evaluate hepatic artery complications. This high detection
rate may result from the advances in CT technology. In our study, MDCT with CT
arteriography could identify a pseudoaneurysm in five of the six CT
examinations; however, single-detector CT identified it in two of the three.
MDCT examinations ensured the selection of the optimal scanning time for the
arterial phase and provided routine acquisition of thin-section images for CT
arteriography. In two patients, CT scans could not show the pseudoaneurysm
itself; other findings, such as hepatic infarction and hematoma, prompted the
performance of hepatic arteriography (Fig.
3A,
3B).
We could find the false-positive diagnosis of pseudoaneurysm in two
patients from the LDLT database. One was an extravasation of contrast material
from the hepatic arterial anastomosis site that mimicked pseudoaneurysm. The
other was a branch of proper hepatic artery that was ligated during surgery.
This hepatic arterial stump was misinterpreted as a pseudoaneurysm. On Doppler
sonography, the false-positive diagnosis was not found. A low suspicion by
radiologists during examination and poor sonic window of arterial anastomosis
site may have been the cause.
In our series, hepatic arterial stenosis was frequently associated with
hepatic artery pseudoaneurysm and was seen in five of 10 patients who
underwent hepatic arteriography. Among these patients, three showed an
abnormal artery flow spectrum on Doppler sonography. Therefore, we believe
that a high index of suspicion and close scrutiny of the arterial anastomosis
site are required in Doppler sonography if there is abnormality in the hepatic
artery flow spectrum, especially in the early postoperative period as
previously reported [20].
Our study has several limitations. First, in five of the 11 patients with
hepatic artery pseudoaneurysm, only one examination (Doppler sonography or CT)
was performed. This may have caused a bias in our study and could have
devalued a comparison of the two techniques. However, in six patients on whom
both Doppler sonography and CT examinations were performed, CT detected
hepatic artery pseudoaneurysms (n = 4) more frequently than Doppler
sonography (n = 1).
Second, we could not obtain sensitivity and specificity of CT and Doppler
sonography because we did not review all CT, Doppler sonography, and hepatic
arteriography images of 530 patients. Practically, it was impossible to review
all radiologic images of these patients.
The third limitation was that our study group included the heterogeneous CT
and sonographic equipment. Hepatic artery pseudoaneurysm is a rare
complication; therefore, we needed a long-term study period. Thus, this
limitation was unavoidable.
In conclusion, patients with hepatic artery pseudoaneurysm after adult LDLT
may show diverse clinical presentations; routine imaging follow-up is
important for its early detection. Although Doppler sonography is limited in
the visualization of hepatic artery pseudoaneurysm, contrast-enhanced CT,
especially MDCT with CT arteriography, is effective in showing hepatic artery
pseudoaneurysm and associated findings in most patients.
Acknowledgments
We thank Bonnie Hami, Department of Radiology, University Hospitals Health
System, Cleveland, Ohio, for editorial assistance in preparing the
manuscript.
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Abstract
Introduction
