AJR 2004; 183:1577-1584
© American Roentgen Ray Society
Does Variant Hepatic Artery Anatomy in a Liver Transplant Recipient Increase the Risk of Hepatic Artery Complications After Transplantation?
Kousei Ishigami1,
Yan Zhang1,
Stephen Rayhill2,
Daniel Katz2 and
Alan Stolpen1
1 Department of Radiology, University of Iowa, Carver College of Medicine, 200
Hawkins Dr., 3885 JPP, Iowa City, IA 52242-1077.
2 Department of Surgery, University of Iowa, Carver College of Medicine, IA
City, Iowa 52242-1077.
Received March 6, 2004;
accepted after revision May 17, 2004.
Address correspondence to K. Ishigami
(kousei-ishigami{at}uiowa.edu).
Abstract
OBJECTIVE. Our aim was to determine whether variant hepatic artery
anatomy in a liver transplant recipient increases the risk of hepatic artery
complications after liver transplantation.
MATERIALS AND METHODS. The study group consisted of 84 patients who
underwent gadolinium-enhanced 3D MR angiography before orthotopic liver
transplantation in which a branch patch arterial anastomosis at the
gastroduodenal takeoff was used. MR angiography studies were retrospectively
reviewed and assessed for the presence and type of variant hepatic artery
anatomy. The diameter of the distal common hepatic artery was measured. The
incidence of posttransplantation hepatic artery stenosis or thrombosis was
assessed.
RESULTS. Seven (8.3%) of the 84 patients developed hepatic artery
complications after transplantation. Of the 24 patients with variant hepatic
artery anatomy, five (20.8%) had posttransplantation/ hepatic artery
complications. In contrast, only two (3.3%) of the 60 patients with classic
hepatic artery anatomy had complications. The higher complication rate in
patients with variant hepatic artery anatomy was statistically significant
(p < 0.05). The odds ratio was 7.6 (95% confidence interval,
1.442.6). The diameter of the distal common hepatic artery was smaller
in patients with variant hepatic artery anatomy compared with those with
classic hepatic artery anatomy (range, 4.37.1 mm [mean, 5.8 mm] vs
4.08.9 mm [mean 6.3 mm], p < 0.05), and it was also smaller
in patients who had posttransplantation hepatic artery complications compared
with those who had no complications (range, 4.26.3 mm [mean, 5.2 mm] vs
4.08.9 mm, [mean, 6.2 mm], p < 0.01).
CONCLUSION. Variant hepatic artery anatomy in a liver transplant
recipient increased the risk of hepatic artery complications after
transplantation. The smaller caliber of the native common hepatic artery may
contribute to the higher risk.
Introduction
Liver transplantation is the treatment of choice for patients with
end-stage liver disease. Vascular complications after liver transplantation
are associated with a poor outcome for both the graft and the patient
[1]. The most common vascular
complication after liver transplantation is hepatic artery thrombosis,
occurring in 212% of transplants
[24].
Hepatic artery stenosis is the second most common vascular complication,
occurring in 211% of transplants
[57].
Variant hepatic artery anatomy is common, with a reported incidence of
2345%
[813].
Conventional angiography is the standard of reference for defining the hepatic
vasculature before liver transplantation, but noninvasive alternatives, such
as MR angiography and CT angiography, are being used with increasing
frequency. The vascular road map provided by CT angiography impacts patient
selection and surgical planning for liver transplantation
[14]. Several reports have
indicated that gadolinium-enhanced 3D MR angiography provides similar
information but does not expose patients to ionizing radiation or nephrotoxic
contrast materials [10,
15]. At our institution, MR
angiography has largely replaced conventional angiography for evaluating
patients before liver transplantation.
A small-caliber native hepatic artery in a liver transplant recipient
increases the surgical complexity of creating a patent and durable anastomosis
between donor and recipient arteries. We have observed that variant hepatic
artery anatomy and a small-caliber common hepatic artery often coexist; this
observation can be explained by the fact that the common hepatic artery, for
example, supplies only the left lobe of the liver if there is a replaced right
hepatic artery from the superior mesenteric artery. In fact, this observation
would be predicted for variants that cause a diminution of flow in the common
hepatic artery [16]. We
hypothesized that variant hepatic artery anatomy in a liver transplant
recipient (as depicted on gadolinium-enhanced 3D MR angiography) increases the
risk of hepatic artery complications after liver transplantation. To our
knowledge, this hypothesis has not been previously explored in the radiology
literature.
Materials and Methods
Patient Population
Between January 2000 and December 2003, 165 consecutive patients underwent
orthotopic liver transplantation at our institution. Comprehensive liver MRI
and gadolinium-enhanced 3D MR angiography were performed preoperatively in 98
of these patients to assess vascular anatomy, detect focal liver lesions, and
identify sequelae of portal hypertension such as varices and enlarged venous
collaterals. Five of the 98 patients were excluded because they had undergone
a prior liver transplantation. Two adult patients who had undergone hepatic
lobectomy for hepatocellular carcinoma (HCC) were also excluded. All three
pediatric patients were excluded because their hepatic vessels were very small
and the liver transplantation technique was different from that used in
adults. Furthermore, four patients who had undergone aortic jump graft were
also excluded because the arterial reconstruction was different and the
diameter of the native common hepatic artery did not affect the incidence of
hepatic artery complications (described in Liver Transplantation). The study
group consisted of the remaining 84 patients, all of whom underwent
preoperative MR angiography and liver transplantation. The institutional
review board at our hospital approved this retrospective study.
Fifty-five males and 29 females who ranged from 13 to 69 years old (mean
age, 52.4 years) were in the study group. The causes of end-stage liver
disease and the indications for liver transplantation are summarized in
Table 1. Hepatitis C
(n = 16) was the most common cause, followed by alcoholic liver
disease (n = 12). Eleven patients had both. Eleven of 84 patients had
HCC. Of the 11 patients with HCC, five underwent radiofrequency ablation
either before (n = 3) or after (n = 2) MR angiography. The
number of HCC tumor nodules ranged from one to four (mean, 1.5), and the size
of the largest nodule ranged from 1.4 to 4.5 cm (mean, 2.6 cm). All three
patients with HCC tumor nodules larger than 3 cm had undergone radiofrequency
ablation before MR angiography. One patient had a transjugular intrahepatic
portosystemic shunt stent placed before MR angiography. However, the stent did
not compromise depiction of the hepatic arteries. None of the patients in the
study group underwent hepatic artery chemoembolization or coronary vein coil
embolization.
The medical records and operative reports were reviewed to determine the
type of hepatic artery anastomosis used for the liver transplant and the
incidence of posttransplantation hepatic artery stenosis and thrombosis. The
postoperative follow-up period ranged from 40 days to 3.7 years (mean, 1.5
years).
MR Angiography
Gadolinium-enhanced 3D MR angiography was performed on a 1.5-T scanner
(CV/i LX, GE Healthcare) equipped with a four-element torso coil. All MR
angiography studies were part of a comprehensive liver examination that
included both MRI and MR angiography. The delay between contrast injection and
image acquisition for the arterial phase of MR angiography was determined
using a contrast-bolus timing run through an oblique sagittal segment of the
mid abdominal aorta. Three milliliters of gadodiamide (Omniscan, Nycomed)
followed by a 25 mL of saline flush was injected into the antecubital vein at
3 mL/sec. MR angiography was a 3D fast spoiled gradient-echo sequence
performed with an axial (n = 75), coronal (n = 4), or
sagittal (n = 5) volume and the following parameters: TR range/TE
range, 45/0.81.3 (fractional echo); flip angle,
1520°; bandwidth, 83 kHz; matrix, 256 x 128160;
partition thickness, 34 mm; partitions, 3050; field of view,
3444 x 2533 cm; signal average, 1; zero-filling in the
slice direction, 2 times; sequential phase-encode ordering; and acquisition
time, 1925 sec. The parameters were adjusted to include the entire
liver and the hepatic vasculature and to provide the highest spatial
resolution within an acceptable breath-hold period for the patient. An
unenhanced MR angiography data set was acquired to familiarize the patient
with the breath-holding instructions, confirm appropriate placement of the
imaging volume, and provide a mask for subtraction images. Subsequently, one
arterial and two venous phase MR angiography data sets were acquired, each
during end-inspiration. Gadodiamide at 0.2 mmol/kg was power-injected
(Spectris, Medrad) through a 20- or 22-gauge IV at 3 mL/sec, followed by a
25-mL saline flush at the same rate.
Liver Transplantation
All patients underwent cadaveric liver transplantation. The interval
between MR angiography and liver transplantation ranged from 3 to 561 days
(mean, 144 days). The standard technique at our institution includes a branch
patch arterial anastomosis, which is almost always formed at the takeoff of
the gastroduodenal artery from the common hepatic artery
[17]
(Fig. 1A). However, four
patients required an infrarenal aortic jump graft, which was formed from the
donor's iliac artery [18]
(Fig. 1B). Of these four
patients, two had variant hepatic artery anatomy and a small-caliber common
hepatic artery (one had a replaced right hepatic artery, and the other had
both a replaced right hepatic artery and an accessory left hepatic artery). A
third patient had a severe stenosis of the native celiac artery, and the
fourth patient had a replaced right hepatic artery and a moderate celiac
stenosis. At our institution, a branch patch anastomosis is preferred to an
aortic jump graft because the former is simpler, and the aortic jump graft is
reserved for possible future retransplantation. The decision concerning
whether to use an aortic graft is based on an intraoperative assessment of the
quality and flow of the vessels. Doppler sonography is not routinely used to
measure hepatic artery flow. Muiesan et al.
[18] reported that the
incidence of hepatic artery thrombosis in aortic jump grafts was similar to
that in standard hepatic artery anastomoses.

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Fig. 1A. Surgical reconstruction of hepatic artery. Schematic of
branch patch arterial anastomosis shows that in recipient, branch patch is
formed at origin of gastroduodenal artery from common hepatic artery. In
donor, branch patch is typically formed at origin of splenic artery from
celiac trunk. RHA = right hepatic artery, LHA = left hepatic artery, GDA =
gastroduodenal artery, PHA = proper hepatic artery, CHA = common hepatic
artery, LGA = left gastric artery.
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Fig. 1B. Surgical reconstruction of hepatic artery. Schematic shows
that aortic jump graft typically consists of common and external iliac
arteries from donor. One end of graft is joined to infrarenal abdominal aorta
in recipient via end-to-side anastomosis; other end of graft is joined to
hepatic artery of donor via branch patch anastomosis, as described in
A.
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The standard surgical technique was also modified whenever there was
variant hepatic artery anatomy in the donor liver, including a replaced right
hepatic artery from a superior mesenteric artery (n = 6), an
accessory left hepatic artery (n = 3), a replaced left hepatic artery
(n = 2), a replaced right hepatic artery and an accessory left
hepatic artery (n = 2), an accessory right hepatic artery (n
= 1), and a replaced right hepatic artery from the celiac trunk (the so-called
double hepatic artery, n = 1). For donor livers with a replaced right
hepatic artery, the hepatic artery anastomosis was formed in two parts: a
primary anastomosis between the donor celiac artery with an aortic patch
(called a Carrel patch) and the recipient branch patch at the gastroduodenal
artery takeoff and a secondary anastomosis between the replaced right hepatic
artery and the proximal stump of the donor splenic artery. For donor livers
with a replaced or accessory left hepatic artery, a similar strategy was used,
but only the primary anastomosis (donor celiac artery with aortic patch) was
formed [17].
Image Analysis
The MR angiography data were transferred to an off-line UNIX-based computer
workstation (Advantage Windows, GE Healthcare) for review and postprocessing.
MR angiograms were reviewed retrospectively using multiplanar reformations and
maximum intensity projections (MIP) (full volume and targeted) by two of the
authors to quantify the degree to which distal hepatic artery branches could
be visualized. For this purpose, the following qualitative scale was
developed: poor, visualization of the proper hepatic artery; fair,
visualization of the main right and left hepatic arteries; good, visualization
of the segmental branches of the right and left hepatic arteries; and
excellent, visualization of the subsegmental branches of the right and left
hepatic arteries. Any MR angiogram receiving a score of poor was considered
unsuitable for evaluating variant hepatic artery anatomy. The retrospective
assessment of hepatic artery anatomy was made by consensus between the two
reviewers. In all cases, the surgical record served as the standard of
reference for the presence and type of variant hepatic artery anatomy.
Two radiologists measured the diameter of the distal common hepatic artery
near the origin of the gastroduodenal artery. In each case, the reviewers used
targeted MIP images generated by each reviewer on the computer workstation to
identify the gastroduodenal artery takeoff. The measurements were obtained
twice on the computer workstation by using electronic calipers and the
magnification tool. The average diameters were calculated and recorded.
Statistical Analysis
The frequency of hepatic artery complications after liver transplantation
was compared for patients having classic and variant hepatic artery anatomy.
In classic anatomy, the right and left hepatic arteries arise from a single
proper hepatic artery, which in turn arises from a single common hepatic
artery, which arises from the celiac artery. The data were analyzed using
Fisher's exact test; a p value of less than 0.05 was considered
significant. The odds ratio and 95% confidence intervals were calculated. A
95% confidence interval for the odds ratio that does not include 1.0 indicates
a statistically significant difference at a p value of 0.05
[19]. The mean diameter of the
distal common hepatic artery was calculated for patients having classic or
variant hepatic artery anatomy and for patients who did or did not have
hepatic artery complications after liver transplantation. These data were
analyzed using a Student's t test; a p value of less than
0.05 was considered to be statistically significant.
Results
Image Quality
Regarding the quality of the 84 MR angiography examinations, 44 (52.4%)
were graded as excellent, 38 (45.2%) as good, and only two (2.4%) as fair. No
MR angiography examination was scored as poor. In the two cases scored as
fair, image quality was mildly degraded by patient motion. In one of these two
cases, the intrahepatic arterial branches were partially obscured by opacified
portal veins; however, the main right and left hepatic arteries were clearly
visualized. Thus, all MR angiography studies were of sufficient quality to
permit evaluation of variant hepatic artery anatomy.
Incidence of Variant Arterial Anatomy
On the basis of the findings at surgery, 24 (28.6%) of 84 patients had
variant hepatic artery anatomy, as defined by the standard classification of
Michels [9]
(Table 2). All cases were
correctly characterized by retrospective review, although there were two cases
of disagreement between the two reviewers. Interestingly, there were two
false-positive and two false-negative characterizations of variant hepatic
artery anatomy in the official reports of the MR angiography studies
(prospective review). All these disagreements or misinterpreted cases were
associated with small accessory hepatic arteries, presumably because of a lack
of careful interpretation of the source images. No equivocal MR angiography
case led to the patient undergoing conventional angiography. In addition,
these misinterpretations did not lead to any significant problems during
surgery. Variant hepatic artery anatomy included a replaced or accessory left
hepatic artery (n = 10, 41.6%), a replaced right hepatic artery
(n = 10, 41.6%), both replaced/accessory right hepatic arteries and
replaced/accessory left hepatic arteries (n = 2, 8.3%), a replaced
common hepatic artery (n = 1, 4.2%), and a celiomesenteric trunk
(n = 1, 4.2%) (Fig.
2A,
2B). Of the 14 replaced right
hepatic artery cases, nine arose from the superior mesenteric artery (Fig.
3A,
3B). In the five remaining
cases, the replaced right hepatic artery arose from the gastroduodenal artery
(n = 2), proximal common hepatic artery (n = 1), celiac
trunk (n = 1), or abdominal aorta (n = 1) (Fig.
4A,
4B). One accessory right
hepatic artery arose from the gastroduodenal artery. All 13 accessory or
replaced left hepatic arteries arose from the left gastric artery.

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Fig. 2A. 57-year-old man with celiomesenteric trunk who developed
hepatic artery thrombosis 132 days after liver transplantation. Oblique
coronal targeted maximum-intensity-projection image from pretransplantation
contrast-enhanced 3D MR angiography (TR/TE, 4.8/1.1; flip angle, 20°)
shows celiac and superior mesenteric arteries (SMA) arising from common trunk
(black arrow). White arrow indicates takeoff of gastroduodenal artery
from common hepatic artery (CHA).
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Fig. 2B. 57-year-old man with celiomesenteric trunk who developed
hepatic artery thrombosis 132 days after liver transplantation. Digital
subtraction aortogram obtained after liver transplantation shows occlusion of
hepatic artery (black arrow). White arrow indicates celiomesenteric
trunk.
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Fig. 3A. 58-year-old man with replaced right hepatic artery who
developed hepatic artery thrombosis 65 days after liver transplantation.
Oblique coronal targeted maximum-intensity-projection image from
pretransplantation contrast-enhanced 3D MR angiography (TR/TE, 4.8/1.1; flip
angle, 15°) reveals right hepatic artery (arrow) arising from
superior mesenteric artery.
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Fig. 3B. 58-year-old man with replaced right hepatic artery who
developed hepatic artery thrombosis 65 days after liver transplantation.
Selective digital subtraction angiogram of celiac trunk after liver
transplantation shows occlusion of hepatic artery (arrow).
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Fig. 4A. 47-year-old man with replaced right hepatic artery from
abdominal aorta who developed hepatic artery stenosis 107 days after liver
transplantation. Oblique axial targeted maximum-intensity-projection image
from pretransplantation contrast-enhanced 3D MR angiography (TR/TE, 4.2/0.9;
flip angle, 20°) shows right hepatic artery (arrow) arising
directly from abdominal aorta just below celiac trunk.
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Fig. 4B. 47-year-old man with replaced right hepatic artery from
abdominal aorta who developed hepatic artery stenosis 107 days after liver
transplantation. Conventional angiogram of common hepatic artery after liver
transplantation shows high-grade stenosis at arterial anastomosis (white
arrow). Pigtail catheter (black arrow) was placed to drain liver
abscess.
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Other findings at MR angiography included celiac artery stenosis in three
patients (3.6%) and nonocclusive portal vein thrombus in five patients (6.0%).
In addition, two other patients with celiac stenosis underwent aortic jump
graft reconstruction, as described in Materials and Methods. All five cases of
celiac stenosis were correctly characterized by preoperative MR
angiography.
Arterial Complications
Seven (8.3%) of 84 patients developed hepatic artery complications after
liver transplantation: three developed hepatic artery thrombosis and four
developed hepatic artery stenosis (summarized in
Table 3). The hepatic artery
complications occurred between 15 and 167 days (mean, 88 days) after liver
transplantation. All seven of these patients had abnormal findings on Doppler
sonography, showing either a low resistive index or loss of flow in the
hepatic artery. Two patients required retransplantation. Two patients with
hepatic artery thrombosis and four with hepatic artery stenosis underwent
conventional angiography (Figs.
2A,
2B,
3A,
3B,
4A,
4B). Six of these patients
subsequently required percutaneous interventions, including angioplasty,
thrombolysis, and stent placement. One of the patients with hepatic artery
stenosis who was treated with stent placement subsequently developed
uncontrolled arterial bleeding from the site of the stent placement and
required retransplantation. Five (71.4%) of the seven patients with
posttransplantation hepatic artery stenosis or thrombosis also developed
nonvascular complications, including biliary stricture (n = 1) and
liver abscess (n = 4).
Of the 24 transplant recipients with variant hepatic artery anatomy, five
(20.8%) developed posttransplantation hepatic artery complications. In
contrast, only two (3.3%) of 60 patients with classic hepatic artery anatomy
developed hepatic artery complications. The odds ratio was 7.6 (95% confidence
interval, 1.442.6) (Table
4), which was statistically significant (p <
0.05).
No hepatic artery complications occurred among the patients who had celiac
artery stenosis preoperatively or who had an aortic jump graft reconstruction.
Among the 14 transplant recipients whose donors had variant hepatic artery
anatomy (Table 5), two (14.3%)
developed hepatic artery complications. In both cases, the recipients also had
variant hepatic artery anatomy. In one of these cases, the donor had a
replaced left hepatic artery and the recipient had an accessory left hepatic
artery. In the other case, the donor and recipient each had a replaced right
hepatic artery. The incidence of hepatic artery complications among patients
whose donor livers had variant hepatic artery anatomy was not significantly
different statistically from those whose donor livers had classic hepatic
artery anatomy (p = 0.330).
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TABLE 5 Incidence of Hepatic Artery Complications After Transplantation:
Combination of Donor and Recipient Hepatic Artery Anatomy
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Diameter of Common Hepatic Artery
The mean diameters of the common hepatic arteries in patients with classic
and variant hepatic artery anatomies are summarized in
Table 6. A small but
statistically significant difference in the mean ± SD diameters of 5.8
± 0.8 mm was seen in patients with variant anatomy versus 6.3 ±
0.9 mm in patients with classic anatomy (p < 0.05). A small but
statistically significant difference was found between the mean diameters of
the common hepatic artery in patients with posttransplantation hepatic artery
complications and those without complications (5.2 ± 0.8 vs 6.2
± 0.9 mm, respectively; p < 0.01). In addition, the mean
diameters of the variant hepatic arteries in the group with complications
tended to be smaller than those of the variant hepatic arteries in the group
without complications, although it was not statistically significant (5.2
± 0.8 vs 6.0 ± 0.7 mm, respectively; p = 0.079).
Discussion
The incidence of hepatic artery thrombosis (3.6%) and stenosis (4.7%) in
our study group was similar to that reported in previous studies
[27].
The interval between liver transplantation and the development of hepatic
artery complications in our study ranged from 15 to 167 days (mean, 88 days)
and thus included both early and late hepatic artery complications
[20]. Hepatic artery
complications were considered to be clinically significant if therapeutic
intervention was required. Two of the seven patients with hepatic artery
complications underwent retransplantation, and six patients underwent
percutaneous arterial interventions such as angioplasty, thrombolysis, and
stent placement.
Hepatic artery stenosis places liver transplantation recipients at risk for
biliary complications related to the development of ischemic strictures
[21]. In our study, five
patients with hepatic artery complications (71.4%) also developed biliary
strictures or liver abscesses, which often arise distal to an obstructed bile
duct. Thus, it is important to search for nonvascular complications in liver
transplant recipients who develop hepatic artery complications.
Various risk factors, both surgical and nonsurgical, have been implicated
in the development of hepatic artery thrombosis in liver transplant
recipients. Nonsurgical factors include an ABO-incompatible graft
[22], anticardiolipin antibody
in the recipient [23],
cigarette smoking [24], and
cytomegalovirus infection
[25]. Surgical factors include
pediatric transplantation, short warm ischemia time, and end-to-end hepatic
artery anastomosis [26]. In
contrast, risk factors for hepatic artery stenosis in liver transplant
recipients have been difficult to document
[27], although the technical
details of creating the arterial anastomosis appear to affect the incidence.
Compression of the celiac artery by the median arcuate ligament, which in turn
decreases blood flow in the celiac artery and across the arterial anastomosis,
has been suggested as a risk factor for hepatic artery thrombosis
[28]. However, our study
failed to show this association, most likely because of the small number of
patients with celiac artery stenosis (n = 3). Interestingly, Richard
et al. [29] reported that the
risk of posttransplantation hepatic artery complications also did not increase
among patients who underwent hepatic artery chemoembolization for HCC before
liver transplantation.
Meroin et al. [17] and
Proposito et al. [30] reported
that variant hepatic artery anatomy is not a risk factor for
posttransplantation complications. These authors described an advantage of a
branch patch technique for the surgical arterial reconstruction in which the
recipient's common hepatic arterygastroduodenal artery bifurcation is
used to form the anastomosis instead of the recipient's proper hepatic artery.
Proposito et al. [30] noted
that variant hepatic artery anatomy in a liver transplant recipient had little
impact on posttransplantation hepatic artery complications as long as the
native artery had appropriate size and flow. However, they also reported that
hepatic artery flow can be reduced when the recipient hepatic artery is small,
multiple, or anomalous [30].
Drazan et al. [31] attributed
inadequate blood flow in the recipient hepatic artery as the cause of
posttransplantation hepatic artery thrombosis in nine of 11 patents. In
addition, Proposito et al.
[26] reported that the risk of
hepatic artery thrombosis is much greater in pediatric recipients; this
outcome may also be a function of the small size of the arteries in pediatric
recipients. Thus, the preponderance of published reports agree that smaller
size and reduced blood flow in the recipient hepatic artery can be responsible
for complications.
We hypothesized that a smaller diameter of the recipient common hepatic
artery might contribute to an increased risk of complications after liver
transplantation. Smaller vessels would be expected to have a lower volume flow
rate. In our study, the patients with variant hepatic artery anatomy had a
slightly smaller common hepatic artery than those with classic hepatic artery
anatomy. Furthermore, among the patients in both variant and classic hepatic
artery groups, those who developed posttransplantation complications had a
smaller caliber common hepatic artery than those who did not develop
complications (Table 6). Three
of the four patients who required an infrarenal arterial jump graft had
variant hepatic artery anatomies. In all three of these cases, a small-caliber
common hepatic artery with poor blood flow was observed intraoperatively.
These examples support our hypothesis that the diameter of the common hepatic
artery is the important factor, and the smaller caliber of common hepatic
artery may explain why variant hepatic artery anatomy is a risk factor.
Sakamoto et al. [32]
compared the incidence of hepatic artery thrombosis after left lobe
living-related liver transplantation between two groups: the one in which the
left hepatic artery graft was used versus the one in which the left gastric
artery or common hepatic artery grafts were used. At their institution, if a
donor had an accessory or replaced left hepatic artery, they used the left
gastric artery graft. If a donor had a replaced right hepatic artery, they
used the common hepatic artery graft. Their results indicated that the
incidence of hepatic artery thrombosis with left hepatic artery grafts was
higher than that with an aberrant left hepatic artery or a common hepatic
artery (8/70 [11.4%] vs 1/31 [3.2%], p = 0.15). They concluded that
the better results seen with an aberrant left hepatic artery were due to a
larger diameter (2.5 ± 0.7 vs 2.0 ± 0.8 mm, p = 0.03)
and longer length. The results of Sakamoto et al. are consistent with, and
thus support, our hypothesis and results.
In our study, a variant donor hepatic artery did not increase the risk of
complications. It should be stressed that this result was not inconsistent
with the theoretic basis of our study. When donor variant hepatic artery
anatomy was present, the hepatic artery anastomosis was performed using a
large celiac trunk or a Carrel patch, making it technically easier. In
contrast, with variant recipient hepatic artery anatomy, a smaller trunk,
missing the contribution of the arterial flow to the other lobe (and
typically, more distal on the artery) was used, making for a smaller diameter
and more difficult anastomosis with greater resistance to flow. This
difference may be the crucial. Cases of hepatic artery complications
(n = 7) in our study included hepatic artery thrombosis or stenosis
at the anastomotic site, which would compromise arterial flow more proximally.
On the other hand, even if the arterial anastomosis between the variant
hepatic artery and the splenic artery stump developed occlusion or stenosis,
it might not be clinically significant because reconstitution of the distal
hepatic artery via the intrahepatic collaterals can compensate the arterial
supply as long as the other hepatic artery (primary arterial anastomosis) is
patent. Intrahepatic arterial branches are not end arteries, and prompt
reconstitution of flow to the contralateral hepatic lobe through collateral
vessels develops after occlusion of a variant vessel
[33]. In addition, this
phenomenon is also supported by the fact that only transient (12 weeks)
liver dysfunction was observed after radical gastrectomy for gastric cancer in
patients with an aberrant left hepatic artery from the left gastric artery
[34].
Our study had several limitations. We focused on a single hypothesis,
mainly that variant hepatic artery anatomy in the recipient increases the risk
of posttransplantation hepatic artery complications. We did not investigate
other risk factors or perform multivariate analysis to determine their
significance. Because our study had a relatively small number of patients, we
could not identify the specific hepatic artery variants that predispose
patients to posttransplantation hepatic artery complications. Certain
variants, such as a small accessory hepatic artery, would be less likely to
increase the risk of postoperative hepatic artery complications than, for
example, a completely replaced hepatic artery because the caliber of the
common hepatic artery would be nearly normal in a patient with a small
accessory hepatic artery. The fact that the diameter of the common hepatic
artery is small (only a few pixels in any direction) might lead to measurement
errors on MR angiography. To minimize such errors, we magnified MIP images of
the distal common hepatic artery on the computer workstation and performed the
measurements twice. To minimize interobserver variation, two radiologists
performed the measurements and arrived at a result through consensus. Although
the spatial resolution of contrast-enhanced 3D MR angiography is inferior to
that of conventional angiography, the latter is subject to measurement errors
related to projection and foreshortening. Technologic advances in MR
angiography, such as parallel imaging, provide vastly improved spatial
resolution and enable more accurate measurement of vascular diameters
[35]. Because of the very
small range of vessel diameters and the small number of patients in our study,
we could not identify a threshold diameter for the common hepatic artery below
which the risk of hepatic artery complications increases significantly. It
will be useful in future studies to measure hepatic artery flow to determine
the relationships between common hepatic artery diameter, flow velocity, and
volume flow rate.
In conclusion, variant hepatic artery anatomy in a liver transplant
recipient increases the risk of posttransplantation hepatic artery
complications beyond that in patients with classic hepatic artery anatomy. Our
data suggest that the increased risk in patients with variant hepatic artery
anatomy is due to the smaller caliber of the native common hepatic artery.
Liver transplantation candidates found to have variant hepatic artery
anatomies and those with classic hepatic artery anatomies but with
small-caliber hepatic arteries on preoperative vascular mapping may benefit
from thoughtful surgical planning and vigilant monitoring of hepatic artery
patency after transplantation.
References
- Tzakis AG. The dearterialized liver graft. Semin Liver
Dis 1985;5:375
376[Medline]
- Tzakins AG, Gordon RD, Shaw BW Jr, Iwatsuki S, Starzl TE. Clinical
presentation of hepatic artery thrombosis after liver transplantation in the
cyclosporine era. Transplantation1985; 40:667
671[Medline]
- Lemmens HP, Neumann U, Bechstein WO, et al. Incidence and outcome
of arterial complications after orthotopic liver transplantation.
Transpl Int1996; 9[suppl 1]:S178
S181
- Langnas AN, Marujo W, Stratta RJ, Wood RP, Shaw BW Jr. Vascular
complications after orthotopic liver transplantation. Am J
Surg 1991;161:76
83[Medline]
- Wozney P, Zajko AB, Brown KM, Point S, Starzl TE. Vascular
complications after liver transplantation: a 5-year experience.
AJR 1986;147:657
663[Abstract/Free Full Text]
- Sanchez-Bueno F, Robles R, Ramirez P, et al. Hepatic artery
complications after liver transplantation. Clin
Transplant 1994;8:399
404[Medline]
- Parera A, Salcedo M, Vaquero J, et al. Arterial complications after
liver transplantation: early and late forms [in Spanish].
Gastroenterol Hepatol1999; 22:381
385[Medline]
- Covey AM, Brody LA, Maluccio MA, Getrajdman GI, Brown KT. Variant
hepatic arterial anatomy revised: digital subtraction angiography performed in
600 patients. Radiology2002; 224:542
547[Abstract/Free Full Text]
- Michels NA. Blood supply and anatomy of the upper
abdominal organs with a descriptive atlas. Philadelphia, PA:
Lippincott, 1955
- Lavelle MT, Lee VS, Rofsky NM, Krinsky GA, Weinreb JC. Dynamic
contrast-enhanced three-dimensional MR imaging of liver parenchyma: source
images and angiographic reconstructions to define hepatic arterial anatomy.
Radiology2001; 218:389
394[Abstract/Free Full Text]
- Hiatt JR, Gabbay J, Busuttil RW. Surgical anatomy of the hepatic
arteries in 1,000 cases. Ann Surg1994; 220:50
52[Medline]
- Rong GH, Sindelar WF. Aberrant perihepatic arterial anatomy
considerations in performing pancreatectomy for malignant neoplasms.
Ann Surg 1987;53:726
729
- Takahashi S, Murakami T, Takamura M, et al. Multi-detector row
helical CT angiography of hepatic vessels: depiction with dual-arterial phase
acquisition during single breath hold. Radiology2002; 222:81
88[Abstract/Free Full Text]
- Nghiem HV, Dimas CT, McVicar JP, et al. Impact of double helical CT
and three-dimensional CT arteriography on surgical planning for hepatic
transplantation. Abdom Imaging1999; 24:278
284[Medline]
- Kopka L, Rodenwaldt J, Vosshenrich R, et al. Hepatic blood supply:
comparison of optimized dual phase contrast-enhanced three-dimensional MR
angiography and digital subtraction angiography.
Radiology1999; 211:51
58[Abstract/Free Full Text]
- Gill RW. Measurement of blood flow by ultrasound: accuracy and
sources of error. Ultrasound Med Biol1985; 11:625
641[Medline]
- Meroin RM, Burth GD, Ham JM, Turcotte JG, Campbell DA. The hepatic
artery in liver transplantation. Transplantation1989; 48:438
443[Medline]
- Muiesan P, Rela M, Nodari F, et al. Use of infrarenal conduits for
arterial revascularization in orthotopic liver transplantation.
Liver Transpl Surg1998; 4:232
235[Medline]
- Medina LS, Zurakowski D. Measurement variability and confident
intervals in medicine: why should radiologist care?
Radiology2003; 226:297
301[Abstract/Free Full Text]
- Bhattacharjya S, Gunson BK, Mirza DF, et al. Delayed hepatic artery
thrombosis in adult orthotopic liver transplantation: a 12-year experience.
Transplantation2001; 71:1592
1596[Medline]
- Orons PD, Sheng R, Zajko AB. Hepatic artery stenosis in liver
transplant recipients: prevalence and cholangiographic appearance of
associated biliary complications. AJR1995; 165:1145
1149[Abstract/Free Full Text]
- Lo CM, Shaked A, Busuttil RW. Risk factor for liver transplantation
across the ABO barrier. Transplantation1994; 58:543
547[Medline]
- Pascual M, Thadhani R, Laposata M, et al. Anticardiolipin
antibodies and hepatic artery thrombosis after liver transplantation.
Transplantation1997; 64:1361
1364[Medline]
- Pungpapong S, Manzarbeita C, Ortiz J, et al. Cigarette smoking is
associated with an increased incidence of vascular complication after liver
transplantation. Liver Transpl2002; 8:588
590[Medline]
- Madalosso C, de Souza NF Jr, Ilstrup DM, Wiesner RH, Krom RA.
Cytomegalovirus and its association with hepatic artery thrombosis after liver
transplantation. Transplantation1998; 66:294
297[Medline]
- Proposito D, Loinaz Segurola C, Garcia Garcia I, et al. Assessment
of risk factors in the incidence of hepatic artery thrombosis in a consecutive
series of 687 liver transplantations [in Italian]. Ann Ital
Chir 2001;72:187
205[Medline]
- Abbasoglu O, Levy MF, Vodapally MS, et al. Hepatic artery stenosis
after liver transplantation: incidence, presentation, treatment, and long term
outcome. Transplantation1997; 63:250
255[Medline]
- Jurim O, Shaked A, Kiai K, Millis JM, Colquhoun SD, Busuttil RW.
Celiac compression syndrome and liver transplantation. Ann
Surg 1993;218:10
12[Medline]
- Richard HM III, Silberzweig JE, Mitty HA, Lou WY, Ahn J, Cooper JM.
Hepatic arterial complications in liver transplant recipients treated with
pretransplantation chemoembolization for hepatocellular carcinoma.
Radiology2000; 214:775
779[Abstract/Free Full Text]
- Proposito D, Loinaz Segurola C, Garcia Garcia I, et al. Role of
anatomic variations and methods of hepatic artery reconstruction in the
incidence of thrombosis following liver transplantation [in Italian].
Ann Ital Chir2001; 72:303
314[Medline]
- Drazan K, Shaked A, Olthoff KM, et al. Etiology and management of
symptomatic adult hepatic artery thrombosis after orthotopic liver
transplantation (OLT). Am Surg1996; 62:237
240[Medline]
- Sakamoto Y, Takayama T, Nakatsuka T, et al. Advantage in using
living donors with aberrant hepatic artery for partial liver graft
arterialization. Transplantation2002; 75:518
521
- Koehler RE, Korobkin M, Lewis F. Arteriographic demonstration of
collateral arterial supply to the liver after hepatic artery ligation.
Radiology1975; 117:49
54[Abstract]
- Okano S, Sawai K, Taniguchi H, Takahashi T. Aberrant left hepatic
artery arising from the left gastric artery and liver function after radical
gastrectomy for gastric cancer. World J Surg1993; 17:70
73[Medline]
- Walter C, Philippi G, Westerhausen R, Kooijman H, Hoffmann HG,
Busch HP. High resolution contrast-enhanced 3D MR-angiography of renal
arteries using parallel imaging (SENSE) [in German]. Rofo Fortschr
Geb Rontgenstr Neuen Bildgeb Verfahr2003; 175:1244
1250[Medline]

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