DOI:10.2214/AJR.07.2938
AJR 2008; 191:221-227
© American Roentgen Ray Society
MR Cholangiopancreatography Features of the Biliary Tree After Liver Transplantation
Sébastien Novellas1,
Thomas Caramella1,
Maud Fournol1,
Jean Gugenheim2 and
Patrick Chevallier1
1 Service of Medical Imagery, Centre Hospitalier Régional et
Universitaire de Nice, Hôpital Archet 2, 151 route de St. Antoine de
Ginestière, B. P. 3079, 06202 Nice Cedex 3, France.
2 Service of Hepatic Surgery, Centre Hospitalier Régional et
Universitaire de Nice, Nice, France.
Received July 25, 2007;
accepted after revision January 27, 2008.
Address correspondence to S. Novellas
(novellas.s{at}chu-nice.fr).
CME
This article is available for CME credit.
See
www.arrs.org
for more information.
Abstract
OBJECTIVE. Our objective was to show the usefulness of MR
cholangiopancreatography in assessing biliary complications after liver
transplantation.
CONCLUSION. MR cholangiopancreatography is the best noninvasive tool
for the diagnosis and assessment of biliary complications.
Keywords: biliary tract liver transplantation MR cholangiography MR cholangiopancreatography
Introduction
Liver transplantation has become the treatment of choice for patients with
end-stage cirrhosis or, more rarely, fulminant hepatic failure. Despite
improvements in surgical techniques, biliary complications are observed on
average in 14% of transplants and are the second most frequent cause of
transplant failure after acute rejection
[1,
2]. Although the diagnosis of
acute rejection is confirmed via histologic analysis of the biopsied liver
transplant, imaging techniques can rule out existing biliary complications
because clinical examination and laboratory testing are often nonspecific.
Techniques involving direct opacification of the biliary tract and their
associated morbidity are being progressively supplanted by MR
cholangiopancreatography (MRCP)
[3,
4]. The goal of this article is
to illustrate the abnormal characteristics of the biliary tract shown on MRCP
after liver transplantation as well as the various biliary complications.
Techniques
Several MRI techniques grouped under the generic term MRCP are available to
explore the biliary tract. One category, T2-weighted imaging, confers a strong
signal to structures composed of fluid. Slices are obtained in a coronal plane
to capture the biliary tree. Sequences performed as a single shot (HASTE) over
a 1-second breath-hold allow slices varying from 5 mm to several centimeters.
Rapid spin-echo sequences (rapid acquisition with relaxation enhancement)
performed without a breath-hold and with a longer acquisition time of several
minutes allow millimeter-sized slices and multiple 3D reconstructions.
Increased patient comfort may be achieved by respiratory gating, which allows
the patient to breathe normally. T2-weighted turbo spin-echo sequences with
fat suppression are performed on an axial plane with a thickness of 5–7
mm. These images complete the examination by permitting visualization of the
hepatic parenchyma and the perihepatic anatomy in addition to studying the
bile ducts.
Recently, a noteworthy study involved the injection of magnetic contrast
material such as mangafodipir that is excreted with bile
[5]. After its excretion and
progression through the biliary tree, this contrast agent allows dynamic
analysis of the bile ducts on T1-weighted images. This type of study is useful
in cases of bile leakage, although such cases could also be diagnosed by the
static sequences of MRCP.
Normal Transplant Anatomy on MRCP
Because biliary complications do not present specific clinical or
laboratory findings, the posttransplantation patient is often referred for
diagnostic imaging. Evaluation with MRCP has become more commonplace even
though biliary complications are found in only two thirds of examinations
[6]. With respect to MRCP, the
normal anatomy in the patient with a liver transplant has similarities but
also certain noteworthy differences compared with control subjects. For
example, the intrahepatic bile ducts should be no more than 2–3 mm and
should not be visible from the hepatic periphery where it abuts the liver
capsule [6,
7]. The diameter of the common
bile duct normally should not exceed 7–8 mm, especially above the
anastomosis. The bile ducts should appear smooth and regular, without
significant variations in their caliber. The biliary anastomosis, whether it
is a choledochocholedochostomy or a choledochojejunostomy, is not always
clearly visible on T2-weighted MRCP. A transitory anastomotic stricture,
caused by edema in the parietal wall of the duct, can occur in the weeks after
the liver transplantation. Strictures can be minor or occasionally more
significant, with loss of visibility of the biliary lumen on MRCP. The absence
of proximal dilation of the bile ducts helps the radiologist avoid erroneously
diagnosing a clinically significant stenosis.
Pathophysiology of Biliary Complications
Biliary complications can occur from several causes. The biliary
anastomosis can be the site of complications due to surgical technique or
ischemia of the parietal wall. The result of either may be a fibrotic stenosis
that can rapidly develop or a biliary leak that causes a perihepatic biloma or
choleperitoneum (Fig. 1). An
isolated leak will lead to the formation of a fibrotic stenosis. Stenoses of
the intrahepatic ducts and bifurcations can result from many causes and are
grouped under the term "ischemic-type biliary lesions" (Fig.
2A,
2B,
2C). The causes are most often
due to thrombosis of the hepatic artery or extended ischemia of the preserved
donor liver before transplantation
[8,
9]. Other causes such as
chronic rejection, cytomegalovirus infection, or recurring primary sclerosing
cholangitis are equally possible. The underlying mechanism of an ischemic-type
biliary lesion is the absence of the parabiliary arterial collateral supply
from the gastroduodenal artery, in which case stenosis or occlusion of the
hepatic artery may result in severe ischemia and bile duct necrosis. Biopsy
specimens from patients with ischemic-type biliary lesions have revealed
biliary obstruction associated with ischemic features and, occasionally,
cellular rejection. Finally, biliary obstruction can occur in association with
biliary sludge or stones that are themselves associated with a preexisting
biliary stenosis in 90% of cases
[10] (Fig.
3A,
3B).

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Fig. 1 —MR cholangiopancreatography 3D sequence 8 days after
orthotopic liver transplantation in 62-year-old man. Bile leak from
choledochocholedochal anastomosis (solid arrow) results in
choleperitoneum (open arrow) and associated proximal dilation of
intrahepatic bile ducts.
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Fig. 2A —MR cholangiopancreatography in 45-year-old man 1 week after
orthotopic liver transplantation with choledococholedocostomy. T2-weighted
turbo spin-echo axial image shows edema in liver (open arrow) and
perihilar effusion (solid arrow).
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Fig. 2B —MR cholangiopancreatography in 45-year-old man 1 week after
orthotopic liver transplantation with choledococholedocostomy. MR image of
liver reveals absence of hepatic artery and hilar necrosis
(arrow).
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Fig. 2C —MR cholangiopancreatography in 45-year-old man 1 week after
orthotopic liver transplantation with choledococholedocostomy. Intrahepatic
bile ducts are irregular and mildly dilated (open arrow), with
lacunar aspect of convergence of primary bile ducts in contact with biloma
(solid arrow).
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Fig. 3A —66-year-old woman 6 months after liver transplantation. MR
cholangiopancreatography image with fine slices reveals intrahepatic bile duct
dilation (open arrow), focal stenosis of choledochocholedochal
anastomosis (long arrow), and lacuna in connection with biliary
sludge in common bile duct (short arrow).
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Fig. 3B —66-year-old woman 6 months after liver transplantation.
Percutaneous cholangiography image shows complete stenosis of anastomosis
(solid arrow) and dilation of proximal bile ducts (open
arrow). Biliary sludge is not clearly identified.
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Pathologic Appearance on MRCP
Anastomotic Stenosis
Stenosis appears on MRCP as a thinning of the hyperintense signal of the
biliary lumen leading to the absence of signal and complete
[3,
4,
6] stenosis (Fig.
4A,
4B). Dilation of the bile ducts
proximal to the stenosis is a classic finding; however, the existence of
secondary biliary cirrhosis can attenuate this finding
[6,
7] (Fig.
5A,
5B). In this scenario, the
differential diagnosis of a transient post operative stricture could still be
entertained.

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Fig. 4A —55-year-old man with jaundice 11 months after liver
transplantation. MR cholangiopancreatography 3D sequence with
maximum-intensity-projection reconstruction shows focal stenosis of
choledochocholedochal anastomosis (arrow) and significant dilation of
biliary tract near stenosis.
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Fig. 5A —53-year-old woman with jaundice 4 years after orthotopic
liver transplantation. MR cholangiopancreatography image reveals short
stenosis of choledochocholedochal anastomosis (long arrow) without
dilation of intrahepatic ducts (short arrow).
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Fig. 5B —53-year-old woman with jaundice 4 years after orthotopic
liver transplantation. Percutaneous cholangiography image confirms complete
stenosis of anastomosis (long arrow). Short arrow indicates
intrahepatic ducts.
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Ischemic-Type Biliary Lesions
In ischemic-type biliary lesions, primary pathologic changes occur in the
medium and larger ducts; however, small peripheral portal areas are primarily
seen in biopsy specimens of allograft livers. Millimeter-sized slices obtained
via turbo spin-echo sequences allow superior spatial resolution and permit the
precise location of the level of obstruction in cases of ischemic-type biliary
lesions (Fig. 6A,
6B,
6C). This degree of resolution
is indispensable in assessing complex hilar stenosis or the smaller
intrahepatic ductules [8,
9] (Fig.
7A,
7B); however, in cases
involving sclerosing cholangitis, early signs of ischemic-type biliary lesions
on MRCP may be absent
[11].

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Fig. 6A —61-year-old man 4 months after liver transplantation. MR
cholangiopancreatography sequence shows predominantly right intrahepatic bile
duct dilation (open arrow) associated with several stenoses,
predominantly in right hepatic duct (long arrow). Common bile duct is
of normal caliber (short arrow).
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Fig. 6C —61-year-old man 4 months after liver transplantation.
Percutaneous cholangiography image confirms biliary dilation and complete
stenosis of right hepatic duct (solid arrow). Bile ducts are
irregular and dilated in association with ischemic-type biliary lesion
(open arrow).
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Fig. 7A —48-year-old man 2 months after liver transplantation. MRI
sequence with maximum-intensity-projection reconstruction shows multiple
intrahepatic stenoses (short arrows) and irregular dilation of
intrahepatic bile ducts (open arrow), which is visible up to
choledochocholedochal anastomosis (long arrow).
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Fig. 7B —48-year-old man 2 months after liver transplantation.
Percutaneous cholangiography image confirms irregular stenoses (short
arrow), dilation of biliary tract (open arrow), and extension to
proximal part of common bile duct. Cholangiography is artifactually distorted
by opacification of lymphatic network surrounding bile ducts (long
arrow).
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Biliary Leak
Of the early complications, bile leakage is by far the most common.
Although small bile duct leakage may resolve spontaneously, more severe
anastomotic leakages have been associated with high morbidity. Bile leaks
cannot be actively visualized due to the static nature of MRCP sequences. For
this problem, most authors still recommend direct opacification of the biliary
system [4,
7]. This technique remains the
method of choice for the detection of bile leaks because of the ability to
detect real-time contrast material extravasation. A bile leak may nevertheless
be suspected on MRCP when a fluid collection occurs near the anastomosis,
especially if the anastomosis enlarges on serial examinations; also, an
irregular or stenotic anastomosis should heighten suspicion (Fig.
8A,
8B).

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Fig. 8A —46-year-old woman 1 month after liver transplantation from a
living donor. MR cholangiopancreatography sequence shows moderate dilation of
intrahepatic bile ducts (long arrows) and perianastomotic biloma
(open arrow). Common bile duct is slender (short
arrows).
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Fig. 8B —46-year-old woman 1 month after liver transplantation from a
living donor. Percutaneous cholangiography image confirms perianastomotic
biliary leak (open arrow), moderate dilation of intrahepatic biliary
tracts (long arrows), and integrity of common bile duct (short
arrows). Biloma (open arrow) was percutaneously drained.
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Biliary Stones
MRI allows the detection of biliary stones that appear as smooth rounded
filling defects in the biliary lumen. Sensitivity approaches 90% for biliary
stones larger than 3 mm in diameter
[6,
12] (Fig.
9A,
9B,
9C). Biliary sludge presents
as irregular filling defects that are occasionally linear in appearance
[7] (Fig.
10A,
10B,
10C). On MRCP 3D sequencing,
the millimeter slices must be carefully analyzed because
maximum-intensity-projection reconstructions can hide a biliary stone by
showing an absence of signal, mimicking a long stenosis (Fig.
11A,
11B,
11C).

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Fig. 9A —41-year-old man 10 years after second orthotopic liver
transplantation. T2-weighted turbo spin-echo axial image reveals atrophy of
right lobe of liver (short arrow) and moderate dilation of
intrahepatic bile ducts in hypertrophied left lobe of liver (long
arrow).
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Fig. 9B —41-year-old man 10 years after second orthotopic liver
transplantation. On MR cholangiopancreatography image, note biliary stone in
left hepatic duct (long arrow) proximal to hepatojejunal anastomosis
(open arrow). Old cystic dilation of biliary tract of atrophied right
lobe of liver (short arrows) is well visualized.
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Fig. 9C —41-year-old man 10 years after second orthotopic liver
transplantation. Percutaneous cholangiography image shows lacunae of left
hepatic duct (long arrow), incomplete stenosis of hepatojejunal
anastomosis (open arrow), and passage of contrast material in loop
(short arrow).
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Fig. 10A —55-year-old man 3 years after liver transplantation. MR
cholangiopancreatography image shows large dilation of left intrahepatic bile
ducts (open arrow) filled with biliary stones presenting as filling
defects. Hepatojejunal anastomosis (solid arrow) appears
stenotic.
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Fig. 10B —55-year-old man 3 years after liver transplantation.
Percutaneous cholangiography image confirms ductal dilation, presence of
innumerable biliary stones (open arrow), and incomplete stenosis of
hepatojejunal anastomosis (solid arrow).
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Fig. 11A —63-year-old man 1 year after liver transplantation. MR
cholangiopancreatography 3D image with maximum-intensity-projection
reconstruction shows large dilation of intrahepatic bile ducts (long
arrow) and long stenosis involving hepatojejunal anastomosis and hepatic
hilum (open arrow). Jejunal loop is well seen (short
arrows).
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Fig. 11B —63-year-old man 1 year after liver transplantation. MR
cholangiopancreatography image with thick slices shows that stenosis of
anastomosis is in fact focal (short arrow). Note proximal biliary
stones involving common bile duct and liver hilum (open arrow). Long
arrow indicates large dilation of intrahepatic bile ducts.
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Fig. 11C —63-year-old man 1 year after liver transplantation.
Percutaneous cholangiography image shows dilation of intrahepatic bile ducts
(long arrow), focal complete stenosis of hepatojejunal anastomosis
(short arrow), and filling defects in bile ducts of hilum (open
arrow).
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Bilomas
An intra- or extrahepatic collection of bile appears on MRCP as a
well-circumscribed rounded homogeneous hyperintense signal of variable size.
MRCP sequencing is useful to show the biloma and proximal bile duct in
continuity (Fig. 12A,
12B).

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Fig. 12A —45-year-old woman 18 months after liver transplantation. MR
cholangiopancreatography sequence shows several round fluid collections
(open arrow) appearing to communicate with bile ducts. Anastomosis
(solid arrow) does not appear to be stenosed.
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Fig. 12B —45-year-old woman 18 months after liver transplantation.
Percutaneous cholangiography image shows communication of bilomas (open
arrow) with bile ducts and confirms anastomotic patency (solid
arrow).
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Conclusion
Biliary complications are common after liver transplantation and can
determine the patient's overall prognosis. MRCP is the best noninvasive tool
for delineating and characterizing stenosis, biliary stones and their precise
location, anastomosis, native common bile duct, hepatic hilum, and
intrahepatic bile ducts. Biliary leaks are often more difficult to diagnosis
with conventional MRCP and require direct antegrade or retrograde
cholangiography.
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