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Gastrointestinal Imaging |
1 From the Department of Radiology, Medical College of Virginia of Virginia Commonwealth University, 401 N 12th St, Main Hospital 3rd Fl, Rm 415, Richmond, VA 23298-0615. Received June 9, 1998; revision requested July 27; revision received September 2; accepted December 16. Address reprint requests to A.S.F.
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Breath-hold half-Fourier rapid acquisition with relaxation enhancement MR cholangiography was performed in 25 patients who had undergone orthotopic liver transplantation. MR cholangiograms were prospectively and independently interpreted by two radiologists for depiction of the biliary tract and ductal anastomosis and for complications (eg, biliary dilatation, stricture, stones). MR cholangiographic findings were correlated with findings from direct cholangiography (n = 24) and surgery (n = 1).
RESULTS: MR cholangiography completely demonstrated first-order intrahepatic bile ducts in 23 (92%) patients, the donor extrahepatic bile duct in 25 (100%), the recipient extrahepatic bile duct in 17 of 18 (94%), and the anastomosis in 24 (96%). The sensitivity, specificity, accuracy, positive predictive value, and negative predictive value of MR cholangiography for detection of biliary dilatation and stricture were each 100%. Complete interobserver agreement occurred in the detection of biliary dilatation and stricture. The sensitivity, specificity, accuracy, positive predictive value, and negative predictive value of MR cholangiography for detection of stones were 100% for one radiologist and 86%, 100%, 96%, 100%, and 95%, respectively, for the other. Both radiologists agreed on the diagnosis of bile duct stones in six of seven cases (
= 0.90).
CONCLUSION: MR cholangiography enables accurate depiction of the biliary tract and detection of biliary complications in patients with an orthotopic liver transplant.
Index terms: Bile ducts, calculi, 76.814 • Bile ducts, MR, 76.121415, 76.12143 • Bile ducts, stenosis or obstruction, 76.2896 • Liver, transplantation, 761.459 • Magnetic resonance (MR), half-Fourier imaging, 76.12146
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Biliary complications constitute the second most common cause of liver dysfunction in patients with a transplant and are exceeded only by rejection (2). These biliary complications include obstruction, leak, strictures, and stone formation and occur in as many as 25% of patients of all ages with a transplant and in 38% of pediatric patients with a transplant (3,4). Because the clinical and biochemical manifestations in patients with biliary complications are often nonspecific and may mimic rejection, radiologic evaluation usually is necessary.
During the 1st several months after transplantation, a biliary catheter often is left in place to provide access to the biliary tract. In the past, once the catheter was removed direct visualization of the biliary tract was possible only with invasive procedures such as endoscopic retrograde cholangiography (ERC) and percutaneous transhepatic cholangiography (PTC). However, with the advent of magnetic resonance (MR) cholangiography, noninvasive visualization of the bile ducts became possible (5). The purpose of this study was to determine the accuracy of MR cholangiography in demonstrating the biliary tract and in helping detect biliary complications in patients who have undergone orthotopic liver transplantation.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The reasons for transplantation included cirrhosis secondary to infection with hepatitis C virus (n = 11), infection with hepatitis B virus (n = 2), primary sclerosing cholangitis (n = 6), autoimmune hepatitis (n = 2), alcoholic hepatitis (n = 2), biliary atresia (n = 1), and biliary cirrhosis related to iatrogenic bile duct injury (n = 1).
Eighteen patients had a duct-to-duct anastomosis, and seven had a biliary-enteric anastomosis (five with choledochojejunostomy, two with hepaticojejunostomy). The time from liver transplantation to performance of MR cholangiography ranged from 14 days to 10 years (mean, 3 years).
MR cholangiography was performed in conjunction with abdominal MR imaging in all patients as part of a standard liver MR protocol at our institution. The MR cholangiographic and MR imaging examinations were requested due to elevated serum alkaline phosphatase level (n = 16), elevated serum alkaline phosphatase level and biliary ductal dilatation at ultrasonography (US) (n = 2), and biliary ductal dilatation at US with normal serum alkaline phosphatase level (n = 2); as routine follow-up (n = 4); and to evaluate focal abnormalities in the liver as noted at US (n = 1) or computed tomography (CT) (n = 1).
MR Cholangiography and Imaging
MR cholangiography was performed with a 1.5-T superconducting magnet (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany) in two patients and with a 1.0-T magnet (Magnetom Expert; Siemens Medical Systems) in 23 patients. The half-Fourier rapid acquisition with relaxation enhancement (RARE) sequence and a circularly polarized, phased-array body coil were used in all patients.
First, the biliary tract was localized with a thick-slab (7-cm) half-Fourier RARE MR study in the 25°–coronal oblique and axial planes, with an acquisition time of 7 seconds. These images were then used as guides for the evaluation of the biliary tract with thin (3–5-mm) sections in the coronal oblique plane parallel to the long axis of the extrahepatic bile duct. The thin-section MR cholangiograms were obtained at various angles, which allowed optimal depiction of the bile duct. Both the thick-slab and the thin-section images were obtained during a breath hold. The patients did not fast prior to MR cholangiography, and antiperistaltic agents were not used.
The half-Fourier RARE parameters for the 1.5-T magnet included 
/95 (repetition time msec/effective echo time msec); refocusing flip angle, 150°; section thickness, 3 mm with no intersection gap; field of view, 270 x 270 mm; one signal acquired; matrix, 240 x 256; acquisition time, 20 seconds. The half-Fourier RARE parameters for the 1.0-T magnet included /88 (effective); refocusing flip angle, 140°; section thickness, 5 mm with no intersection gap; field of view, 270 x 270 mm; one signal acquired; matrix, 240 x 256; acquisition time, 18 seconds. Thirteen images were obtained during each 18–20-second acquisition. Fat saturation and shim adjust were used in all cases. Maximum intensity projection and multiplanar reformatting techniques were applied to the acquired data.
After MR cholangiography, conventional MR imaging of the abdomen was performed for examination of the liver in all patients. MR sequences included nonenhanced T1-weighted breath-hold spoiled gradient-echo (148/5 [repetition time msec/echo time msec]; flip angle, 70°; section thickness, 10 mm with 30% intersection gap; field of view, 300 mm; one signal acquired; matrix, 112 x 256), nonenhanced and contrast material–enhanced T1-weighted fat-suppressed (200/4.4; flip angle, 70°; section thickness, 8 mm with 20% intersection gap; field of view, 380 mm; one signal acquired; matrix, 128 x 256), and nonenhanced T2-weighted breath-hold fast spin-echo (3,500/138 [effective]; section thickness, 8 mm with 25% intersection gap; field of view, 350 mm; one signal acquired; matrix, 116 x 256; echo train length, 29) sequences. Gadopentetate dimeglumine (Magnevist; Berlex, Wayne, NJ) was administered intravenously (dose, 0.1 mmol/kg) as a bolus followed by a flush with normal saline solution.
Image Analysis
The MR cholangiograms were interpreted independently by two experienced abdominal radiologists (the authors) who were blinded to patient identification and all clinical, laboratory, pathologic, and imaging findings, including the conventional MR imaging findings. Both the source images and the three-dimensional reconstructions were reviewed on hard copy and at an interactive workstation. The MR cholangiographic findings were recorded on standardized data sheets.
The MR cholangiograms were evaluated for depiction of the first-order intrahepatic bile ducts, donor extrahepatic bile duct, recipient extrahepatic bile duct in patients with duct-to-duct anastomosis, and ductal anastomosis. The following grading system was used: excellent depiction (complete delineation), good depiction (of at least 90% of the structure of interest), fair depiction (of less than 90% of the structure), and nondepiction.
The following information was recorded for each MR cholangiogram: depiction of the ductal anastomosis, type of ductal anastomosis (duct-to-duct or biliary-enteric anastomosis), and presence of intrahepatic and extrahepatic biliary ductal dilatation, stricture, and stones. The extrahepatic and intrahepatic bile ducts were considered to be dilated if their diameter exceeded 7 mm and 2 mm, respectively (6,7). If biliary ductal dilatation was present, the dilatation was classified relative to level (intrahepatic, extrahepatic, or recipient and/or donor duct) and cause (obstructive or nonobstructive). Biliary ductal dilatation was classified as nonobstructive if there was no evidence of a stricture or of an intraductal filling defect such as a stone and if the intrahepatic bile ducts were normal in caliber.
On completion of the MR cholangiogram interpretations, the study radiologists then compared the MR cholangiographic findings with findings from direct cholangiography (n = 24) and surgery (n = 1), to evaluate the results of the MR cholangiogram interpretations. In addition to the review of the direct cholangiograms, the interpreting radiologists reviewed the dictated reports for those studies that included pertinent endoscopic observations. The direct cholangiograms included T-tube cholangiograms (n = 12), ERC images (n = 8), and PTC images (n = 4). The time between performance of direct cholangiography and MR cholangiography was less than 24 hours (n = 3), 1–7 days (n = 7), 7–30 days (n = 4), or more than 30 days (n = 10). In the one patient in whom surgical correlation was obtained, the time between performance of MR cholangiography and surgery was 6 days.
US (n = 19) and CT (n = 5) findings were available in 20 of the 25 patients and were correlated with the MR cholangiographic findings. The time between performance of MR cholangiography and US or CT was less than 24 hours (n = 2), 1–7 days (n = 13), 7–30 days (n = 3), or more than 30 days (n = 2).
Statistical Analyses
The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of MR cholangiography for the detection of ductal biliary dilatation, strictures, and stones were calculated. Interobserver agreement about the detection of biliary dilatation, stricture, and stones was determined with the use of the statistic. The level of agreement was defined as follows: value of 0, no agreement; value of 0.01–0.40, poor agreement; value of 0.41–0.60, fair agreement; value of 0.61–0.80, good agreement; and value of 0.81–1.00 excellent agreement.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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= 1.00). MR cholangiography enabled differentiation between obstructive (n = 12) and nonobstructive dilatation (n = 7) in all 19 patients with dilated ducts. Of the 12 patients with obstructive dilatation, 10 had strictures and two had stones that resulted in biliary ductal dilatation. Eight of the 19 patients with biliary ductal dilatation demonstrated dilatation of the intrahepatic bile duct, which was associated with a biliary-enteric anastomotic stricture (n = 5), hilar stricture presumably due to ischemia (n = 2), or recurrent primary sclerosing cholangitis involving the extrahepatic bile duct (n = 1). US correlation was available in five of the eight patients with intrahepatic biliary ductal dilatation. US failed to demonstrate a minor degree of ductal dilatation in one patient and resulted in erroneous identification of dilatation in another.
Five of the 19 patients had dilatation of the donor and recipient ducts without evidence of an obstructing lesion at MR cholangiography or direct cholangiography. Direct cholangiograms, which documented the stability of the ductal dilatation for 2–3 years (mean, 2.5 years), were available in four of these five patients; there was no biochemical evidence of obstruction in these patients. The fifth patient showed no biochemical or clinical evidence of a mechanical obstruction during 12-month follow-up after MR cholangiography.
Four patients had dilatation of the recipient duct with normal calibers of the donor and intrahepatic ducts. Two of these four patients had stones in the distal portion of the recipient duct, which resulted in dilatation. The remaining two patients had no obstructing lesion at MR or direct cholangiography or during 8–12-month clinical follow-up.
Two patients demonstrated dilatation of the extrahepatic donor duct without dilatation of the intrahepatic ducts or recipient duct, secondary to a stricture at the duct-to-duct anastomosis.
Stricture
Ten patients examined with MR cholangiography had bile duct strictures; the stricture in these patients was confirmed at direct cholangiography in nine (ERC in five, PTC in three, T-tube cholangiography in one) and at surgery in one. MR cholangiography demonstrated a sensitivity, specificity, accuracy, positive predictive value, and negative predictive value of 100% each for the detection of biliary strictures. There was complete agreement between the two observers in the diagnosis of the presence and location of strictures ( = 1.00).
All strictures were associated with dilatation of the bile duct proximal to the stricture; biliary ductal stones were located proximal to the stricture in five patients. The stricture was anastomotic in seven patients (biliary-enteric anastomosis in five [Fig 3], duct-to-duct anastomosis in two) and nonanastomotic in three.
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Stones
Seven patients had stones identified at MR cholangiography and confirmed and removed at ERC (n = 6) or surgery (n = 1). One study radiologist observed the stones prospectively in all seven patients, and the other observed the stones in six patients, which prospectively yielded excellent interobserver agreement ( = 0.90). In the one patient in whom the stones were not detected initially by one of the study radiologists, the stones measured 2 mm in maximal diameter. Therefore, the sensitivity, specificity, accuracy, positive predictive value, and negative predictive value of MR cholangiography for the detection of biliary ductal stones were 100% each for one radiologist and 86%, 100%, 96%, 100%, and 95%, respectively, for the other.
US was performed prior to MR cholangiography in four patients but helped definitively identify the ductal stones in only one patient. The stones were 2–10 mm in maximal diameter; one patient had a single stone, and six had multiple stones. The ducts proximal to the stones were dilated in five of seven patients. In three patients, the stones occurred in association with a stricture at the site of a biliary-enteric anastomosis. In these three patients, the stones were located immediately proximal to the stricture in two and were intrahepatic in location in the third.
In the remaining four patients, the stones occurred in association with a duct-to-duct anastomosis (Fig 5). In two patients, the stones were located in the donor duct proximal to an anastomotic stricture, whereas in the other two patients, the stones were not associated with a stricture.
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Leak
No patient examined with MR cholangiography was referred for evaluation of a possible biliary ductal leak. One patient with a biliary-enteric anastomosis demonstrated a subhepatic fluid collection adjacent to the anastomosis (Fig 2). This collection did not opacify at T-tube cholangiography; extravasation of contrast material from the duct did not occur. Surgical drainage of the collection revealed a biloma, which presumably was the result of a contained leak at the anastomosis.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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As an alternative, direct cholangiography (T-tube cholangiography, PTC, ERC) provides a method for both diagnostic evaluation and access for the purpose of therapeutic intervention (3,10). After the 1st several months after transplantation, however, biliary catheters are removed, and direct cholangiography is possible only with invasive techniques such as PTC and ERC. Although PTC and ERC provide high-quality images of the biliary tract and allow therapeutic intervention, these procedures are associated with complications that occur in 3.4% of PTC procedures and in 5% of ERC procedures (10,11). Furthermore, the performance of ERC may be difficult or impossible in patients with a biliary-enteric anastomosis.
MR cholangiography allows rapid, noninvasive imaging of the biliary tract without the risks associated with PTC and ERC. Owing to the multiplanar capability of MR imaging, MR cholangiography is well suited for the depiction of complex strictures and surgically altered biliary anatomy. Because MR cholangiography is purely diagnostic, however, it does not provide a means of therapeutic intervention. Nevertheless, MR cholangiography provides a three-dimensional road map of the biliary tract, which can be used to plan percutaneous, endoscopic, and surgical interventions.
MR cholangiography has been shown to be accurate for the demonstration of biliary obstruction and stones and for the examination of patients with a biliary-enteric anastomosis (12–15). Preliminary data (16) indicate that MR cholangiography can delineate ductal anatomy in pediatric patients with a liver transplant from a living, related donor.
For MR cholangiography to be useful in the evaluation of biliary complications after transplantation, the MR cholangiogram must clearly delineate the biliary tract and the ductal anastomosis. In our series, MR cholangiography enabled complete visualization of the extrahepatic bile duct and ductal anastomosis and permitted correct categorization of the anastomosis as a duct-to-duct or biliary-enteric anastomosis in 24 (96%) patients. In one patient, the anastomosis was obscured by an adjacent biloma that was the result of a contained biliary ductal leak.
Owing to negligible susceptibility effects associated with the half-Fourier RARE sequence, surgical clips near the anastomosis do not result in the formation of artifact. In the MR cholangiographic determination of the type of anastomosis, however, a potential pitfall exists in the setting of a biliary-enteric anastomosis; it is possible to mistake a native distal bile duct for the recipient duct of a duct-to-duct anastomosis (Fig 6). This pitfall can be avoided by noting that the native distal bile duct is not continuous with the intrahepatic ducts and that the jejunal limb of the biliary-enteric anastomosis is located in the subhepatic space anterior to the duodenum and native distal bile duct.
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Biliary complications after transplantation include obstruction, stricture, stone formation, and leak. Obstruction occurs more frequently than other complications in both adult and pediatric patients and is most often secondary to an anastomotic stricture that results in dilatation of the donor bile duct (3,4,17). In some instances, however, patients with clinical and biochemical evidence of biliary ductal obstruction and hepatic dysfunction may have dilatation of both the donor and the recipient ducts. Stieber et al (18) proposed that this diffuse ductal dilatation results from papillary dyskinesia due to devascularization or denervation of the papilla of Vater during transplantation. Still other patients have demonstrated dilatation of the donor and/or recipient ducts that remained stable over time and was not associated with obstruction and hepatic dysfunction (19).
In our series, MR cholangiography had 100% accuracy for the detection of biliary ductal dilatation, with complete interobserver agreement, and helped differentiate between obstructive and nonobstructive dilatation. MR cholangiography helped identify the level and cause of obstruction in all 12 patients with obstructive dilatation. In seven patients with nonobstructive dilatation, MR cholangiography demonstrated dilatation of the donor and/or recipient ducts, without evidence of an obstructive lesion. None of these patients had clinical or biochemical evidence of hepatic dysfunction, and direct cholangiograms in all showed prompt passage of contrast material from the duct into the duodenum or jejunum. In the setting of papillary dyskinesia resulting in biliary dilatation, MR cholangiography may demonstrate dilated donor and recipient ducts without an obstructing lesion and may result in a false-negative diagnosis of obstruction. However, correlation with clinical and biochemical evidence of hepatic dysfunction may help prevent this error.
In the determination of ductal caliber, MR cholangiography more accurately demonstrated the ducts in their natural state of distention than did direct cholangiography. The injection of contrast material into the ducts during direct cholangiography may result in overdistention or underdistention of the ducts.
Biliary stricture is the most common cause of biliary obstruction in the patient with a liver transplant, and the stricture may be anastomotic or nonanastomotic in location (2). In the current series, MR cholangiography yielded an accuracy of 100% for the detection of a stricture; complete interobserver agreement occurred in the diagnosis of stricture and in the determination of the stricture location. An anastomotic stricture occurs more commonly than a nonanastomotic stricture and is most often caused by scar formation and less frequently by ischemia (20). In our series, the stricture in seven of 10 patients was anastomotic. The stricture, as well as the associated biliary dilatation proximal to the stricture, was completely depicted at MR cholangiography in each case.
Nonanastomotic stricture occurs in the intrahepatic or extrahepatic donor duct and has multiple causes, including occlusion of the hepatic artery, pretransplantation primary sclerosing cholangitis, and infection (21–23). In our series, a nonanastomotic stricture was detected in three patients. Owing to the high spatial resolution afforded by the half-Fourier RARE sequence, MR cholangiography helped differentiate between the smooth hilar strictures (in two patients), which presumably occurred as the result of ischemia, and the irregular stricture and formation of a pseudodiverticulum of the extrahepatic duct associated with recurrent primary sclerosing cholangitis (in one patient).
The characterization of strictures that MR cholangiography provides can be further improved by performing this technique in conjunction with conventional contrast-enhanced MR imaging. In some instances, performance of these conventional MR sequences may help identify an obstructing mass and thereby assist in differentiation between a benign stricture and a malignant stricture.
In addition to obstruction and stricture formation, stone formation may occur as a posttransplantation complication. Sheng et al (24) noted that biliary filling defects, including sludge, stones, and necrotic debris, occurred with a prevalence of 5.7% and that stones accounted for more that one-third of filling defects. In our series, an intraductal filling defect was detected at MR cholangiography in seven patients; the defect in five was located proximal to an anastomotic stricture. In each of the seven patients, the filling defect was diagnosed at MR cholangiography as due to stones, and the diagnosis was confirmed during removal at endoscopy or surgery. In many instances, stones can be differentiated from sludge and necrotic debris at MR cholangiography by noting the well-defined margins typical of stones, in contrast to the castlike appearance of sludge (25). However, this distinction is not always possible.
Pneumobilia, which may occur in association with a biliary-enteric anastomosis or after biliary intervention, may mimic stones at both MR cholangiography and direct cholangiography, because gas appears as an intraductal filling defect. Often pneumobilia can be distinguished from stones at MR cholangiography by noting the location of gas within the nondependent portion of the ducts.
Biliary ductal leaks occur with a prevalence of 4.3% after transplantation and are most frequently located at the biliary anastomosis or the T-tube exit site (26). At direct cholangiography, biliary ductal leaks may appear as single or multiple bilomas or as extravasation of contrast material along the T-tube track or directly into the peritoneal cavity (26). Although a fluid collection is depicted on the MR cholangiogram as a high-signal-intensity collection, loculated ascitic fluid cannot be distinguished from biloma at MR cholangiography. Direct cholangiography performed with fluoroscopic monitoring will likely remain the method of choice for the detection of biliary ductal leaks, because of the capability of real-time detection of contrast material extravasation. In our study, a biloma was identified in only one patient and was presumably related to a contained anastomotic leak.
Several limitations of this study and of MR cholangiography exist. The major limitation of this study was the relatively small number of patients examined. Although MR cholangiograms permitted visualization of the biliary tract and detection of biliary complications, our findings should be confirmed with a larger, prospective series. Although MR cholangiography demonstrates the bile ducts in their natural degree of distention, the distention that occurs during direct cholangiography may allow better analysis of stricture morphology and provide functional information about the presence of an obstructing lesion. In patients with a biliary catheter in place, therefore, T-tube cholangiography is the study of choice. After removal of the catheter, however, MR cholangiography provides a noninvasive means of evaluating the biliary tract.
In conclusion, during the past several years, MR cholangiography has emerged as an accepted technique for evaluation of various diseases of the biliary tract. Our results in 25 patients with an orthotopic liver transplant demonstrated (a) the ability of MR cholangiography to render diagnostic images of the surgically altered biliary tract and (b) the clinical applications of MR cholangiography in this population. MR cholangiography provides a noninvasive alternative to ERC and PTC for demonstration of the biliary tract after transplantation and is accurate for detection of complications such as biliary obstruction, stricture, and stones.
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, A.S.F.; study concepts, A.S.F., M.A.T.; study design, A.S.F.; definition of intellectual content, A.S.F., M.A.T.; literature research, A.S.F.; data acquisition, A.S.F.; data analysis, A.S.F., M.A.T.; statistical analysis, A.S.F.; manuscript preparation, A.S.F.; manuscript editing and review, A.S.F., M.A.T.
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S. Quiroga, M. C. S |
