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Gastrointestinal Imaging |
1 From the Depts of Diagnostic Radiology (M.S.P., T.K.K., K.W.K., S.W.P., J.K.L., J.H.L., K.A.K., A.Y.K., P.N.K., M.G.L., H.K.H.) and Pathology (J.S.K.), Asan Medical Ctr, Univ of Ulsan College of Medicine, 388–1 Poongnap Dong Songpa-Ku, Seoul 138–040, South Korea; and Dept of Diagnostic Radiology, Yonsei Univ College of Medicine, Seoul, South Korea (M.S.P.). Received Sep 9, 2003; revision requested Nov 20; revision received Dec 31; accepted Feb 4. Address correspondence to T.K.K. (e-mail: taekyoung.kim@uhn.on.ca).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: MRCP and ERCP images in 50 patients (27 with cholangiocarcinoma [18 men, nine women; mean age, 58 years] and 23 with benign cause of stricture [13 men, 10 women; mean age, 60 years]) were retrospectively reviewed to assess the appearance of bile duct strictures. Final diagnosis was based on surgical or biopsy findings. Strictures were described according to their imaging appearance (irregular or smooth margins, asymmetric or symmetric narrowing, abrupt narrowing or gradual tapering, and presence or absence of double-duct sign). Sensitivity, specificity, and accuracy of MRCP and ERCP were calculated by using ratings of confidence in image-based diagnosis. Lengths of stricture were electronically measured and compared by using the Student t test.
RESULTS: Among cholangiographic criteria for malignant biliary stricture, irregular margins and asymmetric narrowing were more common in cholangiocarcinomas (24 [89%] of 27 patients) than in benign strictures (six [26%] and eight [35%] of 23 patients, respectively). Sensitivity, specificity, and accuracy of the two methods for differentiation of malignant from benign causes of biliary stricture were 81% (22 of 27), 70% (16 of 23), and 76% (38 of 50), respectively, for MRCP and 74% (20 of 27), 70% (16 of 23), and 72% (36 of 50), respectively, for ERCP. Mean length (± standard deviation) of cholangiocarcinomas was 30.0 mm ± 8.5, and that of benign strictures was 13.6 mm ± 9.1 (P < .001).
CONCLUSION: Accuracy of MRCP is comparable with that of ERCP. Regardless of modality, a lengthy segment of extrahepatic bile duct stricture with irregular margin and asymmetric narrowing suggests cholangiocarcinoma, and a short segment with regular margin and symmetric narrowing suggests benign cause.
© RSNA, 2004
Index terms: Bile duct radiography, 768.1222 • Bile ducts, neoplasms, 768.3212 • Bile ducts, stenosis or obstruction, 768.288, 768.294, 768.297 • Magnetic resonance (MR), cholangiopancreatography, 768.12149
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The imaging evaluation of patients with extrahepatic biliary stricture has traditionally included computed tomography (CT), ultrasonography (US), angiography, and/or direct cholangiography for diagnosis and staging (3,7). However, despite this multidisciplinary approach, a gray area persists in the diagnosis of some extrahepatic biliary strictures, particularly those in which there is no evidence of a mass or stone (1,8). Magnetic resonance (MR) cholangiopancreatography (MRCP) has gained recognition as an accurate and noninvasive alternative method for evaluating pancreaticobiliary ductal abnormalities and is gradually replacing direct cholangiography (9–11). Many previous studies (9,12–15) have indicated the usefulness of MRCP for the evaluation of extrahepatic biliary disease, especially for determining the level and cause of biliary obstruction.
To our knowledge, however, none have specifically addressed the MRCP and endoscopic retrograde cholangiopancreatographic (ERCP) findings that enable differentiation of extrahepatic bile duct cholangiocarcinoma from benign causes of stricture. Thus, the purpose of our study was to retrospectively evaluate imaging criteria for differentiating extrahepatic bile duct cholangiocarcinoma from benign causes of stricture at MRCP and to compare the diagnostic accuracy of MRCP with that of ERCP.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Reports from our radiology information database from January 1998 through April 2001 were reviewed to identify patients with extrahepatic bile duct stricture at MRCP. One radiologist searched the written radiologic reports of MRCP findings for the words extrahepatic duct and stricture. Stricture was diagnosed when focal luminal caliber change was present with proximal extrahepatic duct dilatation. The extrahepatic duct was considered dilated if its maximum diameter exceeded 7 mm in patients who had not undergone cholecystectomy and 10 mm in patients who had undergone cholecystectomy. Among 130 patients with extrahepatic bile duct stricture at MRCP, 23 patients were excluded because they had not undergone ERCP. We also searched the pathology records of the remaining 107 patients to identify those with histopathologically confirmed extrahepatic bile duct cholangiocarcinoma or benign stricture. Twelve patients with pancreatic carcinoma (n = 12), ampulla of Vater carcinoma (n = 11), metastasis (n = 4), duodenal carcinoma (n = 2), or gallbladder carcinoma (n = 1) were excluded from our study population. Twenty-seven others, in whom the cause of stricture was not histopathologically confirmed, also were excluded.
Our retrospective study population included 27 patients with extrahepatic bile duct stricture due to cholangiocarcinoma (18 men and nine women; mean age, 58 years; age range, 37–80 years) and 23 patients with benign extrahepatic bile duct stricture (13 men and 10 women; mean age, 60 years; age range, 25–79 years) confirmed by histopathologic findings. There were no statistically significant differences in age or sex between patients with cholangiocarcinoma and patients with benign cause of stricture (P = .67). Findings at surgery and/or biopsy were the standard of reference both for patients with cholangiocarcinoma (surgery, n = 22; biopsy, n = 5) and for patients with benign cause of stricture (surgery, n = 8; biopsy, n = 15). Four patients with cholangiocarcinoma and six patients with benign cause of stricture underwent preoperative biopsy. The causes of all 23 benign lesions were histopathologically confirmed to be chronic inflammation with fibrosis and/or ulceration (n = 17), mucosal hyperplasia of the ampulla of Vater (n = 3), or chronic papillitis (n = 3). Three of the 23 patients with benign biliary stricture also had chronic pancreatitis.
Examination Techniques
MRCP examinations were performed with a 1.5-T MR imaging system (Magnetom Vision; Siemens, Erlangen, Germany). A circular polarized phased-array body coil with four elements was used. No medication or contrast medium was administered prior to imaging. Two different MRCP sequences, single-shot rapid acquisition with relaxation enhancement (RARE) and multisection half-Fourier RARE (HASTE; Siemens), were applied as part of the comprehensive MR imaging examination typically performed in patients with biliary obstruction. One of several radiologists (K.W.K., S.W.P., J.K.L., J.H.L.) was present during the entire examination and determined the acquisition angle that optimally delineated the biliary ducts; the radiologists’ experience with MRCP ranged from 4 to 7 years. Thick-slab single-shot RARE images were obtained at three oblique coronal angles (–20°, 0°, and +20°) to allow optimal visualization of the bile ducts. Thin-section (multisection) half-Fourier RARE images were obtained at an angle of 20°–35° to the coronal plane, to simulate the right anterior oblique projection at direct cholangiography.
The parameters for single-shot RARE imaging were as follows: repetition time msec/effective echo time msec, 
/1200; echo train length, 240; flip angle, 150°; slab thickness, 50–70 mm; field of view, 260–340 mm; matrix, 240 x 256; and acquisition time, 2.32 seconds. The parameters for multisection half-Fourier RARE imaging were as follows: /95; echo train length, 128; flip angle, 150°; section thickness, 4 mm; no gap between sections; number of sections, 13–15 (volume of coverage, 52–60 mm); field of view, 260–340 mm; matrix, 240 x 256; and acquisition time, 18–20 seconds. Postprocessing of multisection half-Fourier RARE images was not performed.
ERCP examinations were performed by three experienced gastroenterologists during conscious sedation of the patient; the gastroenterologists’ experience with ERCP ranged from 10 to 15 years. Under fluoroscopic guidance, 10–30 mL of water-soluble contrast material was injected into the bile duct. Then multiple images of the bile duct were obtained with the patient in the prone position to optimally demonstrate the entire ductal anatomy and reveal any abnormalities.
Image Analysis
Three board-certified radiologists (M.S.P., K.W.K., S.W.P.) reviewed all MRCP and ERCP images retrospectively by using a picture archiving and communication system (PACS) workstation monitor; the radiologists’ experience with MRCP ranged from 6 to 7 years. MRCP images were initially stored on and retrieved from the PACS system, whereas the ERCP film images were scanned into the PACS system. Image interpretations were performed in consensus. Neither retrospective reader was involved in the prospective clinical interpretation of images. All cases were reviewed randomly and without knowledge of clinical data or whether extrahepatic bile duct strictures were diagnosed as malignant or benign at surgery or biopsy.
The three radiologists first reviewed the single-shot RARE and multisection half-Fourier RARE MRCP images. They classified the lesions into three groups according to anatomic location: proximal extrahepatic bile duct (common hepatic duct), middle extrahepatic bile duct (supraduodenal segment of the common bile duct), and distal extrahepatic bile duct (retroduodenal and intrapancreatic segments of the common bile duct). Cases with involvement of the bifurcation were excluded from our study because it was difficult to measure the length of such strictures and the maximum diameter of the bile duct. If a lesion extended across more than one defined ductal segment, the most proximal part of the extrahepatic duct involved by the lesion was used to define the anatomic location.
The radiologists classified each lesion according to its appearance (irregular or smooth margins, asymmetric or symmetric narrowing, abrupt narrowing or gradual tapering, and, in distal extrahepatic duct lesions, presence or absence of the double-duct sign). They then used a five-point scale to rate their confidence in evaluating the cause of biliary stricture: 1, definitely benign; 2, probably benign; 3, indeterminate; 4, probably malignant; and 5, definitely malignant. The cause of stricture was assumed to be malignant if the stricture was characterized by an irregular margin, asymmetric narrowing, abrupt narrowing, and/or association with the double-duct sign.
To avoid any bias from readers’ memory of findings on MRCP images, review of ERCP images was performed 1 week later. Readers were given a list of case (patient) numbers in random order and reviewed the ERCP images by using the same method used for review of the MRCP images.
One of the readers (J.W.L.) used electronic calipers available at the workstation to measure the length of the stricture and the maximum diameter of the dilated extrahepatic ductal segment proximal to the stenosis on MRCP images at a PACS workstation. The same reader reviewed and tabulated the serum levels of total bilirubin, alkaline phosphatase, and carbohydrate antigen 19–9 that were measured at initial admission, as well as the results of endoscopic biopsy at ERCP.
Statistical Analysis
To measure the agreement between findings at MRCP and at ERCP in the assessment of the appearance of a stricture (irregular or smooth margin, asymmetric or symmetric narrowing, and abrupt narrowing or gradual tapering), 
values were calculated. A value greater than 0 was considered to indicate a positive (0.01–0.40, marginal; 0.41–0.70, good; 0.71–1.00, excellent) correlation.
To measure the agreement between confidence ratings in the assessment of the cause of stricture at MRCP and at ERCP, weighted values were calculated. A weighted value greater than 0 was considered to indicate a positive (0.01–0.40, marginal; 0.41–0.70, good; and 0.71–1.00, excellent) correlation. Confidence ratings were used also to calculate the sensitivity, specificity, and accuracy of diagnosis based on MRCP and ERCP findings. A rating of 1 or 2 was considered to indicate a diagnosis of benign cause; a rating of 3, indeterminate cause; and a rating of 4 or 5, malignant cause. Sensitivity, specificity, and accuracy were calculated as follows: sensitivity = (IM/PM) · 100, where IM is the number of correct imaging-based diagnoses of malignancy and PM is the number of proved malignancies; specificity = (IB/PB) · 100, where IB is the number of correct imaging-based diagnoses of benign stricture and PB is the number of proved benign strictures; and accuracy = [(IM + IB)/(PM + PB)] · 100.
The mean values for length of stricture, maximum diameter of the extrahepatic duct, and serum levels of total bilirubin, alkaline phosphatase, and carbohydrate antigen 19–9 in malignant and benign biliary strictures were compared by means of the Student t test. A P value of less than .05 was considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our comparison of the stricture shape in cholangiocarcinoma and in benign conditions at MRCP is illustrated in Figure 1. Among the standard cholangiographic criteria for malignant biliary stricture, irregular margins and asymmetric shape were more common in cholangiocarcinomas (Fig 2) (both were seen in 24 [89%] of 27 patients) than in benign strictures (seen in six [26%] and eight [35%] of 23 patients, respectively); abrupt narrowing, however, was encountered with similar frequency in cholangiocarcinomas (19 [70%] of 27 patients) and benign strictures (17 [74%] of 23 patients) (Figs 3, 4). The frequency of appearance of the double-duct sign was not significantly different between cholangiocarcinomas (seven [26%] of 27 patients) and benign strictures (eight [35%] of 23 patients).
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values calculated for agreement between findings at MRCP and those at ERCP indicated good agreement between the two modalities (Table 1).
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value for agreement between MRCP and ERCP in level of confidence in evaluation of the cause of the biliary stricture indicated good agreement between the two imaging modalities (Table 1).
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Among the tissue samples from the nine patients with cholangiocarcinoma who underwent endoscopic biopsy, samples were insufficient in one patient (11%), negative for malignancy in two patients (22%), and showed adenocarcinoma in six patients (67%). Among the tissue samples from the 21 patients with benign stricture who underwent endoscopic biopsy, samples were insufficient in four patients (19%), composed of atypical cells in one patient (5%), and negative for malignancy in 16 patients (76%).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Preoperative histologic diagnosis of extrahepatic cholangiocarcinoma depends solely on endoscopic tissue sampling and cytologic analysis. Endoscopic biopsy or brushing of the stricture requires a high degree of skill on the part of the endoscopist, and the lesions may not always be accessible; sensitivity of the test therefore ranges from 44% to 100% (21,22). In our study, endoscopic biopsy samples could be obtained in only nine (33%) of 27 patients with cholangiocarcinoma. Moreover, in the infiltrative type (the most common type of extrahepatic bile duct carcinoma), endoscopic findings and tissue sampling frequently are unsatisfactory because intramural spread beneath the bile duct epithelium and abundant fibrosis interfere with adequate tissue sampling and lead to high false-negative rates (1,8,23). In our study, the biopsy results were false-negative in three (33%) of nine patients with cholangiocarcinoma who underwent endoscopic biopsy. It is necessary to find another diagnostic modality and reliable diagnostic criteria for differentiating extrahepatic cholangiocarcinoma from benign stricture so that patients with cholangiocarcinoma will have access to appropriate surgical cure and patients with benign stricture will be spared unnecessary surgery.
MRCP has been reported to be highly sensitive (72%–98%) for the diagnosis of biliary obstruction (9,12). The reported sensitivity of MRCP for differentiating benign from malignant biliary obstructions, however, ranges very widely, from 30% to 98% (9,12–15). In several studies (9,12–15), the study populations had malignant biliary obstructions with various causes, including pancreatic head carcinoma, cholangiocarcinoma, duodenal carcinoma, or metastasis. In these studies, MRCP image interpretations, in accordance with the known direct cholangiographic criteria, were based on the assumption that abrupt, irregular, and asymmetric luminal narrowing associated with the double-duct sign indicates a malignant rather than benign cause. In our study, an irregular and asymmetric stricture margin was more common in cholangiocarcinoma, and a smooth and symmetric stricture margin was more common in benign stricture, findings that confirm these cholangiographic criteria. Irregular margins and asymmetric narrowing, however, were not specific to malignant strictures but were seen also in benign strictures in our study (in 26% and 35% of cases, respectively). In addition, in our study, gradual tapering was common in strictures due to cholangiocarcinoma, as well as in benign strictures, and abrupt narrowing was common in benign strictures, as well as in strictures due to cholangiocarcinoma; our findings do not confirm these cholangiographic criteria.
In our study, a correlation was found between the length of stricture and the cause of stricture; the involved segment was longer in cholangiocarcinoma than in benign stricture. The degree of bile duct dilatation and the frequency of depiction of the double-duct sign, however, did not differ significantly between cholangiocarcinoma and benign stricture.
Histologically, most extrahepatic bile duct carcinomas have an infiltrative growth pattern, and the infiltrative type of bile duct carcinoma spreads intramurally, beneath the bile duct epithelium (2,3). This growth pattern helps to explain not only the long ductal segment typically involved in such strictures but also the relatively frequent appearance of gradual tapering. We believe that abundant fibrosis and desmoplastic reaction without definite mass formation in some bile duct carcinomas may lead to a stricture that involves a long ductal segment and appears gradually tapered and without mass effect rather than abruptly narrowed.
Despite the widely accepted criteria for characterizing benign and malignant lesions, difficulties persist in the differentiation of some benign and malignant strictures of the bile duct (9,12–15). Some authors (15) have suggested that these difficulties might be due to the lower spatial resolution and lower contrast of MRCP images compared with ERCP images. Our study results show that the sensitivity, specificity, and accuracy of MRCP are not significantly different from those of ERCP. Our results suggest that the diagnostic capability provided by MRCP, although it is dependent on the depicted morphology of the stricture, is not inferior to that provided by ERCP for the differentiation of extrahepatic cholangiocarcinomas from benign biliary strictures.
There are several limitations to our study. First, dynamic contrast material–enhanced MR images were not acquired in most of the patients in our study, and we did not analyze the cross-sectional MR imaging data. In daily practice, we sometimes must differentiate malignant from benign strictures on the basis of MRCP images alone. At other institutions, too, many patients with suspected biliary disease first undergo CT or US and then MRCP without dynamic contrast-enhanced MR imaging. Therefore, we think that the analysis of the MRCP images without cross-sectional MR images is useful for the differentiation of extrahepatic bile duct cholangiocarcinoma from benign stricture.
Second, we could not measure the length of the stricture and the maximum diameter of the extrahepatic bile duct on the ERCP images we reviewed, because these images were obtained with secondary scanning of the original film images.
Third, the extrahepatic bile duct distal to the obstruction may have been collapsed at the time of MRCP, which may have caused overestimation of the length of the stricture on MRCP images in our study.
Fourth, although the parameters (stricture morphology) that we evaluated are somewhat subjective and likely to be observer dependent, we did not measure the agreement between observers.
Fifth, extrinsic compression due to chronic pancreatitis may produce a long, symmetric, and smooth stricture in the distal common bile duct (24). Although only three of our study patients (13%) with benign stricture had chronic pancreatitis, this possibility should be included among the diagnostic considerations.
In conclusion, a lengthy biliary stricture with asymmetric narrowing and an irregular margin may indicate cholangiocarcinoma rather than a benign lesion. On the other hand, a short stricture with symmetric narrowing and a smooth margin may indicate a benign lesion rather than cholangiocarcinoma. The presence of the double-duct sign, the degree of ductal dilatation, and an appearance of gradual tapering or abrupt narrowing were not helpful for differentiating cholangiocarcinoma from benign stricture.
The performance of MRCP in enabling differentiation of benign strictures from strictures caused by extrahepatic cholangiocarcinoma is comparable with that of ERCP, and this differentiation may be similarly difficult with both tests.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, T.K.K.; study concepts and design, M.S.P., T.K.K.; literature research, M.S.P.; clinical studies, K.W.K., S.W.P., J.S.K.; data acquisition, K.A.K.; data analysis/interpretation, J.H.L.; statistical analysis, J.K.L.; manuscript preparation, M.S.P.; manuscript definition of intellectual content, A.Y.K., P.N.K., M.G.L., H.K.H.; manuscript editing, revision/review, and final version approval, T.K.K.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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uz M, Erkoçak E. Biliary tuberculosis mimicking cholangiocarcinoma: treatment with metallic biliary endoprosthesis. Am J Gastroenterol 2000; 95:1069-1071.[CrossRef][Medline]
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