Magnetic Resonance Cholangiography: Applications in Patients with Calculus Disease of the Biliary Tract

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1 Original Article Magnetic Resonance Cholangiography: Applications in Patients with Calculus Disease of the Biliary Tract Terrence H. Liu and Claude H. Organ, Jr., Department of Surgery, University of California at San Francisco and the Alameda County Medical Center, Oakland, California, U.S.A. Magnetic resonance cholangiography (MRC) is a non-invasive imaging modality that has become widely available. In the short time since its introduction, MRC has been shown to possess excellent accuracy for the diagnosis of various biliary pathologies, including choledocholithiasis. Investigations of the clinical applications of MRC are ongoing. This review summarizes the diagnostic capabilities of MRC and discusses its application in the management of patients with gallstone diseases. [Asian J Surg 2004;27(2):99 107] Introduction Calculous disease of the biliary tract is common. Clinically, patients may present with symptoms or complications related to stones in the gallbladder or bile ducts. Cholesterol stones account for most stones encountered in patients in the Western hemisphere, whereas black and brown pigment stones are encountered frequently among patients in the Far East. 1 Ultrasonography is more than 95% effective for the diagnosis of cholelithiasis, but it is insensitive for the diagnosis of choledocholithiasis. 2 Therefore, common bile duct stones (CBDS) have traditionally been identified by direct contrast radiography through endoscopic, percutaneous or operative approaches. In more than 90% of patients with choledocholithiasis, the process develops due to stone passage from the gallbladder into the extrahepatic biliary tract (secondary choledocholithiasis), 1 so management generally requires the removal of a gallbladder with CBDS. Choledocholithiasis is discovered in 8% to 20% of patients undergoing cholecystectomy, with most patients having clinical, biochemical or sonographic abnormalities suggestive of CBDS. 3 5 During the era of open cholecystectomy, preoperative indicators were frequently used to select patients for cholangiography. When selected, patients underwent intraoperative cholangiography (IOC), where CBDS may be identified and treated during the same operation. Following the introduction of laparoscopic cholecystectomy (LC), several treatment options have emerged for the management of patients with gallbladder disease and suspected choledocholithiasis. The one-step approach involves LC, intraoperative diagnosis and laparoscopic management of CBDS. The two-step approach frequently relies on the preoperative diagnosis and treatment of CBDS prior to LC or, alternatively, CBDS are identified during LC and treated postoperatively by endoscopic sphincterotomy (ES). Although the one-step approach is an effective and safe option for many patients, 6,7 it has not gained wide acceptance among surgeons for various reasons. The debate regarding the optimal treatment approach for patients with CBDS is ongoing, unresolved, and beyond the scope of the current review. As many surgeons continue to approach patients with gallbladder disease by attempting to identify and treat CBDS prior to LC, endoscopic retrograde cholangiography (ERC) has remained the most commonly applied technique for the preoperative detection of CBDS, and ES is commonly applied during ERC to facilitate CBDS removal. 3 Although ERC is effective for the diagnosis of choledocholithiasis, the procedure is invasive and has been reported to be associated with Address correspondence and reprint requests to Dr. Terrence H. Liu, Department of Surgery, University of California at San Francisco, UCSF-East Bay, 1411 East 31 st Street, Oakland, CA 94602, U.S.A. LiuT@surgery.ucsf.edu Date of acceptance: 27 th April, Elsevier. All rights reserved. ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL

2 LIU AND ORGAN complications in approximately 3% of all cases. 8 As some surgeons continue to apply traditional indicators to select patients for preoperative imaging by ERC, in some practices 30% to 70% of patients undergoing this procedure have no CBDS identified. 3 Concerns with the morbidity and costs associated with ERC have led to the development of alternative imaging methodologies for biliary tract evaluations. Table 1 lists the available biliary imaging modalities and Table 2 3,9 42 lists the diagnostic efficacies, advantages and disadvantages of each. Magnetic resonance cholangiography (MRC) is one of the newer imaging tools that have emerged as potential diagnostic tools to replace ERC. 35,43 This review summarizes the clinical experience with MRC and discusses its status in the management of patients with calculous disease of the biliary tract. Table 1. Available biliary imaging modalities Non-invasive Transabdominal ultrasonography Magnetic resonance cholangiography Computed tomography cholangiography Invasive Intravenous cholangiography Endoscopic ultrasonography Endoscopic retrograde cholangiography Percutaneous transhepatic cholangiography Operative Laparoscopic ultrasonography Intraoperative cholangiography Intraoperative choledochoscopy Techniques and limitations MRC applies a heavily T2-weighted pulse sequence to delineate biliary tract anatomy and pathology. With this technique, the relatively static fluid within the biliary and pancreatic ducts appears as a white, rapidly flowing fluid, and background tissue appears hypodense; solid structures such as stones produce localized signal voids and appear black (Figure 1). Either a single breath-hold technique or a non-breath-hold technique may be used for image acquisition. Some radio- graphers favour the breath-hold technique, citing association with fewer motion artifacts. The non-breath-hold technique may offer advantages for patients who may be uncooperative or unable to follow verbal instructions. MRC is generally well tolerated by patients, 44 and the procedure may be completed in approximately 10 to 15 minutes without exposure to ionizing radiation or the application of sedatives or contrast material. Due to the small, enclosed space of the MR scanner, patients may be deemed unsuitable for this examination because of large body habitus or claustrophobia. Several patient fac- Figure 1. Magnetic resonance cholangiography (MRC). Coronal and axial MRC views demonstrating the presence of a 3 mm common bile duct stone in the distal common bile duct. 100 ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL /20

3 MAGNETIC RESONANCE CHOLANGIOGRAPHY tors have been shown to affect MRC accuracy; for example, the presence of ascites, periductal inflammation, periampullary duodenal diverticulum and crossing blood vessels may obscure the ductal fluid signal and lead to inadequate visualization of the distal CBD. 45 False-positive findings have been reported to occur as the result of a prominent sphincter of Oddi, duct tortuosity, cystic duct insertion, pneumobilia and surgical clips. 45 Additionally, radiographer inexperience contributes to inadequate application of image angles during image acquisition, resulting in the non-visualization of small CBDS. 45 Once obtained, the interpretation of MRC images by independent observers is consistent and reproducible. 12 Table 2. Efficacy of biliary imaging modalities Method Diagnostic efficacy for CBDS Sensitivity, % Specificity, % Advantages Disadvantages ERC (mean, 98) (mean, 98) Therapeutic capabilities; Requires sedation/ identifies anatomy and analgesia; patient anomalies discomfort; complications MRC (mean, 90) (mean, 96) Non-invasive; reproducible; No therapeutic capability identifies anatomy and anomalies Transabdominal Identifies cholelithiasis in Limited sensitivity for CBDS US 24,25,32 95% of patients; easy to interpret CT 23,33,34 Unenhanced CT: Widely available; Expertise required in the inter- CT/oral contrast: non-invasive pretation of unenhanced CT Endoscopic (mean, 95) Equipment and expertise Requires sedation/ US 3,18,23,35 (mean, 96) required analgesia; may miss stones in hepatic ducts Intravenous cho Identifies anatomy and Adverse reactions reported langiography anatomical variants in 0 12% of patients, with severe reactions reported in 0 9% of patients; not FDA approved in the USA IOC 23,31, (mean, 90) (mean: 95) Identifies anatomy and (reduced with static anatomical variants; cholangiography) special skills and equipment not needed Laparoscopic (mean, 95) (mean, 99) More sensitive than ERC Requires special equipment US and MRC at identifying and expertise CBDS < 3 mm; may be repeated during the operation Laparoscopic cho- Success rate, %: Therapeutic Requires expertise and ledochoscopy 42 (mean, 91) capabilities equipment; may cause pancreatitis, bleeding and perforation CBDS = common bile duct stones; ERC = endoscopic retrograde cholangiography; MRC = magnetic resonance cholangiography; US = ultrasonography; CT = computed tomography; IOC = intraoperative cholangiography; FDA = Food and Drug Administration. ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL

4 LIU AND ORGAN MRC accuracy We are not aware of any randomized prospective studies published to date evaluating MRC accuracy and utility. However, between 1995 and 2002, numerous case control series were published comparing the diagnostic characteristics of MRC to standard imaging Cumulatively, these investigations have reported MRC sensitivity of 90% (57 100%) and specificity of Table 3. Results of magnetic resonance cholangiography (MRC) for the detection of choledocholithiasis Source n Study Patient CBDS Comparison Sensitivity/specificity/ design disease prevalence, % study accuracy, % Reinhold et al Prospective Stones 27 ERC and IOC 90/100/97 Stiris et al Prospective Mixed disease 56 ERC 88/94/90 Mendler et al Prospective Mixed disease 58 ERC 86/97/91 Laokpessi, et al Prospective Stones 76 ERC and IOC 93/100 Magnuson et al Prospective Mixed disease 49 ERC and PTC 92/99 Liu et al Prospective Stones 30 ERC and IOC 85/90/89 Soto et al Prospective Stones 49 ERC / (Interpretations correlated between observers) Scheiman et al Prospective Stones and 17 ERC and EUS 40/96 stricture Holzknecht et al Prospective Stones and 40 ERC 93/96 stricture Zidi et al Prospective Mixed disease 70 ERC and IOC 57/100 Lomas et al Prospective Mixed disease 13 ERC 100/97 Soto et al Prospective Stones 51 ERC and CT cho- 96/100 langiography Varghese et al Prospective Mixed disease 30 ERC, PTC, and 93/99/97 IOC Varghese et al Prospective Mixed disease 18 ERC, PTC, US, 91/98/97 and IOC Chan et al Prospective Stones 42 ERC 95/95/89 Demartines et al Prospective Stones 52 ERC and IOC 100/96 Sugiyama et al Retrospective Stones 35 ERC and US 91/100/97 Guibaud et al Retrospective Mixed disease 25 ERC, PTC, and 81/98/94 IOC Fulcher et al Retrospective Mixed disease 5 ERC, PTC, and 100/100/100 IOC Calvo et al Prospective Stones 29 ERC 91/90 CBDS = common bile duct stones; ERC = endoscopic retrograde cholangiopancreatography; IOC = intraoperative cholangiography; PTC = percutaneous transhepatic cholangiography; EUS = endoscopic ultrasound; CT = computed tomography; US = ultrasonography. 102 ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL /20

5 MAGNETIC RESONANCE CHOLANGIOGRAPHY 96% (73 100%) for CBDS detection. Table summarizes the findings from the major series. In these reports, the minimal resolution of MRC for CBDS was in the range of 2 to 3 mm. However, one group has reported decreased sensitivity of MRC in identifying CBDS of less than 6 mm in diameter. 21 Generally, the reported MRC accuracy for CBDS is comparable with the accuracies reported for ERC and IOC. MRC has been shown to possess superior diagnostic accuracy for visualization of intrahepatic stones when compared to ERC. 46 Applications prior to LC The concept of being able to rapidly and non-invasively image the biliary tract prior to LC is appealing to patients and physicians who may prefer to identify and treat CBDS prior to LC. Therefore, preoperative patients represent the most extensively investigated patient to date. When applied in this setting, MRC accurately visualized CBDS in selected patients who were thought to benefit from preoperative endoscopic stone extraction. 15,17,27 Similarly, MRC identified patients without choledocholithiasis, eliminating unnecessary ERC in these individuals. These initial experiences have led some physicians to conclude that MRC is a valuable diagnostic tool in this patient ,27 While recognizing these advantages of MRC, most investigators agree that MRC is unnecessary and inappropriate in the management of patients for whom there is high suspicion of choledocholithiasis, such as those with cholangitis or severe jaundice. 17,27,31,47 At the same time, some physicians believe that the liberal application of preoperative MRC in patients with low clinical suspicion for choledocholithiasis may contribute to delays and unnecessary expenses in patient management. 17 The initial results have prompted some physicians to question the value of MRC in patient management. 48 The cost effectiveness of various diagnostic options for patients with biliary pancreatitis was the focus of an investigation by Arguedas et al. 49 By applying a decision-tree analysis model, these investigators determined that ERC was the most cost-effective initial study when applied to patients with more than 58% probability of having CBDS, while observation and IOC were the most cost-effective strategies for patients with less than 15% probability of having choledocholithiasis. For patients with moderate probability of having CBDS (15 58%), either MRC or endoscopic ultrasonography was the most costeffective initial diagnostic strategy. 49 As data from mathematical modelling have indicated that patients with a moderate risk of having choledocholithiasis are the most appropriate patients to undergo initial imaging with MRC, there have been limited clinical data published to specifically guide patient selection for MRC prior to LC. In the study by Liu et al, patients were identified and triaged preoperatively into four categories based on the probability of choledocholithiasis. 47 Patients with high probability were directed to ERC/ES prior to LC. Moderate-probability patients were directed to MRC and subsequent ERC/ES when CBDS were visualized. Low-probability patients were directed Table 4. Designation of choledocholithiasis probability Probability of CBDS Clinical diagnosis Ultrasonography results Serum chemistry results High Absence of cholecystitis CBD diameter 5 mm Presence of 2 indicators: total bilirubin or pancreatitis 1.5 mg/dl; alkaline phosphatase 150 U/L; AST 100 U/L; ALT 100 U/L Moderate Presence of pancreatitis, CBD diameter 5 mm Presence of 2 indicators: total bilirubin cholecystitis, or resolving 1.5 mg/dl; alkaline phosphatase 150 U/L; choledocholithiasis AST 100 U/L; ALT 100 U/L Low Any diagnosis CBD < 5 mm Presence of 2 indicators: total bilirubin 1.5 mg/dl; alkaline phosphatase 150 U/L; AST 100 U/L; ALT 100 U/L Very low No evidence of jaundice, CBD < 5 mm Total bilirubin < 1.5 mg/dl; alkaline cholangitis, or pancreatitis phosphatase < 150 U/L; AST < 100 U/L; ALT < 100 U/L CBDS = common bile duct stones; CBD = common bile duct; AST = aspartate transaminase; ALT = alanine transaminase. Adapted with permission from reference 46. ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL

6 LIU AND ORGAN Patient with gallstone disease, LC considered Clinical, laboratory, and ultrasonographic evaluation High probability Moderate probability Low probability Very low probability ERC/ES MRC LC/IOC LC CBDS clearance ( CBDS) (+ CBDS) (+ CBDS) LC ERC/ES ERC/ES CBDS clearance LC Figure 2. Selective imaging strategy based on the probability of choledocholithiasis. LC = laparoscopic cholecystectomy; ERC = endoscopic retrograde cholangiopancreatography; ES = endoscopic sphincterotomy; MRC = magnetic resonance cholangiography; IOC = intraoperative cholangiography; CBDS = common bile duct stones. Adapted with permission from reference 46. to LC with IOC, and very low-probability patients underwent LC without any imaging. These patient assignment criteria and the triage scheme are depicted in Table 4 and Figure 2. Prospective application of this treatment algorithm resulted in finding choledocholithiasis in 92.6%, 32.4%, 3.8% and 0.9% of patients in the four groups, respectively. With this triage scheme, 95% of patients who underwent ERC had CBDS identified, and unexpected CBDS were found in 1.4% of all patients. MRC use was limited to 8.4% of the patients, representing a significant reduction from the 23.5% application in patients treated during the time period immediately prior to the study. Based on the findings from this study, it appears that stratification of CBDS risk improves resource utilization. However, additional research is needed to further improve patient management and define the roles of ERC and MRC in the perioperative setting. Applications after LC Considerations of bile leak, retained CBDS and bile duct injury are the usual indications leading to imaging of bile ducts in the postoperative setting. While there is less experience with MRC application in patients following LC, this approach possesses similar diagnostic accuracy for choledocholithiasis as in the preoperative setting. MRC accurately identifies and helps to characterize cystic duct leak, bile duct strictures and major bile duct injuries in the postoperative setting The selection of an imaging modality in this setting should take into consideration the degree of suspicion for complications and the patient s intended treatment plan. When the clinical suspicion for complications is high and the problem is amenable to non-operative management, ERC or percutaneous transhepatic cholangiography should be considered initially to avoid unnecessary delays in therapy. MRC may be considered when patients with low to moderate suspicion of having biliary complications are encountered, where initial MRC imaging may prevent the use of unnecessary invasive procedures. Similarly, MRC may be useful for preoperative evaluation of selected patients with biliary tract injuries requiring operative reconstruction. Based on our review of published results, there are no available data to help identify patients who may benefit from MRC evaluation in this setting. Evaluation of primary CBDS Primary CBDS form de novo in the bile ducts and these are generally calcium bilirubinate stones. 1 The formation of primary CBDS is generally due to the combined effects of bacterial overgrowth and biliary stasis. Calcium bilirubinate stones 104 ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL /20

7 MAGNETIC RESONANCE CHOLANGIOGRAPHY have greater fluidity than cholesterol stones; therefore, primary stones are generally associated with a lesser degree of signal void and may appear less distinct than cholesterol stones on MRC. 26,54 Chan et al in Hong Kong retrospectively assessed the accuracy of T2-weighted MRC and reported a sensitivity of 87% for primary CBDS identification. 54 This high accuracy was achieved despite the mixed signal intensity found in 21% of stones in these patients. This group subsequently conducted a prospective evaluation of MRC accuracy for CBDS identification, in which MRC was found to possess sensitivity of 95% and specificity of 85% for CBDS identification when compared to ERC findings. 26 During this study, pneumobilia was recognized as a cause of false-positive results. These results suggest that MRC is accurate and may be useful for preoperative imaging in selected patients with primary CBDS. The reported rate of recurrent CBDS following ERC ranges from 4% to 10% Several risk factors for recurrence have been reported, including a CBD diameter of more than 20 mm, pneumobilia, and the presence of periampullary diverticulum It has been suggested that regular surveillance ERCP is useful for early identification of recurrent CBDS and in preventing the development of cholangitis. 56,57 Although the effectiveness of surveillance MRC has not been evaluated specifically, it would appear that this modality would be highly useful for long-term follow-up in these patients. Summary The diagnostic capabilities of MRC have undergone rigorous evaluations and these investigations have generally confirmed that MRC possesses diagnostic accuracies that are similar to those of direct cholangiography. MRC provides a safe, effective and non-invasive method to identify CBDS. The availability of MRC has made a dramatic impact on the management of patients with suspected choledocholithiasis in whom preoperative treatment of CBDS is contemplated. There is general agreement that MRC reduces and may eliminate the need for diagnostic ERC and it may reduce the occurrence of ERC-related morbidity. Clinical evidence suggests that MRC may be most beneficial and cost-effective when applied to patients with a moderate probability of having choledocholithiasis, but there are limited clinical data available to guide patient selection. Future investigations should be directed toward the development of safe and efficient MRC application strategies that are consistent with the goals and objectives of a minimally invasive approach to patient care. References 1. Liu TH, Moody FG. Pathogenesis and presentation of common bile duct stones. Semin Laparosc Surg 2000;7: Lichtenbaum RA, McMullen HF, Newman RM. Preoperative abdominal ultrasound may be misleading in risk stratification for presence of common bile duct abnormalities. Surg Endosc 2000;14: Erratum in: Surg Endosc 2000;14: Paul A, Millat B, Holthausen U, et al. Diagnosis and treatment of common bile duct stones (CBDS): result of a consensus development conference. Surg Endosc 1998;12: Golub R, Cantu R Jr, Tan M. The prediction of common bile duct stones using a neural network. J Am Coll Surg 1998;187: Trondsen E, Ewin B, Faerden AE, et al. Prediction of common bile duct stones prior to cholecystectomy. Arch Surg 1998;133: Rhodes M, Sussman L, Cohen L, Lewis MP. Randomized trial of laparoscopic exploration of common bile duct versus postoperative endoscopic retrograde cholangiography for common bile duct stones. Lancet 1998;351: Cuschieri A, Lezoche E, Morino M, et al. E.A.E.S. multicenter prospective randomized trial comparing two-stage vs single-stage management of patients with gallstone disease and ductal calculi. Surg Endosc 1999;13: Masci E, Toti A, Mariani S, et al. Complications of diagnostic and therapeutic ERCP: a prospective multicenter study. Am J Gastroenterol 2001;96: Erickson RA, Carlson B. The role of endoscopic retrograde cholangiography in patients with laparoscopic cholecystectomy. Gastroenterology 1995;109: Cotton PB. Endoscopic retrograde cholangiopancreatography and laparoscopic cholecystectomy. Am J Surg 1993;165: Cotton PB, Baillie J, Pappas TN, Meyers WS. Laparoscopic cholecystectomy and the biliary endoscopist. Gastrointest Endosc 1991;37: Reinhold C, Taourel P, Bret PM, et al. Choledocholithiasis: evaluation of MR cholangiography for diagnosis. Radiology 1998;209: Stiris MG, Tennoe A, Aadland E, Lunde OC. MR cholangiopancreatography and endoscopic retrograde cholangiopancreatography in patients with suspected common bile duct stones. Acta Radiol 2000;41: Mendler MH, Bouillet P, Sautereau D, et al. Value of MR cholangiography in the diagnosis of the biliary tree: a study of 58 cases. Am J Gastroenterol 1998;93: Laokpessi A, Bouillet P, Sautereau D, et al. Value of magnetic resonance cholangiography in the preoperative diagnosis of common bile duct stones. Am J Gastroenterol 2001;96: Magnuson TH, Bender JS, Duncan MD, et al. Utility of magnetic resonance cholangiography in the evaluation of biliary obstruction. J Am Coll Surg 1999;189: Liu TH, Consorti ET, Kawashima A, et al. The efficacy of magnetic resonance cholangiography for the evaluation of patients with suspected choledocholithiasis before laparoscopic cholecystectomy. Am J Surg 1999;178: Soto JA, Barish MA, Alverez O, Medina S. Detection of choledocholithiasis with MR cholangiography: comparison of three-dimensional fast spin-echo and single- and multisection half-fournier ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL

8 LIU AND ORGAN rapid acquisition with relaxation enhancement sequences. Radiology 2000;215: Scheiman JM, Carlos RC, Barnett JL, et al. Can endoscopic ultrasound or magnetic resonance cholangiography replace ERCP in patients with suspected biliary disease? A prospective trial and cost analysis. Am J Gastroenterol 2001;96: Holzknecht N, Gauger J, Sackmann M, et al. Breath-hold MR cholangiography with snapshot techniques: prospective comparison with endoscopic retrograde cholangiography. Radiology 1998;206: Zidi SH, Le Guen O, Rondeau Y, et al. Use of magnetic resonance cholangiography in the diagnosis of choledocholithiasis: prospective comparison with a reference imaging method. Gut 1999;44: Lomas DJ, Bearcroft WP, Gimson AE. MR cholangiopancreatography: prospective comparison of a breath-hold 2D projection technique with diagnostic ERCP. Eur Radiol 1999;9: Soto JA, Alvarez O, Munera F, et al. Diagnosing bile duct stones: comparison of unenhanced helical CT, oral contrast-enhanced CT, cholangiography, and MR cholangiography. AJR Am J Roentgenol 2000;175: Varghese JC, Liddell RP, Farrell MA, et al. The diagnostic accuracy of magnetic resonance cholangiopancreatography and ultrasound compared with direct cholangiography in the detection of choledocholithiasis. Clin Radiol 1999;54: Erratum in: Clin Radiol 2000;55: Varghese JC, Liddell RP, Farrell MA, et al. Diagnostic accuracy of magnetic resonance cholangiopancreatography and ultrasound compared with direct cholangiography in the detection of choledocholithiasis. Clin Radiol 2000;55: Erratum in: Clin Radiol 2000;55: Chan YL, Chan AC, Lam WW, et al. Choledocholithiasis: comparison of MR cholangiography and endoscopic retrograde cholangiography. Radiology 1996;200: Demartines N, Eisner L, Schnabel K, et al. Evaluation of magnetic resonance cholangiography in the management of bile duct stones. Arch Surg 2000;135: Sugiyama M, Atomi Y, Hachiya J. Magnetic resonance cholangiography using half-fourier acquisition for diagnosing choledocholithiasis. Am J Gastroenterol 1998;93: Guibaud L, Bret PM, Reinhold C, et al. Bile duct obstruction and choledocholithiasis: diagnosis with MR cholangiography. Radiology 1995; 197: Fulcher AS, Turner MA, Capps GW, et al. Half-Fourier RARE MR cholangiography: experience with 300 subjects. Radiology 1998;207: Calvo MM, Bujanda L, Calderon A, et al. Role of magnetic resonance cholangiography in patients with suspected choledocholithiasis. Mayo Clin Proc 2002;77: Barkun AN, Barkun JS, Fried GM, et al. Useful predictors of bile duct stones in patients undergoing laparoscopic cholecystectomy. Ann Surg 1994;220: Neitlich JD, Topazian M, Smith RC, et al. Detection of choledocholithiasis: comparison of unenhanced helical CT and endoscopic retrograde cholangiopancreatography. Radiology 1997;203: Soto JA, Velez SM, Guzman J. Choledocholithiasis: diagnosis with oral-contrast-enhanced CT cholangiography. AJR Am J Roentgenol 1999;172: Raval B, Kramer LA. Advances in the imaging of common duct stones using magnetic resonance cholangiography, endoscopic ultrasonography, and laparoscopic ultrasonography. Semin Laparosc Surg 2000;7: Grugge WR. Endoscopic ultrasonography: the current status. Gastroenterology 1998;115: Lindsey I, Nottle PD, Sacharias N. Preoperative screening for common bile duct stones with infusion cholangiography: review of 1000 patients. Ann Surg 1997;226: Nilsson U. Adverse reaction to iotroxate at intravenous cholangiography: a prospective clinical investigation and review of the literature. Acta Radiol 1987;28: Barteau JA, Castro D, Arrequi ME, Tetik C. A comparison of intraoperative ultrasound versus cholangiography in the evaluation of the common bile duct during laparoscopic cholecystectomy. Surg Endosc 1995;9: Birth M, Ehlers KU, Delinikolas K, et al. Prospective randomized comparison of laparoscopic ultrasonography using flexible-tip ultrasound probe and intraoperative dynamic cholangiography during laparoscopic cholecystectomy. Surg Endosc 1998;12: Halpin VJ, Dunnegan D, Soper NJ. Laparoscopic intracorporeal ultrasound versus fluoroscopic intraoperative cholangiography: after the learning curve. Surg Endosc 2002;16: Wood T, McFadyen BV Jr. Diagnostic and therapeutic choledochoscopy. Semin Laparosc Surg 2000;7: Tanner AR, Dwaraknath AD, Tait NP. The potential impact of highquality MRI of the biliary tree on ERCP workload. Eur J Gastroenterol 2000;12: Menon K, Barkun AN, Romagnuolo J, et al. Patient satisfaction after MRCP and ERCP. Am J Gastroenterol 2001;96: Fulcher AS, Turner MA. Pitfalls of MR cholangiopancreatography (MRCP). J Comput Assist Tomogr 1998;22: Kim TK, Kim BS, Kim JH, et al. Diagnosis of intrahepatic stones: superiority of MR cholangiopancreatography over endoscopic retrograde cholangiopancreatography. AJR Am J Roentgenol 2002;179: Liu TH, Consorti ET, Kawashima A, et al. Patient evaluation and management with selective use of magnetic resonance cholangiography and endoscopic retrograde cholangiopancreatography before laparoscopic cholecystectomy. Ann Surg 2001;234: Sahai AV, Devonshire D, Yeoh KG, et al. The decision-making value of magnetic resonance cholangiopancreatography in patients seen in a referral center for suspected biliary and pancreatic disease. Am J Gastroenterol 2001;96: Arguedas MR, Dupont AW, Wilcox CM. Where do ERCP, endoscopic ultrasound, magnetic resonance cholangiopancreatography, and intraoperative cholangiography fit in the management of acute biliary pancreatitis? A decision analysis model. Am J Gastroenterol 2001;96: Khalid TR, Casillas VJ, Montalvo BM, et al. Using MR cholangiography to evaluate iatrogenic bile duct injury. AJR Am J Roentgenol 2001;177: Yeh TS, Jan YY, Tseng JH, et al. Value of magnetic resonance cholangiopancreatography in demonstrating major bile duct injuries following laparoscopic cholecystectomy. Br J Surg 1999;86: Vitellas KM, El-Dieb A, Vaswani KK, et al. Using contrast-enhanced 106 ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL /20

9 MAGNETIC RESONANCE CHOLANGIOGRAPHY MR cholangiography with IV mangafodipir trisodium (Teslascan) to evaluate bile duct leaks after cholecystectomy: a prospective study of 11 patients. AJR Am J Roentgenol 2002;179: Chaudhary A, Negi SS, Puri SK, Narang P. Comparison of magnetic resonance cholangiography and percutaneous transhepatic cholangiography in the evaluation of bile duct strictures after cholecystectomy. Br J Surg 2002;89: Chan YL, Lam WW, Metreweli C, Chung SC. Detectability and appearance of bile duct calculus on MR imaging of the abdomen using axial T1- and T2-weighted sequences. Clin Radiol 1997;52: Ando T, Tsuyuguchi T, Okugawa T, et al. Risk factors for recurrent bile duct stones after endoscopic papillotomy. Gut 2003;52: Costamagna G, Tringali A, Shah SK, et al. Long-term follow-up of patients after endoscopic sphincterotomy for choledocholithiasis, and risk factors for recurrence. Endoscopy 2002;34: Geenen DJ, Geenen FM, Jafri WJ, et al. The role of surveillance endoscopic retrograde cholangiopancreatography in preventing episodic cholangitis in patients with recurrent common bile duct stones. Endoscopy 1998;30: ASIAN JOURNAL OF SURGERY VOL 27 NO 2 APRIL

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