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Original Article

Role of Magnetic Resonance Cholangiopancreatography in Patients With Suspected Choledocholithiasis

MARI M. CALVO, MD, PHD; LUIS BUJANDA, MD, PHD; ANGEL CALDERN, MD; IAKI HERAS, MD; JOS L. CABRIADA, MD; ANTONIO BERNAL, MD; VICTOR ORIVE, MD; AND ANGEL CAPELASTEGI, MD

Objectives: To investigate the diagnostic efficacy of magnetic resonance cholangiopancreatography (MRCP) in choledocholithiasis and to determine whether use of MRCP may eliminate the need for purely diagnostic endoscopic retrograde cholangiopancreatography (ERCP). Patients and Methods: A total of 116 patients with suspected biliopancreatic pathology were studied prospectively between November 1996 and February 1998. Choledocholithiasis was initially suspected in 61 patients and rated before ERCP and MRCP as being of low, intermediate, or high probability based on clinical, laboratory, and/or imaging findings (Cotton criteria). Results: The sensitivity of choledocholithiasis diagnosis was 91%, with a global efficacy of 90%. The level of duct stone obstruction was visualized in all patients. Suprastenotic dilatation also showed a good correlation to ERCP. Choledocholithiasis was found in 32 patients (65%) and 3 patients (33%) in the high- and intermediate-

probability groups, respectively. None of the low-probability patients had choledocholithiasis. Endoscopic retrograde cholangiopancreatography was performed for only a diagnostic (not therapeutic) purpose in 3 patients (6%) and 2 patients (22%) of the high- and intermediateprobability cases, respectively. Conclusions: Magnetic resonance cholangiopancreatography seems to be effective in diagnosing choledocholithiasis. It plays a fundamental role in patients with a low or intermediate risk of choledocholithiasis, contributing to the avoidance of purely diagnostic ERCP. Mayo Clin Proc. 2002;77:422-428
CT = computed tomography; ERCP = endoscopic retrograde cholangiopancreatography; HASTE = half-Fourier acquisition single-shot turbo spin echo; MRCP = magnetic resonance cholangiopancreatography

ndoscopic retrograde cholangiopancreatography (ERCP) is the reference diagnostic technique for visualizing biliary tract lithiasis.1,2 However, the technique is invasive, and the associated morbidity and mortality are considerable.1-3 Abdominal ultrasonography is a good exploratory option for visualizing biliary tract morphology, although its etiologic diagnostic sensitivity for the different causes of obstruction is low.4-7 Magnetic resonance cholangiopancreatography (MRCP) is a new technique that provides images similar to those of ERCP but without the need for contrast medium. Magnetic resonance cholangiopancreatography is noninvasive and involves no morbidity, provided its limited indications are observed.8-13

We investigated the diagnostic efficacy of MRCP in patients with suspected choledocholithiasis. For editorial comment, see page 407. PATIENTS AND METHODS A total of 116 patients with suspected pancreaticobiliary diseases (mean age, 67 years; male-female ratio, 1.08:1) were subjected to diagnostic and/or therapeutic ERCP and MRCP over 15 months (November 1996 to February 1998). In all patients, MRCP was performed within 72 hours before ERCP. The inclusion and exclusion criteria are indicated in Table 1. Initially, 61 patients were suspected of having choledocholithiasis based on clinical and/or laboratory findings and/or a dilated biliary tree visualized by ultrasonography (Cotton criteria, Table 2).14 A complete cholangiogram was obtained with ERCP in 60 of these patients (with failure in the 61st patient because of cannulation of the papilla due to a lodged duct stone). Magnetic resonance cholangiopancreatography was then used to visualize the biliary system in all 61 patients (Table 2). The study was approved by the local committee on human research, and all patients gave written informed consent to participation.
422 2002 Mayo Foundation for Medical Education and Research

From the Department of Gastroenterology (M.M.C., I.H., J.L.C., A.B.) and Department of Radiology (Osatek-RM) (A.C.), Galdakao Hospital, Galdakao, Spain; Department of Gastroenterology, San Eloy Hospital, Baracaldo, Spain (L.B.); and Department of Gastroenterology, Basurto Hospital, Bilbao, Spain (A.C., V.O.). Presented in part at the Gastroenterology Spanish Association annual meeting; Madrid, Spain; March 2001. Individual reprints of this article are not available. Address correspondence to Luis Bujanda, MD, PhD, C/Ocharan Mazas, 13 Q-1 A, 39700 Castro Urdiales (Cantabria), Spain (e-mail: digestivo .saneloy@hsel.osakidetza.net). Mayo Clin Proc. 2002;77:422-428

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Table 1. Inclusion and Exclusion Criteria* Inclusion criteria 1. Patients with suspected biliopancreatic pathology requiring ERCP between November 1996 and February 1998 2. Age >18 y 3. All patients in whom ERCP was started were included, even those in whom the pyloroduodenal region was not passed, the papilla could not be cannulated, or the desired therapy was not performed 4. All patients in whom MRCP was started were included, even those in whom exploration could not be completed 5. Informed written consent was required of the patient or relatives for both procedures Exclusion criteria 1. Patients with at least 1 absolute contraindication to either technique 2. Certain patients with degenerative or ankylotic conditions or those with senile dementia, because of the impossibility of patient cooperation in MRCP 3. Patients with severe clinical conditions in whom therapeutic requirements were urgent *ERCP = endoscopic retrograde cholangiopancreatography; MRCP = magnetic resonance cholangiopancreatography.

MRCP Technique All MRCP images were obtained by using a 1.5-T superconducting magnet with a gradient strength of 20 mT/ m (Magnetom Expert, Siemens, Erlangen, Germany), with a body-phased array coil through the liver and pancreas. The mean time of the MRCP examination with evaluation was 15 minutes. Magnetic resonance cholangiopancreatography was performed by using 2 HASTE sequences (half-Fourier acquisition single-shot turbo spin echo), with selective fat saturation. The first sequence afforded a single image with a dimension of 10 to 80 mm, and it exhibited the following

parameters: TR/TE/FA (2800/1100/180), matrix 240 256, field of view of 300 mm, and acquisition time of 7 seconds. The second sequence yielded 13 contiguous 5mm slices and presented the following parameters: TR/TE/ FA (10.92/87/180), matrix 240 256, field of view of 280 mm, and acquisition time of 19 seconds. Both sequences were acquired with breath-hold; as a result, adequate patient cooperation was essential. No type of contrast medium or medication was administered, and the patients were instructed to fast for 4 to 6 hours before the examination to prevent gastric contents from producing artifacts. The slice most suitable for further evaluation was selected. From this slice, we selected right and left oblique coronal (10-40) and coronal projections with a HASTE fat-suppressed sequence by using the aforementioned parameters with additional fat suppression. The individual images were examined with maximum intensity projections and multiplanar reconstructions. The HASTE and HASTE fat-suppressed modalities were breath-hold volume image acquisition sequences that permit 3-dimensional reconstruction and viewing in multiple planes. A long echo train was used, and because of the T2 decrease during data acquisition, the low-T2 tissues generated practically no signal; this and the fat saturation virtually suppressed the background signal. Only high-T2 tissues such as static fluids (eg, in the biliary tree) yielded high signal intensities. The MRCP images were analyzed by radiologists with experience in the field who were informed of the most relevant clinical data and results of other imaging studies performed (eg, ultrasonography). At no time was there any communication between investigators and radiologists.

Table 2. Initial Classification of Suspected Choledocholithiasis According to Cotton Criteria as Determined by ERCP and MRCP* Cotton criteria Group 3 (high probability) High risk due to cholangitis, pancreatitis, or jaundice; anomalies in liver tests (more than twice the normal level); and dilatation of the common biliary duct (>10 mm) Group 2 (intermediate probability) History of stone migration (antecedents of cholangitis or biliary pancreatitis), anomalies in liver tests (less than twice the normal level), and moderate dilatation of the common biliary duct (8-10 mm) Group 1 (low probability) Normal hepatic tests, no history of stone migration, and narrow common biliary duct (7 mm on ultrasonography) No. of patients 50 ERCP (No.) 49 MRCP (No.) 50

*ERCP = endoscopic retrograde cholangiopancreatography; MRCP = magnetic resonance cholangiopancreatography.

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Table 3. Comparative Results of ERCP and MRCP in High-Probability Patients (n=49)* ERCP (No.) 32 MRCP (No.) 29 1 1 4 2 1 10 1 2 2 1 1 1 8 2 4 2 1 7 Therapeutic ERCP (No.) 32

Findings Gallstones Normal Diagnostic doubt between gallstone and aerobilia Diagnostic doubt between gallstone lodged in papilla and ampulloma Papillitis Diagnostic doubt Ampulloma Diagnostic doubt between ampulloma and obstructive choledocholithiasis Cholangiocarcinoma Normal Diagnostic doubt with aerobilia

*ERCP = endoscopic retrograde cholangiopancreatography; MRCP = magnetic resonance cholangiopancreatography.

The radiologists reading the MRCP did not know the results of the ERCP. ERCP Technique Endoscopic retrograde cholangiopancreatography was considered the reference technique for determining the sensitivity and specificity of MRCP for choledocholithiasis, and it was always performed and interpreted by the same endoscopy team. Both exploratory techniques were used to assess the size of the biliary and pancreatic tracts, rating them as either normal or dilated, and to determine the presence or absence of obstruction, its level, and the underlying etiology. Sphincter of Oddi manometry was not performed; consequently, the suspected diagnosis of papillitis or dysfunction of the sphincter of Oddi as determined by ERCP was based on the following parameters: filiform papillary stenosis, delayed contrast medium elimination, and/or pain in response to contrast medium injection.
Table 4. Comparative Results of ERCP and MRCP in Intermediate-Probability Patients (n=9)* ERCP (No.) 3 2 4 MRCP (No.) 3 1 1 4 Therapeutic ERCP (No.) 3 2 2

Statistical Analysis The descriptive study consisted of the calculation of mean and median values, SD, and range. The sensitivity, specificity, and positive and negative predictive values were used to compare the 2 imaging techniques, ie, the performance of MRCP vs that of the gold standard (ERCP). Analysis focused on the comparison of cholangiography and pancreatography as obtained with both techniques. The 2 test was used to compare groups. Statistical significance was set at P<.05. The Epi-Info version 6.4 program and the SAS statistical package for Windows (version 6.12) were used throughout. RESULTS Endoscopic retrograde cholangiopancreatography visualized stones in 32 (65%) of the 49 patients with a high probability of choledocholithiasis (Table 3) and in 3 (33%) of the 9 patients with an intermediate probability of choledocholithiasis (Table 4) (Figures 1, 2, and 3). Cholangiography by ERCP and MRCP was normal in the 2 patients with a low probability of choledocholithiasis. Magnetic resonance cholangiopancreatography correctly diagnosed the 3 patients with choledocholithiasis in the intermediate-probability group, and in the highprobability group MRCP confirmed 29 of the 32 cases diagnosed by ERCP; ie, there were 3 false-negative readings by MRCP. In 1 patient a firm diagnosis of biliary tract normality was obtained; in another patient a differential diagnosis of aerobilia was considered; and in a third patient, doubts were raised about an obstructive duct stone or an ampullary neoplasm. Choled-

Findings Gallstones Papillitis Diagnostic doubt Normal

*ERCP = endoscopic retrograde cholangiopancreatography; MRCP = magnetic resonance cholangiopancreatography.

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Figure 1. Left, Choledocholithiasis detected by magnetic resonance cholangiopancreatography. A signal void is observed (arrow), corresponding to a duct stone. Right, Choledocholithiasis (arrow) detected by endoscopic retrograde cholangiopancreatography.

ocholithiasis was confirmed by ERCP in this last-mentioned patient. Two false-positive findings were recorded involving normal ERCP results in the presence of uncertainty between aerobilia and choledocholithiasis by MRCP. Another patient had filling defects at the ampullary level with a differential diagnosis of ampullary neoplasm or obstructive choledocholithiasis (ERCP confirmed an ampullary neoplasm). Another false-positive result with MRCP was classified as papillary dysfunction by the reference technique. Overall, MRCP had a sensitivity of 91%, a specificity of 84%, a positive predictive value of 89%, a negative predictive value of 88%, and a diagnostic accuracy of 90% in the diagnosis of choledocholithiasis. The level of duct obstruction was clearly visualized in all patients, with a good correlation to ERCP. In 1 patient both techniques identified a stone at the bifurcation of the hepatic ducts, together with a case of Mirizzi syndrome. In the rest of the patients the stone was located at middle or distal duct level. In no patient was intrahepatic lithiasis detected. Suprastenotic dilatation was also well correlated to ERCP, and no false-positive or false-negative results were obtained. Purely diagnostic ERCP was performed in 3 highprobability patients (6%) (Table 3), with interventional measures in the remaining patients; this included some patients with normal ERCP findings at the time, due to the risk of biliary colic, who had spontaneous stone elimination. In the intermediate-probability group (Table 4), pure-

ly diagnostic ERCP was performed in 2 patients (22%), and in the low-probability group the technique was strictly exploratory in both patients. Morbidity was 4% (2 of 49 patients) and consisted of mild acute pancreatitis and digestive tract bleeding sec-

Figure 2. Magnetic resonance cholangiopancreatography coronal acquisition showing a duct stone located in the hepatic hilum (arrow) and causing intrahepatic biliary tract dilatation.

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Figure 3. Various stones located in the middle and distal duct, identified by magnetic resonance cholangiopancreatography.

ondary to sphincterotomy that required endoscopic sclerotherapy. Purely diagnostic ERCP caused no morbidity. Mortality was zero. DISCUSSION Choledocholithiasis is the most common cause of biliary tract obstruction. Approximately 15% of patients with choledocholithiasis present with stones in the duct. Cholelithiasis may occasionally cause complications in the form of cholangitis, liver abscesses, pancreatitis, or biliary cirrhosis. Thus, establishing a correct diagnosis is extremely important before any form of therapy is attempted. With the introduction of computed tomography (CT) and ultrasonography, both oral and intravenous cholangiography have been relegated to a secondary role or simply are not performed. However, neither CT nor ultrasonography is effective in exploring the distal duct or ampullary region. In this context, the sensitivity of ultrasonography and CT in the diagnosis of choledocholithiasis is about 38% to 65% and 60% to 85%, respectively.4-7 The development of ERCP was a turning point in the management of such patients. This technique performs direct cholangiography and pancreatography, and it allows diagnosis, treatment, and/or palliative measures in the same procedure.1,2 Currently considered the reference technique in biliary and pancreatic pathology, ERCP affords a high diagnostic sensitivity. However, it has complications. The associated morbidity has been estimated to be around 0.8% to 10% (pancreatitis, perforation, hemorrhage, or cholangitis). Moreover, analgesia is required, and the technique is operator dependent.1-3 In this context, cannulation failure is reported in up to 3% to 9% of cases, even in experienced hands. Magnetic resonance cholangiopancreatography provides images similar to those of ERCP but without the

need for contrast medium of any kind. Thus, MRCP is considered a noninvasive technique that requires no patient sedation and is less operator dependent than ERCP. It provides images or sections in all 3 spatial dimensions.8-13 However, in some patients with claustrophobia it is necessary to administer sedation before MRCP is performed. Also, to obtain high-quality images with MRCP, patients must observe strict breath-holding. As a result, patients who have an altered mental status or are too ill may be unable to undergo MRCP. In the present study, the global efficacy of MRCP in diagnosing choledocholithiasis was high (90%) and similar to the results obtained by other authors (Table 5).15-30 In the study by Zidi et al,20 the sensitivity was low (57%). However, this may be because half the patients with choledocholithiasis had small stones and the patients fasted before MRCP. The main source of false-positive and false-negative results was the differential diagnosis of choledocholithiasis or aerobilia. Determination of the cause of signal voids within hyperintense bile was difficult with MRCP. By means of axial acquisitions, MRCP can attempt to distinguish between aerobilia and lithiasis because air bubbles are located in the upper portion of the duct, whereas stones tend to settle. In such situations, ERCP offers the advantage over MRCP by being able to perform tract cleaning or sweeps with balloons, verifying the diagnosis of lithiasis if stones are extracted. Other differential diagnoses (in addition to choledocholithiasis and aerobilia) that should be considered in the presence of signal voids in the biliary tract are hemobilia and intraductal tumors.31 In our study there were 2 false-positive MRCPs (ERCP was normal). It is possible that the stones present at the time of MRCP were spontaneously passed during the lapse (<72 hours) before ERCP was performed. Another difficult situation for MRCP is the differential diagnosis between a stone lodged in the papilla and ampullary neoplasm, which occurred in 2 of our patients. The ERCP interpretations in these cases were a papillary tumor in 1 patient and obstructive choledocholithiasis in the other. Another source of false-negative MRCP readings is very small stones, eg, impacted calculi (not surrounded by bile) and stones smaller than 3 to 5 mm.32 One of the patients endoscopically diagnosed with papillary stenosis was identified as having choledocholithiasis by MRCP. A retrospective evaluation suggested that this false-positive result may have been a pseudocalculus sign due to retrograde sphincter contraction with invagination of the proximal portion.33 Of the 50 patients considered to have a high probability of choledocholithiasis, ERCP found a stone in the biliary tract in 65.3%. These results agree with those of Cotton,14

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Table 5. Value of MRCP in the Diagnosis of Choledocholithiasis in Reports by Other Authors With More Than 24 Cases of Choledocholithiasis* No. of patients with calculi/total No. of patients with suspected calculi 46/129 113/147 32/50 25/70 30/100 49/70 76/286 30/99 28/58 34/97 30/110 30/92 60/136 26/108 25/106 32/126 32/61 Positive predictive value (%) 84 100 97 93 97 100 91 77 96 100 82-100 77 96 93 89 Negative predictive value (%) 99 89 82 100 97 50 97 94 88 95 96 96 98 94 88

Reference Taylor et al,15 2002 Laokpessi et al,16 2001 Stiris et al,17 2000 Demartines et al,18 2000 Varghese et al,19 1999 Zidi et al,20 1999 Boraschi et al,21 1999 Liu et al,22 1999 Mendler et al,23 1998 Sugiyama et al,24 1998 Reinhold et al,25 1998 Simeone et al,26 1997 Lomanto et al,27 1997 Becker et al,28 1997 Laghi et al,29 1996 Guibaud et al,30 1995 Current study

Sensitivity (%) 98 93 87 100 93 57 92 85 86 91 90 98 92 88 92 81 91

Specificity (%) 89 100 94 96 99 100 97 90 97 100 93-100 96 100 91 99 98 84

Diagnostic accuracy (%) 90 97 95 89 91 97 92-97 97 97 91 97 94 90

*MRCP = magnetic resonance cholangiopancreatography. Ellipses indicate that data not provided in study.

with stones in 50% to 80% of patients. In 3 patients (6%) the exploration was purely diagnostic. Some patients were subjected to papillotomy despite the fact that no choledocholithiasis was identified at the time. Therefore, in patients with a high probability of choledocholithiasis and who are candidates for interventional measures, ERCP is a good diagnostic/therapeutic option because it is possible to eliminate the need for MRCP and thus limit costs and unnecessary delays in treatment. Sahai et al34 reported that MRCP prevented less than 4% of diagnostic and therapeutic ERCP procedures. In that study, 62.3% had jaundice or abnormal liver enzymes or high suspicion for structural disease (high probability according to Cotton criteria), and in these cases the need for therapeutic ERCP was more frequent, as it was in our own study. Despite the few intermediate-probability patients in our study, this group may benefit from an initial MRCP to avoid purely diagnostic ERCP in up to 22% of cases. Magnetic resonance cholangiopancreatography played a fundamental role in the diagnosis of patients thought to have a low probability of choledocholithiasis, for in most such situations ERCP failed to detect choledocholithiasis despite the limited number of patients involved in our series. Additionally, MRCP may play an important role in confirming spontaneous elimination of choledocholithiasis after ERCP and sphincterotomy, in suspected choledocholithiasis among patients with previous biliary or gastric surgery, in subjects with gallbladder in place and amenable

to laparoscopic cholecystectomy, and in patients in whom ERCP has failed. We have not conducted a cost-efficacy evaluation of MRCP, although other authors saw an improved cost-efficacy ratio of MRCP in patients with intermediate risk of choledocholithiasis.35 CONCLUSIONS In our study, MRCP had high diagnostic accuracy in the evaluation of choledocholithiasis. In our opinion, MRCP may replace ERCP in patients with a low or intermediate probability of choledocholithiasis based on Cotton criteria. Patients with a high probability of choledocholithiasis should be referred for ERCP. In fact, 46 (94%) of the 49 high-probability patients who underwent ERCP required some type of endoscopic intervention. This strategy should reduce unnecessary ERCP without missing pronounced choledocholithiasis.
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