Magnetic resonance cholangiopancreatography (MRCP) is

CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2008;6:967 977 CLINICAL IMAGING Magnetic Resonance Cholangiopancreatography: Current Use and Future Applications VIKRAM A. SAHNI and KOENRAAD J. MORTELE Division of Abdominal Imaging and Intervention, Department of Radiology, Brigham and Women s Hospital, Harvard Medical School, Boston, Massachusetts Magnetic resonance pancreatography (MRCP) is now established as a robust noninvasive tool for the evaluation of biliary and pancreatic pathology. Its diagnostic performance is comparable with endoscopic retrograde cholangiopancreatography without the associated risks. This article aims to familiarize the reader with the technique, clinical indications, and limitations of the investigation. Common pitfalls in interpretation also are addressed. Emerging applications and techniques are discussed that include recent advances in technology and the development of functional imaging. Magnetic resonance cholangiopancreatography (MRCP) is a noninvasive diagnostic technique that was developed for the visualization of the biliary and pancreatic ducts. Its use was first reported in 1991, 1 and since then the method has evolved along with the advances in magnetic resonance imaging (MRI) hardware and imaging sequences. MRCP does not expose the patient to the risks associated with endoscopic retrograde cholangiopancreatography (ERCP) or percutaneous cholangiography. These can occur in up to 5% of ERCP procedures. 2 In addition, there is no use of ionizing radiation or iodinated contrast. It has, therefore, become the investigation of choice for many conditions when evaluating pancreaticobiliary ductal disease. Invasive cholangiography remains the investigation of choice when intervention is required. This review aims to familiarize the reader with current techniques, indications, limitations, pitfalls, and future applications of MRCP. Technique Patient preparation initially involves excluding any condition that may preclude an MRI. Patients are required to fast for 4 to 6 hours before the examination, to permit gallbladder filling and promote gastric emptying. T2-negative oral contrast can be administered to reduce the signal from the overlapping stomach and duodenum. 3 Pineapple juice has been used successfully as a negative oral contrast agent because of its high manganese content. 4,5 It is widely available and cheaper than commercially produced superparamagnetic preparations. No intravenous contrast or antispasmodics are administered routinely. MRCP ideally is performed on a high field system with high performance gradients and a phased-array torso coil. 6 MRCP uses heavily T2-weighted sequences to return high signal from slow moving fluid in the biliary and pancreatic ducts, which have long T2 relaxation times. 7 Signal from background tissue is suppressed because of its shorter T2 relaxation time. This maximizes duct visibility and contrast. Ultra-fast T2-weighted imaging is optimally performed by using single-shot fast spin echo sequences. 8 These sequences can be performed in a breathhold and, therefore, reduce breathing and motion artifact. 9 The data obtained can be displayed in a variety of formats that usually involve the axial, coronal, and oblique coronal planes. The coronal images can be viewed as either thin collimation (3 5 mm) source images or thick slabs (30 50 mm) (Figure 1A). In addition, the thin collimation images can be manipulated to produce maximum intensity projection 3-dimensional reconstructions (Figure 1B). Both the thick slab and the maximum intensity projections produce cholangiogram-like projectional images. These, however, have inferior spatial resolution compared with the thin collimation images and can miss abnormalities such as stones. 10 The thin collimation images should always be reviewed to avoid missing pathology. By optimizing techniques, ducts with diameters of less than 1 mm can be visualized. 11 A relatively recent adjunct to routine MRCP has been functional imaging. This involves dynamic pancreatography after intravenous (IV) stimulation by human or porcine secretin 12 (Figure 2). Secretin leads to stimulation of the exocrine pancreatic gland. In addition, it temporarily increases the tone of the sphincter of Oddi during the first 5 to 6 minutes after injection, thereby inhibiting release of fluid through the papilla of Vater. After this the tone decreases. 13 Secretin, therefore, initially improves delineation of the pancreatic duct, facilitating the demonstration of anatomic variants or morphologic changes in the normal or diseased pancreas. 14 The exocrine function of the pancreas also can be evaluated, by qualitatively or semiquantitatively assessing the increase in fluid in the duodenum after the sphincter of Oddi relaxes. 15 T2-weighted single-shot fast spin echo images are obtained every 30 seconds after IV secretin stimulation (0.2 mcg/kg of body weight) for at least 10 minutes. MRCP often is combined with conventional abdominal MRI to provide extraductal and parenchymal evaluation. MR angiography also can be performed in the same session if indicated. Abbreviations used in this paper: CT, computerized tomography; ERCP, endoscopic retrograde cholangiopancreatography; IPMN, intraductal papillary mucinous neoplasm; IV, intravenous; MRCP, magnetic resonance cholangiopancreatography; MRI, magnetic resonance imaging. 2008 by the AGA Institute 1542-3565/08/$34.00 doi:10.1016/j.cgh.2008.05.017

968 SAHNI AND MORTELE CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 6, No. 9 of duct injury is twice that of open cholecystectomy. 20 MRCP is 98% accurate in the diagnosis of aberrant hepatic ducts and 95% accurate in the diagnosis of cystic duct variants. 21 There is also variability in the pancreatic ductal anatomy. In 91% of individuals, the duct of Wirsung is the major drainage route of the pancreas through the major papilla. A patent duct of Santorini drains through the minor papilla in 44% of the population. 7 Pancreas divisum and annular pancreas are important conditions to diagnose. Pancreas divisum occurs in 4% to 10% of the population. 22 The ventral and dorsal pancreatic ducts fail to fuse, with the majority of the pancreatic secretions emptying through the duct of Santorini and the minor papilla. The clinical importance of pancreas divisum is its possible association with recurrent pancreatitis. 23,24 MRCP diagnosis is made by visualizing 2 separate ducts with independent drainage sites. The dominant dorsal duct lies anterior to the common duct and enters into the minor papilla (Figure 4). MRCP has been shown to be 100% accurate in diagnosing pancreas divisum. 25 Annular pancreas, characterized by pancreatic tissue encircling the second part of the duodenum, also can be diagnosed by MRCP 26 (Figure 5). Figure 1. (A) Oblique coronal, thick slab MRCP image and (B) maximum intensity projection MRCP image show normal common duct (short arrow), main pancreatic duct (long arrow), and gallbladder (*). This has been referred to as the all-in-one technique or the one-stop-shopping technique. Classic Indications Delineation of Anatomy The diagnosis of congenital and developmental biliary and pancreatic anomalies is an important indication for MRCP. Liver resection, living related donor transplantation, biliary intervention, and laparoscopic cholecystectomy are several procedures in which the prospective identification of congenital biliary variants may prevent inadvertent injury. Normal biliary anatomy is present only in 58% of the population 14 ; the most common anomaly is drainage of the right posterior duct into the left hepatic duct in 13% to 19% of the population. 16 18 The right posterior duct drains into the right anterior duct in 12% 17 and there is a triple confluence of the right anterior, right posterior, and left hepatic ducts in 11% 16 (Figure 3). Common cystic duct anomalies include low or medial insertion into the common hepatic duct and a long parallel course with the common hepatic duct. 19 Identification of these variants is important before laparoscopic cholecystectomy, in which the risk Choledocholithiasis Stones within the common duct are identified as lowsignal filling defects within high-signal intensity bile on MRCP examinations (Figure 6). Stones as small as 2 mm have been identified, even in nondilated ducts. 27,28 The performance of MRCP for common duct stones is superior to ultrasound and computerized tomography (CT), 29 and comparable with ERCP. 30 Studies have yielded sensitivities ranging from 81% to 100%, and specificities ranging from 96% to 100%. 28,31 35 Negative predictive values are also very high (94% 100% 28,31 35 ); MRCP is, therefore, a good test in patients with a low to intermediate probability of having choledocholithiasis, to exclude stones and prevent these patients from being subjected to an unnecessary ERCP procedure and its associated complications. Neoplasms Malignant disease of the biliary system and the pancreas frequently results in ductal obstruction. MRCP has been shown to be accurate in identifying the presence, cause, and level of obstruction. 35 38 Cholangiocarcinoma, pancreatic ductal adenocarcinoma, liver parenchymal tumors, ampullary neoplasms, and duodenal adenocarcinoma all can cause ductal obstruction. 39 MRCP, compared with contrast cholangiography, can visualize the duct before and after an obstructing lesion, thereby providing a roadmap for any future intervention. Also, the examination is noninvasive so there is no risk of cholangitis and the procedure can be combined with routine abdominal MRI to stage the tumor at the same time. 6 MRCP findings of cholangiocarcinoma include an abrupt biliary obstruction with dilatation of the ducts above (Figure 7). MRCP plays an important role in staging hilar (Klatskin) tumors. 40 The investigation is important in determining resectable disease and providing guidance for palliative biliary intervention. 41 The disease has a 5-year survival rate of 1%, 42 but by using diagnostic imaging to select appropriate surgical candidates a 5-year survival rate of 20% can be achieved. 43,44 Tumors are staged according to the Bismuth-Corlette 45 classification, with MRCP showing an accuracy of 84%. 46 In combination with

September 2008 MAGNETIC RESONANCE CHOLANGIOPANCREATOGRAPHY 969 Figure 2. Oblique coronal, thick slab MRCP images (A) before, (B) 5 minutes after, and (C) 10 minutes after intravenous injection of secretin. (B) Normal early mild dilatation of the pancreatic duct (black arrow) with (C) return to baseline shows normal pancreatic duct compliance. (A C) Progressive filling of the duodenum (white arrows) shows normal exocrine pancreatic function. conventional MRI, biliary, vascular, and liver involvement can be assessed to determine resectability. 41 MRCP depicts obstruction and encasement of the pancreatic duct by pancreatic ductal adenocarcinoma. Smooth homogenous dilatation of the duct with an abrupt termination favors malignancy. 47 If the lesion is in the head then biliary obstruction can occur; this results in the double duct sign in 77%, 48 which is highly suggestive of malignancy 49 (Figure 8). MRCP alone has been shown to be more sensitive and specific than ERCP in detecting pancreatic carcinoma. 50 Combining MRCP with conventional MRI and MR angiography has been reported to be superior in staging and determining resectability than the combination of ultrasound, CT, and conventional angiography. 51 Intraductal papillary mucinous neoplasm (IPMN) is a mucin-producing tumor of the pancreas and is thought to originate in the main pancreatic duct or its branches 52 (Figure 9). It has either hyperplastic, dysplastic, or malignant epithelium. 11 Multiple IPMNs may be present in 23% of patients. 53 On MRCP, segmental or diffuse dilatation of the main pancreatic duct or a unilocular or multilocular cystic lesion is typical. 54 Communication between the main pancreatic duct and the cystic lesion may be depicted. Papillary projections may be present. Bulging of the papilla, biliary obstruction, and large caliber of the main pancreatic duct ( 1 cm) are more common in patients with malignant IPMNs. 55 MRCP is considered superior to ERCP in diagnosing IPMN, 56 and ERCP on occasion may not be possible because the thick mucin restricts complete opacification of the ductal system. The use of IV secretin stimulation is thought to be useful in depicting the communication of branch duct IPMNs with the main pancreatic duct. 57 MRCP, however, cannot differentiate fluid from mucin and sampling with ERCP may be required. Postsurgical Conditions ERCP is either difficult or impossible to perform in patients who have undergone certain surgical procedures because of unfavorable anatomy. Biliary-enteric, pancreaticoenteric, and Billroth II anastomoses all provide a diagnostic challenge. Duodenal and gastric obstruction and anatomic variants such as juxta-ampullary diverticula and choledochal cysts also may contraindicate ERCP. In these cases, MRCP can provide useful information. Intraductal stones and strictures can be shown with sensitivities of 90% and 100%, respectively, in patients with biliary-enteric anastomoses. 58

970 SAHNI AND MORTELE CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 6, No. 9 Figure 3. Oblique coronal, thick slab MRCP image shows triple confluence of the right anterior, right posterior, and left hepatic ducts (arrow). MRCP also can be used to evaluate for late biliary complications after liver transplantation. 47,59 These occur in up to 34% of patients and include anastomotic strictures, ischemic cholangiopathy, and stones. 60 Accurate noninvasive diagnosis can prevent unnecessary interventional procedures. Sensitivities of 93% and specificities of 92% have been reported in detecting post liver transplant biliary complications. 61 Intrahepatic Biliary Disease Primary sclerosing cholangitis occurs in up to 7.5% of patients with ulcerative colitis and 3.4% of patients with Crohn s disease. 62 Seventy percent to 80% of patients with Figure 5. Annular pancreas. (A) Oblique coronal, thick slab MRCP image shows a pancreatic duct (solid white arrow) that encircles the second part of the duodenum (open arrow). (B) Axial T1-weighted, unenhanced, 3-dimensional spoiled gradient-echo fat-suppressed MR image shows pancreatic parenchyma (arrow) encircling the duodenum. Figure 4. Oblique coronal, thick slab MRCP image shows pancreas divisum. The dorsal duct (short solid white arrow) crosses anterior to the common bile duct (open arrow) to empty into the minor papilla. An incidental intraductal papillary mucinous neoplasm is seen to arise from the ventral duct (long solid white arrow). primary sclerosing cholangitis have ulcerative colitis. 63 Cholangiography, usually ERCP, is considered the gold standard for the diagnosis of primary sclerosing cholangitis. 64 Complications, such as infection and pancreatitis, 65 are thought to occur

September 2008 MAGNETIC RESONANCE CHOLANGIOPANCREATOGRAPHY 971 in detecting and characterizing the cysts. 80 Complications such as cholangiocarcinoma and choledocholithiasis also have been shown with excellent accuracy with MRCP. 79 Appearances depend on the type of choledochal cyst and are characterized by variable dilatation of the intrahepatic and extrahepatic biliary system (Figure 11). MRCP also can show an anomalous pancreaticobiliary junction. 79 This results in a long common channel after the common bile duct and duct of Wirsung unite. This has been proposed as the cause for certain types of choledochal cysts owing to reflux of pancreatic secretions into the bile duct. 19,80 Acute and Chronic Pancreatitis Figure 6. Oblique coronal, thick slab MRCP image shows an impacted low-signal stone in the distal common duct (*) with intrahepatic (arrows) and extrahepatic biliary dilatation. The use of MRCP in acute pancreatitis is based primarily on establishing etiology. Common duct stones are well visualized on MRCP. 27,28 In addition, congenital abnormalities associated with pancreatitis, such as pancreas divisum and more frequently in patients with primary sclerosing cholangitis rather than those without. 66 MRCP provides an alternative diagnostic tool without the aforementioned problems. It also allows the assessment of ducts proximal to the obstruction and in combination with routine liver MRI sequences can evaluate the duct wall and hepatic parenchyma. 67 Complications of primary sclerosing cholangitis, such as cholangitis and cholangiocarcinoma, can therefore be diagnosed. The classic appearance of primary sclerosing cholangitis on MRCP images is the presence of multiple diffuse short (1 2 mm) strictures that alternate with normal or slightly dilated segments 68 (Figure 10). This can affect both the intrahepatic and extrahepatic biliary system, producing a beaded appearance. Peripheral duct side branches become obliterated as the disease progresses, resulting in pruning. Other abnormalities identified are webs, diverticula, and stones. 67 Conventional liver MRI may show parenchymal areas of T2 signal hyperintensity and peripheral areas of increased enhancement 69 ; both may be caused by acute cholangitis or confluent hepatic fibrosis. Morphologic hepatic changes 70 and lymphadenopathy also may be seen. Cholangiocarcinoma occurs in 10% to 15% of patients with primary sclerosing cholangitis. 65 Features that suggest the diagnosis include high-grade ductal narrowing, long strictures, rapid progression of strictures, marked proximal dilatation distal to strictures, and polypoid lesions. 71 ERCP has superior spatial resolution and may, therefore, be more sensitive for detecting ductal wall irregularity, which is seen in the early stages of primary sclerosing cholangitis. 72 However, multiple studies have compared the diagnostic capabilities of each test and shown comparable diagnostic accuracy. 73 76 MRCP even may depict more strictures of the peripheral intrahepatic ducts. 77 Nevertheless, results thus far, using MR imaging to determine clinical severity and prognosis, have been disappointing. 78 Choledochal cysts are potential precursors of cholangiocarcinoma and, therefore, accurate diagnosis is imperative. 79 Although most are diagnosed in childhood, 20% manifest in adulthood. 19 MRCP has been shown to be equivalent to ERCP Figure 7. Klatskin tumor. (A) Oblique coronal, thick slab MRCP image shows an obstructing tumor (*) with intrahepatic left and right lobe biliary dilatation (arrows). (B) Contrast-enhanced late portal venous axial T1- weighted 3-dimensional spoiled gradient-echo fat-suppressed MR image shows an ill-defined enhancing mass at the liver hilum (white arrows). Dilated biliary ducts are present (black arrows).

972 SAHNI AND MORTELE CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 6, No. 9 Figure 8. Pancreatic adenocarcinoma. (A) Contrast-enhanced axial T1-weighted 3-dimensional spoiled gradient-echo fat-suppressed MR image shows a hypointense mass in the head of the pancreas (arrow). Oblique coronal, thick slab (B) MRCP image and (C) ERCP image show dilatation of the common duct (open arrow) and the pancreatic duct (solid white arrow) by a pancreatic adenocarcinoma (* in B). anomalous pancreatobiliary junction, can be diagnosed. Combining the examination with conventional MR can give further information regarding fluid collections, necrosis, ductal disruption, and ductal communication with pseudocysts. 6 IV secretin stimulation may be helpful for the latter 2 indications. Although good correlation has been shown between CT and MR in acute pancreatitis, 81 CT still has several advantages; CT is widely accessible and less costly than MRI, and is more sensitive in detecting small gas bubbles and calcifications. MRCP in chronic pancreatitis can be used to identify the ductal changes and evaluate residual exocrine function. MRCP findings include dilatation, stricturing, and irregularity of the main pancreatic duct, dilated side branches, and filling defects in the ductal system caused by stones or debris 82 (Figure 12). ERCP has been considered the most sensitive modality for evaluating the pancreatic duct and its side branches. 83 However, recent data have shown that MRCP correlates well with and may be superior to ERCP. 84 86 An area of current research interest is the radiologic diagnosis of early chronic pancreatitis before the presence of any morphologic changes. 87 Abnormalities in pancreatic exocrine function are thought to predate imaging findings in patients with early pancreatitis. At this stage the disease may be potentially reversible. 88 Secretin-enhanced MR cholangiography can determine pancreatic exocrine function with the degree of duodenal filling and improves the pancreatic duct and side-branch delineation. 15 Changes in pancreatic duct compliance also can be used as an indicator of early chronic pancreatitis 89 (Figure 13). Limitations and Pitfalls Several limitations and pitfalls are recognized in the performance and interpretation of MRCP. 90,91 Awareness of these is imperative to evaluate the investigation correctly. A complete review is beyond the scope of this article but several common sources of error are described later. The spatial resolution of MRCP compared with ERCP is inferior. This may limit the visualization of nondistended pancreatic ductal side branches or peripheral intrahepatic ducts. Early changes of conditions such as chronic pancreatitis or primary sclerosing cholangitis therefore may be missed. Small filling defects also may be obscured by reviewing only the maximum intensity projection and thick slab images. These are projectional techniques and are prone to partial volume effects. 10 Although the performance of MRCP in evaluating choledocholithiasis is excellent, 28,31 35 stones can be mimicked by several entities. These include air, tumor, and blood clots within the biliary tree. Susceptibility artifacts from surgical clips and

September 2008 MAGNETIC RESONANCE CHOLANGIOPANCREATOGRAPHY 973 coils and duodenal air can result in local signal loss. A signal void also can be seen in the central bile duct; this is an artifact related to flow and is recognizable by its characteristic central location. Finally, excessive contraction of the sphincter of Oddi may mimic an impacted stone. Vascular compression may cause artifactual narrowing of the biliary duct. The hepatic arteries and the gastroduodenal artery may be responsible for this. The most common site of pseudoobstruction is the common hepatic duct caused by a crossing right hepatic artery. 90 Examining a collapsed pancreatic duct in the fasting state also may mimic stenoses. Strategies to avoid misinterpretation include always reviewing the source thin-collimation images, obtaining coronal imaging from multiple angles, performing conventional abdominal MR concurrently, repeating the scan if sphincter spasm is suspected, and administering IV secretin to exclude any real stenoses of the pancreatic duct. Figure 10. Oblique coronal, thick slab MRCP image shows multiple short intrahepatic biliary strictures (arrows) alternating with areas of mild dilatation in keeping with primary sclerosing cholangitis. Future Advances and Applications Technological advances continue to improve the performance of MRCP and increase its applications for use. Current imaging methods produce thin-slice 2-dimensional images. Three-dimensional imaging is a recently developed method of image acquisition. 92 This method produces thinner slices that have been shown to have superior signal intensity and contrast than conventional 2-dimensional imaging, 93 with improved visibility of the pancreatic duct and biliary tree. 94 These images can be postprocessed to provide projectional views of the biliary system in any plane. Three-dimensional imaging thus far has been limited by long acquisition times. Breath-hold sequences, however, now can be used, which will promote the use of 3-dimensional MRCP into routine clinical care. The increased Figure 9. (A) Oblique coronal, thick slab MRCP image shows a cystic pleomorphic pancreatic head mass (arrow) connected to the main pancreatic duct. Findings are in keeping with a side-branch duct IPMN. (B) Single ERCP image shows contrast filling of the same lesion (arrow). Figure 11. Oblique coronal, thick slab MRCP image shows multiple intrahepatic and extrahepatic choledochal cysts (type IVA choledochal cysts).

974 SAHNI AND MORTELE CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 6, No. 9 Figure 12. Oblique coronal, thick slab MRCP image shows irregular main duct dilatation with side-branch ectasia (short white solid arrows) compatible with chronic pancreatitis. A stricture is noted in the midpancreatic duct (long white arrow). Also note smooth tapering of the intrapancreatic common bile duct (open arrow). use of high-field 3 Tesla MR systems also should improve examinations by increasing the signal-to-noise ratio. The use of MRCP in assessing pancreatic exocrine function has involved grading the duodenal filling volume after injection of intravenous secretin. This traditionally has been performed by a qualitative or semiquantitative method. 12 Recent reports, however, have quantified the pancreatic exocrine function 95,96 determined from secretin-enhanced MRCP. This has been correlated with noninvasive pancreatic exocrine function tests and clinical symptoms in patients with a variety of pancreatic disorders. 96 This technique shows great promise in noninvasively determining pancreatic exocrine function. There is current interest in the use of hepatobiliary contrast agents such as mangafodipir trisodium. These agents are hepatocyte-selective T1-weighted MR agents that are administered intravenously and excreted primarily through the biliary system. 97 T1-weighted imaging postcontrast usually is performed in conjunction with conventional MRCP acquisitions. The technique has been used successfully to identify bile duct leaks postsurgery, 97,98 document biliary anatomy in right-lobe living donors, 99 and to diagnose functional biliary disorders. 100 Despite the advances in MRCP, one limitation is the assessment of segmental nondilated biliary ducts owing to the spatial Figure 13. Oblique coronal, thick slab MRCP images (A) before, (B) 5 minutes after, and (C) 10 minutes after intravenous injection of secretin. There is impaired main duct compliance with reduced and delayed dilatation after the secretin injection. Progressive side branch dilatation (arrows) also is noted. These findings are all in keeping with chronic pancreatitis.

September 2008 MAGNETIC RESONANCE CHOLANGIOPANCREATOGRAPHY 975 resolution of the technique. Secretin-augmented MRCP has been shown to improve visualization of the pancreatic duct. 12 Other drugs such as morphine 101 and fentanyl, 102 however, can be used to improve visualization of the biliary system. These drugs cause sphincter of Oddi contraction, resulting in upstream dilatation. Further research in this area would be of use for evaluating donor biliary anatomy before liver transplant, 103 determining resectability for certain tumors, and diagnosing early changes of ductal disease. Conclusions MRCP is a useful tool in the diagnosis of biliary and pancreatic pathology. Its diagnostic ability has improved significantly since its introduction. As a consequence, ERCP is now reserved in many centers for intervention or when MRCP fails to establish the diagnosis. 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Preoperative liver donor evaluation: imaging and pitfalls. Liver Transpl 2003;9:S6 S14. Address requests for reprints to: Koenraad J. Mortele, MD, Department of Radiology, Brigham and Women s Hospital, Harvard Medical School, 75 Francis Street, Boston, Massachusetts 02115. e-mail: kmortele@partners.org; fax: (617) 732-6317. The research contributing to this article was supported by ChiRho- Clin, Inc. (ChiRhoStim) (K.J.M.).