Magnetic resonance imaging of the pancreas and biliary tree

Magnetic Resonance Imaging of the Pancreas and Biliary Tree Joseph F. Mammone, Evan S. Siegelman, and Eric K. Outwater MRI of the pancreas and bile ducts is becoming more widely used due to recent advances in surface coils, breath-hold imaging techniques, and magnetic resonance cholangiopancreatography (MRCP). MRI provides a comprehensive and accurate examination for the detection, staging, and characterization of a variety of developmental, inflammatory, and neoplastic processes that involve the pancreas.

Copyright© 1998by W.B. Saunders Company

HE PANCREAS AND bile ducts have been among the more difficult organs to image by MRI. This has been attributed to motion artifacts from respiration and cardiac pulsations, bowel peristalsis, and chemical shift artifact. 14 Fortunately, newer imaging techniques, 6 such as breathhold imaging, fat saturation, and dynamic contrastenhanced imaging, have enabled the performance of diagnostic MRI examinations of the pancreas and bile ducts.

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IMAGING CONSIDERATIONS Pancreas

The pancreas is best imaged at high field strength, which allows for faster imaging, higher signal to noise, and increased separation of water and fat frequencies, a Surface coils are also used to improve the signal to noise ratio (SNR).7 The increased SNR obtained with phased array surface coils allows one to use a smaller field of view and thinner slices to detect and characterize small foci of pancreatic pathology. Tl-weighted imaging of the pancreas is a useful imaging sequence because of its high lesion to parenchyma contrast. 5 The physical basis for the observed tissue contrast may be explained by the relative relaxation of the pancreas compared with other structures in the abdomen) The pancreas has the shortest T1 of the abdominal organs and is slightly shorter than normal liver. Therefore, on Tl-weighted pulse sequences, signal intensity in the pancreas should equal or slightly exceed the intensity of normal liver (Fig 1). Any type of insult to the pancreas (except for subacute hemorrhage and fatty replacement) lowers the signal intensity of the organ on Tl-weighted images. T 1-weighted imaging of the pancreas and the abdomen in general can be performed with an in-phase breath-hold multisection fast (eg, FLASH, FMPSPGR) gradient echo (GRE) sequence (T1GRE). This sequence provides Tl-weighted images that are free of respiratory artifacts and are of sufficient temporal resolution for dynamic contrast-

enhanced studies. 2 Typical imaging parameters for the T1-GRE sequence at 1.5T are a TR > 100 ms, flip angle of 90, TE = 4.2 ms, and an image matrix size of 128 × 256. This sequence is preferred to a conventional spin echo (CSE) sequence primarily because of speed. Mitchell et al5 reported better image quality for the T1-CSE versus the T1-GRE. However, this finding is partly attributable to the fact that the T1-GRE sequence used in the study was opposed-phase. The pancreas is interspersed with fat and contains many fat-parenchyma borders that produce an etching artifact on opposed phase images. This artifact is less serious in larger organs such as the liver, kidney, and spleen. Although Tl-weighted imaging is important, the images are dominated by high fat signal that can create motion artifacts and reduces the dynamic range of nonfatty tissues. By using fat suppression, excellent images of the pancreas can be obtained. 9 A radiofrequency selective fat suppression pulse followed by spoiling provides images of the pancreas with increased dynamic range, tissue contrast, and reduced artifact from fat (Fig 2). Fat suppressed Tl-weighted sequences are excellent for depicting normal pancreatic borders? removing ghosting artifacts, and improving contrast to noise ratios. 3 With fat saturation, chemical shift artifacts are eliminated. One could alternatively perform a breath-hold fat-suppressed T1-GRE sequence using an opposed phase technique. 9 Also by minimizing TE, there is increased T1 weighting, increased

From the Department of Diagnostic Radiology and Nuclear Medicine, UMDNJ, Robert Wood Johnson Medical School, Cooper Hospital-University Medical Center, Camden, NJ, Department of Radiology, Hospital of the University of Pennsylvania, Philadelphia, and Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, PA. Address reprint requests to Joseph F. Mammone, MD, PhD, Department of Diagnostic Radiology and Nuclear Medicine, UMDNJ, Robert Wood Johnson Medical School, Cooper Hospital-University Medical Center, Camden, NJ 08103. Copyright © 1998 by W.B. Saunders Company 0887-2171/98/1901-000458. 00/0

Seminars in Ultrasound, CT, andMRI, Vo119, No I (February), 1998: pp 35-52

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Fig 1, Normal pancreas. (A) Breath-hold axial T1-GRE (TR = 118 msec, TE = 2.1 msec) images of the pancreas shows the normal contrast relationships between the pancreas, liver and spleen, with the pancreas being isointense to slightly hyperintense compared with normal liver. Because of the very short TE used, an opposed-phase effect is observed. (B) Breath-hold axial T1-GRE (TR = 118 msec, TE = 2.1 msec) image of the pancreas in the arterial phase after dynamic infusion of intravenous contrast. The normal pancreas exhibits marked enhancement in the arterial phase. Note the lack of contrast in the hepatic veins, renal cortical-medullary differention, and early heterogeneous enhancement of the spleen.

SNR, and an increased number of slices obtained with each TR. Conventional spin echo T2-weighted images of the pancreas suffer from motion artifact, poor lesion to parenchyma contrast, and longer scan times.4 T2-weighted hybrid rapid acquisition relaxation enhancement (RARE or turbo spin echo [TSE] or fast spin echo [FSE]) techniques offer the advantages of reduced scan time, better depiction of tissue planes, and increased signal to noise. 1° In an initial evaluation of RARE techniques, image degradation by motion was a frequent problem, 5 but this problem can be improved by gradient moment nulling. One disadvantage of gradient moment nulling is increased intravascular signal and associated ghosting artifact. Therefore, when gradient moment nulling is used, saturation bands should be placed superior and inferior to the volume to be imaged to eliminate rephased signal in the aorta and inferior vena cava. Fat suppression will also reduce motion artifact and improve softtissue contrast. Other motion compensation techniques include respiratory gating, u and the use of

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breath-hold T2-weighted sequences such as half Fourier single-shot turbo spin echo (HASTE). 12 T2-weighted images are particularly important when imaging islet cell tumors, the pancreatic duct, and bile ducts. T h e pancreas is a very vascular organ and enhances intensely during the arterial phase of a dynamic bolus of intravenous gadolinium chelates.1 Contrast enhancement is typically performed during breath-hold Tl-weighted GRE imaging. Accurate timing of the injection is necessary to image at peak enhancement (Figs 1 and 2). The pancreas does not contain abundant extracellular water, so there will be washout of the chelate after the arterial phase (in contrast to pancreatic carcinoma, which gradually accumulates the chelate). Although gadolinium chelates are passive agents that diffuse throughout the extracellular water, similar to iodinated contrast agents used in CT, a manganese chelate (Mn-DPDP) has been demonstrated to show uptake by the pancreas. 13 MnDPDP was originally designed for imaging in liver disease, where it is taken up by normal hepatocytes. Mn-DPDP use has been suggested to improve

Fig 2. Normal pancreas. (A) Breath-hold axial fat-suppressed T1-GRE (TR = 203 msec, TE = 4 msec) image of the pancreas. The normal pancreas exhibits high signal intensity on this sequence. (B) Breath-hold axial fat suppressed T1-GRE (TR = 203 msec, TE = 4 msec) image in the arterial phase after dynamic infusion of contrast.

MRI OF THE PANCREAS AND BILIARY TREE

detection of pancreatic adenocarcinoma in MR imaging. ~3 A variety of oral agents are available that provide contrast between the duodenum and the pancreas. These include "negative" contrast agents such as fluorocarbons, 14,15 superparamagnetic iron oxide particles, 16A7 barium sulfate, 18,19 and "biphasic" agents such as clays. 2°,21 Water, which is well tolerated and adds no cost to the imaging examination, has also been described as a useful oral contrast agent. 22 Negative agents on Tl-weighted images provide good distinction between the duodenum and pancreas. Negative agents on T2-weighted images eliminate motion artifact from the stomach and duodenum. We prefer to use water before T1-GRE imaging and dynamic contrast imaging after T2-weighted imaging.

Biliary Imaging MRI of the biliary tree has become widely utilized due to advances in imaging technology. There is now a rather large body of literature indicating that magnetic resonance cholangiopancreatography (MRCP) can show ductal pathology noninvasively and with increasing accuracy?3-25As with the pancreas, biliary imaging is best performed at high field strength and with a dedicated phased array torso coil. Fasting before the examination is also helpful to fill the gallbladder and to allow the stomach to empty. MRCP imaging of the biliary tree depends on the long T2 relaxation time of static fluid. When images are heavily T2-weighted, biliary and pancreatic fluid exhibits relatively high signal intensity, whereas the signal of the adjacent tissues is low because of their comparatively short T2. A number of strategies have been used to exploit this difference in transverse relaxation. Wallner et al26 initially described a two-dimensional T2-weighted gradient recalled echo sequence called contrastenhanced Fourier acquired steady-state technique (CE-FAST). The images were post-processed via maximum intensity projections (MIP), which created a cholangiogram that could be viewed from multiple angles. Although the images were limited and the biliary tree was not shown in all patients, the diagnostic potential of the technique was identified. 26,27 GRE sequences (such as the CE-FAST) seem attractive because of the short acquisition

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time, short TRs, and reasonable tissue contrast. However, the technique is motion-sensitive and the breath-hold periods are rather long. Transmitted cardiac pulsations are a particular problem in the left lobe of the liver. Intra-abdominal fat has a relatively high signal intensity, which decreases contrast between the extrahepatic ducts and adjacent tissue. The signal-to-noise ratio is relatively low, the slices are thick, and relatively small acquisition matrices, are used. This makes imaging of smaller diameter ducts problematic. Wallner et a126 failed to demonstrate the (nondilated) biliary tree in three of five healthy volunteers. Imaging of biliary strictures in which the diameter is reduced even further is also compromisedY Two-dimensional nonbreath-hold hybrid RARE or fast spin echo (FSE) sequences depict the biliary tree in both obstructed systems and normal patients, and was introduced to overcome the limitations of the GRE sequences, z9 The technique has a higher SNR and is less sensitive to susceptibility artifacts than GRE techniques. The higher SNR permits thin sections to be used to acquire an appropriate data set for three-dimensional (3D) reconstructions. The effective TE is typically greater than 180 msec so that the surrounding soft tissue (eg, liver) will have little signal. Long echo train lengths (16 or 32) are used to reduce the scan time. Fat signal that is relatively high on FSE sequences is suppressed via radiofrequency selective fat excitation. This also reduces ghosting artifact from fat. Because of these advantages, fast spin echo quickly became the technique of choice for MRCE 3°-33In a prospective comparison of a heavily T2-weighted FSE and a 3D CE-FAST sequence, the extrahepatic bile ducts were observed in 96% of patients with fast spin echo and only 44% of patients on CEFAST. 34 There was also better visualization of the intrahepatic and pancreatic ducts. The fast spin echo technique has been modified to obtain even thinner slices by using a 3D acquisition. 35,36Consistent demonstration of the extrahepatic ducts in nondilated systems is reported with variable demonstration of intrahepatic ducts, but scan times can be long and range from 5 to 13 minutes. HASTE is a more recent innovation that is a modification of FSE to acquire all data for an image by sampling just over half of K-space in a single echo train. Whereas FSE uses multiple excitation

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pulses to complete the slice data set, HASTE uses a single excitation pulse and half-Fourier acquisition. Breath-hold HASTE MRCP has been described in both a single slice (Fig 3) 37,38 and multislice acquisition. 37 In a comparison between the two approaches, breath-hold single shot MRCP was favored because of the absence of misregistration and speed of image acquisition. 39 There are some limitations of the MRCP tech-

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nique. One problem is that the biliary tree is not selectively depicted. Any fluid that has a long T2 relaxation time will exhibit high signal intensity. For example, bowel contents, ascites or any large strategically located fluid collection in the abdomen can have high signal and obscure the bile ducts on MIP images. A potential solution to this problem is the use of a negative contrast agent to eliminate the signal in the adjacent gastrointestinal tract. 4° A second limitation is that anything within the ductal system that shortens the T2 relaxation time of the bile (eg, blood, protein, air, debris) can lead to nonvisualization of the duct or simulate a filling defect such as a stone. Third, if a filling defect such as a calculus is entirely surrounded by fluid, it may be obscured on the MIP reconstruction images (Fig 4). It is important, therefore, to view the source images from the original data set for complete interpretation. Fourth, magnetic susceptibility artifact from adjacent surgical clips may obscure or simulate disease. Such artifacts are minimized with the use of a FSE type sequence as opposed to a conventional T2-weighted or GRE sequence.41 Lastly, resolution is not nearly that of endoscopic retrograde cholangiopancreatography (ERCP), so move subtle abnormalities of the ducts may be undetected by MRCP. In clinical practice, MRCP is a fast, noninvasive method that is capable of depicting the biliary tree and causes of biliary duct obstruction with a high degree of accuracy. It offers diagnostic value for some applications approaching that of ERCP and without its associated risks .42 PANCREATIC NEOPLASMS DuctaI Adenocarcinoma

The most common neoplasm of the pancreas is ductal adenocarcinoma, which represents 75% to Fig 3. Ampullary carcinoma in an 84-year-old man. (A) Coronal single shot fat-suppressed heavily T2-weighted image obtained in a single breath-hold (TR = 17,000 msec, TE = 187 msec, 11 consecutive 4-mm slices obtained in 17 seconds) shows a double duct sign and intrahepatic ductal dilatation suggestive of distal common bile duct obstruction. (B) Contrast-enhanced coronal fat-suppressed T1-GRE (TR = 68 msec, TE = 1.7 msec, flip angle = 60 °) image shows a dilated distal common bile duct and pancreatic duct. The ducts have low signal intensity ("black bile cholangiography"). There is a hypovascular mass whose epicenter is in the ampulla (arrow). {C) Contrast-enhanced axial fat-suppressed T1-GRE (TR = 150 msec, TR = 1.7 msec) image shows the ampullary mass extending into the duodenal lumen (white arrowhead). A moderately differentiated adenocarcinoma of the ampulla was subsequently removed.

MRI OF THE PANCREAS AND BILIARY TREE

Fig 4. Single shot breath-hold fast spin-echo MRCP (TR = infinity, TE = 530 msec) demonstrating choledocholithiasis. (A) In this coronal MIP image, a common bile duct stone is poorly depicted. (B) in this single coronal slice from the original dataset, a common bile duct stone (white arrow) is now observed which does not project well in the MIP image because it is surrounded by fluid. This emphasizes the need for a systematic review of the original source images.

92% of primary malignancies of the pancreas. 43 Ductal adenocarcinoma of the pancreas is the fifth leading cause of deaths from cancer and represents 5% of all cancer-related deaths. 44 It has an extremely poor prognosis with a 5-year survival of less than 5%. 45 The primary goal of imaging is sensitive detection of smaller lesions and accurate preoperative staging, so that optimal treatment can be defined for

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each patient. In routine clinical applications, CT has been the primary imaging modality in detecting and staging pancreatic adenocarcinoma. CT and MRI were found to be of similar accuracy with older MR sequence protocols that did not include fat suppression or dynamic breath-holding techniques. 46 With the new techniques, MRI has been shown to be superior in both detection and in defining local tumor extension. 47,48Dynamic gadolinium-enhanced MR imaging has a reported sensitivity of 90% in the detection of tumor.48 On Tl-weighted fat-suppressed images, pancreatic adenocarcinoma appears as a relatively low signal intensity mass within the high signal intensity of the pancreatic parenchyma. There can be secondary atrophy of the pancreas distal to the tumor (ie, in the body and tail) which also produces abnormally low signal intensity. Sometimes T1weighted images alone are sufficient to determine that a pancreatic adenocarcinoma is unresectable (Fig 5). Pancreatic adenocarcinoma is relatively hypovascular with respect to the normal pancreas, but does contain increased extracellular water. Tumor tissue, therefore, exhibits relatively low signal intensity with respect to normal pancreas during the arterial phase of dynamic contrast enhancement, but the tumor can gradually become isointense as contrast diffuses into the mass over time (Fig 6). The increased parenchyma-to-lesion contrast during the arterial phase has been shown to facilitate the detection and characterization of small pancreatic cancers which do not alter the contour of the gland. 47 Small ampullary carcinomas can also be diagnosed by MR149 and are well-depicted in the coronal plane (Fig 3). Criteria which make pancreatic carcinoma unresectable at most centers include extrapancreatic extension, hepatic metastases, involvement of the superior mesenteric vein-portal vein confluence, and encasement/thrombosis of the celiac axis or superior mesenteric artery. Routine Tl-weighted images are excellent for depicting the borders of the low signal intensity extraparenchymal tumor against the high signal intensity of retroperitoneal fat. This may establish a diagnosis of vascular encasement (Fig 5). MRI is also capable of detecting metastatic disease to the liver.5°,51 Two dimensional time-of-flight (gradient recalled echo with flow compensation) techniques provide excellent depiction of flowing blood and regional vascular

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of pancreatic adenocarcinoma. MRI is used first in place of CT in the setting of an iodinated contrast allergy or renal insufficiency. MRI is also helpful if CT is equivocal or if there is a strong clinical suspicion of disease and CT is negative. 52 MRI can characterize suspected parenchymal abnormalities, such as focal fatty infiltration, which are found on CT. An example of such a pancreatic "pseudolesion" is depicted in Fig 7. In patients who are candidates for surgical resection, MRI may be of value to avoid "understaging" on the basis of CT examination.

Islet Cell Tumors

Fig 5. Unresectable pancreatic adenocarcinoma in a 45year-old woman. (A) Four consecutive axial Tl-weighted spin-echo {TR -- 450 msec, TE = 10 msec) images show an infiltrative mass in the pancreatic head and neck that encases both the superior mesenteric artery and portions of the celiac axis. (B) Fat-suppressed axial Tl-weighted image (TR = 450 msec, TE = 10 msec) at the same level as the highest slice in (A) demonstrates low signal intensity surrounding the celiac axis. On the basis of this image alone, it is not clear whether the low signal intensity represents suppressed fat or tumor, Because of this, T1-weighted imaging without fat saturation should also be performed in the evaluation of pancreatic cancer.

anatomy. This permits the diagnosis of vessel encasement or occlusion. Often, however, the T1weighted images and contrast-enhanced T1-GRE images are sufficient for demonstrating vascular involvement by tumor. At present, contrast-enhanced CT is the imaging modality most widely used for the initial evaluation

Islet cell tumors are less common than pancreatic adenocarcinoma and have an approximate annual incidence of 1/270,000. 55 The lesions can occur anywhere in the pancreas and can be single or multiple, and benign or malignant. The two most common islet cell neoplasms are insulinomas and gastrinomas. Hormonally hyperfunctioning lesions can be very small in symptomatic patients. Nonfunctioning islet cell tumors are the third most common type. When non-hyperfunctioning, islet cell tumors may go undetected until they present late with symptoms of localized mass effect or metastatic disease. Larger lesions are associated with calcification and malignant behavior, which includes local invasion, vascular involvement, and metastatic disease. 56 The T1 and T2 relaxation times of islet cell tumors are long relative to the normal pancreas. 22,56 This difference allows for good lesion-to-parenchyma tissue contrast, which is especially important in detecting small tumors. The longer relaxation time causes these tumors to exhibit high signal intensity relative to pancreas on T2-weighted images (Fig 8). These tumors are usually hypervascular and are well-depicted following dynamic imaging during the arterial phase of a contrastenhanced scan. ~7,58 Hepatic metastases are readily detected and characterized by MRI. In a study of 10 patients with 11 islet cell tumors, MR imaging depicted all 11 lesions, whereas CT depicted 7 of 11.57 The lesions not observed on CT were typically smaller in size.

Cystic Neoplasms Cystic neoplasms of the pancreas are uncommon tumors and are classified into two groups: serous

MRI OF THE PANCREAS AND BILIARY TREE

microcystic adenoma and mucinous cystic neoplasms. The former are almost always benign, but the latter are considered low grade malignancies. Microcystic adenomas most frequently occur in middle-aged and elderly women (average age, 62). 59 They are comprised of numerous small cysts ranging from 1 to 20 mm in diameter. The entire mass typically ranges in size from 4 to 25 cm. 59 Patients with von Hippel-Lindau syndrome have an increased incidence of both pancreatic cysts and microcystic adenomas 6° (Fig 9). On MR imaging

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the lesion exhibits very high signal intensity on T2-weighted images because of its cystic composition. The lesion may also contain a central low signal scar. Its lobulated morphology and septae are identified on T2-weighted images. 6a Spontaneous hemorrhage within the cysts may also be identified via MRI. 6z Mucinous cystic neoplasms also exhibit a female predominance but present at a somewhat younger age (mean age, 50) than microcystic adenomas. 59 They contain larger unilocular or multilocular cysts. The cyst contents are typically thick mucin. The cyst walls may be shaggy or thick and can exhibit papillary projections. 61,63 The mucinous contents show very high signal intensity on T2weighted images, mimicking simple fluid.64,65 The Tl-weighted signal varies depending on the protein content of the cyst (Fig 10). Mucinous cystic neoplasms may be difficult to characterize as benign or malignant based on histological criteria, and they are best considered low grade malignancies. It may be the radiologist, and not the pathologist, who establishes a diagnosis of malignancy by demonstrating metastatic disease.

Other Neoplasms of Ductal Epithelium Solid and papillary epithelial neoplasm is a rare tumor with low malignant potential typically observed in young women. The lesion is a large, well-encapsulated mass that exhibits varying de-

c

Fig 6. Adenocarcinoma of the pancreas. (A) Breath-hold axial in-phase T1-GRE (TR = 150 msec, TE = 4 msec) image at the level of the pancreatic head before the administration of contrast demonstrates a low signal intensity mass replacing part of the pancreas (solid arrow), Some residual normal pancreatic parenchyma remains (open arrows). (B) Breathhold axial in-phase T1-GRE image (TR = 150 msec, TE = 4 msec) during the arterial phase after administration of contrast demonstrates marked enhancement of the normal pancreatic tissue and minimal enhancement of the relatively hypovascular tumor, providing increased pancreas-to-tumor contrast. A stent within the bile duct (black dot) is noted to be surrounded by tumor. Note the presence of contrast in the superior mesenteric artery (arrowhead) which is surrounded by normal fat. The superior mesenteric vein (curved arrow) is unenhanced during the arterial phase. (C) Delayed breath-hold axial in-phase T1-GRE image (TR = 150 msec, TE = 4 msec) demonstrates heterogeneous enhancement of the tumor as contrast has now had time to diffuse into the lesion. Contrast now opacities the inferior vena cava, hepatic veins, superior mesenteric vein, and medullary spaces of the kidneys.

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Fig 7. Pseudomass of the pancreatic head due to focal fatty replacement. The patient was referred for MRI because a suspicious hypoattenuating mass was observed on CT but a CT-guided biopsy yielded normal tissue, (A) Axial T1 spin echo (TR = 500 msec, TE = 12 msec) image demonstrates a focal area of heterogeneously increased signal (arrow) in the pancreatic head. A focal neoplasm of higher signal intensity than the surrounding pancreas would be distinctly unusual. The increased signal may be attributable to focal fatty replacement. (B) Axial breath-hold fat suppressed in-phase T1-GRE (TR = 203 msec, TE = 4 msec) image demonstrates loss of signal within the "mass" proving its lipid content, (C) Axial breath-hold opposed-phase T1-GRE (TR = 161 msec, TE = 6,8 msec) image demonstrates a marked decrease in signal in the fatty area compared with the T1 spin echo (which by definition is an in-phase image). This difference is due to the opposed-phase effect of the coexistent fat and water protons. (D) Axial breath-hold fat-suppressed contrast-enhanced in-phase T1-GRE (TR = 203 msec, TE = 4 msec) image shows enhancement of both fatty pancreatic tissue and the surrounding uncinate process. Focal fatty infiltration and focal fatty sparing have been described in both the CT and ultrasound literature,s3,s4Chemical shift imaging and fat suppression are capable of detecting and characterizing such pseudolesions.

grees of cystic and hemorrhagic degeneration (Fig 11). MRI demonstrates a well-circumscribed pancreatic mass of heterogeneous signal intensity. Characteristic fluid-debris levels and the identification of blood products may be helpful in diagnosing this tumor. 66,67

Mucinous ductal ectasia is a rare tumor manifesting as cystic dilatation of a side branches of the main pancreatic duct. 6s There is no sex predilection as compared with the cystic neoplasms of the pancreas. These tumors may affect the main pancreatic duct, producing ductal dilatation. Side branches dilatation may produce an appearance of multilocular cysts (Fig 12). MRI has been reported to be superior to CT in providing better definition of the cyst borders and tumor extent on T2-weighted images, 69 and particularly on MRCP images.

NON-NEOPLASTIC PANCREATIC ABNORMALITIES

Pancreatitis

Acute pancreatitis is typically a clinical diagnosis. CT has been the primary modality in confirming the diagnosis and predicting or detecting potential complications that could alter patient management. In uncomplicated acute pancreatitis, the signal intensity of pancreas may be normal on MRI, but the pancreas may exhibit morphological changes of either focal or diffuse enlargement. On Tl-weighted images, low signal intensity peripancreatic stranding may be seen within the retroperitoneal fat. 7° T2-weighted fat-suppressed images show the extent of peripancreatic edema and acute fluid collections.

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tissue does not enhance. Pancreatic pseudocysts are delineated as homogeneous, unilocular, high signal intensity lesions on T2-weighted images. They typically communicate with the pancreatic duct. Splenic or portal vein thrombosis may be identified on two-dimensional time-of-flight pulse sequences or on contrast-enhanced T1-GRE images. Chronic pancreatitis is characterized by irreversible destruction of pancreatic tissue, which is replaced by dense fibrosis as well as ductal abnormalities (strictures, dilatations, and calculi). The signal intensity of the pancreas on MRI is decreased on Tl-weighted images 4 due to replacement of parenchyma. There is also decreased enhancement on dynamic infusion of contrast, because of the parenchymal fibrosis and concomitant diminished vascularity. 7° Dilatation of the pancreatic ducts, strictures, and calculi are best identified on T2-weighted and MRCP images. The MRI appearance of inflanmaatory strictures of the common bile duct and/or pancreatic duct in chronic

Fig 8. Pancreatic islet cell tumors (insulinomas) in a 31-yearold woman with a history of multiple endocrine neoplasia Type 1. (A) Axial fat suppressed T2-weighted FSE (TR = 4,000 msec, TE = 90 msec) image demonstrates two masses of the superior pancreatic body and tail that are of heterogeneous high signal intensity compared to liver. (B) Image obtained at a lower level shows additional subcentimeter lesions (arrows) that were confirmed at surgery with intraoperative ultrasound. (C) Axial fatsuppressed breeth-hold T1-GRE (TR = 150 msec, TE = 2.6 msec) image obtained at the same level as in (A) shows the heterogeneous marked enhancement of the two dominant masses, which is characteristic of islet cell neoplasms.

Pancreatic necrosis is a complication of acute pancreatitis that is depicted with contrast-enhanced MRI. Viable pancreas enhances normally during the arterial phase, whereas necrotic pancreatic

Fig 9. Microcystic adenoma in a 53-year-old woman with family members with von Hippel Lindau syndrome. (A and B) Two axial FSE T2-weighted (TR = 4,200 msec, TE = 120 msec) images demonstrate near-complete replacement of the pancreas by multiple cysts that measure between 5 and 15 mm, Low signal central foci present in the superior aspect of the neoplasm represent the fibrous/calcific scars that are characteristic of this benign neoplasm (open arrowheads).

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pancreatitis may be difficult to distinguish from cancer in some cases.

Metabolic Disorders Hemochromatosis is an autosomal recessive disorder in which there is excess iron absorption from

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the gastrointestinal tract. This results in iron overload in the liver, heart, and pancreas, the latter of which can cause islet cell dysfunction and diabetes. MRI demonstrates the presence of parenchymal iron on both T2-weighted and GRE pulse sequences. 71 GRE images are more sensitive and show a progressive loss of pancreatic signal with increasing TE ,due to T2* effects. The optimum TE should be in the range of 11 to 15 ms. 72 Genetic hemochromatosis can be distinguished on MRI from secondary iron overload due to chronic anemias or multiple transfusions. In secondary iron overload, iron uptake by the reticuloendothelial system results in decreased signal in the liver, spleen, and bone marrow. The pancreas in these instances is of normal signal intensity. Examples of this condition are illustrated in the liver article by Siegelman in this issue. Cystic fibrosis is an autosomal recessive disorder and is a cause of exocrine pancreatic insufficiency. Several patterns of fibrofatty infiltration on MRI have been described. 73,74 These patterns include a lobulated, enlarged pancreas with complete fat replacement, a small atrophic pancreas with partial replacement by fat, and diffuse atrophy.73

Pancreatic Transplants Pancreatic transplants are being offered more frequently for patients with Type I diabetes mellitus. Routine T1- and T2-weighted images provide excellent morphological detail of the pancreas, but do not correlate with function. 75 However, dynamic contrast enhanced GRE images of the pancreas have been suggested as a reliable indicator of early pancreatic transplant dysfunction. In cases of pancreas transplant dysfunction, a significant decrease in parenchymal enhancement was measured during the first minute after contrast injection, as compared with normally functioning allografts. 76 Dynamic contrast enhancement is also helpful in the evaluation of possible pancreatic transplant artery stenosis or thrombosis (Fig 13).

Fig 10. A 29-year-old pregnant woman with mucinous cystic neoplasm of the pancreas. (A) Axial spin-echo T1weighted (TR = 500 msec, TE = 11 msec) and (B), axial fatsuppressed FSE (TR = 6,920 msec, TE = 144 msec) images demonstrate a focal mass (arrow) at the body-tail junction of the pancreas which exhibits low signal intensity on the Tl-weighted image and very high signal intensity on FSE, consistent with mucin within the multiple cysts in the mass. Linear high signal intensity tracks around the tail of the pancreas from pancreatitis. (C) The gross specimen demonstrates the multilocular cystic nature of the lesion.

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Fig 11. Solid and papillary epithelial neoplasm of the pancreas in a 25-year-old Asian woman. (A) Axial Tl-weighted fat suppressed Spin-echo (TR = 600 msec, TE = 10 msec) image obtained through the superior portion of the mass shows that the portions of the normal pancreatic head (white arrowheads) are splayed around a low to intermediate signal intensity mass. (B) Corresponding axial fat-suppressed T2-weighted FSE (TR = 3,600 msec, TE = 85 msec) image shows a heterogenous mass with small foci of very high signal intensity, suggesting cystic change. (C) and (D) Coronal T1-GRE images (TR = 125 msec, TE = 2.9 msec, flip angle = 60°) obtained before (C) and during the arterial phase of contrast infusion (D) reveals the cranial-caudal extent of the mass, the well-defined margin s and the small foci of non-enhancement representing small cysts. The uninvolved pancreatic head and uncinate process enhance intensely after contrast. (E) Gross specimen shows both the solid and cystic portions of the tumor. A large encapsulated pancreatic neoplasm in a young woman Should always suggest a diagnosis of solid and papillary epithelial neoplasm.

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Fig 13. MR arteriogram in a 25-year-old woman 4 days after a pancreatic transplant. The MR was requested to evaluate a vascular etiology for patient's pancreatic dysfunction. Coronal oblique MiP (TR = 5.2 msec, TE = 1.1 msec, flip angle = 60*) image demonstrates patent arterial branches to both the pancreatic body and head (arrows). Note early filling of a patent splenic vein.

STONE DETECTION

Fig 12. Ductectatic mucinouS tumor (side branch type) in a 55-year-old man. (A) Axial T1-GRE (TR = 110 msec, TE = 4.2 msec) and (B) axial T2-weighted single shot FSE (TR = infinity, TE = 93 msec) images demonstrate a multicystic mass in the uncinate process (arrow). (C) Coronal MRCP image shows the musticystic mass contiguous with a slightly dilated main pancreatic duct (arrow). The dilated duct results from tumor growth into the main duct and distinguishes this tumor from a mucinous cystic tumor.

Although the specificity of ultrasound in the detection of common bile duct stones is high, its sensitivit3/ is variable. MRCP can visualize the extrahepatic bile ducts throughout their entire length. The reported sensitivity and specificity for the detection of choledocholithiasis are 81% to 95% and 85% to 98%, respectively.31,33The MIP images display intraductal fluid as high signal intensity, which superficially resembles an ERCP. Biliary calculi appear as low signal intensity filling defects regardless of stone composition, due to a lack of mobile protons. A characteristic meniscus sign may be present. Final interpretation requires evaluation of the Source images, because MIP reconstructions may obscure intraluminal filling defects33 (Fig 4). MRCP may be of benefit in the evaluation of eholedocholithiasis when ultrasound fails to detect any stones and there is high clinical suspicion for choledocolithiasis. 3°,31 The goal is to obviate a diagnostic ERCP, and limit this procedure to patents with stones who may benefit from intervention. MRCP is also helpful after unsuccessful or incomplete ERCP. 77 MRCP can also help in the detection of multiple calculi. For example, a stone

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wedged in the papilla may prevent retrograde passage of contrast into the ductal system on ERCP. BILIARY STRICTURES

More than 80% of all benign strictures are iatrogenic and are typically due to inadvertent trauma during cholecystectomy,v8 Although most present during the immediate postoperative period, some patients present after several years. Other causes of benign biliary strictures include blunt abdominal trauma, chronic pancreatitis, sclerosing cholangitis (Fig 14), and inflammatory ampullary stenosis. Ampuilary stenosis is most commonly encountered as a complication of stone passage. Biliary strictures may also be seen as a complication of liver transplantation. Malignant biliary strictures may be caused by pancreatic adenocarcinoma, cholangiocarcinoma (Fig 15), ampullary carcinoma (Fig 3), and gallbladder carcinoma. The bile ducts can also be extrinsically compressed by adjacent lymphadenopathy or metastases. In the evaluation of malignant disease, MRCP can accurately detect the site and degree of obstruction. Usually a comprehensive abdominal MR examination is necessary, however, to adequately characterize the cause of a stricture. The appearance of benign strictures on MRCP is that of a more tapered or funnel-like narrowed segment. No intrinsic or extrinsic mass is discernible. In malignant strictures, there is typically an abrupt interruption of tile dilated duct. There may

Fig 14. Sclerosing cholangitis. Coronal MIP MRCP (TR = 12,000 msec, TE = 259 msec) image demonstrating segmental areas of alternating stricture (eg, open arrowheads) and dilatation within the intrahepatic bile ducts.

Fig 15.

Klatskin tumor. Coronal MIP MRCP (TR = 5,500

msec, TE = 252 msec) image demonstrates marked dilatation of the intrahepatic bile ducts w i t h abrupt termination in the region of the porta hepatis secondary to a Klatskin tumor (arrow).

be associated asymmetry or irregularity of the strictured segment. The presence of the "double duct sign" of a dilated pancreatic and common bile duct is also suggestive of malignancy (Figs 3 and 16). Neoplasm may also present as a filling defect in the biliary system. MRCP depicts the common bile duct in its

Fig 16. Pancreatic adenocarcinoma. Coronal MIP MRCP (TR = 9,630 msec, TE = 259 msec) image demonstrates the "double duct sign" of a dilated pancreatic duct (arrowhead) and dilated common bile (open arrowhead) and intrahepatic bile ducts. Non-cholangiographic MR images are necessary to

appropriately stage the tumor to assess for resectability.

MAMMONE, SIEGELMAN, AND OUTWATER

48

physiological state. Therefore, the ampullary segment is not depicted directly by MRCP and its location must be inferred. For this reason, dilatation of the common bile duct to the level of the ampulla may represent either calculus impacted in the ampulla, ampullary rumor, benign stricture, or sphincter of Oddi dysfunction. These entities are difficult to distinguish by MRCE PANCREATOGRAPHY

MRCP has been shown to be a valuable modality for depiction of the normal pancreatic ductal system as well as its congenital and acquired abnormalities.79~The normal pancreatic duct measures approximately 2 mm in diameter and has numerous perpendicular side branches draining the pancreatic lobules. The sensitivity for MRCP in the detection of pancreatic ductal dilatation is high and has been reported at 87% to 100%. The same study reported a specificity of 69% on the MIP images, which increased to 81% when the source images were reviewed. 79 Unfortunately, side branches are not well shown by MRCP unless severely dilated. The exogenous administration of secretin has been suggested to improve the sensitivity for the diagnosis of pancreatic papil!ary stenosis or dysfunction. 8° This technique is based on an increase in pancreatic fluid flow in response to secretin stimulation. Matos et al 8° reported improved delineation of ductal morphological features in both normal volunteers and a group clinically suspected of having pancreatic disease. In cases of papillary Stenosis, a clinically significant stenosis may be inapparent in a nonstimulated pancreasr but may result in an abnormally dilated duct following stimulation. Thus, patients with less advanced disease may be diagnosed earlier. In theory, the technique is also able to evaluate pancreatic exo: crine function reserve. Dilatation of the pancreatic duct may be caused by neoplasia, pancreatitis, or inflammatory stenoses. With neoplasia, the pancreatic duct is dilated and abruptly interrupted. The dilated portion of the duct is typically regular and smooth. There may also be a double duct sign with concomitant dilatation of the common bile duct. In chronic pancreatitis, MRCP may exhibit characteristic ductal abnormalities. As opposed to neoplastic obstruction, the dilated duct in chronic pancreatitis exhibits an irregular and beaded appearance. There may also be calculi in the ducts appearing as filling

defects. In a comparison with ERCP, MRCP identified intraductal filling defects in 92% to 100% of cases, depending on location, and strictures were detected by MRCP in 70% to 92% of cases. 81 MRCP also can detect the presence of pseudocysts and identify their relationship to the ductal system and pancreatic parenchyma (Fig 17). In acute pancreatitis, MRCP may help identify the etiology, such as in gallstone pancreatitis. DEVELOPMENTAL ANOMALIES

Pancreas divisum is a result of the failure of the ventral and dorsal ducts to fuse embryologically, which normally occurs in the second month in utero. The main pancreatic duct, therefore, drains through the minor papilla of Santorini. The ventral and common bile duct drain via the main papilla of Wirsung (ampulla of Vater), without communication between the ductal systems. It has been suggested that this anomaly is associated with a higher incidence of pancreatitis in the dorsal segment, due to relative stenosis of the minor papillaY Focal pancreatitis of the ventral pancreas can occur in cases of bile reflux. On imaging, this entity is diagnosed by the identification of two separate ducts entering the duodenum 83 (Fig 18). The main

Fig 17. Pseudocyst. Coronal MIP MRCP (TR = 6,000 msec, TE = 252 msec) image demonstrates the presence of a pseudocyst at the pancreatic body-tail junction (white arrowhead). The pancreatic (small white arrow)and common bile (open white arrowhead) duct s are well seen. Based on this MIP image alone it would be difficult to exclude a cystic pancreatic neoplasm.

MRI OF THE PANCREAS AND BILIARY TREE

Fig 18. Panacreas divisum in a 60-year-old woman, MIP image created from a two-dimensional fat-suppressed heavily T2-weighted FSE data set (TR = 4,900 maec, TE = 180 msec) shows a separate dorsal pancreatic duct (three white arrowheads) that empties into the duodenum at the accessory papilla that does not connect with the common bile duct (white arrow) which is diagnostic for pancreas divisum.

pancreatic duct crosses anterior to the common bile duct in divisum to terminate in the minor papilla. This finding is more easily shown on axial than on coronal images. Because of limited resolution, MRCP cannot exclude a connection between the dorsal and ventral ductal systems. Therefore, MRCP can really only diagnose a "dorsal dominant" duct rather than specifically true divisum. However, dorsal dominant and true divisum ductal anatomies have similar clinical implications. Annular pancreas is an uncommon anomaly in which the pancreatic head surrounds the second portion of the duodenum. The ring of pancreatic tissue may be complete or incomplete. Annular pancreas has been associated with duodenal stenosis and obstruction. The extension of pancreatic tissue around the duodenum is demonstrated with MRI, 84,85 as well as the aberrant pancreatic duct encircling and extending to the right of the duodenum (Fig 19). MRCP may also be useful in the diagnosis of various developmental anomalies. With the use of a phased-array torso coil, the observed incidence of pancreas divisum was similar to that reported in autopsy series. 86 MRCP has also been evaluated in the diagnosis of anatomic variants associated with Fig 19. Annular pancreas in a 42,year-old woman. (A) Axial T1-GRE (TR = 110 msec, TE = 4.2) and (B) axial fat-suppressed 3D GRE (TR = 6.9 msec, TE = 2.2 msec) images show a thin rim of pancreatic tissue (arrows) surrounding the second portion of the duodenum. (C) Axial fat-suppressed FSE (TR = 7,058 msec, TE = 100 msec) image demonstrates the aberrant pancreatic duct in the annular pancreas (white arrow).

49

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c h o l e c y s t e c t o m y , s u c h as cystic d u c t a n o m a l i e s a n d a b e r r a n t r i g h t h e p a t i c duct. sv W h e r e a s m o s t cases o f p a n c r e a t i t i s i n adults are d u e to gallstones, a l c o h o l abuse, or are i a t r o g e n i c , a c o m m o n c a u s e in t h e p e d i a t r i c p o p u l a t i o n is a n a b n o r m a l p a n c r e a t i c o -

biliary arrangement, which has been evaluated u s i n g M R C R T h e entities t h a t h a v e b e e n d e s c r i b e d include congenital dilatation of the common bile duct, c h o l e d o c h a l cysts, a n d a n a b n o r m a l u n i o n at the p a n c r e a t i c o b i l i a r y j u n c t i o n . 8s

REFERENCES

1. Chezmar JL, Rendon CN, Small WC, et al: Magnetic resonance imaging of the pancreas with gadolinium-DTPA. Gastrointest Radiol 16:139-142, 1991 2. Semelka RC, Simm FC, Recht MP, et al: MR imaging of the pancreas at high field strength: Comparison of six sequences. J Comput As sist Tomogr 15:966-971, 1991 3. Mitchell DG, Vinitski S, Saponaro S, et al: Liver and pancreas: Improved spin-echo T1 contrast by shorter echo time and fat suppression at 1.5 T. Radiology 178:76-71, 1991 4. Semelka RC, Ascher SM: MR imaging of the pancreas. Radiology 188:593-602, 1993 5. Mitchell DG, Winston CB, Outwater EK, et al: Delineation of pancreas with MR imaging: Multiobserver comparison of five pulse sequences. J Magn Reson Imag 5:193-199, 1995 6. Riederer SJ: Recent technical advances in MR imaging of the abdomen. J Magn Reson Imag 6:822-832, 1996 7. Simeone JF, Edelman RR, Stark DD, et al: Surface coil MR imaging of abdominal viscera. Part III. The pancreas. Radiology 157:437-441, 1985 8. Stark DD, Moss AA, Goldberg HI, et al: Magnetic resonance and CT of the normal and diseased pancreas: A comparative study. Radiology 150:153-162, 1984 9. Siegelman ES, Outwater EK, Vinitski S, et al: Fat suppression by saturation/opposed-phase hybrid technique: Spin echo versus gradient echo imaging. Magn Reson Imag 13:545-548, 1995 10. Mitchell DG, Outwater EK, Vinitski S: Hybrid RARE: Implementations for abdominal MR imaging. J Magn Reson Imag 4:109-117, 1994 11. Spritzer CE, Keogan MT, DeLong DM, et al: Optimizing fast spin echo acquisitions for hepatic imaging in normal subjects. J Magn Resort Imaging 6:128-135, 1996 12. Semelka RC, Kelekis NL, Thomasson D, et al: HASTE MR imaging: Description of technique and preliminary results in the abdomen. J Magn Resort Imag 6:698-699, 1996 13. Gehl HB, Urhahn R, Bnhndorf K, et al: Mn-DPDP on MR imaging of pancreatic adenocarcinoma: Initial clinical experience. Radiology 186:795-798, 1993 14. Mattrey RF, Hajek PC, Gylys-Morin VM, et al: Perfluorochemicals as gastrointestinal contrast agents for MR imaging. AmJ Roentgenol 148:1259-1263, 1987 15. Mattrey RF, Trambert MA, Brown JJ, et al: Perflubron as an oral contrast agent for MR imaging: Results of a phase III clinical trial. Radiology 191:841-848, 1994 16. Hahn PF, Stark DD, Lewis JM, et al: First clinical trial of a new superparamagnetic iron oxide for use as an oral gastrointestinal contrast agent in MR imaging. Radiology 175:695-700, 1990 17. Tortes GM, Erquiaga E, Ros PR, et al: Preliminary results of MR imaging with superparamagnetic iron oxide in pancreatic and retroperitoneal disorders. Radiographics 11:785-791, 1991 18. King CR Tart RP, Fitzsimmons JR, et al: Barium sulfate

suspension as a negative oral MRI contrast agent: In vitro and human optimization studies. Magn Reson Imag 9:141-150, 1991 19. Ernst O, Sergent G, L'Hermine C: Oral administration of a low-cost negative contrast agent: A three-year experience in routine practice. J Magn Reson Imag 7:495-498, 1997 20. Listinsky JJ, Bryant RG: Gastrointestinal contrast agents. A diamagnetic approach. Magn Reson Med 8:285-292, 1988 21. Mitchell DG, Vinitski S, Mohamed FB, et al: Comparison of Kaopectate with barium for negative and positive enteric contrast at MR imaging. Radiology 181:475-480, 1991 22. Pavone P, Mitchell DG, Leonetti F, et al: Pancreatic beta-cell tumors: MRI. J Comput Assist Tomogr 17:403-407, 1993 23. Reinhold C, Bret PM: MR cholangiopancreatography. Abdom Imaging 21:105-116, 1996 24. Reinhold C, Bret PM: Current status of MR cholangiopancreatography. Am J Roentgenol 166:1285-1295, 1996 25. Reinhold C, Bret PM, Guiband L, et al: MR cholangiopancreatography: Potential clinical applications. Radiographics 16:309-320, 1996 26. Wallner BK, Schumacher KA, Weidenmaier W, et al: Dilated biliary tract: Evaluation with cholangiography with a T2-weighted contrast-enhanced fast sequence. Radiology 181: 805-808, 1991 27. Morimoto K, Shimoi M, Shirakawa T, et al: Biliary obstruction: Evaluation with three-dimensional MR cholangiography. Radiology 183:578-580, 1992 28. Hall Craggs MA, Allen CM, Owens CM, et al: MR cholangiography: Clinical evaluation in 40 cases. Radiology 189:423-427, 1993 29. Outwater EK: MR cholangiography with a fast spin-echo sequence. J Magn Reson Imag 3:131, 1993 30. Gniband L, Bret PM, Reinhold C, et al: Diagnosis of choledocholithiasis: Value of MR cholangiography. Am J Roentgenol 163:847-850, 1994 31. Guiband L, Bret PM, Reinhold C, et al: Bile duct obstruction and choledocholithiasis: Diagnosis with MR cholangiography. Radiology 197:109-115; 1995 32. Macaulay SE, Schulte SJ, Sekijima JH, et al: Evaluation of a non-breathhold MR cholangiography technique. Radiology 196:227-232, 1995 33. Chart Y, Chan ACW, Lam WWM, et al: Choledocholithiasis: Comparison of MR cholangiography and endoscopic retrograde cholangiography. Radiology 200:85-89, 1996 34. Reinhold C, Guibaud L, Genin G, et al: MR cholangiopancreatography: Comparison between two-dimensional fast spinecho and three-dimensional gradient-echo pulse sequences. J Magn Resort lmag 4:379-384, 1995 35. Barish MA, Yucel EK, Soto JA, et al: MR cholangiopancreatography: Efficacy of three-dimensional turbo spin-echo technique. Am J Roentgenol 165:295-300, 1995 36. Soto JA, Barish MA, Yucel EK, et al: MR cholangiopan-

MRI OF THE PANCREAS AND BILIARY TREE

creatography: Findings on 3D fast spin-echo imaging. Am J Roentgenol 165:1397-1401, 1995 37. Miyazaki T, Yamashita Y, Tsuchigame T, et al: MR cholangiopancreatography using HASTE sequences. Am J Roentgeuol 166:1297-1303, 1996 38. Reuther G, Kiefer B, Tuchmann A, et al: Imaging findings of pancreaticobiliary duct diseases with single-shot MR cholangiopancreatography. Am J Roentgenol 168:453-459, 1997 39. Yamashita Y, Abe Y, Tang Y, et al: In vitro and clinical studies of image acquisition in breath-hold MR cholangiopancreatography: Single-shot projection technique versus multislice technique. Am J Roentgenol 168:1449-1454, 1997 40. Hirohashi S, Hirohashi R, Uchida H, et al: MR cholangiopancreatography and MR urography: Improved enhancement with a negative oral contrast agent. Radiology 203:281-285, 1997 41. Tartaglino LM, Flanders AE, Vinitski S, et al: Metallic artifacts on MR images of the postoperative spine: Reduction with fast spin-echo techniques. Radiology 190:565-569, 1994 42. Lee MG, Lee HJ, Kim MH, et al: Extrahepatic biliary diseases: 3D MR cholangiopancreatography compared with endoscopic retrograde cholangiopancreatography. Radiology 202:663-669, 1997 43. Warshaw AL, Castillo CF: Pancreatic carcinoma. N Engl J Med 326:455-465, 1992 44. Wingo PA, Tong T, Bolden S: Cancer statistics, 1995. CA 45:8-30, 1995 45. Williamson RCN: Pancreatic cancer: The greatest oncological challenge. Br Med J 296:445-446, 1988 46. Megibow AJ, Zhou XH, Rotterdam H, et al: Pancreatic adenocarcinoma: CT versus MRI imaging in the evaluation of resectability-Report of the Radiology Diagnostic Oncology Group. Radiology 195:327-332, 1995 47. Gabata T, Matsui O, Kadoya M, et al: Small pancreatic adenocarcinomas: Efficacy of MR imaging with fat suppression and gadolinium enhancement. Radiology 193:683-688, 1994 48. Ichikawa T, Haradome H, Hachiya J, et al: Pancreatic ductal adenocarcinoma: Preoperative assessment with helical CT versus dynamic MR imaging. Radiology 202:655-662, 1997 49. Semelka RC, Kelekis NL, John G, et al: Ampullary carcinoma: Demonstration by current MR techniques. J Magn Resort Imag 7:153-156, 1997 50. de Lange EE, Mugter JP, Gay SB, et al: Focal liver disease: Comparison of breath-hold Tl-weighted MP-GRE MR imaging and contrast enhanced CT--Lesion detection, localization, and characterization. Radiology 200:465-473, 1996 51. Lewis KI-I, Chezmar JL: Hepatic metastases. MRI Clin North Am 5:319-330, 1997 52. Semelka RC, Kelekis NL, Molina PL, et al: Pancreatic masses with inconclusive findings on spiral CT: Is there a role for MRI? J Magn Reson Imag 6:585-588, 1996 53, Atri M, Nazarnia S, Mehio A, et al: Hypoecbogenic embryologic ventral aspect of the head and uncinate process of the pancreas: In vivo correlation of US with histopathologic findings. Radiology 190:441-444, 1994 54. Jacobs JE, Coleman BG, Arger PH, et al: Pancreatic sparing of focal fatty infiltration. Radiology 190:437-439, 1994 55. Buchanan KD, Johnston CF, O'Hare MMT, et al: Neuroendocrine tumors. Am J Med 81:14-22, 1986 (suppl 6B) 56. Buetow PC, Parrino TV, Buck JL, et al: Islet cell tumors of the pancreas: Pathologic-imaging correlation among size,

51

necrosis and cysts, calcification, malignant behavior, and functional status. Am J Roentgenol 165:1175-1179, 1995 57. Semelka RC, Cumming MJ, Shoenut JP, et al: Islet cell tumors: Comparison of dynamic contrast-enhanced CT and MR imaging with dynamic gadolinium enhancement and fat suppression. Radiology 186:799-802, 1993 58. Moore NR, Rogers CE, Britton BJ: Magnetic resonance imaging of endocrine tumours of the pancreas. Br J Radiol 68:341-347, 1995 59. Friedman AC, Lichtenstein JE, Dachman AH: Cystic neoplasms of the pancreas. Radiology 149:45-50, 1983 60. Buck JL, Hayes WS: Microcystic adenoma of the pancreas. Radiographics 10:313-322, 1990 61. Minami M, Itai Y, Ohtomo K, et al: Cystic neoplasms of the pancreas: Comparison of MR imaging with CT. Radiology 171:53-56, 1989 62. Ros PR, Hamrick-Turner JE, Chiechi MV, et al: Cystic masses of the pancreas. Radiographics 12:673-686, 1992 63. Mathieu D, Guigui B, Valette PJ, et al: Pancreatic cystic neoplasms. Radiol Clin North Am 27:163-176, 1989 64. Machado MC, Montagnini AL, Machado MA, et al: Cystic neoplasm diagnosed as pancreatic pseudocyst: Report of 5 cases and review of the literature. Rev Hosp Clin Fac Med Sao Paulo 49:246-249, 1994 65. de Calan L, Levard H, Hennet H, et al: Pancreatic cystadenoma and cystadenocarcinoma: Diagnostic value of preoperative morphological investigations. Eur J Surg 161:3540, 1995 66, Ohtomo K, Furui S, Onoue M, et al: Solid and papillary epithelial neoplasm of the pancreas: MR imaging and pathologic correlation. Radiology 184:567-570, 1992 67. Buetow PC, Buck JL, Pantongrag-Brown L, et al: Solid and papillary epithelial neoplasm of the pancreas: Imagingpathologic correlation in 56 cases. Radiology 199:707-711, 1996 68. Itai Y, Ohhashi K, Nagai H, et al: "Ductectatic" mucinous cystadenoma and cystadenocarcinoma of the pancreas. Radiology 161:697-700, 1986 69. Lee MG, Auh YH, Cho KS, et al: Mucinous ductaI ectasia of the pancreas: MRI. J Comput Assist Tomogr 16:495496, 1992 70. Semelka RC, Shoenut JR Kroeker MA, et al: Chronic pancreatitis: MR imaging features before and after administration of gadopentetate dimeglumine. J Magn Resort Imag 3:7982, 1993 71. Siegelman ES, Mitchell DG, Rubin R, et al: Parenchymal versus reticuloendothelial iron overload in the liver: Distinction with MR imaging. Radiology 179:361-366, 1991 72. Siegelman ES: MR imaging of diffuse liver disease: Hepatic fat and iron. Radiol Clin North Am 5:347-365, 1997 73. Tham RTOTA, Heyerman HGM, Falke THM, et al: Cystic fibrosis: MR imaging of the pancreas. Radiology 179:183186, 1991 74. Ferrozzi F, Bova D, Campodonico F, et al: Cystic fibrosis: MR assessment of pancreatic damage. Radiology 198:875-879, 1996 75. Kelcz F, Sollinger HW, Pirsch JD: MRI of pancreas transplant: Lack of correlation between imaging and clinical status. Magn Reson Med 21:30-38, 1991 76. Fernandez M, Bernardino ME, Neylan JF, et al: Diagnosis of pancreatic transplant dysfunction: Value of gadopentetate

52 dimeglumine-enhanced MR imaging. Am J Roentgenol 156: 1171-1176, 1991 77. Soto JA, Yucel EK, Barish MA, et al: MR cholangiopancreatography after unsuccessful or incomplete ERCP. Radiology 199:91-98, 1996 78. Lillemoe KD, Pitt HA, Cameron JL: Postoperative bile duct strictures. Surg Clin North Am 70:1355-1380, 1990 79. Soto JA, Barish MA, Yucel EK, et al: Pancreatic duct: MR cholangiopancreatography with a three dimensional fast spin-echo technique. Radiology 196:459-464, 1995 80. Marts C, Metens T, Deviere J, et al: Pancreatic duct: Morphologic and functional evaluation with dynamic MR pancreatography after secretin stimulation. Radiology 203:435441, 1997 81. Takehara Y, Ichijo K, Tooyama N, et al: Breath-hold MR cholangiopancreatography with a long-echo-train fast spin-echo sequence and a surface coil in chronic pancreatitis. Radiology 192:73-78, 1994

MAMMONE, SIEGELMAN, AND OUTWATER

82. Delhaye M, Engelholm L, Cremer M: Pancreas divisum: Controversial clinical significance. Digest Dis 6:30-39, 1988 83. Zeman RK, McVay LV, et al: Pancreas divisnm: Thinsection CT. Radiology 169:395-398, 1988 84. Reinhart RD, Brown JJ, Foglia RP, et al: MR imaging of annular pancreas. Abdom Imag 19:301-303, 1994 85. Desai MB, Mitchell DG, Munoz SJ: Asymptomatic annular pancreas: Detection by magnetic resonance imaging. Magn Reson Imag 12:683-685, 1994 86. Bret PM, Reinhold C, Taourel P, et al: Pancreas divisum: Evaluation with MR cholangiopancreatography. Radiology 199: 99-103, 1996 87. Taourel P, Bret PM, Reinhold C, et al: Anatomic variants of the biliary tree: Diagnosis with MR cholangiopancreatography. Radiology 199:521-527, 1996 88. Hirohashi S, Hirohashi R, Uchida H, et al: Pancreatitis: Evaluation with MR cholangiopancreatography in children. Radiology 203:411-415, 1997