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Miller et al. MRI of the Pancreas

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C E N T U R Y

MEDICAL

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IMAGING

Frank H. Miller1 Nancy J. Rini Ana L. Keppke Miller FH, Rini NJ, Keppke AL

MRI of Adenocarcinoma of the Pancreas OBJECTIVE. CT is the established imaging technique for evaluation of pancreatic adenocarcinoma. MRI, however, can play a major role in this disease. The objective of this study is to illustrate the strengths of MRI for evaluating pancreatic adenocarcinoma. CONCLUSION. The superior soft-tissue contrast of MRI compared with CT is useful in the detection and characterization of non–contour-deforming pancreatic masses. MRI compared with CT may be more sensitive in the detection of distant disease, better for defining appropriate surgical candidates, and better for characterizing small liver metastases and peritoneal and omental metastases. ancreatic ductal adenocarcinoma is the fourth leading cause of cancer death. Most cases are advanced and unresectable at the time of diagnosis. Pancreatic carcinoma commonly metastasizes to the lymph nodes, liver, and peritoneum. The indications for surgical resection vary throughout medical centers. Contraindications to surgical resection include liver and peritoneal metastases, distant lymph node metastases, arterial encasement, and greater than 50% encasement of major venous structures [1].

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CT is the established imaging technique for the evaluation of pancreatic adenocarcinoma. MRI, however, can play a major role in this disease. The superior soft-tissue contrast of MRI compared with CT is useful in the evaluation of subtle non–contour-deforming pancreatic masses. MRI compared with CT may be more sensitive in the detection of distant disease, better for defining appropriate surgical candidates, and better for characterizing small liver metastases and peritoneal and omental metastases. Recent advances in abdominal MRI allow fast acquisition of multiple sequences

Keywords: adenocarcinoma, cancer, MRI, pancreas, pancreatic neoplasms DOI:10.2214/AJR.05.0875 Received May 23, 2005; accepted after revision July 12, 2005.

Fig. 1—49-year-old man with small non–contourdeforming pancreatic mass caused by adenocarcinoma. A, Axial contrastenhanced MDCT image shows atrophy of pancreatic tail and pancreatic duct dilation (arrow). Discrete mass is difficult to identify. (Fig. 1 continues on next page)

1All authors:

Department of Radiology, Northwestern Memorial Hospital, Northwestern University, The Feinberg School of Medicine, 676 N. St. Clair, Ste. 800, Chicago, IL 60611. Address correspondence to F. H. Miller ([email protected]). WEB This is a Web exclusive article.

AJR 2006; 187:W365–W374 0361–803X/06/1874–W365 © American Roentgen Ray Society

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Miller et al.

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Fig. 1 (continued)—49-year-old man with small non–contour-deforming pancreatic mass caused by adenocarcinoma. B, Axial T2-weighted HASTE MR image (5-mm slice thickness) shows pancreatic ductal dilation (arrow) with associated atrophy of pancreatic tail. Duct dilation is easily seen on T2-weighted images and may be better seen than on MDCT. C, Axial venous-phase gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows 1.8-cm hypointense mass (arrowhead) in pancreatic body, consistent with pancreatic carcinoma. Pancreatic duct dilation (long arrow) and pancreatic atrophy upstream from mass are seen. Ill-defined soft tissue (short arrows) surrounding celiac artery was proven to be malignant.

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Fig. 2—31-year-old man with suspected pancreatic mass on MDCT. A, Axial contrast-enhanced MDCT image shows prominent pancreatic head (arrow) suggesting possibility of subtle mass. B, Axial T1-weighted in-phase gradient-recalled echo MR image shows prominent pancreatic head (arrow) with normal signal intensity. (Fig. 2 continues on next page)

free of artifacts. Our routine MRI protocol is detailed in Appendix 1. This pictorial essay illustrates the strengths of MRI for evaluating pancreatic adenocarcinoma.

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Non–Contour-Deforming Pancreatic Mass The normal pancreas shows high signal intensity on unenhanced T1-weighted fat-

suppressed sequences because of the presence of acinar proteins. It also shows homogeneous intense enhancement on the early arterial phase and becomes isointense to the

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MRI of the Pancreas

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Fig. 2 (continued)—31-year-old man with suspected pancreatic mass on MDCT. C, Axial T1-weighted opposed-phase gradient-recalled echo MR image shows signal dropout in pancreatic head (arrow) because of fatty infiltration without evidence of underlying mass. D, Axial arterial-phase gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows normal homogeneous enhancement of head of pancreas (arrow) without mass.

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Fig. 3—60-year-old man with mass in uncinate process of pancreas that proved to be pancreatic adenocarcinoma. Patient had elevated creatinine and could not receive iodinated contrast material on CT. A, Coronal T2-weighted RARE MR cholangiopancreatography image shows dilation of common bile duct (short arrow) and pancreatic duct (long arrow) with abrupt termination at confluence of ducts (arrowhead). This double duct sign is highly suspicious for malignancy. B, Axial late arterial-phase gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows 2.5-cm hypointense mass (short arrow) in head of pancreas responsible for double duct sign seen on MR cholangiopancreatography. Fat plane between superior mesenteric artery and pancreatic mass (long arrow) is obscured, suggesting vascular invasion.

liver on more delayed enhanced sequences [2]. Conversely, pancreatic adenocarcinoma is hypointense to the normal pancreas on T1weighted fat-suppressed sequences, shows decreased enhancement on the arterial

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phase, and shows progressive enhancement on delayed sequences. These MRI features are related to the fibrotic nature of the tumor. The arterial phase of imaging yields the greatest conspicuity of pancreatic carci-

noma, which appears hypointense compared with the adjacent normal pancreas [3]. Small pancreatic masses may not deform the pancreatic contour and may be difficult to detect even on thin-section arterial and venous

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Miller et al.

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B Fig. 4—55-year-old man with pancreatic adenocarcinoma and suspected liver metastases shown by MRI but inconspicuous on MDCT. A, Axial venous-phase contrast-enhanced MDCT image shows hypodense mass (arrow) in pancreatic head. Note homogeneous liver enhancement, without evidence of metastases. B, Axial arterial-phase gadolinium-enhanced T1-weighted fat-suppressed gradientrecalled echo MR image performed 3 days after MDCT shows several ringenhancing liver lesions (short white arrows) suggestive of liver metastases. These lesions were not bright on T2-weighted images, suggesting bile lakes or abscesses. Patient was afebrile. These lesions were inconspicuous on MDCT. There is susceptibility artifact because of biliary stent (arrowhead) with adjacent dilated pancreatic duct en face (long arrow). Note poorly defined hypointense mass (black arrow) in pancreatic head. C, Axial venous-phase gadolinium-enhanced T1-weighted fat-suppressed gradientrecalled echo MR image confirms the ring-enhancing lesions (arrows).

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MDCT. The excellent contrast resolution of MRI facilitates detection of a small tumor, which may appear as a hypointense mass within the enhancing pancreas on gadoliniumenhanced fat-suppressed images. Important secondary signs may be present to suggest that an underlying pancreatic mass exists. Focal pancreatic atrophy or pancreatic duct dilation may be seen on CT because of an underlying downstream pancreatic mass not well seen on CT, for which MRI may be helpful (Fig. 1). Prominent Pancreatic Head on CT A prominent pancreatic head may be seen on contrast-enhanced CT and may be

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difficult to distinguish from a mass. MRI may help to detect or exclude neoplasm in patients with indeterminate pancreatic enlargement. Focal fat of the pancreas can occasionally present as a mass on CT or sonography and potentially be confused with a tumor. On MRI, fatty abnormalities may show increased signal on T1-weighted images, decreased signal intensity with fat suppression, and phase cancellation on opposed-phase images. These typical MRI features allow noninvasive characterization of fatty abnormalities and distinguish them from cancer (Fig. 2).

Double Duct Sign T2-weighted sequences and MR cholangiopancreatography (MRCP) are valuable for assessing the pancreaticobiliary ducts. Dilation of the common bile duct and the pancreatic duct (double duct sign) may result from either benign or malignant causes, but is most commonly associated with cancer (Fig. 3). Duct dilation may be smooth or beaded with an abrupt or gradual transition in caliber. Karasawa et al. [4] found the pancreatic duct to be smooth or beaded with malignancy and more irregularly dilated when associated with chronic pancreatitis. MRCP is valuable in characterizing the obstruction and its location and causes, including stones or masses.

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MRI of the Pancreas

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B Fig. 5—55-year-old man with metastatic pancreatic adenocarcinoma. A, Axial T2-weighted HASTE MR image shows multiple, moderately hyperintense liver lesions (arrows) caused by metastases. B, Axial unenhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows multiple hypointense liver masses (arrows). C, Axial arterial-phase gadolinium-enhanced T1-weighted fat-suppressed gradientrecalled echo MR image shows ring-enhancing lesions (white arrows) and wedgeshaped perilesional enhancement (black arrows) of metastases.

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Fig. 6—57-year-old woman with newly diagnosed pancreatic carcinoma and peritoneal metastases. Axial venous-phase gadolinium-enhanced T1-weighted fatsuppressed gradient-recalled echo MR image shows right-sided peritoneal implant (black arrow). Hypointense pancreatic mass (open arrow) and pseudocyst (short white arrow) are seen. Mass in left adrenal gland (long arrow) does not have imaging characteristics of adenoma on other imaging sequences and may represent metastasis or lipid-poor adenoma.

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Fig. 7—53-year-old man with pancreatic carcinoma metastatic to liver and greater omentum. A, Axial unenhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows low-signal-intensity lesions (arrows) in liver, consistent with metastases. B, Axial gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows enhancement along left side of greater omentum (arrow), consistent with metastases. Hypointense liver metastases (arrowheads) are also identified.

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Fig. 8—36-year-old man with clinical history of pancreatitis was subsequently proven to have pancreatic carcinoma with axillary lymph node metastases. A, Axial arterial-phase contrast-enhanced MDCT image shows prominence of pancreatic tail (arrow), mild peripancreatic fat stranding, and multiple retroperitoneal lymph nodes (arrowheads). B, Axial unenhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows subtle enlargement of pancreatic tail (arrow) and multiple small lymph nodes (arrowheads) along celiac artery. (Fig. 8 continues on next page)

Liver Metastases The detection of liver metastases is critical for properly staging pancreatic carcinoma, as

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this finding deems the patient unresectable. Thin-collimation CT detects liver lesions smaller than 1 cm, which are often difficult to

characterize (Fig. 4). MRI may further delineate these lesions as cysts, hemangiomas, or metastases, which significantly influences patient

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MRI of the Pancreas

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Fig. 8 (continued)—36-year-old man with clinical history of pancreatitis was subsequently proven to have pancreatic carcinoma with axillary lymph node metastases. C, Axial venous-phase gadolinium-enhanced T1-weighted fat-suppressed gradientrecalled echo MR image shows pancreatic tail mass (arrow), which proved to be pancreatic carcinoma, more conspicuously than MDCT. Multiple retroperitoneal lymph nodes (arrowheads) are also identified around celiac artery.

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Fig. 9—59-year-old man with unexplained acute recurrent pancreatitis on MDCT examinations performed 2 years apart. The patient subsequently proved to have pancreatic carcinoma. A, Axial arterial-phase contrast-enhanced MDCT image from 2002 shows nonenhancing, ill-defined pancreatic body (white arrow) with moderate peripancreatic fat stranding and fluid (arrowheads), which is consistent with pancreatitis. Normal enhancement in pancreatic tail is seen (black arrow). B, Axial arterial-phase contrast-enhanced MDCT image from 2004 shows poorly defined, nonenhancing pancreatic body and tail suggestive of necrosis (white arrow). There were findings suggestive of pancreatic mass (black arrow). (Fig. 9 continues on next page)

workup and prognosis. Danet et al. [5] described liver metastases as minimally hypointense on T1-weighted images and isointense to moderately hyperintense on T2-weighted images. These authors found that although the primary tumor is generally hypovascular, a spectrum is seen of hypovascular-to-hypervascular liver

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metastases with ring- or wedge-shaped perilesional enhancement after IV gadolinium (Fig. 5). Reticuloendothelial system-specific contrast agents (ferumoxides) and hepatocyteselective contrast agents (mangafodipir trisodium) may increase the conspicuity of liver metastases through selective enhancement of the

normal liver, although we do not routinely use these agents [6]. Peritoneal and Omental Metastases Detection of extrapancreatic disease is critical because it prevents the patient from undergoing unnecessary surgery. The perito-

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D Fig. 9 (continued)—59-year-old man with unexplained acute recurrent pancreatitis on MDCT examinations performed 2 years apart. The patient subsequently proved to have pancreatic carcinoma. C, Axial T2-weighted HASTE MR image performed 3 weeks after MDCT (B) shows pancreatic duct dilation and atrophy of pancreatic tail (arrow). D, Axial unenhanced T1-weighted fat-suppressed gradient-recalled echo MR image at lower level than C shows mass (arrow) in body of pancreas. Bowel (arrowhead) is seen adjacent to pancreatic mass. E, Axial gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows hypointense mass (arrow) suspicious for tumor in body of pancreas. Endoscopic sonography with biopsy showed adenocarcinoma. Bowel (arrowhead) is seen adjacent to pancreatic mass.

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neum is often involved in metastatic pancreatic carcinoma, and MRI may be more sensitive than CT for detecting peritoneal enhancement and implants. Low et al. [7] found MRI to be superior to CT in detection of upper abdominal peritoneal metastases and implants smaller than 1 cm, which are best seen in the presence of ascites (Figs. 6 and 7). Pancreatitis Mimicking Pancreatic Cancer Patients with pancreatic carcinoma often develop chronic pancreatitis related to duct obstruction by the pancreatic mass. Chronic pancreatitis may be difficult to differentiate from cancer because of similar imaging features. These include hypointensity on unen-

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hanced T1-weighted fat-suppressed images and delayed enhancement on dynamic gadolinium-enhanced T1-weighted fat-suppressed sequences [8]. Pancreatitis without an appropriate clinical history should prompt further investigation for an underlying mass. The characteristics of the pancreatic duct dilation may suggest chronic pancreatitis or pancreatic carcinoma as the cause. Karasawa et al. [4] found that the ratio of duct to gland was larger in carcinoma compared with chronic pancreatitis. Pancreatic carcinoma can also present with gland enlargement, abnormal enhancement, and peripancreatic stranding, mimicking acute pancreatitis (Figs. 8 and 9). Additional findings, such as retroperitoneal lymph-

adenopathy, may suggest an underlying malignancy. Lymph Node Metastases Pancreatic carcinoma commonly metastasizes to the peripancreatic and porta hepatis lymph nodes. Size criteria are of limited use because microscopic disease may be present in normal-size lymph nodes. Pathologically enlarged lymph nodes (i.e., larger than 1 cm in short-axis diameter) determined by imaging criteria should raise suspicion for disease involvement and prompt further evaluation (Fig. 10). Vascular Invasion Encasement of the celiac, superior mesenteric, or hepatic artery is a contraindication

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MRI of the Pancreas

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Fig. 10—55-year-old man with metastatic pancreatic carcinoma. A, Axial T2-weighted HASTE MR image shows multiple periaortic lymph nodes (white arrows) and hyperintense metastasis (black arrow) in liver and paraspinal muscles (arrowhead). B, Axial gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows multiple, ring-enhancing, periaortic lymph nodes (short arrows). Ringenhancing liver metastasis (arrowhead) and multiple enhancing foci (long arrows) in paraspinal muscles caused by metastases are seen.

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Fig. 11—49-year-old man with locally advanced pancreatic carcinoma. A, Axial gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows abnormal enhancing soft tissue (arrows) surrounding celiac artery, which is suspicious for vascular encasement. B, Coronal gadolinium-enhanced T1-weighted fat-suppressed gradient-recalled echo MR image shows abnormal soft tissue (arrow) surrounding origin of celiac and superior mesenteric arteries. This tissue was positive for malignancy by fine-needle aspiration. C, Corresponding axial MDCT image shows abnormal soft tissue surrounding celiac axis (arrows).

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Miller et al. to surgical resection. Limited involvement of the portal vein or superior mesenteric vein by tumor may be treated with a surgical bypass. However, extensive involvement of major venous structures by tumor is a surgical contraindication [1]. In a patient with a history of pancreatic carcinoma, obliteration of the fat planes surrounding the superior mesenteric artery is highly suggestive of tumor encasement (Fig. 11). CT or MR angiography is usually not necessary, but could be performed in inconclusive cases. Conclusion MRI may significantly impact therapy and prognosis in patients with pancreatic cancer. Although CT is the established imaging technique for evaluation of pancreatic carcinoma, the superior contrast resolution of MRI may

better detect and characterize non–contourdeforming lesions of the pancreas, small liver metastases, and peritoneal disease. Specific indications for MRI include suboptimal CT results and inability to administer iodinated contrast material because of renal insufficiency or contrast allergy.

References 1. Alexakis N, Halloran C, Raraty M, Ghaneh P, Sutton R, Neoptolemos JP. Current standards of surgery for pancreatic cancer. Br J Surg 2004; 91:1410–1427 2. Ly J, Miller FH. MR imaging of the pancreas: a practical approach. Radiol Clin North Am 2002; 40:1289–1306 3. Obuz F, Dicle O, Coker A, Sagol O, Karademir S. Pancreatic adenocarcinoma: detection and staging with dynamic MR imaging. Eur J Radiol 2001; 38:146–150

4. Karasawa E, Goldberg HI, Moss AA, Federle MP, London SS. CT pancreatogram in carcinoma of the pancreas and chronic pancreatitis. Radiology 1983; 148:489–493 5. Danet IM, Semelka RC, Nagase LL, Woosely JT, Leonardou P, Armao D. Liver metastases from pancreatic adenocarcinoma: MR imaging characteristics. J Magn Reson Imaging 2003; 18:181–188 6. Semelka RC, Helmberger KG. Contrast agents for MR imaging of the liver. Radiology 2001; 218:27–38 7. Low RN, Barone RM, Lacey C, Sigeti JS, Alzate GD, Sebrechts CP. Peritoneal tumor: MR imaging with dilute oral barium and intravenous gadolinium containing contrast agents compared with unenhanced MR imaging and CT. Radiology 1997; 204:513–520 8. Johnson PT, Outwater EK. Pancreatic carcinoma versus chronic pancreatitis: dynamic MR imaging. Radiology 1999; 212:213–217

APPENDIX I: Pancreatic MRI Protocol Sequence 1. 2. 3. 4. 5. 6. 7. 8. 9.

Acquisition Time (seconds)

Axial HASTE T2-weighted sequence Coronal HASTE T2-weighted sequence Axial in- and opposed-phase T1-weighted GRE sequence Axial unenhanced fat-saturated T1-weighted GRE sequence Coronal unenhanced fat-saturated T1-weighted GRE sequence Axial T1-weighted fat-saturated Gd-enhanced GRE at 15–20 seconds (fluoro-preparation timed sequence) and at 45 seconds Coronal T1-weighted fat-saturated Gd-enhanced GRE at 90 seconds Axial T1-weighted fat-saturated Gd-enhanced GRE at 120 seconds Optional RARE MRCP

30 30 18 18 18 18 × 2 = 36 18 18 3 × 6 = 18

Note—GRE = gradient-recalled echo, Gd = gadolinium, MRCP = MR cholangiopancreatography.

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