30 Magnetic Resonance Imaging of Neoplasmsof the Pancreatobiliary System

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1. BACKGROUND

Magnetic resonance imaging (MRI) and magnetic resonance cholangiopancreatography (MRCP) are noninvasive imaging techniques that can detect, characterize, and stage neoplasms of the biliary system and pancreas. In patients with suspected pancreatic cancer, MRI/MRCP can help distinguish those patients who are unresectable from those who are potentially resectable. In patients with pancreatic cysts, MRI assists in the distinction among pseudocysts, benign cystic lesions, and cystic pancreatic malignancies. Limitations of current MRI techniques include the inability to detect subcentimeter peritoneal metastases and the lack of sensitivity for identifying microscopic metastases within normal-sized lymph nodes.

2. INTRODUCTION

MRI/MRCP is a noninvasive imaging modality that has been shown to be an accurate technique for diagnosing and staging neoplasms of the pancreatobiliary system. In some clinical circumstances, MRI/MRCP can replace endoscopic retrograde cholangiopancreatography (ERCP) as the study of choice for diagnostic evaluation of the pancreatobiliary tract. This chapter reviews the rationale, technique, and role of MRI/MRCP in the evaluation of neoplasms that involved the pancreas and bile ducts. Additional information concerning applications in non- neoplastic disease may be found in a concurrently published review (1).

From: Endoscopic Oncology: Gastrointestinal Endoscopy and Cancer Management. Edited by: D. O. Faigel and M. L. Kochman © Humana Press, Totowa, NJ

Magnetic Resonance Imaging of Neoplasms of the Pancreatobiliary System

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CONTENTS

BACKGROUND

INTRODUCTION

RATIONALE FORMRI/MRCP

PANCREATOBILIARYMRI/MRCP TECHNIQUE

MRI/MRCP EVALUATION OFSPECIFICBILIARYOBSTRUCTION

MRI/MRCP EVALUATION OFSPECIFICNEOPLASTICCONDITIONS OF THEPANCREATICOBILIARYSYSTEM

EVALUATION OF THEPANCREAS ANDPANCREATICDUCT

CONCLUSIONS

REFERENCES

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3. RATIONALE FOR MRI/MRCP

MRI/MRCP has been advocated as a comprehensive diagnostic imaging modality of the pancreas and biliary system. MRI/

MRCP is currently the single imaging modality that can most reli- ably provide information on the pancreatobiliary ducts, surrounding tissues, vasculature, and function in one session. Relative strengths and limitations of MRI/MRCP are presented in Table 1.

MRI is noninvasive, does not use ionizing radiation, and utilizes a safe intravenous contrast agent (Gadolinium chelate) that is not nephrotoxic and has a low rate of allergic reactions (2). MRCP is less operator-dependent than modalities such as ERCP, sonography, and percutaneous transhepatic cholangio- graphy (PTC). Menon et al. (3) found MRI/MRCP to be well tolerated and preferred by patients over ERCP, with patients reporting less pain and discomfort. MRI/MRCP has excellent soft tissue contrast, with especially high sensitivity for detection of fat, fluid, hemorrhage, and contrast enhancement.

Images can be directly obtained in any specified plane, optimizing views, and thereby the information.

4. PANCREATOBILIARY MRI/MRCP TECHNIQUE The abdomen from the diaphragm to the iliac crest is imaged when MRI is requested for evaluation of a potential neoplasm of the pancreatobiliary system. The specific sequences that are performed may vary by institution specific protocols. However, as a rule, both T1- and T2-weighted sequences are obtained in various planes, in addition to MRCP (heavily T2-weighted) sequences. Dynamic enhanced imaging with gadolinium is performed with breath-hold two or three dimensional T1-weighted gradient echo sequences. At some

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institutions, MRCP is performed exclusively without use of conventional MRI sequences or dynamic contrast-enhanced imaging. However, performing a complete abdominal MRI examination in addition to MRCP is often necessary for a complete patient evaluation.

MRCP is performed using heavily T2-weighted sequences that result in high signal from static or slow-moving fluid such as bile and pancreatic juice in the pancreatobiliary tract. Images are acquired or postprocessed to resemble the projection images obtained at ERCP. Currently, MRI techniques are used that can acquire an image in less than a second. These breath-hold techniques result in decreased artifacts from abdominal gas, respi- ratory motion, surgical clips, and biliary stents whereas increasing signal-to-noise ratio and spatial resolution.

Two complementary techniques are performed as part of MRCP. One technique acquires one or more thick (30–80 mm) slabs in the coronal and/or coronal oblique planes. The other technique obtains multiple thin (2–5 mm) sections in the axial and/or coronal planes. A maximal intensity projection can then be con- structed from the thin-slice tomographic source images. On these heavily T2-weighted sequences, any fluid present within the imaging volume (e.g., fluid-filled stomach or bowel segment) will also be depicted as high signal intensity and in some cases may obscure visualization of the pancreatobiliary system.

5. MRI/MRCP EVALUATION OF SPECIFIC BILIARY OBSTRUCTION

A recent meta-analysis (4) reviewed 498 abstracts published from January 1987 to March 2003 and selected 67 studies (4711 patients) to assess the performance of MRCP in the evaluation of biliary obstruction. In the studies examined, findings on MRCP were compared with various gold standards including intraoper- ative cholangiography, ERCP, intravenous cholangiography, surgical exploration, or a combination of these procedures. MRCP was found to be highly accurate for diagnosing the presence of obstruction, with a sensitivity of 97% and specificity of 98%.

MRCP identified the level of obstruction with a sensitivity of 98% and specificity of 98%. Accurate determination of the level and specific location of obstruction not only aids in the differential diagnosis, but also in choice of potential therapeutic intervention.

Patients with distal bile duct obstruction are better evaluated and treated via a retrograde endoscopic approach whereas those with proximal obstruction may be better treated by percutaneous transhepatic cholangiography or by selective intrahepatic duct cannulation at ERCP (5).

With biliary obstruction, the increased ductal caliber increases the conspicuity of third and fourth order peripheral ducts on MRCP, which are not well depicted when normal in caliber. The biliary ducts both proximal and distal to an obstruction are well demonstrated on MRCP, whereas retrograde contrast injection at ERCP may not opacify ducts proximal to a high-grade obstruction, or do so at the risk of inducing sepsis if the ducts visualized are not subsequently successfully drained.

The use of T1 and less-heavily-weighted T2 sequences pro- vides information about surrounding tissues and assists in deter- mining the nature of the obstruction. The ductal caliber seen on MRCP may more closely approximate the true caliber, which may be overestimated at ERCP owing to the distension effect of contrast injection.

Although MRCP is highly accurate for detecting and localizing biliary obstruction, it has variable accuracy ranging from 30 to 98% for differentiation between benign and malignant causes of obstruction. The sensitivity and specificity of MRCP in the evaluation of malignancy is 88 and 95%, respectively (4). Some studies have only evaluated MRCP sequences in isolation, but the addition of T1, T2, and contrast- enhanced sequences can increase the sensitivity, specificity, and accuracy up to 20% (6).

6. MRI/MRCP EVALUATION OF SPECIFIC NEOPLASTIC CONDITIONS

OF THE PANCREATICOBILIARY SYSTEM 6.1. CHOLANGIOCARCINOMA

Cholangiocarcinoma (CCA) in or outside the setting of primary sclerosing cholangitis can be difficult to diagnose with available tests or imaging modalities, as findings may be nonspecific and subtle. The peripheral type of CCA typically pres- ents at an advanced stage as a mass with peripheral duct dilation (Fig. 1). A suggestive MRI feature of peripheral CCA is central foci of low T2 signal, intensity that shows delayed contrast enhancement

• Direct multiplanar sections

• Shows ducts proximal to obstruction

• Higher patient satisfaction over ERCP

• Lower cost than ERCP

CT, computed tomography; ERCP, endoscopic retrograde cholangiopancreatography; US, ultrasound.

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enhancement, a finding that correlates with intratumoral fibro- sis (7,8). Rarely, liver metastases from colon carcinoma can result in peripheral duct dilation that can mimic peripheral CCA. Detection of the primary colon cancer can help establish a correct diagnosis (Fig. 2).

The hilar (Klatskin’s) and extrahepatic types of CCA present earlier with obstructive signs and symptoms. These types cir- cumferentially infiltrate the duct walls, and might be depicted as an obstructing stricture with irregular contours and abrupt ter- mination, referred to as the “shoulder sign” that is suggestive of malignancy. Occasionally, a papillary growth projecting into the lumen may be revealed as a filling defect. MRI/MRCP has been advocated as the current optimal initial evaluation for suspected CCA, providing information on local extent, hepatic metastases, and vascular involvement (Fig. 3) (9,10).

Enhancing bile duct walls that are more than 5 mm in width suggests a diagnosis of CCA, but is not a sensitive indicator of malignancy. Wall thickening and enhancement can be present in various infectious and inflammatory disorders of the biliary tract, including ascending cholangitis and primary sclerosing cholangitis. It is difficult to differentiate benign and malignant disease, but performance of MRCP can be improved by the use of T1- and T2-weighted and gadolinium-enhanced sequences to detect features such masses, abscesses, or cirrhosis that may help distinguish among the different entities. One should con- sider performing MRI/MRCP in the evaluation of suspected CCA prior to intervention, as inflammation related to stent placement can subsequently result in wall thickening and enhancement and lead to overestimation of the extent of disease. In patients with inconclusive MRCP, ERCP or before bile duct brushing, positron emission tomography (PET) could be considered to potentially aid in the diagnosis and staging of a suspected CCA (11).

7. EVALUATION OF THE PANCREAS AND PANCREATIC DUCT

The pancreatic duct is smaller in caliber than the common bile duct and is more difficult to evaluate in its entirety with MRI/MRCP unless it is dilated. Imaging sequences that are most effective for evaluating the pancreatic parenchyma often empha- size contrast differences between the high signal intensity on

T1-weighted images of the normal pancreatic tissue and the rela- tively lower signal intensity of many pathological processes. The pancreas demonstrates the highest signal intensity on T1-weighted imaging of all the parenchymal abdominal organs owing to its high-protein content. MRI is also highly sensitive for detection of presence of contrast enhancement. Patterns of enhancement depicted after gadolinium administration help differentiate various pathological conditions. The following reviews the various types of neoplastic conditions that involve the pancreas.

7.1. PANCREATIC DUCTAL ADENOCARCINOMA A wide range of imaging modalities has been applied to detect and stage pancreatic adenocarcinoma including CT, percutaneous sonography, endoscopic sonography, MRI/MRCP, ERCP, and PET with variable success (12). In a prospective study by Adamek et al. (13) MRI/MRCP was determined to be more accurate for detection of pancreatic adenocarcinoma than ERCP.

MRI/MRCP was 84% sensitive and 97% specific compared with ERCP, which was 70% sensitive and 94% specific.

Studies have also shown that MRI is superior to nonhelical and single detector CT for the detection and staging of pancre- atic malignancy (14), but in clinical practice, patients are often routinely referred for helical CT. The basis for better performance of MRI over CT has been attributed to MRI’s superior soft tissue contrast and sensitivity to contrast enhancement that renders small tumors more conspicuous. MRI/MRCP accu- rately evaluates for vascular involvement, regional invasion, and distant metastases—all factors that determine lesion resectability (15,16). The accuracy of newer multidetector hel- ical CT scanning compared with MRI/MRCP has yet to be determined. One recent study suggests that the excellent spatial resolution of multidetector helical CT improves the detection of small (<2 cm) pancreatic tumors (17).

Differentiating carcinoma from chronic pancreatitis based on imaging criteria can be difficult in some patients. The “double duct sign” at MRCP, as it is at ERCP, is highly suggestive of a pancreatic adenocarcinoma indicating mass effect in the head of the pancreas obstructing both the pancreatic and common bile ducts(Fig. 4A). However, this finding is not specific for pancreatic cancer and can also be present secondary to strictures from chronic pancreatitis, leading to false-positive diagnoses (15). On conventional MRI sequences, presence of a focal Fig. 1. Magnetic resonance imaging illustration of a peripheral cholangiocarcinoma (CCA). (A) Projection magnetic resonance cholangiopancre- atography image shows segmental biliary obstruction of the left hepatic ducts (curved arrows). The ducts occlude at the level of the tumor (arrow).

Pancreatic divisum is revealed as the accessory pancreatic duct (double small arrows) drains into the minor papilla and does not communicate with the common bile duct B and C. (B) T2 and contrast enhanced (C) T1-weighted images shows the rim enhancing CCA (arrow) and dilated periph- eral ducts (curved arrows).

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mass that is lower in signal intensity on T1-weighted images relative to the normal surrounding higher signal intensity pancreatic parenchyma supports the diagnosis of adenocarcinoma.

However, focal chronic pancreatitis may also appear well circum- scribed and hypointense on T1-weighted imaging. Enhancement characteristics may also be similar, with delayed enhancement relative to the surrounding parenchyma reflecting the hypovascu- larity and fibrotic nature of both disease processes (18). The presence of normal pancreatic tissue surrounding the mass favors malignancy. However, a nonborder deforming pancreatic head mass in a patient with chronic pancreatitis may represent either an adenocarcinoma that has resulted in secondary postob- structive chronic pancreatitis or benign inflammatory tissue.

Detection and characterization of lymph nodes and metastatic disease is also required in order to stage a patient with a potential pancreatic carcinoma. One of the limitations of current imaging techniques is that differentiating benign from malignant lymph nodes is often based on size criteria alone. Unfortunately, metastatic pancreatic carcinoma may be present in normal-sized nodes and both CT and MRI techniques are not accurate in pre- dicting the presence or absence of tumor in nodes in patients with

pancreatic cancer (19). More than half of resected lymph nodes in patient’s with pancreatic adenocarcinoma that have a normal appearance at histology will reveal occult involvement by cancer with molecular biological techniques (20–22). It is hoped that in the future novel contrast agents may help to characterize

“micrometastases” to normal-sized nodes and exclude tumor in enlarged reactive nodes (23,24).

Some centers use laparoscopy and laparoscopic ultrasonography in order to identify a subset of patients with occult unresectable disease (including malignant adenopathy and occult peritoneal metastases) who would not benefit from an attempt at curative resection (25,26). However, others feel that laparoscopic staging does not detect enough patients with occult unresectable disease to warrant its routine use (27). Because different sur- geons have different opinions concerning what defines resectable or unresectable disease, one should engage in active discussion with ones surgical colleagues in order to understand the information desired to optimally stage a patient for treatment. Both MRI and multidetector CT can detected and characterize liver metas- tases from pancreatic cancer (15,28) (Fig. 4B,C). By establishing an accurate diagnosis of metastatic disease to the liver, the patient can avoid unnecessary attempt at curative laparotomy and can be referred for appropriate palliative care. Whereas endoscopic ultrasound produces high-resolution images of the primary tumor, often it is detection of disease outside of the field of view of the ultrasound probe that may ultimately determine an individual patient’s treatment and prognosis.

7.2. ISLET CELL NEOPLASMS (NEUROENDOCRINE TUMORS)

Contrast-enhanced MRI/MRCP appears to be sensitive for detection of pancreatic islet cell tumors, although studies are often limited by small patient populations and different pro- portions of the various subtypes of tumors. Islet cell tumors are well demonstrated on multiple imaging sequences on MRI/MRCP (29,30). Compared with CT, MRI demonstrates better soft tissue contrast and increased sensitivity for intravenous contrast enhancement that potentially makes smaller tumors more apparent.

The three most common types are insulinomas, gastrinomas, and nonfunctioning tumors. Most insulinomas are benign, whereas the majority of gastrinomas and nonfunctioning tumors Fig. 3. MR illustration of a Klatskin tumor. Axial T2-weighted image

shows a central heterogeneous mass (arrow at top of image) with associated dilation of both the left and right bile ducts (curved arrows).

Fig. 2. Magnetic resonance findings of metastatic colon cancer that mimics intrahepatic cholangiocarcinoma (A,B). Two T2-weighted images show peripheral dilated left sided ducts (curved arrows in B) and a central heterogeneous left lobe mass (arrow). The presence of a second lesion (small arrow) in the liver dome is more suggestive of metastatic disease. (C) T2-weighted image obtained inferiorly shows the primary circumferential adenocarcinoma of the transverse colon (arrows).

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are malignant. Functional islet cell tumors are generally small (<2 cm) at the time of diagnosis because of clinical manifesta- tions related to hormone elaboration. Functioning islet cell tumors typically show high signal intensity on T2-weighted images and appear lower in signal intensity than surrounding pancreas on T1-weighted images. They are hypervascular and demonstrate avid enhancement on arterial phase images, although exceptions occur when the tumor demonstrates scirrhous features.

Nonfunctioning tumors are often advanced at presentation with a diameter greater than 5 cm and carry a poorer prognosis.

These are also hypervascular with enhancement characteristics similar to the functioning tumors. However, nonfunctioning tumors frequently demonstrate heterogeneous signal intensity with prominent areas of necrosis and cystic degeneration (Fig. 5).

Symptoms are related to mass effect on the pancreatic duct and adjacent organs. Hypervascular liver metastases may be identified. In contrast to pancreatic ductal adenocarcinoma, islet cell tumors less often result in pancreatic ductal obstruction, vascular encasement, vascular thrombosis, or peritoneal metastases.

7.3. CYSTIC PANCREATIC NEOPLASMS

The pseudocyst accounts for about 90% of all cystic pancreatic lesions. The remaining 10% represent cystic neoplasms. The imaging findings of pancreatitis and pseudocysts are beyond the purview of this review. However, most pseudocysts have typical imaging features and are associated with other imaging findings of pancreatitis. However, in some lesions the differentiation between a pseudocyst and cystic pancreatic neoplasm can be difficult (31).

The appearances of the various cystic neoplasms can be nonspecific, but in some cases imaging with MRI/MRCP may be able to strongly suggest a specific diagnosis. Cystic structures are well depicted on MRI/MRCP, better than on CT, with fluid demonstrating very high signal intensity on T2- and heavily T2-weighted sequences. As a result, there is excellent contrast between the fluid and the solid components of pancreatic cystic lesions. This allows for a more confident assessment of the number and size of cysts as well as definition of cyst mar- gins (32). Accurate assessment of these features is important for differentiation between serous and mucinous cystic neoplasms, with implications for patient management.

Fig. 4. Magnetic resonance cholangiopancreatography (MRCP) demonstration of the “double-duct” sign in a man with pancreatic cancer and liver metastases. (A) Coronal projection image from a MRCP shows a dilated common bile duct and pancreatic duct (arrows). The MRCP sug- gests of a diagnosis of a pancreatic head tumor. However, if interpreted in isolation, one can determine if a responsible tumor is resectable or unresectable. (B,C) Axial T1-weighted images obtained before (B) and after contrast show a T1 hypointense pancreatic cancer (arrows) in (B) that is hypoenhancing in (C). A hypovascular liver metastases establishes the presence of unresectable disease (curved arrow).

Fig. 5. Magnetic resonance demonstration of a primary nonfunctioning neuroendocrine tumor of the pancreas with metastatic disease to the liver. Axial T2-weighted image shows a heterogeneous low and high signal intensity mass (arrow) of the pancreatic neck with associated peripheral duct dilation. A similar appearing liver metastases is also revealed (curved arrow).

Fig. 6. Benign microcystic adenoma of the pancreas in an asympto- matic woman as revealed on magnetic resonance. Axial T2-weighted image shows a well-circumscribe high intensity lesion (arrow) made up of innumerable small cysts. Multiple internal septa coalesce in a central “scar” (curved arrow).

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Serous cystadenomas are benign and typically demonstrate multiple clustered cysts that measure less than 2 cm (Fig. 6).

Larger tumors may have a characteristic fibrous central scar exhibiting delayed enhancement. Serous cystadenomas are man- aged conservatively. Mucinous cystic neoplasms are typically made up of uni- or multilocular macrocysts greater than 2 cm in diameter. Invasion of surrounding structures and presence of liver metastases indicate malignancy, but otherwise, imaging features are not specific for malignant transformation of mucinous tumors. Mucinous cystic neoplasms are all considered potentially malignant and thus are potentially surgical lesions.

Less common primary cystic lesions of the pancreas include intraductal papillary mucinous tumor (IPMT) and solid and papillary epithelial neoplasm. The gold standard for diagnosis of a main branch IPMT has been ERCP, which identifies the presence of intraductal mucin with direct inspection. However, some authors suggest that MRI/MRCP is not only complemen- tary, but also superior to ERCP for evaluation of IPMT (33) (Fig. 7). Copious amounts of mucin may impede retrograde contrast injection resulting in incomplete examination at ERCP, whereas the mucin itself allows facilitates an excellent depiction of the pancreatic ducts on MRI/MRCP (34). Features that are suggestive of malignancy of IPMT on MRCP include maximum main duct diameter of 15 mm, diffuse dilation of the main pancreatic duct, and mural nodules within the duct (35). Regarding solid and papillary epithelial neoplasm, the appearance of a large well encapsulated, hemorrhagic mass in a young woman is virtually pathognomonic. The presence of hemorrhagic degeneration in these tumors is well character- ized by MRI.

8. CONCLUSIONS

MRI/MRCP has been successfully used for diagnostic evaluation of a wide variety of pancreatobiliary neoplasms. In some circumstances, it has become the study of choice, replac- ing ERCP and other imaging modalities because of its safety and accuracy. In other scenarios, MRI/MRCP has proven reli- able as a complementary or alternative imaging modality, providing additional information that determines need for treatment and directs choice of therapies. MRI/MRCP shows promise as a comprehensive “all-in-one” initial approach for diagnosis and staging of pancreatobiliary neoplasms.

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