Imaging Biliary Strictures—A Pictorial Review Sushilkumar K. Sonavane, MD,a and Christine O. Menias, MDb
The diagnosis of biliary diseases may be delayed or missed because of an unpredictable clinical course and presentation. Some biliary diseases carry the risk of morbidity and mortality and are difficult to treat. The purpose of this article is to revisit the various causes and the appearances of biliary strictures on different imaging modalities and to emphasize the role of magnetic resonance imaging (MRI) with magnetic resonance cholangiopancreatography (MRCP) in their evaluation compared with endoscopic retrograde cholangiopancreatography. MRI with MRCP is advantageous to endoscopic retrograde cholangiopancreatography for being a 1-stop shop to provide biliary, soft tissue, and vascular information that is helpful for planning intervention or surgery. Thus it serves as a superb imaging modality for the evaluation of biliary strictures.
Objective This article reviews the various causes of biliary strictures and their features on different imaging modalities with particular emphasis on magnetic resonance imaging (MRI) with magnetic resonance cholangiopancreatography (MRCP).
Introduction The diagnosis of a biliary stricture is often delayed or missed because of its indolent clinical presentation. Dilatation of the biliary ductal system should be carefully evaluated for strictures or filling defects. Biliary strictures are caused by a spectrum of benign and malignant conditions. Ultrasound (US), computed From the aDepartment of Radiology, Cardiopulmonary Radiology Section, University of Alabama at Birmingham, Birmingham, AL; and bDepartment of Radiology, Mayo Clinic, Scottsdale, Az. n Reprint requests: Sushilkumar K. Sonavane, MD, Department of Radiology, Cardiopulmonary Radiology Section, University of Alabama at Birmingham, 619 South 19th St, Birmingham, AL 35294. E-mail: [email protected] Curr Probl Diagn Radiol 2014;43:14–34. & 2013 Published by Mosby Inc. 0363-0188/$36.00 + 0 http://dx.doi.org/10.1067/j.cpradiol.2013.10.002
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tomography (CT), endoscopic retrograde cholangiopancreatography (ERCP), and percutaneous transhepatic cholangiography (PTC) have been used for evaluation of the biliary tree. However, with rapid advances in MRI techniques, MRI with MRCP is now becoming the diagnostic procedure of choice. In this review, we describe the various appearances of biliary strictures, their characteristics, and the causes that help radiologists to differentiate between benign and malignant types.
Classification The biliary strictures can be broadly categorized into benign and malignant types. Some of the frequent causes are included in Table 1. Certain characteristics might help differentiating benign from malignant types of biliary stricture and these are summarized in Table 2. Despite considerable overlap, there are some imaging features that may indicate malignant or benign features. A typical malignant stricture manifests as an irregularly shaped, eccentric narrowing with shouldering margins; whereas a benign stricture is seen as a circumferential narrowing with smooth margins and gradual transition to a normalcaliber duct.
Imaging Modalities The modalities used for imaging the biliary tree include US, CT, ERCP, PTC, MRI, and MRCP.
Ultrasound Biliary disease presents clinically with a wide range of manifestations from being asymptomatic to overt signs of biliary obstruction in the form of jaundice or elevated liver function tests. US remains the first modality of choice for evaluation of the liver and the biliary tree in these cases owing to its inherent advantages. These include ready availability, lack of ionizing radiation, and no significant patient discomfort. However, the disadvantages include potential
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TABLE 1. Causes of biliary strictures Benign
Malignant
Ampullary stenosis Inflammatory Pancreatitis Autoimmune pancreatitis-cholangitis complex (IgG4 related) Primary sclerosing cholangitis Mirizzi Syndrome Iatrogenic Anastomosis Nonanastomotic Congenital Caroli disease Extrinsic compression Portal biliopathy Lymphadenopathy Peribiliary cysts Hepatic cysts Miscellaneous Cystic fibrosis Sarcoidosis Tuberculosis Chemotherapy
Cholangiocarcinoma Gallbladder carcinoma Hepatic metastasis Pancreatic head carcinoma Periampullary carcinoma
poor or inadequate visualization of the extrahepatic biliary duct and the pancreatic duct because of a poor acoustic window and overlying bowel gas. The main role of US in the evaluation of patients with clinical cholestasis is to establish the presence of biliary ductal dilatation. In some cases, it may be possible to trace the transition point and determine the etiology.
Computed Tomography CT, being a cross-sectional imaging modality, has an advantage over US in determining the exact location, extent, and nature of biliary stricture and serves as a good roadmap for surgical planning. In cases of biliary malignancy, multiphase, contrastenhanced CT not only aids in establishing the diagnosis TABLE 2. Characteristics strictures
of
biliary
Benign
Malignant
Multiple Short or long segment Smooth margins Smooth transition No shouldering
Solitary Short segment Irregular margins Abrupt transition Shouldering of edges
These characteristics may help to differentiate benign from malignant strictures. However, these are not specific.
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FIG 1. Ampullary stenosis in a 39-year-old man with recurrent right upper quadrant pain and mildly elevated serum transaminases and alkaline phosphatase. Coronal MIP image from MRCP demonstrates a smooth, short segment stricture of the distal common bile duct with tapering margins (arrow) resulting in moderate dilatation of the extrahepatic duct and mild dilatation of the intrahepatic ducts and the pancreatic duct. No stone or mass was identified in this patient with ampullary stenosis. MIP, maximum intensity projection.
but also assesses the degree of local disease extent, lymphadenopathy, and metastasis. With multiphase CT, arterial phase (20-30 seconds) and portal venous phase (70-80 seconds) images are acquired after intravenous contrast administration. If a cholangiocarcinoma is suspected, delayed images in 10-15 minutes are obtained for evaluation of contrast retention to aid in its diagnosis and to determine the actual tumor extent. Cholangiocarcinoma, owing to its fibrous nature, tends to retain contrast on delayed sequences and become more conspicuous relative to the less enhanced hepatic parenchyma on delayed postcontrast imaging. Complications such as cholangitis (seen as biliary wall thickening and enhancement) and cholangitic abscesses are nicely depicted with CT.
Endoscopic Retrograde Cholangiopancreatography ERCP has traditionally been the gold standard for delineation of the biliary tree and evaluation of strictures. However, it is an invasive procedure that carries a complication rate of 3%-9% and mortality rate of 0.2%-0.5%.1,2 The major advantage of ERCP is to obtain tissue samples to diagnose the etiology of the biliary stricture, be it benign or malignant, and to
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FIG 2. Acute pancreatitis in a 51-year-old man. ERCP image (A) shows a long segment stricture with a smooth margin and gradual transition (arrow) involving the intrapancreatic portion of the CBD resulting in moderate dilatation of the extrahepatic biliary duct and mild dilatation of the intrahepatic ducts. Note the recent placement of pancreatic (black arrowhead) and bile (white arrowhead) duct stents. Postcontrast coronal image (B) demonstrates edema of the pancreatic head with fluid in the pancreaticoduodenal groove consistent with acute pancreatitis (black arrow).
decompress the biliary system with interventional procedures such as balloon dilatation or stent placement. The disadvantage is the inability to visualize the
adjacent soft tissue component of the stricture and many times, not being able to visualize the biliary system beyond a tight stricture.
FIG 3. Acute-on-chronic pancreatitis in a 47-year-old man. Coronary MIP image from MRCP (A) shows a smooth, segmental stricture (arrow) of the intrapancreatic portion of the common bile duct with moderate upstream dilatation of the intrahepatic and extrahepatic ducts. The dilatation, irregularity, and strictures of the main pancreatic duct and side branches can be noted, consistent with changes of chronic pancreatitis. The postgadolinium contrast-enhanced axial MR image (B) in the same patient shows mild enlargement and heterogeneous enhancement of the head of the pancreas, suggestive of acute pancreatitis. MIP, maximum intensity projection.
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FIG 4. Autoimmune pancreatitis in a 42-year-old woman who presented with epigastric pain. ERCP (A) and contrast-enhanced coronal CT (C) images show a tight, segmental stricture of the distal CBD with smooth margins and gradual cutoff in the suprapancreatic portion (arrow). Note diffuse enlargement of the pancreas without focal mass on the CT image. Contrast-enhanced axial CT image (C) shows diffuse enlargement of the entire pancreas with loss of normal lobulations giving a “sausage appearance” with a hypodense soft tissue rind (arrowhead). The patient had elevated IgG4 levels, confirming the diagnosis of autoimmune pancreatitis.
MRI with MRCP MRI-MRCP has several advantages over ERCP, which include noninvasive evaluation of the entire biliary system, including the segments proximal to a tight stricture, as well as assessment of the adjacent abdominal viscera, especially liver and pancreas. Other advantages of MRI include evaluation of the postoperative patient where cannulation of the biliary enteric anastomoses may not be feasible. MRCP has been shown to be comparable to ERCP in detecting biliary obstruction, with a sensitivity, specificity, and accuracy of 91%, 100%, and 94%, respectively.3
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Technique Recent advances in MR techniques and hardware over the last decade have revolutionized the diagnostic evaluation of the biliary system. High–field strength magnets, parallel imaging, multichannel surface coils, and respiratory gating allow improved image quality with reduced image acquisition times.4,5 Ideally, the patient fasts 3-6 hours before the procedure to increase gallbladder filling, reduce residual stomach fluid, and decrease duodenal peristalsis. Medications to reduce bowel peristalsis and increase pancreatic and biliary secretions, such as secretin, have been advocated.6 MRCP is performed with
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FIG 5. Sclerosing cholangitis-autoimmune pancreatitis complex in a 48-year-old woman who presented with jaundice. ERCP image (A) shows visualization of the peripheral intrahepatic ducts with multifocal ductal strictures and dilatations. Contrast-enhanced axial CT image (B) shows a hypodense, nonenhancing soft tissue rind around the body and tail (arrow). The patient had increased IgG4 levels on follow-up, thereby confirming her diagnosis of sclerosing cholangitis with autoimmune pancreatitis.
FIG 6. Sclerosing cholangitis in a 51-year-old man presenting with elevated levels of liver function enzymes and jaundice. ERCP (A), MRCP coronal MIP (B), and 3D volume-rendered (C) images show smoothly marginated strictures with gradual transition involving the right (thick arrow) and left hepatic ducts (thin arrow) near their confluence to the common hepatic duct obscuring visualization of the central ducts. Note the visualization of the peripheral intrahepatic ducts. MIP, maximum intensity projection.
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FIG 7. Sclerosing cholangitis and superimposed infective component in a 53-year-old man with leukocytosis and elevated levels of liver function enzymes. ERCP image (A) shows alternate areas of smooth strictures and dilatations of the intrahepatic ducts; findings of intermediate features of sclerosing cholangitis. The contrast-enhanced axial MR image (B) shows wall enhancement along the intrahepatic ducts (arrow), likely from superimposed cholangitis. Note patchy heterogeneous enhancement in the periphery of the left hepatic lobe.
FIG 8. Intermediate features of sclerosing cholangitis in a 56-year-old man with long-standing history of ulcerative colitis. ERCP (A) and MRCP coronal MIP image (B) show alternate areas of moderately tight strictures and dilatation involving the intrahepatic and extrahepatic ducts. MIP, maximum intensity projection.
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15-90 minutes to delineate the biliary tree. An advantage of this technique determining that the fluid intensity is actually within the biliary tree and not outside as seen with peribiliary cysts, abscess, bowel, or even extraluminal bile in the cases of biliary leak. The disadvantage is a relatively longer waiting time to allow sufficient biliary excretion of contrast before imaging.
FIG 9. Late features of sclerosing cholangitis in a 59-year-old man with a prolonged history of ulcerative colitis. ERCP image shows beading and diverticula involving the intrahepatic ducts due to the segmental biliary strictures.
heavily T2-weighted sequences, such as single-shot rapid acquisition with refocused echoes or half Fourier acquisition single-shot turbo spin echo, which exploit the relatively higher signal intensity of static fluid in the biliary tree.4,5 Current standard protocols acquire both thick-slab single-section and thin-slab multisection sequences. T1-weighted images are obtained before and after contrast administration in multiple phases. Newer, 3-dimensional (3D) isotropic MRCP has the advantage of thinner sections without intersection gaps compared with 2D MRCP.7 The disadvantage is longer acquisition times compared with 2D MRCP, even with use of parallel imaging. Respiratory triggering can be used in patients who are unable to hold their breath for a longer time. Secondary to longer acquisition times, there are more blurring and ghosting artifacts observed. Contrast-enhanced MRCP is performed by using the property of predominant biliary excretion of some contrast agents such as gadoxetate disodium or Gd-EOB-DTPA (Eovist or Primovist; Bayer Healthcare, Leverkusen, Germany), or Gd-BOPTA (MultiHance, Bracco Diagnostics).8 These hepatocytespecific contrast agents increase the T1 relaxation time of bile with resultant higher signal intensity on T1-weighted imaging. Depending on the drug pharmacokinetics, imaging with single–breath hold 3D gradient-recalled echo sequence can be performed in
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Postprocessing Multiplanar reformats, standard or curved, that are defined by the centerline of a tubular structure are an easy way to begin evaluation after reviewing the axial data set. Maximum intensity projection images obtained from thin-section MRCP data set provide images comparable to ERCP. Smaller filling defects may not be visualized. Performing subvolume maximum intensity projection images may minimize this disadvantage. Minimum intensity projection images may be obtained demonstrating the relatively dark biliary tree compared with the enhancing surrounding structures especially on CT and postcontrast MR.9 Additionally, volume-rendered images of the biliary tree are used to increase reader confidence.
Percutaneous Transhepatic Cholangiography At present, the role of PTC is reserved as a therapeutic option to decompress the biliary tree in difficult cases. For cases where navigation of the biliary stricture is difficult with ERCP, PTC can be used for therapeutic purposes of biliary drainage and stent placement. Benign Biliary Strictures Ampullary Stenosis. This is a benign condition, a result of functional dysfunction of the sphincter of Oddi. The patient may present with recurrent biliary colic and mildly elevated levels of liver enzymes. On MRCP, it is seen as a tight narrowing of the distal common bile duct (CBD) with mild upstream dilatation of the CBD and the pancreatic ducts in the absence of an underlying cause like a mass or a stone (Fig 1). On ERCP, there is delayed contrast drainage from a mildly dilated pancreatic and CBD. In equivocal cases, pressure manometry at the sphincter may establish the diagnosis.10 Endoscopic sphincterotomy can offer a good clinical response.10 Pancreatitis. In acute pancreatitis, the edema and inflammation causes mass effect on the intrapancreatic
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FIG 10. Mirizzi syndrome in a 38-year-old woman who presented with biliary colic and jaundice. Coronal MIP image from MRCP (A) shows a stricture involving the proximal hepatic duct (arrowhead), mild intrahepatic ductal dilatation, and marked distension of the gallbladder. T2 HASTE axial (B) and coronal (C) images show a low signal intensity focus in the gallbladder neck (arrow), consistent with a stone. ERCP image (D) demonstrates the common hepatic duct stricture due to extrinsic mass effect and resultant intrahepatic ductal dilatation from impacted stone in the gallbladder neck (arrow). HASTE, half Fourier acquisition single-shot turbo spin echo; MIP, maximum intensity projection.
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FIG 11. Biliary anastomotic stricture in a 58-year-old man with a history of liver transplant and elevated levels of liver function enzymes 2 years before presentation. A coronal MIP MRCP image (A) and an ERCP (B) image show a focal stricture at the bile duct anastomosis (arrow) resulting in mild upstream extrahepatic and intrahepatic ductal dilatation. The stricture was subsequently dilated and treated with stent placement (not shown). MIP, maximum intensity projection.
portion of the CBD with upstream dilatation (Figs 2 and 3). In chronic pancreatitis, the biliary strictures are secondary to recurrent inflammation, subsequent fibrosis, or extrinsic compression from pseudocysts. Cross-sectional imaging with CT or MRI aids in the diagnosis by demonstrating evidence of pancreatitis in the form of parenchymal atrophy, pancreatic ductal dilatation, pseudocysts, and pancreatic calcifications. The causative factor such as obstruction of the distal CBD from stone, fibrosis, or mass is also better evaluated with cross-sectional imaging. Autoimmune Pancreatitis (IgG4 Sclerosing Disease).
Immune-mediated inflammation of the pancreas results in this form of pancreatitis, which results in a benign-appearing distal CBD stricture.11,12 The specific laboratory abnormality observed is elevation of the serum IgG4 levels and the presence of serum autoantibodies such as antinuclear antibody and rheumatoid arthritis factor. The imaging features on MRI or CT (Fig 4) are edema of the pancreas with loss of its normal lobulations, which results in a “sausageshaped” appearance of the pancreas, as well as a hypodense hypointense peripancreatic rind of soft tissue with or without faint delayed enhancement.12 In late cases, involution of the tail of the pancreas can be observed.11,12
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A course of corticosteroids treatment may offer relief of symptoms.13 Autoimmune Pancreatitis and Sclerosing Cholangitis Syndrome. As the immune-mediated inflammatory
process can involve both the pancreatic and biliary ducts, these may be seen in conjunction (Fig 5). Variable degree of associated intra and extra hepatic ductal involvement may be seen less frequently. sclerosing cholangitis (PSC) is a sequela of chronic inflammation and fibrosis of the intrahepatic and extrahepatic bile ducts that occurs more frequently in middle-aged individuals (40-50 years) and in men, and is associated with inflammatory bowel disease (70%),14 most commonly ulcerative colitis.15 Several other autoimmune diseases are observed with increased frequency in these patients.16 The early imaging features on ERCP or MRCP are visualization of the peripheral bile ducts and central prominence of the bile ducts with peripheral pruning (Fig 6). The intermediate features are multiple, short segment (1-2 cm) strictures or stenoses with intervening dilated segments giving a beaded appearance (Figs 7 and 8). Biliary diverticula and webs are seen as late features (Fig 9), being the result of progressive fibrosis, biliary stasis, and recurrent infections.14 Primary
Sclerosing
Cholangitis. Primary
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FIG 12. Biliary ischemic strictures in a 51-year-old man following liver transplant 48 hours before presentation with leukocytosis and increased liver function tests. Coronal MIP MRCP (A) and ERCP (B) showing extensive strictures, dilatations, and bile leaks along the intrahepatic and extrahepatic ducts, features of biliary necrosis. Axial postcontrast MR angiogram image (C) at the level of the celiac artery shows a signal void in the hepatic artery consistent with thrombosis (arrow). MIP, maximum intensity projection.
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neck or in the cystic duct with upstream dilatation of the common hepatic and the intra hepatic ducts. The common bile duct is normal in caliber. Combined CT and MRI has been reported to have a sensitivity of 96%, specificity of 93.5%, and accuracy of 94%.21 The erosion of the gallstone into the common hepatic duct is a known complication in this condition, and accordingly, the Mirizzi syndrome is classified in 4 types.22 Surgical exploration and cholecystectomy is the definitive treatment. Iatrogenic. Iatrogenic bile duct injury is the most common cause of postoperative biliary strictures, accounting for up to 80% of cases in some studies.23 FIG 13. Recurrent sclerosing cholangitis in a 57-year-old man with history of liver transplant for PSC performed 7 years before presentation. Coronal MIP MRCP image shows strictures of the extrahepatic duct (arrow) and visualization of the peripheral intrahepatic ducts consistent with recurrent PSC. MIP, maximum intensity projection.
Other associated findings seen are increased T2 signal intensity around the portal tracts (periportal edema), patchy areas of peripheral arterial enhancement, prominent periportal lymph nodes, and changes of cirrhosis in advanced stages.17,18 MRCP has a sensitivity of 80%-88% and specificity of 87%-99%.19 Clinically, these patients have a protracted course with symptoms of fatigue, weight loss, fever, and cholestatic features of intermittent jaundice and pruritus. The complications with this condition are biliary stasis leading to recurrent infections, stone formation, and ultimately, hepatic failure. There is an increased risk for cholangiocarcinoma of 1.5% per year.14 Though palliative balloon dilatation of symptomatic biliary stricture, ursodeoxycholic acid, and immunosuppressive drugs have been tried, the ultimate treatment is liver transplantation.20 MRI with MRCP serves as the imaging modality of choice not only to diagnose the condition but also for surveillance of complications, particularly cholangiocarcinoma. Mirizzi Syndrome. Mirizzi syndrome is characterized by obstruction of the common hepatic duct due to mechanical compression, with or without inflammation, from an impacted stone in the gallbladder neck or cystic duct. It is seen with increased incidence in patients with a low insertion of the cystic duct (Fig 10). The findings of Mirizzi syndrome include impacted stone at the gallbladder
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Postcholecystectomy. Ligation of cystic duct close to the hepatic duct or inadvertent ligation of the hepatic duct or CBD during surgery is the most common cause. Transplant Strictures. Orthotopic liver transplant is an increasingly recognized cause of biliary stricture. This can be further divided into anastomotic and nonanastomotic categories.24 The anastomotic stricture results from fibrotic proliferation rather than ischemia and is seen as a late complication. The predisposing factors include ductal mismatch between donor and recipient common duct and suture retraction24 (Fig 11). The nonanastomotic strictures usually result from ischemia and are seen in the early postoperative period.24 In a posttransplant liver, the hepatic artery is the only source of blood supply to the biliary tree. So hepatic artery thrombosis, stenosis, or preservation injury can lead to biliary tree ischemia and intrahepatic bilomas, with subsequent inflammation and fibrosis, resulting in strictures (Fig 12). These are multiple, variable sized, randomly distributed strictures (over the territory of ischemia) that typically start near the hilum and progressively involve the intrahepatic ducts. Other less common causes of nonanastomotic biliary strictures after orthotopic liver transplant are infection or preexisting biliary disease (Fig 13). Post–Liver
Caroli Disease. Caroli disease is a congenital autosomal recessive condition resulting in segmental (83%) or diffuse (17%), cystic or saccular intrahepatic ductal dilatation that present at middle age (30-40 years).25 The classic imaging feature is the central
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FIG 14. Caroli disease in a 9-year-old girl. ERCP (A) and coronary MIP MRCP (B) images show extensive saccular dilatations of the intrahepatic ducts with a normal extrahepatic duct. Axial contrast-enhanced MR images (C and D) confirm the cholangiographic findings with a “central dot” sign corresponding to the central enhancing hepatic artery and portal vein branches (circle). MIP, maximum intensity projection.
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FIG 15. Portal vein cavernoma causing extrinsic stricture in a 45-year-old man who presented with jaundice. Coronal MIP MRCP (A) and ERCP (B) images show a smooth abrupt stricture of the middle common bile duct (arrowhead) resulting in proximal ductal dilatation. Axial contrastenhanced MR images (C and D) demonstrate cavernous transformation of the portal vein with a large collateral vessel causing an extrinsic effect and focal stricture of the proximal CBD (arrow). Note the gallbladder wall varices, a feature associated with cavernous transformation (thin arrow). MIP, maximum intensity projection.
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FIG 16. Peribiliary cysts with extrinsic biliary stricture in a 58-year-old man with cirrhosis. ERCP (A) shows alternate areas of intrahepatic duct strictures and dilatations mimicking sclerosing cholangitis. Note the normal extrahepatic duct. Coronal MIP image from MRCP (B) shows multiple large, round, tubular cysts obscuring the biliary system (arrowhead). Note the disparity between the biliary tree dilatation on ERCP and MRCP. Axial contrast-enhanced MR images (C and D) demonstrate multiple cystic structures along the course of the intrahepatic biliary tree resulting in extrinsic mass impressions on the bile ducts. Note the cirrhotic appearance of the liver. MIP, maximum intensity projection.
fibrovascular bundle of hepatic artery and portal vein branches surrounded by dilated intrahepatic bile ducts referred to as “central dot sign”24 (Fig 14). The complications are stones, recurrent cholangitis, liver fibrosis, cirrhosis, and cholangiocarcinoma (7%).25 Compression. Structures surrounding the biliary tree when enlarged can lead to benign strictures from extrinsic compression, for example, portal cavernomas (portal biliopathy)26 (Fig 15), lymph nodes, vessels, hepatic cysts, and peribiliary cysts (Fig 16).
Extrinsic
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Miscellaneous Causes. Rare causes of benign biliary strictures include sarcoidosis, tuberculosis, radiation, chemotherapy, vasculitis, cystic fibrosis, eosinophilic cholangitis, and xanthogranulomatous cholangitis.
Malignant Biliary Strictures Cholangiocarcinoma. Cholangiocarcinoma is a malig-
nant neoplasm of the biliary tree. There are 3 types of cholangiocarcinomas depending on the morphologic appearance: mass forming, periductal infiltrating, and intraductal growing.27,28 The risk factors for the
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FIG 17. Klatskin tumor in a 61-year-old woman. Coronal MIP MRCP (A) and ERCP (B) images demonstrate a high-grade, short segment stricture with shouldering margins (arrow) at the confluence of the right and left hepatic ducts with extension into the proximal common hepatic duct. Ultrasound image (C) shows an ill-defined isoechoic mass (arrowhead) at the corresponding area of the malignant stricture. Delayed postcontrast axial MR image (D) shows a soft tissue mass with retention of contrast characteristic of the fibrous tumor matrix of cholangiocarcinoma (arrowhead). MIP, maximum intensity projection.
development of cholangiocarcinoma include inflammatory bowel disease (ulcerative colitis and PSC spectrum), biliary parasites, and choledochal cysts.27,28 The most common site of involvement is the confluence of the right and left hepatic ducts called a Klatskin or hilar cholangiocarcinoma (50%-60%) (Fig 17). The
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next common site is the extrahepatic duct (30%-35%) with intrahepatic being the least common site (10%). On imaging, these can be seen as malignant strictures with upstream biliary ductal dilatation. Often, with the periductal variant, it is difficult to perceive a mass lesion of cholangiocarcinoma (Fig 18). Owing to the predominant fibrous tissue component of Curr Probl Diagn Radiol, January/February 2014
FIG 18. Cholangiocarcinoma (periductal infiltrating type) in a 65-year-old woman who presented with jaundice and elevated liver function tests. ERCP (A) and coronal MIP MRCP (B) images show an abrupt, high-grade stricture of the middle common bile duct (arrow) with shouldering margins. Proximal ductal dilatation is less prominent because of the placement of the stent across the stricture. Delayed postcontrast axial MR shows an illdefined, circumferential area of contrast retention in the area of ductal stricture (circle). MIP, maximum intensity projection.
cholangiocarcinoma, delayed contrast enhancement (typically beyond 5-10 minutes) is observed. Gallbladder Carcinoma. Adenocarcinoma of the gallbladder accounts for more than 90% of gallbladder malignancies29 and commonly affects females (M:F ¼ 1:3), with a mean age of 72 years. Risk factors
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implicated in the development of gallbladder cancer include chronic cholecystitis, gallstones, porcelain gallbladder (20%), and PSC.29 The various imaging features of gallbladder carcinoma include an intraluminal polypoidal mass, focal or diffuse gallbladder wall thickening, and a mass
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FIG 19. Gallbladder cancer spreading along the cystic duct and involving the middle CBD in a 58-year-old woman who presented with RUQ pain. Coronal MIP MRCP image (A) demonstrates an abrupt, high-grade stricture in the middle common duct (arrow) with proximal ductal dilatation. The middle and distal common bile ducts are normal. Ultrasound image (B) shows a large nondependent soft tissue mass arising from the gallbladder fundus (white arrowhead). Contrast-enhanced transaxial CT image (C) again shows the heterogeneously enhancing gallbladder fundal mass (white arrowhead) invading the adjacent liver (black arrowhead) and growing along the cystic duct to involve the common hepatic duct (black arrow). MIP, maximum intensity projection; RUQ, right upper quadrant.
replacing the gallbladder fossa. The spread of tumor can be via direct extension into the adjacent liver parenchyma or through the hepatoduodenal ligament and transverse mesocolon. The growth along the cystic duct with progressive involvement of common duct leads to an isolated “mid-CBD stricture” that is a characteristic late finding of this entity. The 30
differential for a mid-CBD malignant stricture includes cholangiocarcinoma and metastases (Fig 19). Liver Metastases. Diffuse hepatic metastases can lead
to multifocal strictures of the intrahepatic ducts primarily from extrinsic compression and from contiguous involvement. Metastases from colorectal
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FIG 20. Hepatic metastases from colon cancer causing extrinsic biliary strictures in a 60-year-old man who presented with right upper quadrant pain. Coronal MIP MRCP (A) and ERCP (B) images demonstrate multiple smooth strictures of the intrahepatic ducts due to extrinsic impressions. Note the normal extrahepatic duct. Postcontrast axial liver MR image in portal venous phase (C) shows multiple round, low–signal intensity hepatic metastases (arrowhead). MIP, maximum intensity projection.
carcinoma are the most common cause of metastatic malignant biliary strictures.30 The features on ERCP and MRCP include smooth or irregular intrahepatic ductal strictures depending on the site and degree of compression (Figs 20 and 21) with upstream dilatation of the biliary tree associated with the masses seen on cross-sectional imaging. Pancreatic Carcinoma. Pancreatic carcinoma is the
second most common GI malignancy and accounts
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for 85%-90% of all pancreatic neoplasms.31 The most common site of occurrence of pancreatic adenocarcinoma is the head of pancreas (60%). The various classic signs described include the “double duct sign”30—dilatation of both the pancreatic and the CBDs from a focal T1 hypointense, hypovascular mass. There is a variable degree of parenchymal atrophy involving the body and tail of the pancreas (Fig 22). There is an abrupt termination of the distal common duct with upstream dilatation. Periampullary
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FIG 21. Hepatic metastases from colon cancer causing extensive biliary strictures in a 55-year-old man with a history of sigmoid adenocarcinoma. Coronal MIP MRCP (A) image shows diffuse right and left intrahepatic ductal dilatation with an abrupt cutoff near the confluence of the right and left hepatic ducts. The middle and distal CBDs are normal in caliber (arrowhead); an appearance similar to Klatskin-type cholangiocarcinoma. Contrast-enhanced axial liver MR image (B) shows multiple heterogeneously enhancing hepatic metastases, the largest one at the confluence of the hepatic ducts (arrow). MIP, maximum intensity projection.
FIG 22. Pancreatic adenocarcinoma in a 63-year-old man who presented with weight loss and epigastric pain. ERCP (A) shows diffuse pancreatic (thin arrow) and common bile (thick arrow) ductal dilatation to the level of the ampulla producing the “double duct” sign. Contrast-enhanced axial CT image (B) depicts a hypovascular mass in the pancreatic head (arrowhead).
carcinoma and duodenal adenocarcinoma may also result in the “double duct” sign (Fig 23).
Conclusion In comparison with ERCP, MRI with MRCP has the advantages of being noninvasive, without ionizing
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radiation and offers additional soft tissue information that is essential in determining the etiology of the biliary strictures. The imaging appearance may help to differentiate between benign and malignant strictures; however, cytologic studies are needed in equivocal cases. For diagnosis and surveillance of biliary strictures MRCP is comparable to ERCP and the latter
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FIG 23. Periampullary carcinoma in a 58-year-old woman who presented with jaundice and abdominal pain. 3D volume-rendered MRCP image (A) shows a “double duct” sign with diffuse pancreatic (thin arrow) and common bile ducts (thick arrow) to the level of the ampulla. Contrastenhanced axial MR image (B) demonstrates soft tissue thickening and heterogeneous enhancement of the second portion of the duodenum (arrowhead).
should be reserved for interventional procedures such as tissue sampling, balloon dilatation, or stent placement.
REFERENCES 1. Hekimoglu K, Ustundag Y, Dusak A, et al. MRCP vs. ERCP in the evaluation of biliary pathologies: review of current literature. J Dig Dis 2008;9:162-9. 2. Yeh BM, Liu PS, Soto JA, et al. MR imaging and CT of the biliary tract. Radiographics 2009;29:1669-88. 3. Guibaud L, Bret PM, Reinhold C, et al. Bile duct obstruction and choledocholithiasis: diagnosis with MR cholangiography. Radiology 1995;197:109-15. 4. Choi JY, Lee JM, Lee JY, et al. Navigator-triggered isotropic three-dimensional magnetic resonance cholangiopancreatography in the diagnosis of malignant biliary obstructions: comparison with direct cholangiography. J Magn Reson Imaging 2008;27:94-101. 5. Vitellas KM, Keogan MT, Spritzer CE, et al. MR cholangiopancreatography of bile and pancreatic duct abnormalities with emphasis on the single-shot fast spin-echo technique. Radiographics 2000;20:939-57 [quiz, 1107-1108, 1112]. 6. Halefoglu AM. Magnetic resonance cholangiopancreatography: a useful tool in the evaluation of pancreatic and biliary disorders. World J Gastroenterol 2007;13:2529-34. 7. Sodickson A, Mortele KJ, Barish MA, et al. Threedimensional fast-recovery, fast spin-echo MRCP: comparison with two-dimensional single-shot fast spin-echo techniques. Radiology 2006;238:549-59. 8. Yeh BM, Breiman RS, Taouli B, et al. Biliary tract depiction in living potential liver donors: comparison of conventional MR, mangafodipir trisodium–enhanced excretory MR, and multi–detector row CT cholangiography—initial experience. Radiology 2004;230:645-51.
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9. Kim HC, Yang DM, Jin W, et al. Multiplanar reformations and minimum intensity projections using multi-detector row CT for assessing anomalies and disorders of the pancreaticobiliary tree. World J Gastroenterol 2007;13:4177-84. 10. Soper NJ, Swanstrom LL, Eubanks WS. Mastery of Endoscopic and Laparoscopic Surgery. 3rd ed. Philadelphia: Lippincott Williams & Wilkins, 295. 11. Bodily KD, Takahashi N, Fletcher JG, et al. Autoimmune pancreatitis: pancreatic and extrapancreatic imaging findings. Am J Roentgenol 2009;192:431-7. 12. Naitoh I, Nakazawa T, Ohara H, et al. Clinical significance of extrapancreatic lesions in autoimmune pancreatitis. Pancreas 2010;39:e1-5. 13. Kamisawa T, Takeuchi T. Treatment of autoimmune pancreatitis with the anecdotes of the first report. Int J Rheumatol 2012;2012:597643. 14. Menias CO, Surabhi VR, Prasad SR, et al. Mimics of cholangiocarcinoma: spectrum of disease. Radiographics 2008;28:1115-29. 15. Chapman RW. The colon and PSC: new liver, new danger? Gut 1998;43:595-6. 16. Saarinen S, Olerup O, Broome U. Increased frequency of autoimmune diseases in patients with primary sclerosing cholangitis. Am J Gastroenterol 2000;95:3195-9. 17. Bader TR, Beavers KL, Semelka RC. MR imaging features of primary sclerosing cholangitis: patterns of cirrhosis in relationship to clinical severity of disease. Radiology 2003;226: 675-85. 18. Dodd GD III, Baron RL, Oliver JH III, et al. End-stage primary ssclerosing cholangitis: CT findings of hepatic morphology in 36 patients. Radiology 1999;211:357-62. 19. Fulcher AS, Turner MA, Franklin KJ, et al. Primary sclerosing cholangitis: evaluation with MR cholangiography—a case-control study. Radiology 2000;215:71-80.
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20. Baluyut AR, Sherman S, Lehman GA, et al. Impact of endoscopic therapy on the survival of patients with primary sclerosing cholangitis. Gastrointest Endosc 2001;53:308-12. 21. Yun EJ, Choi CS, Yoon DY, et al. Combination of magnetic resonance cholangiopancreatography and computed tomography for preoperative diagnosis of the mirizzi syndrome. J Comput Assist Tomogr 2009;33:636-40. 22. Csendes A, Diaz JC, Burdiles P, et al. Syndrome and cholecystobiliary fistula: a unifying classification. Br J Surg 1989;76:1139-43. 23. Martin RF, Rossi RL. Bile duct injuries: spectrum, mechanisms of injury, and their prevention. Surg Clin North Am 1994;74:781-803 [discussion, 805-807]. 24. Hoeffel C, Azizi L, Lewin M, et al. Normal and pathologic features of the postoperative biliary tract at 3D MR cholangiopancreatography and MR imaging. Radiographics 2006;26:1603-20. 25. Miller WJ, Sechtin AG, Campbell WL. Imaging findings in Caroli's disease. Am J Roentgenol 1995;165:333-7.
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26. Chandra R, Kapoor D, Tharakan A, et al. Portal biliopathy. J Gastroenterol Hepatol 2001;16:1086-92. 27. Choi J-Y, Kim M-J, Lee JM. Hilar cholangiocarcinoma: role of preoperative imaging with sonography, MDCT, MRI, and direct cholangiography. Am J Roentgenol 2008;191: 1448-57. 28. Sainani Nisha I, Onofrio A, et al. Cholangiocarcinoma: current and novel imaging techniques. Radiographics 2008;28: 1263-87. 29. Catalano OA, Sahani DV, Kalva SP, et al. MR imaging of the gallbladder: a pictorial essay. Radiographics 2008;28:135-55. 30. Kartik S, Jhaveri KS, Halankar J, et al. Intrahepatic bile duct dilatation due to liver metastases from colorectal carcinoma. Am J Roentgenol 2009;193:752-6. 31. Freeny PC, Bilbao MK, Katon RM. “Blind” evaluation of endoscopic retrograde cholangiopancreatography (ERCP) in the diagnosis of pancreatic carcinoma: the “double duct” and other signs. Radiology 1976;119:271-4.
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The diagnosis of biliary diseases may be delayed or missed because of an unpredictable clinical course and presentation. Some biliary diseases carry the risk of morbidity and mortality and are difficult to treat. The purpose of this article is to revisit the various causes and the appearances of biliary strictures on different imaging modalities and to emphasize the role of magnetic resonance imaging (MRI) with magnetic resonance cholangiopancreatography (MRCP) in their evaluation compared with endoscopic retrograde cholangiopancreatography. MRI with MRCP is advantageous to endoscopic retrograde cholangiopancreatography for being a 1-stop shop to provide biliary, soft tissue, and vascular information that is helpful for planning intervention or surgery. Thus it serves as a superb imaging modality for the evaluation of biliary strictures.
Objective This article reviews the various causes of biliary strictures and their features on different imaging modalities with particular emphasis on magnetic resonance imaging (MRI) with magnetic resonance cholangiopancreatography (MRCP).
Introduction The diagnosis of a biliary stricture is often delayed or missed because of its indolent clinical presentation. Dilatation of the biliary ductal system should be carefully evaluated for strictures or filling defects. Biliary strictures are caused by a spectrum of benign and malignant conditions. Ultrasound (US), computed From the aDepartment of Radiology, Cardiopulmonary Radiology Section, University of Alabama at Birmingham, Birmingham, AL; and bDepartment of Radiology, Mayo Clinic, Scottsdale, Az. n Reprint requests: Sushilkumar K. Sonavane, MD, Department of Radiology, Cardiopulmonary Radiology Section, University of Alabama at Birmingham, 619 South 19th St, Birmingham, AL 35294. E-mail: [email protected] Curr Probl Diagn Radiol 2014;43:14–34. & 2013 Published by Mosby Inc. 0363-0188/$36.00 + 0 http://dx.doi.org/10.1067/j.cpradiol.2013.10.002
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tomography (CT), endoscopic retrograde cholangiopancreatography (ERCP), and percutaneous transhepatic cholangiography (PTC) have been used for evaluation of the biliary tree. However, with rapid advances in MRI techniques, MRI with MRCP is now becoming the diagnostic procedure of choice. In this review, we describe the various appearances of biliary strictures, their characteristics, and the causes that help radiologists to differentiate between benign and malignant types.
Classification The biliary strictures can be broadly categorized into benign and malignant types. Some of the frequent causes are included in Table 1. Certain characteristics might help differentiating benign from malignant types of biliary stricture and these are summarized in Table 2. Despite considerable overlap, there are some imaging features that may indicate malignant or benign features. A typical malignant stricture manifests as an irregularly shaped, eccentric narrowing with shouldering margins; whereas a benign stricture is seen as a circumferential narrowing with smooth margins and gradual transition to a normalcaliber duct.
Imaging Modalities The modalities used for imaging the biliary tree include US, CT, ERCP, PTC, MRI, and MRCP.
Ultrasound Biliary disease presents clinically with a wide range of manifestations from being asymptomatic to overt signs of biliary obstruction in the form of jaundice or elevated liver function tests. US remains the first modality of choice for evaluation of the liver and the biliary tree in these cases owing to its inherent advantages. These include ready availability, lack of ionizing radiation, and no significant patient discomfort. However, the disadvantages include potential
Curr Probl Diagn Radiol, January/February 2014
TABLE 1. Causes of biliary strictures Benign
Malignant
Ampullary stenosis Inflammatory Pancreatitis Autoimmune pancreatitis-cholangitis complex (IgG4 related) Primary sclerosing cholangitis Mirizzi Syndrome Iatrogenic Anastomosis Nonanastomotic Congenital Caroli disease Extrinsic compression Portal biliopathy Lymphadenopathy Peribiliary cysts Hepatic cysts Miscellaneous Cystic fibrosis Sarcoidosis Tuberculosis Chemotherapy
Cholangiocarcinoma Gallbladder carcinoma Hepatic metastasis Pancreatic head carcinoma Periampullary carcinoma
poor or inadequate visualization of the extrahepatic biliary duct and the pancreatic duct because of a poor acoustic window and overlying bowel gas. The main role of US in the evaluation of patients with clinical cholestasis is to establish the presence of biliary ductal dilatation. In some cases, it may be possible to trace the transition point and determine the etiology.
Computed Tomography CT, being a cross-sectional imaging modality, has an advantage over US in determining the exact location, extent, and nature of biliary stricture and serves as a good roadmap for surgical planning. In cases of biliary malignancy, multiphase, contrastenhanced CT not only aids in establishing the diagnosis TABLE 2. Characteristics strictures
of
biliary
Benign
Malignant
Multiple Short or long segment Smooth margins Smooth transition No shouldering
Solitary Short segment Irregular margins Abrupt transition Shouldering of edges
These characteristics may help to differentiate benign from malignant strictures. However, these are not specific.
Curr Probl Diagn Radiol, January/February 2014
FIG 1. Ampullary stenosis in a 39-year-old man with recurrent right upper quadrant pain and mildly elevated serum transaminases and alkaline phosphatase. Coronal MIP image from MRCP demonstrates a smooth, short segment stricture of the distal common bile duct with tapering margins (arrow) resulting in moderate dilatation of the extrahepatic duct and mild dilatation of the intrahepatic ducts and the pancreatic duct. No stone or mass was identified in this patient with ampullary stenosis. MIP, maximum intensity projection.
but also assesses the degree of local disease extent, lymphadenopathy, and metastasis. With multiphase CT, arterial phase (20-30 seconds) and portal venous phase (70-80 seconds) images are acquired after intravenous contrast administration. If a cholangiocarcinoma is suspected, delayed images in 10-15 minutes are obtained for evaluation of contrast retention to aid in its diagnosis and to determine the actual tumor extent. Cholangiocarcinoma, owing to its fibrous nature, tends to retain contrast on delayed sequences and become more conspicuous relative to the less enhanced hepatic parenchyma on delayed postcontrast imaging. Complications such as cholangitis (seen as biliary wall thickening and enhancement) and cholangitic abscesses are nicely depicted with CT.
Endoscopic Retrograde Cholangiopancreatography ERCP has traditionally been the gold standard for delineation of the biliary tree and evaluation of strictures. However, it is an invasive procedure that carries a complication rate of 3%-9% and mortality rate of 0.2%-0.5%.1,2 The major advantage of ERCP is to obtain tissue samples to diagnose the etiology of the biliary stricture, be it benign or malignant, and to
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FIG 2. Acute pancreatitis in a 51-year-old man. ERCP image (A) shows a long segment stricture with a smooth margin and gradual transition (arrow) involving the intrapancreatic portion of the CBD resulting in moderate dilatation of the extrahepatic biliary duct and mild dilatation of the intrahepatic ducts. Note the recent placement of pancreatic (black arrowhead) and bile (white arrowhead) duct stents. Postcontrast coronal image (B) demonstrates edema of the pancreatic head with fluid in the pancreaticoduodenal groove consistent with acute pancreatitis (black arrow).
decompress the biliary system with interventional procedures such as balloon dilatation or stent placement. The disadvantage is the inability to visualize the
adjacent soft tissue component of the stricture and many times, not being able to visualize the biliary system beyond a tight stricture.
FIG 3. Acute-on-chronic pancreatitis in a 47-year-old man. Coronary MIP image from MRCP (A) shows a smooth, segmental stricture (arrow) of the intrapancreatic portion of the common bile duct with moderate upstream dilatation of the intrahepatic and extrahepatic ducts. The dilatation, irregularity, and strictures of the main pancreatic duct and side branches can be noted, consistent with changes of chronic pancreatitis. The postgadolinium contrast-enhanced axial MR image (B) in the same patient shows mild enlargement and heterogeneous enhancement of the head of the pancreas, suggestive of acute pancreatitis. MIP, maximum intensity projection.
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Curr Probl Diagn Radiol, January/February 2014
FIG 4. Autoimmune pancreatitis in a 42-year-old woman who presented with epigastric pain. ERCP (A) and contrast-enhanced coronal CT (C) images show a tight, segmental stricture of the distal CBD with smooth margins and gradual cutoff in the suprapancreatic portion (arrow). Note diffuse enlargement of the pancreas without focal mass on the CT image. Contrast-enhanced axial CT image (C) shows diffuse enlargement of the entire pancreas with loss of normal lobulations giving a “sausage appearance” with a hypodense soft tissue rind (arrowhead). The patient had elevated IgG4 levels, confirming the diagnosis of autoimmune pancreatitis.
MRI with MRCP MRI-MRCP has several advantages over ERCP, which include noninvasive evaluation of the entire biliary system, including the segments proximal to a tight stricture, as well as assessment of the adjacent abdominal viscera, especially liver and pancreas. Other advantages of MRI include evaluation of the postoperative patient where cannulation of the biliary enteric anastomoses may not be feasible. MRCP has been shown to be comparable to ERCP in detecting biliary obstruction, with a sensitivity, specificity, and accuracy of 91%, 100%, and 94%, respectively.3
Curr Probl Diagn Radiol, January/February 2014
Technique Recent advances in MR techniques and hardware over the last decade have revolutionized the diagnostic evaluation of the biliary system. High–field strength magnets, parallel imaging, multichannel surface coils, and respiratory gating allow improved image quality with reduced image acquisition times.4,5 Ideally, the patient fasts 3-6 hours before the procedure to increase gallbladder filling, reduce residual stomach fluid, and decrease duodenal peristalsis. Medications to reduce bowel peristalsis and increase pancreatic and biliary secretions, such as secretin, have been advocated.6 MRCP is performed with
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FIG 5. Sclerosing cholangitis-autoimmune pancreatitis complex in a 48-year-old woman who presented with jaundice. ERCP image (A) shows visualization of the peripheral intrahepatic ducts with multifocal ductal strictures and dilatations. Contrast-enhanced axial CT image (B) shows a hypodense, nonenhancing soft tissue rind around the body and tail (arrow). The patient had increased IgG4 levels on follow-up, thereby confirming her diagnosis of sclerosing cholangitis with autoimmune pancreatitis.
FIG 6. Sclerosing cholangitis in a 51-year-old man presenting with elevated levels of liver function enzymes and jaundice. ERCP (A), MRCP coronal MIP (B), and 3D volume-rendered (C) images show smoothly marginated strictures with gradual transition involving the right (thick arrow) and left hepatic ducts (thin arrow) near their confluence to the common hepatic duct obscuring visualization of the central ducts. Note the visualization of the peripheral intrahepatic ducts. MIP, maximum intensity projection.
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Curr Probl Diagn Radiol, January/February 2014
FIG 7. Sclerosing cholangitis and superimposed infective component in a 53-year-old man with leukocytosis and elevated levels of liver function enzymes. ERCP image (A) shows alternate areas of smooth strictures and dilatations of the intrahepatic ducts; findings of intermediate features of sclerosing cholangitis. The contrast-enhanced axial MR image (B) shows wall enhancement along the intrahepatic ducts (arrow), likely from superimposed cholangitis. Note patchy heterogeneous enhancement in the periphery of the left hepatic lobe.
FIG 8. Intermediate features of sclerosing cholangitis in a 56-year-old man with long-standing history of ulcerative colitis. ERCP (A) and MRCP coronal MIP image (B) show alternate areas of moderately tight strictures and dilatation involving the intrahepatic and extrahepatic ducts. MIP, maximum intensity projection.
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15-90 minutes to delineate the biliary tree. An advantage of this technique determining that the fluid intensity is actually within the biliary tree and not outside as seen with peribiliary cysts, abscess, bowel, or even extraluminal bile in the cases of biliary leak. The disadvantage is a relatively longer waiting time to allow sufficient biliary excretion of contrast before imaging.
FIG 9. Late features of sclerosing cholangitis in a 59-year-old man with a prolonged history of ulcerative colitis. ERCP image shows beading and diverticula involving the intrahepatic ducts due to the segmental biliary strictures.
heavily T2-weighted sequences, such as single-shot rapid acquisition with refocused echoes or half Fourier acquisition single-shot turbo spin echo, which exploit the relatively higher signal intensity of static fluid in the biliary tree.4,5 Current standard protocols acquire both thick-slab single-section and thin-slab multisection sequences. T1-weighted images are obtained before and after contrast administration in multiple phases. Newer, 3-dimensional (3D) isotropic MRCP has the advantage of thinner sections without intersection gaps compared with 2D MRCP.7 The disadvantage is longer acquisition times compared with 2D MRCP, even with use of parallel imaging. Respiratory triggering can be used in patients who are unable to hold their breath for a longer time. Secondary to longer acquisition times, there are more blurring and ghosting artifacts observed. Contrast-enhanced MRCP is performed by using the property of predominant biliary excretion of some contrast agents such as gadoxetate disodium or Gd-EOB-DTPA (Eovist or Primovist; Bayer Healthcare, Leverkusen, Germany), or Gd-BOPTA (MultiHance, Bracco Diagnostics).8 These hepatocytespecific contrast agents increase the T1 relaxation time of bile with resultant higher signal intensity on T1-weighted imaging. Depending on the drug pharmacokinetics, imaging with single–breath hold 3D gradient-recalled echo sequence can be performed in
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Postprocessing Multiplanar reformats, standard or curved, that are defined by the centerline of a tubular structure are an easy way to begin evaluation after reviewing the axial data set. Maximum intensity projection images obtained from thin-section MRCP data set provide images comparable to ERCP. Smaller filling defects may not be visualized. Performing subvolume maximum intensity projection images may minimize this disadvantage. Minimum intensity projection images may be obtained demonstrating the relatively dark biliary tree compared with the enhancing surrounding structures especially on CT and postcontrast MR.9 Additionally, volume-rendered images of the biliary tree are used to increase reader confidence.
Percutaneous Transhepatic Cholangiography At present, the role of PTC is reserved as a therapeutic option to decompress the biliary tree in difficult cases. For cases where navigation of the biliary stricture is difficult with ERCP, PTC can be used for therapeutic purposes of biliary drainage and stent placement. Benign Biliary Strictures Ampullary Stenosis. This is a benign condition, a result of functional dysfunction of the sphincter of Oddi. The patient may present with recurrent biliary colic and mildly elevated levels of liver enzymes. On MRCP, it is seen as a tight narrowing of the distal common bile duct (CBD) with mild upstream dilatation of the CBD and the pancreatic ducts in the absence of an underlying cause like a mass or a stone (Fig 1). On ERCP, there is delayed contrast drainage from a mildly dilated pancreatic and CBD. In equivocal cases, pressure manometry at the sphincter may establish the diagnosis.10 Endoscopic sphincterotomy can offer a good clinical response.10 Pancreatitis. In acute pancreatitis, the edema and inflammation causes mass effect on the intrapancreatic
Curr Probl Diagn Radiol, January/February 2014
FIG 10. Mirizzi syndrome in a 38-year-old woman who presented with biliary colic and jaundice. Coronal MIP image from MRCP (A) shows a stricture involving the proximal hepatic duct (arrowhead), mild intrahepatic ductal dilatation, and marked distension of the gallbladder. T2 HASTE axial (B) and coronal (C) images show a low signal intensity focus in the gallbladder neck (arrow), consistent with a stone. ERCP image (D) demonstrates the common hepatic duct stricture due to extrinsic mass effect and resultant intrahepatic ductal dilatation from impacted stone in the gallbladder neck (arrow). HASTE, half Fourier acquisition single-shot turbo spin echo; MIP, maximum intensity projection.
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FIG 11. Biliary anastomotic stricture in a 58-year-old man with a history of liver transplant and elevated levels of liver function enzymes 2 years before presentation. A coronal MIP MRCP image (A) and an ERCP (B) image show a focal stricture at the bile duct anastomosis (arrow) resulting in mild upstream extrahepatic and intrahepatic ductal dilatation. The stricture was subsequently dilated and treated with stent placement (not shown). MIP, maximum intensity projection.
portion of the CBD with upstream dilatation (Figs 2 and 3). In chronic pancreatitis, the biliary strictures are secondary to recurrent inflammation, subsequent fibrosis, or extrinsic compression from pseudocysts. Cross-sectional imaging with CT or MRI aids in the diagnosis by demonstrating evidence of pancreatitis in the form of parenchymal atrophy, pancreatic ductal dilatation, pseudocysts, and pancreatic calcifications. The causative factor such as obstruction of the distal CBD from stone, fibrosis, or mass is also better evaluated with cross-sectional imaging. Autoimmune Pancreatitis (IgG4 Sclerosing Disease).
Immune-mediated inflammation of the pancreas results in this form of pancreatitis, which results in a benign-appearing distal CBD stricture.11,12 The specific laboratory abnormality observed is elevation of the serum IgG4 levels and the presence of serum autoantibodies such as antinuclear antibody and rheumatoid arthritis factor. The imaging features on MRI or CT (Fig 4) are edema of the pancreas with loss of its normal lobulations, which results in a “sausageshaped” appearance of the pancreas, as well as a hypodense hypointense peripancreatic rind of soft tissue with or without faint delayed enhancement.12 In late cases, involution of the tail of the pancreas can be observed.11,12
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A course of corticosteroids treatment may offer relief of symptoms.13 Autoimmune Pancreatitis and Sclerosing Cholangitis Syndrome. As the immune-mediated inflammatory
process can involve both the pancreatic and biliary ducts, these may be seen in conjunction (Fig 5). Variable degree of associated intra and extra hepatic ductal involvement may be seen less frequently. sclerosing cholangitis (PSC) is a sequela of chronic inflammation and fibrosis of the intrahepatic and extrahepatic bile ducts that occurs more frequently in middle-aged individuals (40-50 years) and in men, and is associated with inflammatory bowel disease (70%),14 most commonly ulcerative colitis.15 Several other autoimmune diseases are observed with increased frequency in these patients.16 The early imaging features on ERCP or MRCP are visualization of the peripheral bile ducts and central prominence of the bile ducts with peripheral pruning (Fig 6). The intermediate features are multiple, short segment (1-2 cm) strictures or stenoses with intervening dilated segments giving a beaded appearance (Figs 7 and 8). Biliary diverticula and webs are seen as late features (Fig 9), being the result of progressive fibrosis, biliary stasis, and recurrent infections.14 Primary
Sclerosing
Cholangitis. Primary
Curr Probl Diagn Radiol, January/February 2014
FIG 12. Biliary ischemic strictures in a 51-year-old man following liver transplant 48 hours before presentation with leukocytosis and increased liver function tests. Coronal MIP MRCP (A) and ERCP (B) showing extensive strictures, dilatations, and bile leaks along the intrahepatic and extrahepatic ducts, features of biliary necrosis. Axial postcontrast MR angiogram image (C) at the level of the celiac artery shows a signal void in the hepatic artery consistent with thrombosis (arrow). MIP, maximum intensity projection.
Curr Probl Diagn Radiol, January/February 2014
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neck or in the cystic duct with upstream dilatation of the common hepatic and the intra hepatic ducts. The common bile duct is normal in caliber. Combined CT and MRI has been reported to have a sensitivity of 96%, specificity of 93.5%, and accuracy of 94%.21 The erosion of the gallstone into the common hepatic duct is a known complication in this condition, and accordingly, the Mirizzi syndrome is classified in 4 types.22 Surgical exploration and cholecystectomy is the definitive treatment. Iatrogenic. Iatrogenic bile duct injury is the most common cause of postoperative biliary strictures, accounting for up to 80% of cases in some studies.23 FIG 13. Recurrent sclerosing cholangitis in a 57-year-old man with history of liver transplant for PSC performed 7 years before presentation. Coronal MIP MRCP image shows strictures of the extrahepatic duct (arrow) and visualization of the peripheral intrahepatic ducts consistent with recurrent PSC. MIP, maximum intensity projection.
Other associated findings seen are increased T2 signal intensity around the portal tracts (periportal edema), patchy areas of peripheral arterial enhancement, prominent periportal lymph nodes, and changes of cirrhosis in advanced stages.17,18 MRCP has a sensitivity of 80%-88% and specificity of 87%-99%.19 Clinically, these patients have a protracted course with symptoms of fatigue, weight loss, fever, and cholestatic features of intermittent jaundice and pruritus. The complications with this condition are biliary stasis leading to recurrent infections, stone formation, and ultimately, hepatic failure. There is an increased risk for cholangiocarcinoma of 1.5% per year.14 Though palliative balloon dilatation of symptomatic biliary stricture, ursodeoxycholic acid, and immunosuppressive drugs have been tried, the ultimate treatment is liver transplantation.20 MRI with MRCP serves as the imaging modality of choice not only to diagnose the condition but also for surveillance of complications, particularly cholangiocarcinoma. Mirizzi Syndrome. Mirizzi syndrome is characterized by obstruction of the common hepatic duct due to mechanical compression, with or without inflammation, from an impacted stone in the gallbladder neck or cystic duct. It is seen with increased incidence in patients with a low insertion of the cystic duct (Fig 10). The findings of Mirizzi syndrome include impacted stone at the gallbladder
24
Postcholecystectomy. Ligation of cystic duct close to the hepatic duct or inadvertent ligation of the hepatic duct or CBD during surgery is the most common cause. Transplant Strictures. Orthotopic liver transplant is an increasingly recognized cause of biliary stricture. This can be further divided into anastomotic and nonanastomotic categories.24 The anastomotic stricture results from fibrotic proliferation rather than ischemia and is seen as a late complication. The predisposing factors include ductal mismatch between donor and recipient common duct and suture retraction24 (Fig 11). The nonanastomotic strictures usually result from ischemia and are seen in the early postoperative period.24 In a posttransplant liver, the hepatic artery is the only source of blood supply to the biliary tree. So hepatic artery thrombosis, stenosis, or preservation injury can lead to biliary tree ischemia and intrahepatic bilomas, with subsequent inflammation and fibrosis, resulting in strictures (Fig 12). These are multiple, variable sized, randomly distributed strictures (over the territory of ischemia) that typically start near the hilum and progressively involve the intrahepatic ducts. Other less common causes of nonanastomotic biliary strictures after orthotopic liver transplant are infection or preexisting biliary disease (Fig 13). Post–Liver
Caroli Disease. Caroli disease is a congenital autosomal recessive condition resulting in segmental (83%) or diffuse (17%), cystic or saccular intrahepatic ductal dilatation that present at middle age (30-40 years).25 The classic imaging feature is the central
Curr Probl Diagn Radiol, January/February 2014
FIG 14. Caroli disease in a 9-year-old girl. ERCP (A) and coronary MIP MRCP (B) images show extensive saccular dilatations of the intrahepatic ducts with a normal extrahepatic duct. Axial contrast-enhanced MR images (C and D) confirm the cholangiographic findings with a “central dot” sign corresponding to the central enhancing hepatic artery and portal vein branches (circle). MIP, maximum intensity projection.
Curr Probl Diagn Radiol, January/February 2014
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FIG 15. Portal vein cavernoma causing extrinsic stricture in a 45-year-old man who presented with jaundice. Coronal MIP MRCP (A) and ERCP (B) images show a smooth abrupt stricture of the middle common bile duct (arrowhead) resulting in proximal ductal dilatation. Axial contrastenhanced MR images (C and D) demonstrate cavernous transformation of the portal vein with a large collateral vessel causing an extrinsic effect and focal stricture of the proximal CBD (arrow). Note the gallbladder wall varices, a feature associated with cavernous transformation (thin arrow). MIP, maximum intensity projection.
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Curr Probl Diagn Radiol, January/February 2014
FIG 16. Peribiliary cysts with extrinsic biliary stricture in a 58-year-old man with cirrhosis. ERCP (A) shows alternate areas of intrahepatic duct strictures and dilatations mimicking sclerosing cholangitis. Note the normal extrahepatic duct. Coronal MIP image from MRCP (B) shows multiple large, round, tubular cysts obscuring the biliary system (arrowhead). Note the disparity between the biliary tree dilatation on ERCP and MRCP. Axial contrast-enhanced MR images (C and D) demonstrate multiple cystic structures along the course of the intrahepatic biliary tree resulting in extrinsic mass impressions on the bile ducts. Note the cirrhotic appearance of the liver. MIP, maximum intensity projection.
fibrovascular bundle of hepatic artery and portal vein branches surrounded by dilated intrahepatic bile ducts referred to as “central dot sign”24 (Fig 14). The complications are stones, recurrent cholangitis, liver fibrosis, cirrhosis, and cholangiocarcinoma (7%).25 Compression. Structures surrounding the biliary tree when enlarged can lead to benign strictures from extrinsic compression, for example, portal cavernomas (portal biliopathy)26 (Fig 15), lymph nodes, vessels, hepatic cysts, and peribiliary cysts (Fig 16).
Extrinsic
Curr Probl Diagn Radiol, January/February 2014
Miscellaneous Causes. Rare causes of benign biliary strictures include sarcoidosis, tuberculosis, radiation, chemotherapy, vasculitis, cystic fibrosis, eosinophilic cholangitis, and xanthogranulomatous cholangitis.
Malignant Biliary Strictures Cholangiocarcinoma. Cholangiocarcinoma is a malig-
nant neoplasm of the biliary tree. There are 3 types of cholangiocarcinomas depending on the morphologic appearance: mass forming, periductal infiltrating, and intraductal growing.27,28 The risk factors for the
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FIG 17. Klatskin tumor in a 61-year-old woman. Coronal MIP MRCP (A) and ERCP (B) images demonstrate a high-grade, short segment stricture with shouldering margins (arrow) at the confluence of the right and left hepatic ducts with extension into the proximal common hepatic duct. Ultrasound image (C) shows an ill-defined isoechoic mass (arrowhead) at the corresponding area of the malignant stricture. Delayed postcontrast axial MR image (D) shows a soft tissue mass with retention of contrast characteristic of the fibrous tumor matrix of cholangiocarcinoma (arrowhead). MIP, maximum intensity projection.
development of cholangiocarcinoma include inflammatory bowel disease (ulcerative colitis and PSC spectrum), biliary parasites, and choledochal cysts.27,28 The most common site of involvement is the confluence of the right and left hepatic ducts called a Klatskin or hilar cholangiocarcinoma (50%-60%) (Fig 17). The
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next common site is the extrahepatic duct (30%-35%) with intrahepatic being the least common site (10%). On imaging, these can be seen as malignant strictures with upstream biliary ductal dilatation. Often, with the periductal variant, it is difficult to perceive a mass lesion of cholangiocarcinoma (Fig 18). Owing to the predominant fibrous tissue component of Curr Probl Diagn Radiol, January/February 2014
FIG 18. Cholangiocarcinoma (periductal infiltrating type) in a 65-year-old woman who presented with jaundice and elevated liver function tests. ERCP (A) and coronal MIP MRCP (B) images show an abrupt, high-grade stricture of the middle common bile duct (arrow) with shouldering margins. Proximal ductal dilatation is less prominent because of the placement of the stent across the stricture. Delayed postcontrast axial MR shows an illdefined, circumferential area of contrast retention in the area of ductal stricture (circle). MIP, maximum intensity projection.
cholangiocarcinoma, delayed contrast enhancement (typically beyond 5-10 minutes) is observed. Gallbladder Carcinoma. Adenocarcinoma of the gallbladder accounts for more than 90% of gallbladder malignancies29 and commonly affects females (M:F ¼ 1:3), with a mean age of 72 years. Risk factors
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implicated in the development of gallbladder cancer include chronic cholecystitis, gallstones, porcelain gallbladder (20%), and PSC.29 The various imaging features of gallbladder carcinoma include an intraluminal polypoidal mass, focal or diffuse gallbladder wall thickening, and a mass
29
FIG 19. Gallbladder cancer spreading along the cystic duct and involving the middle CBD in a 58-year-old woman who presented with RUQ pain. Coronal MIP MRCP image (A) demonstrates an abrupt, high-grade stricture in the middle common duct (arrow) with proximal ductal dilatation. The middle and distal common bile ducts are normal. Ultrasound image (B) shows a large nondependent soft tissue mass arising from the gallbladder fundus (white arrowhead). Contrast-enhanced transaxial CT image (C) again shows the heterogeneously enhancing gallbladder fundal mass (white arrowhead) invading the adjacent liver (black arrowhead) and growing along the cystic duct to involve the common hepatic duct (black arrow). MIP, maximum intensity projection; RUQ, right upper quadrant.
replacing the gallbladder fossa. The spread of tumor can be via direct extension into the adjacent liver parenchyma or through the hepatoduodenal ligament and transverse mesocolon. The growth along the cystic duct with progressive involvement of common duct leads to an isolated “mid-CBD stricture” that is a characteristic late finding of this entity. The 30
differential for a mid-CBD malignant stricture includes cholangiocarcinoma and metastases (Fig 19). Liver Metastases. Diffuse hepatic metastases can lead
to multifocal strictures of the intrahepatic ducts primarily from extrinsic compression and from contiguous involvement. Metastases from colorectal
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FIG 20. Hepatic metastases from colon cancer causing extrinsic biliary strictures in a 60-year-old man who presented with right upper quadrant pain. Coronal MIP MRCP (A) and ERCP (B) images demonstrate multiple smooth strictures of the intrahepatic ducts due to extrinsic impressions. Note the normal extrahepatic duct. Postcontrast axial liver MR image in portal venous phase (C) shows multiple round, low–signal intensity hepatic metastases (arrowhead). MIP, maximum intensity projection.
carcinoma are the most common cause of metastatic malignant biliary strictures.30 The features on ERCP and MRCP include smooth or irregular intrahepatic ductal strictures depending on the site and degree of compression (Figs 20 and 21) with upstream dilatation of the biliary tree associated with the masses seen on cross-sectional imaging. Pancreatic Carcinoma. Pancreatic carcinoma is the
second most common GI malignancy and accounts
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for 85%-90% of all pancreatic neoplasms.31 The most common site of occurrence of pancreatic adenocarcinoma is the head of pancreas (60%). The various classic signs described include the “double duct sign”30—dilatation of both the pancreatic and the CBDs from a focal T1 hypointense, hypovascular mass. There is a variable degree of parenchymal atrophy involving the body and tail of the pancreas (Fig 22). There is an abrupt termination of the distal common duct with upstream dilatation. Periampullary
31
FIG 21. Hepatic metastases from colon cancer causing extensive biliary strictures in a 55-year-old man with a history of sigmoid adenocarcinoma. Coronal MIP MRCP (A) image shows diffuse right and left intrahepatic ductal dilatation with an abrupt cutoff near the confluence of the right and left hepatic ducts. The middle and distal CBDs are normal in caliber (arrowhead); an appearance similar to Klatskin-type cholangiocarcinoma. Contrast-enhanced axial liver MR image (B) shows multiple heterogeneously enhancing hepatic metastases, the largest one at the confluence of the hepatic ducts (arrow). MIP, maximum intensity projection.
FIG 22. Pancreatic adenocarcinoma in a 63-year-old man who presented with weight loss and epigastric pain. ERCP (A) shows diffuse pancreatic (thin arrow) and common bile (thick arrow) ductal dilatation to the level of the ampulla producing the “double duct” sign. Contrast-enhanced axial CT image (B) depicts a hypovascular mass in the pancreatic head (arrowhead).
carcinoma and duodenal adenocarcinoma may also result in the “double duct” sign (Fig 23).
Conclusion In comparison with ERCP, MRI with MRCP has the advantages of being noninvasive, without ionizing
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radiation and offers additional soft tissue information that is essential in determining the etiology of the biliary strictures. The imaging appearance may help to differentiate between benign and malignant strictures; however, cytologic studies are needed in equivocal cases. For diagnosis and surveillance of biliary strictures MRCP is comparable to ERCP and the latter
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FIG 23. Periampullary carcinoma in a 58-year-old woman who presented with jaundice and abdominal pain. 3D volume-rendered MRCP image (A) shows a “double duct” sign with diffuse pancreatic (thin arrow) and common bile ducts (thick arrow) to the level of the ampulla. Contrastenhanced axial MR image (B) demonstrates soft tissue thickening and heterogeneous enhancement of the second portion of the duodenum (arrowhead).
should be reserved for interventional procedures such as tissue sampling, balloon dilatation, or stent placement.
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