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Noninvasive Imaging of the Biliary Tree for the Interventional Radiologist
Noninvasive Imaging of the Biliary Tree for the Interventional Radiologist Myra K. Feldman, MD, and Christopher P. Coppa, MD Patients with suspected biliary tract disease often pose a diagnostic challenge to the clinician and radiologist. Although advances across all imaging modalities, including ultrasound, computed tomography, and magnetic resonance, have improved our diagnostic accuracy for biliary disease, many of the imaging findings remain nonspecific. Recognition of key imaging findings combined with knowledge and understanding of the clinical context is essential to piecing together a diagnosis and guiding management for patients with biliary disease. Although there is a wide range of biliary pathology, interventional radiologists most commonly play a role in the management of biliary obstruction and leak. Tech Vasc Interventional Rad 18:184-196 C 2015 Elsevier Inc. All rights reserved. KEYWORDS Biliary imaging, biliary obstruction, biliary stricture, bile leak
Introduction Biliary obstruction may be suspected in a patient who presents with colicky right upper quadrant abdominal pain, abnormal liver and bile chemistries, or jaundice. Initial imaging studies are typically obtained to establish the presence or absence of biliary obstruction. When biliary obstruction is confirmed, imaging studies must then be scrutinized to determine the level, and if possible, the cause of obstruction. Bile duct stones and benign and malignant strictures are the most commonly encountered sources of biliary obstruction. Interventional procedures aimed at alleviating or bypassing biliary obstructions can offer symptomatic relief, treat complications of obstruction, or act as a bridge before definitive surgery or intervention. Biliary leak may be iatrogenic or result from trauma. Patients with biliary leak typically present with significant abdominal pain, anorexia, and malaise. Initial imaging studies may show the presence of free fluid or a fluid collection in the abdomen. Advanced imaging can confirm biliary leak and in some instances can show the location of
Section of Abdominal Imaging, Imaging Institute, Cleveland Clinic, Cleveland, OH. Address reprint requests to Myra K. Feldman, MD, Section of Abdominal Imaging, Imaging Institute, Cleveland Clinic, 9500 Euclid Ave A-21, Cleveland, OH 44195. E-mail: [email protected]
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the leak. Interventional procedures can then be used to confirm the diagnosis and control or bypass the leak. In this article, common causes of biliary obstruction (including stone disease and benign and malignant strictures) and biliary leaks are reviewed. Emphasis is placed on using a multimodality approach to assess the imaging findings of biliary pathology frequently encountered by the interventional radiologist.
Imaging Ultrasound (US) is often the first imaging study ordered in a patient with suspected biliary disease. Compared with other imaging modalities, US is less expensive, is widely available, does not use ionizing radiation, and is well tolerated by patients. US is widely regarded as a highly sensitive study for the detection of biliary obstruction. Studies have shown that for the evaluation of patients with acute right upper quadrant pain, US is more effective than computed tomography (CT) because of its superior sensitivity for the detection of cholelithiasis, a common cause of these symptoms.1 US is also useful for establishing the level of biliary obstruction, with a reported accuracy of more than 90%.2 This modality falls short when it comes to identifying the cause of obstruction, with accuracy rates ranging from 30%-70%.3 US may also be technically compromised in individuals with large body habitus, limited scanning window, or excessive bowel gas.
1089-2516/15/$ - see front matter & 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2015.07.001
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CT and magnetic resonance (MR) imaging with or without MR cholangiopancreatography (MRCP) can also be used to evaluate the biliary tract. Both modalities allow visualization of the bile ducts beyond an obstruction, as well as sources of extrinsic duct narrowing. In addition, both modalities image a large field of view and may reveal abnormalities outside the biliary tract contributing to a patient’s symptoms. Advantages of CT include quicker scanning and fewer image artifacts as compared with MR. MR offers imaging without ionizing radiation and improved identification of stones. Ultimately, the choice of which modality to use may rely on preference or local expertise.4 Unenhanced CT imaging plays a limited role in evaluation of the biliary tract but can potentially add value as some biliary stones cause high attenuation and may be more conspicuous on CT scans performed without contrast (Fig. 1). Dilated bile ducts can be seen with standard portal venous phase contrast-enhanced CT obtained 70-80
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seconds after intravenous contrast administration. Arterial phase imaging can be helpful when pancreatic, hepatic, or other hypervascular malignancies are suspected. When cholangiocarcinoma is suspected, imaging performed 1020 minutes after contrast administration may be helpful owing to delayed enhancement of the fibrous stroma within these tumors (Fig. 1). Positive enteric contrast should be avoided in patients with suspected biliary pathology, as this contrast may obscure pathology at the ampulla. Administration of a neutral contrast agent such as VoLumen (Bracco Diagnostics, Monroe Township, NJ) immediately before the scan distends the duodenum and improves visualization (Fig. 1). Coronal and sagittal reconstructions and 3-dimensionally (3D) rendered postprocessing techniques may also be helpful in evaluation of the biliary tree. Direct CT cholangiography can be performed with contrast injected into the biliary system via the percutaneous or endoscopic retrograde cholangiopancreatography approach. Indirect CT cholangiography can be
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Figure 1 Coronal reformatted contrast-enhanced CT image (A) shows dilated CBD with abrupt cutoff. Highattenuation material in the lumen of the distal CBD (white arrowhead) could be a stone or a mass. Axial unenhanced CT image (B) from the same patient shows that the filling defect is a well-defined, round, highattenuation stone (white arrow). Axial contrast-enhanced CT (C) performed during the portal venous phase in a different patient shows an intrahepatic cholangiocarcinoma with heterogeneous enhancement and indistinct borders (black arrows). Axial contrast-enhanced CT (D) performed 10 minutes after contrast administration shows the same lesion with homogeneous delayed enhancement (dashed black arrows). Coronal contrast-enhanced CT (E) performed during the arterial phase of contrast enhancement with neutral enteric contrast agent shows a hypervascular carcinoid tumor in the second portion of the duodenum (dashed white arrow). The duodenum is well distended by the neutral oral contrast agent, allowing excellent visualization of this tumor. There is no associated biliary obstruction in this case.
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186 performed with agents that are excreted into the biliary system. This practice is not widespread and has the potential for increased risk of allergy.4,5 The biliary system can be evaluated by standard MR sequences with and without contrast enhancement. MRCP imaging can be performed using 2D or 3D heavily T2weighted techniques. The 2D “thick-slab” MRCP technique is a useful way to evaluate the entire biliary system. These thick-section images are often obtained in coronal and oblique views and include the entire pancreaticobiliary tree in a single image. The 3D MRCP technique typically covers the biliary tree in 15-20 images. These thinner sections are helpful for identifying filling defects such as stones and are not compromised by intersection gaps. A maximum intensity projection image can be created from the 3D data sets to obtain a similar overall view of the biliary tree as seen in the 2D technique (Fig. 2). The main disadvantage of the 3D technique is increased time for image acquisition compared with the 2D technique.4 Newer hepatocyte-specific contrast agents such as gadoxetate (gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid [Gd-EOBDTPA], Eovist; Bayer HealthCare,
Berlin, Germany) are excreted via the biliary system (in addition to the urinary system) and can be used to create an MR cholangiogram by opacifying the bile ducts. This is accomplished by acquiring 3D gradient echo T1-weighted images 20-40 minutes after injection, at which time the bile ducts are opacified with contrast. These agents have the potential to delineate bile duct anatomy and morphology and to assess for bile duct leaks (Fig. 2).6
Biliary Obstruction There is variability in the literature regarding the normal size of the common bile duct (CBD). In general, the common hepatic duct and CBD should measure less than 7 mm by US (luminal diameter measurement) or less than 8-10 mm by CT and MR (measurements inclusive of biliary walls). Intrahepatic bile ducts are considered dilated by CT or MR when they measure greater than 2 mm or greater than 40% of the adjacent portal vein diameter.7 When dilated bile ducts are identified by any modality, the next step is to identify the level of obstruction.
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Figure 2 Thick-slab 2D MRCP image (A) in a patient with PSC shows multiple segmental strictures (white arrowheads). Coronal maximum intensity projection (MIP) MRCP image (B) acquired from the same patient on the same day shows more branches and strictures (white arrows) of the biliary tree compared with the 2D technique. MIP MRCP image (C) in a different patient with acute cholecystitis shows dilated intrahepatic bile ducts but fails to show the cystic duct (dashed white arrow) and gallbladder stones (white arrowheads) that were identified on the 3D MRCP image (D). These stones were not seen on the MIP image, which displays only the maximum-intensity signal. MIP image from 3D MRCP (E) in a potential living donor for hepatic transplant shows that the CBD is normal in course and caliber. The intrahepatic ducts are not seen. Coronal T1-weighted image (F) obtained during the hepatobiliary phase after intravenous administration of gadoxetate in the same patient as seen in (B). The bile ducts are now well visualized as hyperintense branching structures. The right hepatic duct joins the CBD (black arrow). This variant anatomy was not seen with the standard MRCP technique; knowledge about this anatomy is crucial for surgical planning.
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Figure 3 Transabdominal US image of the CBD in the sagittal plane (A) shows echogenic shadowing stone in the CBD (white arrow). Smaller stones more distally in the CBD are echogenic but do not shadow (dashed white arrow). Axial contrast-enhanced CT image (B) in a different patient shows a high-attenuation stone in the CBD (white arrowhead). The stone in the gallbladder is of peripherally high attenuation but centrally has attenuation similar to that of bile (black arrow). Thick-slab MRCP image (C) shows T2 hypointense filling defect in the CBD compatible with a stone (curved dashed white arrow). Unenhanced T1-weighted gradient echo image (D) shows that this stone is T1 hyperintense (curved white arrow).
Different disease processes affect characteristic portions of the biliary tree, so defining the level of the obstruction can be a clue to the underlying etiology. The presence or absence of intraductal filling defects should be established. Bile duct wall thickness, enhancement, and texture (smooth vs irregular) should be scrutinized. Peribiliary tissues should be evaluated for edema or masses. If present, stricture morphology and length can also help determine the cause of obstruction. Commonly encountered causes of biliary obstruction include choledocholithisis, iatrogenic injury, primary sclerosing cholangitis (PSC), neoplasm, and secondary forms of cholangitis such as chronic pancreatitis, autoimmune-mediated disease, and ischemic cholangitis.
Choledocholithasis Choledocholithasis is the most common cause of biliary obstruction. It is possible to detect CBD stones by US when a suitable imaging window is present. The CBD is often identified at the hepatic hilum on US but may be obscured by the ampulla because of shadowing by bowel gas. Imaging the patient in the left lateral decubitus position can improve visualization of this region, as the gallbladder serves as an acoustic window. Biliary stones appear as echogenic structures within the duct with
posterior acoustic shadowing. Stones smaller than 3 mm may not produce an acoustic shadow (Fig. 3). On MR and CT, stones lie in the dependent portion of the bile ducts. Stones have a variable appearance on CT based on their composition. Biliary stones may be of high attenuation on CT because of calcium content or low attenuation because of nitrogen gas content. Stones with cholesterol content may be isoattenuating to bile and thus difficult to see on CT (Fig. 3).4 The overall sensitivity for detection of choledocholithiasis by multidetector CT is modest, ranging from 72%-78%, whereas specificity is high, ranging from 95%-96%.8 MRCP is both highly sensitive (95%) and highly specific (90%) for the detection of CBD stones.9 On MR, calculi are best seen on T2-weighted images, where they stand out as hypointense filling defects against a background of hyperintense bile. The T1 signal characteristics of stones vary with composition. Some pigmented stones show mild T1 hyperintense signal, whereas cholesterol stones classically demonstrate T1 hypointense signal (Fig. 3).10 It is important to confirm the presence of a filling identified on an MRCP image in more than a single sequence or plane to avoid a potential misdiagnosis. Pneumobilia also appears as a T2 hypointense filling defect on MR but can be differentiated from stones by its nondependent position in the ducts. Occasionally, the hepatic artery may simulate a filling defect on MRCP images where it
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Figure 4 Thick-slab 2D MRCP image (A) shows an apparent filling defect in the common hepatic duct, which could be mistaken for a stone (white arrow). Sagittal half-Fourier acquisition single-shot turbo spin echo (HASTE) image (B) in the same patient shows flow void from the hepatic artery (dashed white arrow) adjacent to the T2 hyperintense common hepatic duct. There is no stone or filling defect in the CBD.
crosses the CBD (Fig. 4). Surgical clips may also cause apparent filling defects on MRCP. In this case, a comparison with CT (if available) can be helpful. Choledocholithiasis is usually managed endoscopically, but there is a role for percutaneous transhepatic
management for patients with altered anatomy (eg, patients with Roux-en-Y gastric bypass or biliary enteric anastomosis) or for patients in whom the endoscopic approach fails.11 Transhepatic techniques can also be used in patients with hepatolithiasis.
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Figure 5 Thick-slab MRCP (A) and coronal HASTE (B) images in a patient with prior hepaticojejunostomy show marked intrahepatic biliary duct dilation with stricture of the duct at the hepaticojejunostomy (white arrow). Images from percutaneous transhepatic cholangiogram during placement of external-internal biliary catheter show the smooth stricture (black arrow) (C) and the external-internal biliary catheter positioned across the stricture (D).
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Figure 6 MIP 3D MRCP image (A) shows multiple strictures (white arrows) of the intrahepatic bile ducts with intervening normal-caliber bile ducts in a patient with PSC and prior choledochoduodenostomy. Thick-slab 2D MRCP image (B) in a different patient shows more conspicuous changes of PSC with innumerable focal intrahepatic bile duct strictures alternating with mildly dilated ducts, creating a “string of beads” appearance. Axial T1 contrast-enhanced MR image (C) from a different patient with PSC shows multiple focally dilated bile ducts with circumferential wall thickening and increased enhancement (black arrows). Coronal contrast-enhanced CT image (D) from a different patient with PSC shows circumferential wall thickening involving the common hepatic duct (dashed white arrows). Axial contrast-enhanced CT image (E) in a different patient with PSC-associated cirrhosis. The lateral lobe (white arrowhead) is atrophic and the caudate is hypertrophied (dashed black arrows), giving the liver a round, macrolobulated shape.
Iatrogenic Stricture Iatrogenic injury is the most common cause of benign biliary stricture. Iatrogenic biliary strictures occur after upper gastrointestinal tract surgeries (cholecystectomy, orthotopic liver transplantation [OLT], choledochocyst repair, and choledochojejunostomy) or endoscopic procedures.3 Operative injuries following cholecystectomy can
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be attributed to variant anatomy or technical failure and tend to involve the common hepatic duct or CBD.12 Biliary strictures are the most common complication after OLT, with strictures most commonly identified at the biliary anastomosis due to fibrosis. Biliary strictures proximal to the anastomosis in patients who have undergone OLT are usually secondary to ischemic injury, described later in
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Figure 7 Thick-slab MRCP image (A) shows markedly dilated bile ducts (dashed white arrows) and pancreatic duct (white arrowhead) with abrupt cutoff at the level of the pancreatic head (white star). This is the “double-duct sign,” indicative of pancreatic adenocarcinoma, the diagnosis in this patient. Coronal HASTE image (B) in a different patient with long-segment CBD stricture (white arrow). Axial T1 contrast-enhanced MR image (C) in the same patient as in (B) shows enhancing carcinomatosis in the porta hepatis at the level of obstruction (curved arrows).
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Figure 8 Transabdominal US image of the left lobe (A) shows dilated intrahepatic bile ducts (dashed white arrow). MRCP image (B) in the same patient shows markedly dilated left intrahepatic ducts (dashed white arrow) and mildly dilated right intrahepatic ducts (solid white arrow). The right and left ducts do not communicate because of a Klatskin tumor involving the biliary confluence. Axial unenhanced T1 MR image (C) from a different patient with intrahepatic mass-forming cholangiocarcinoma and overlying hepatic capsular retraction (white arrowheads). Axial T1 contrast-enhanced MR performed during the arterial (D) and venous (E) phase of contrast enhancement shows early peripheral enhancement (black arrow) and delayed central enhancement (dashed black arrow) of the tumor. Images also show capsular retraction and vascular encasement. Axial contrast-enhanced CT (F and G) from a different patient with peribiliary cholangiocarcinoma (black star), which extends along the right hepatic duct (F) and CBD (G).
this article.3,13 In general, iatrogenic strictures are identified on imaging by their location at the surgical site and smooth, tapered appearance (Fig. 5). Although these features may suggest iatrogenic injury as the underlying cause of a stricture, tissue diagnosis is often required to exclude underlying malignancy.
Primary Sclerosing Cholangitis PSC is a chronic disorder characterized by inflammation and fibrosis of the bile ducts. In patients of Northern European descent, 62%-83% of those with PSC also have
inflammatory bowel disease, typically ulcerative colitis.14 MRCP is highly sensitive and specific for the diagnosis of PSC.15 The disorder can involve the intrahepatic and extrahepatic bile ducts. Isolated intrahepatic involvement occurs in roughly 28% of patients; isolated extrahepatic involvement is rare.14 Imaging findings of PSC vary based on the stage or severity of disease. Initially, focal biliary strictures alternating with segments of normal-caliber ducts are identified. When focal strictures are accompanied by mildly dilated bile ducts, the biliary tree is likened to a “string of beads” on MRCP images (Fig. 6). Imaging in patients with
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Figure 9 Coronal contrast-enhanced CT image (A) shows smooth distal CBD stricture (white arrowheads) with upstream dilation of CBD in a patient with chronic pancreatitis. Coronal contrast-enhanced CT through the pancreatic head (B) shows multiple pancreatic calcifications (black arrows) with no associated mass, a characteristic finding of chronic pancreatitis.
more advanced disease may demonstrate longer strictures with obliteration of ducts. When the peripheral ducts become obliterated, the biliary tree may have a “pruned tree” appearance on MRCP. The degree of duct dilation in patients with PSC is usually not marked due to peribiliary fibrosis. Circumferential bile duct wall thickening with increased enhancement may be seen on contrast-enhanced CT or MR (Fig. 6). Patients with PSC may also develop biliary stones (hepatolithiasis).13,16 Many patients with PSC go on to develop cirrhosis. Caudate hypertrophy occurs more commonly in patients with PSC-associated cirrhosis than in those with other forms of cirrhosis. Macronodular cirrhotic liver morphology, peripheral atrophy, and peripheral wedge or bandlike areas of parenchymal fibrosis are also seen in patients with PSC cirrhosis (Fig. 6).17 Patients with PSC are at increased risk for the development of cholangiocarcinoma, which can be difficult to detect. Recognition of a new mass, a dominant stricture, or dilated bile ducts in a segment of the liver out of proportion to the degree of dilation in other portions
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of the liver should raise suspicion for underlying cholangiocarcinoma.18
Neoplasm Malignant obstruction of the bile ducts can be caused by primary malignancy of the bile ducts (cholangiocarcinoma), malignant tumor invasion of the biliary tree, or external compression. Compared with benign strictures, neoplastic biliary strictures tend to cause abrupt duct cutoff. The degree of upstream dilation may be greater than with a benign obstruction. Extrinsic tumors can displace or encase the bile ducts, causing narrowing or complete obstruction. Pancreatic adenocarcinoma located in the pancreatic head can obstruct both the CBD and pancreatic duct, causing the “double-duct sign” (Fig. 7). Other local primary malignancies (gallbladder, duodenal, and gastric adenocarcinomas) and metastatic disease (nodal or carcinomatosis) may obstruct the biliary tree in a similar manner (Fig. 7). Hepatocellular carcinoma can extrinsically compress or
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Figure 10 Coronal MRCP image (A) from a patient with a clinical diagnosis of ISD shows multiple focal intrahepatic strictures (white arrows). There is also a stricture of the common hepatic duct (dashed white arrow). Axial contrastenhanced T1-weighted MR images (B and C) show circumferential wall thickening of the intrahepatic bile ducts (B) (solid black arrow) and extrahepatic common hepatic duct (C) (dashed black arrow). The degree of wall thickening is greater than is typically seen with PSC.
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Figure 11 Axial arterial phase contrast-enhanced CT image (A) in a patient who has undergone OLT shows thrombosis of the hepatic artery (white arrow). Axial portal venous phase contrast-enhanced CT image (B and C) shows irregular fluid attenuation tracks in a biliary or peribiliary distribution (black arrows), compatible with biliary necrosis from ischemic injury.
invade the biliary tree. Lymphoma can surround the ducts without causing obstruction.7 Cholangiocarcinoma is a primary malignant neoplasm of the bile ducts. Chronic inflammation of the bile ducts due to a variety of underlying etiologies leads to an increased risk for cholangiocarcinoma. In Western countries, PSC is a leading risk factor. Cholangiocarcinoma can involve the intrahepatic or extrahepatic bile ducts and is classified into 3 distinct morphologic forms: periductal infiltrating, mass forming, and intraductal. In the periductal infiltrating form of cholangiocarcinoma, the tumor grows along the bile duct without forming a distinct mass. This form is most often seen at the hepatic hilum (Klatskin tumor).19,20 On contrast-enhanced MR and CT, this type of tumor causes irregular increased enhancement along the ducts. Dilated bile ducts in the right and left lobes that do not communicate at the confluence should raise suspicion for a hilar cholangiocarcinoma (Fig. 8). The mass-forming subtype of cholangiocarcinoma most commonly involves the intrahepatic bile ducts.21 On imaging, these lesions show peripheral enhancement early on with gradual central enhancement on delayed imaging obtained 10-15 minutes after contrast administration. The center of the tumor may enhance less than the background liver on delayed images when necrosis or mucin is present. Capsular retraction, satellite nodules, vascular encasement, and hepatic atrophy may also be observed. On unenhanced MR images, the lesions are typically T1 hypointense and T2 hyperintense.22 The signal within the lesions centrally on T2-weighted imaging is variable based on the amount of fibrous tissue, mucin, or necrosis (Fig. 8). The intraductal form of cholangiocarcinoma tends to be a slow-growing malignancy with a better prognosis.23 This form of cholangiocarcinoma has a varied appearance on imaging, including sessile or polypoid intraductal masses, cast-like intraductal mass, and stricture.24
Chronic Pancreatitis Patients with chronic pancreatitis may develop strictures in the distal pancreatic portion of the CBD because of repeated episodes of inflammation and subsequent
fibrosis. The reported incidence of benign biliary strictures in patients with chronic pancreatitis varies widely in the literature, ranging from 3%-46%. Clinically, patients with this condition may present with abdominal pain, jaundice, and biochemical abnormalities. Some individuals are asymptomatic, with strictures discovered incidentally.25 In addition to distal CBD strictures, other imaging manifestations of chronic pancreatitis, including pancreatic calcifications, pancreatic atrophy, and an irregularly dilated pancreatic duct, may be seen on imaging studies (Fig. 9).
Autoimmune-Mediated Disease IgG4 systemic disease (ISD) was first recognized as a disease with effects on the biliary system in 2003.26 The
Figure 12 Coronal MR HASTE image in a patient with AIDSrelated cholangiopathy shows dominant distal CBD stricture to the level of the ampulla (dashed white arrow). Extrahepatic strictures are commonly seen in AIDS-related cholangiopathy, with papillary stenosis occurring in up to 75% of patients. The intrahepatic ducts are irregular, with focal intrahepatic strictures (white arrows) and a dilated, beaded appearance. Intrahepatic imaging findings of HIV cholangiopathy are identical to those seen with PSC. This rare disorder is typically seen in severely immunocompromised patients (CD4 less than 100).34
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Figure 13 Patient with a history of biliary ischemia and multifocal biliary strictures and leaks presented to the emergency department with new-onset abdominal pain and fever. Axial contrast-enhanced CT image (A) shows multiple dilated bile ducts with internal high-attenuation material (white arrow). T2 MR image (B) in the same patient shows T2 hypointense material centrally within the duct with surrounding T2 hyperintense bile (dashed white arrows). The material did not enhance on postcontrast imaging (not shown). Subsequent ERCP revealed pus and blood products within the ducts. Contrast-enhanced CT image (C and D) from a different patient with chronic biliary obstruction from PSC and new-onset cholangitis shows dilated bile ducts in the left lobe (C) and new left portal vein thrombosis (black arrow) (D). Contrast-enhanced T1 MR image (E) in the same patient shows smooth, circumferential bile duct wall thickening with increased enhancement (curved white arrow) and peripheral areas of transient increased hepatic signal (white arrowheads).
disease is characterized by inflammation, fibrosis, and a lymphoplasmacytic infiltrate rich in IgG4 plasma cells. The biliary system is the second most common site of ISD outside the pancreas. MR with MRCP imaging is the preferred imaging modality for the evaluation of patients with suspected ISD affecting the bile ducts. Imaging in these patients shows bile duct wall thickening with postcontrast enhancement and luminal narrowing (Fig. 10). There is overlap between the imaging appearance of ISD-related biliary disease and that of PSC; distinguishing between the 2 conditions on imaging can be difficult.27 A study by Tokala et al28 showed that CBD wall thickness greater than 2.5 mm, continuous biliary tree involvement, gallbladder involvement, and absence of liver parenchyma abnormalities can be used to predict a diagnosis of ISD as opposed to PSC. Imaging findings of other extrabiliary forms of ISD (pancreatic, renal, or retroperitoneal) may also help narrow the diagnosis. Ultimately, the diagnosis is made based on a combination of elevated serum IgG4 levels, typical imaging findings of ISD involving the biliary
system or other characteristic locations, and typical features on histopathology.29 It is important that this condition be diagnosed correctly, as patients with ISD-related strictures may respond to treatment with steroids, potentially obviating the need for invasive interventions.
Ischemic Cholangiopathy Unlike the hepatic parenchyma, which receives its vascular supply from both the portal venous system and the hepatic arteries, the bile ducts are supplied solely by the hepatic artery. Ischemic bile duct injuries were originally described in the setting of hepatic artery thrombosis, but in patients who have undergone OLT, this pattern of injury has also been identified in those without hepatic artery thrombosis. Studies have shown that in the OLT population, ischemictype biliary injuries may also arise from prolonged ischemia time, reperfusion injury, preservation solutions, or immunologic injury.30 When biliary ischemia leads to necrosis, dilated bile ducts and bilomas are identified on
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Figure 14 Axial contrast-enhanced CT image (A) in a patient with increasing abdominal pain and leukocytosis 2 days after cholecystectomy shows free fluid (white arrows) surrounding the liver. Image from CT-guided aspiration and drain placement (B) shows needle tip within the fluid (dashed white arrow). The diagnosis of biliary leak was confirmed by percutaneous aspiration. Image from hepatobiliary iminodiacetic acid (HIDA) scan performed 90 minutes after radiotracer injection (C) in a different patient with bile leak from a perforated gallbladder. Leaked radiotracer has accumulated along the right lateral surface of the liver (black arrow). Axial T1weighted MR image obtained during the hepatobiliary phase (D) after gadoxetate disodium injection in a different patient with prior hepaticojejunostomy shows excreted T1 hyperintense contrast in the biliary tree (curved white arrow). T1-weighted MIP image (E) obtained during the hepatobiliary phase of contrast enhancement shows bile leak at the level of the hepaticojejunostomy with extra luminal contrast accumulated anteriorly (black arrowheads).
imaging. This pattern is usually seen in conjunction with arterial thrombosis (Fig. 11). Hilar strictures, dilated bile ducts, and biliary casts can be seen in cases of biliary ischemia with or without arterial thrombosis.31 Chemotherapy-induced cholangitis after hepatic arterial chemotherapy is also an ischemic type of secondary cholangiopathy. This form of cholangitis causes segmental or diffuse biliary strictures. The cystic duct and common hepatic duct may be involved, but the intrapancreatic segment of the CBD is spared, likely due to a separate vascular supply by the gastroduodenal artery.32
Secondary Sclerosing Cholangitis Secondary sclerosing cholangiopathies may have imaging features that overlap with those of PSC, but these conditions arise from a known underlying pathologic process. In addition to some of the more commonly encountered causes of secondary cholangitis previously described (eg, chronic pancreatitis, autoimmune sclerosing disease, and
ischemic cholangiopathy), there are many other causes, including AIDS-related cholangiopathy (Fig. 12), portal biliopathy, eosinophilic cholangitis, inflammatory pseudotumor, and recurrent pyogenic cholangitis.33,34 These are rarely encountered and beyond the scope of this review.
Ascending Cholangitis Acute (ascending) cholangitis is a complication of biliary obstruction but may also arise as a complication after transhepatic or endoscopic biliary procedures. Patients with this condition commonly present with Charcot’s triad of symptoms, including right upper quadrant abdominal pain, fever, and jaundice. Imaging should be performed to evaluate the site and cause of obstruction so that an approach to biliary decompression can be planned. Imaging by any modality may show dilated bile ducts. Purulent material may cause the bile to have a complex appearance with increased attenuation on CT (Fig. 13). The bile duct walls may also appear thickened with increased
Noninvasive imaging of the biliary tree enhancement (Fig. 13).7 Areas of transient hepatic attenuation difference are often identified during the arterial phase of contrast-enhanced CT imaging in patients with acute cholangitis.35 Scans should also be evaluated for complications of acute cholangitis, including hepatic abscess, bile peritonitis, portal vein thrombus, and biliary strictures (Fig. 13).36
Biliary Leak Bile leaks may occur after trauma or as an iatrogenic injury after surgery (cholecystectomy, OLT, liver resection, or biliary enteric anastomosis), liver biopsy, liver ablation procedures, or biliary stent manipulation. Clinically, patients may present with significant abdominal pain, anorexia, and malaise.37 Bile duct leaks appear as intrahepatic or extrahepatic fluid on all imaging modalities (US, CT, and MR). This appearance is nonspecific, as other low-attenuation abdominal fluid such as seroma, leak from another source, or ascites can have a similar appearance. Although the location of fluid and clinical context may suggest the diagnosis, confirmatory imaging or aspiration to confirm the location may be warranted. Hepatobiliary scintigraphy can be used to confirm the presence of a biliary leak (Fig. 14). In these studies, the radiotracer is taken up by hepatocytes and excreted into the biliary system. Identification of radiotracer in the peritoneum that does not conform to the bowel is evidence of a leak. These studies can confirm the presence of a leak but do not reveal the source or site of the leak. In recent years, MR imaging with hepatobiliary contrast agents has been shown to be a powerful diagnostic option for the detection and characterization of bile leaks. As discussed earlier, these agents are taken up by hepatocytes and partially excreted in bile. Imaging during the hepatobiliary phase may not only show a leak as extravasated contrast but also identify the precise location of the injury (Fig. 14). If hepatocyte function is impaired, biliary excretion is diminished, which could decrease diagnostic sensitivity. Standard MRCP imaging is also helpful in the evaluation of bile duct trauma. These sequences may show the injury as a stricture or disruption of the duct. Free fluid adjacent to the duct may also be seen.38 Image-guided aspiration may be required to confirm the diagnosis. Smaller leaks may resolve without intervention. Larger leaks may require percutaneous drainage, stent placement, or surgical repair.37
Conclusion Patients with suspected biliary disease can pose a diagnostic challenge because of nonspecific clinical symptoms, physical findings, and laboratory abnormalities. A specific diagnosis can often be made when key imaging findings are assessed in the context of pertinent clinical information. Diagnostic imaging plays a crucial role in the initial evaluation and surveillance of patients with biliary disease.
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References 1. Harvey RT, Miller WT Jr.: Acute biliary disease: Initial CT and follow-up US versus initial US and follow-up CT. Radiology 213:831-836, 1999 2. Blackbourne LH, Earnhardt RC, Sistrom CL, et al: The sensitivity and role of ultrasound in the evaluation of biliary obstruction. Am Surg 60:683-690, 1994 3. Shanbhouge AK, Tirumani SH, Prasad SR, et al: Benign biliary strictures: A current comprehensive clinical and imaging review. Am J Roentgenol 197:W295-W306, 2011 4. Yeh BM, Liu PS, Soto JA, et al: MR imaging and CT of the biliary tract. Radiographics 29:1669-1688, 2009 5. Tamm EP, Balachandran A, Bhosale P, et al: Update on 3D and multiplanar MDCT in assessment of biliary and pancreatic pathology. Abdom Imaging 34:64-74, 2009 6. Gupta RT, Brady CM, Lotz J, et al: Dynamic MR imaging of the biliary system using hepatocyte-specific contrast agents. Am J Roentgenol 195:405-413, 2010 7. Baron RL, Tublin ME, Peterson MS: Imaging the spectrum of biliary tract disease. Radiol Clin North Am 40:1325-1354, 2002 8. Anderson SW, Rho E, Soto JA: Detection of biliary duct narrowing and choledocholithiasis: Accuracy of portal venous phase multidetector CT. Radiology 247:418-427, 2008 9. Mandelia A, Gupta AK, Verma DK, et al: The value of magnetic resonance cholanio-pancreatography (MRCP) in the detection of choledocholithiasis. J Clin Diagn Res 7:1941-1945, 2013 10. Tsai HM, Lin XZ, Chen CY, et al: MRI of gallstones with different compositions. Am J Roentgenol 182:1513-1519, 2004 11. Milella M, Alfa-Wali M, Leuratta L, et al: Percutaneous transhepatic cholangiography for choledocholithiasis after laparoscopic gastric bypass surgery. Int J Surg Case Rep 5:249-252, 2014 12. Moser AJ: Benign biliary strictures. Curr Treat Options Gastroenterol 4:377-387, 2001 13. Vitellas KM, Keogan MT, Freed KS, et al: Radiologic manifestations of sclerosing cholangitis with emphasis on MR cholangiopancreatography. Radiographics 20:959-975, 2000 14. Karlsen TH, Schrumpf E, Boberg KM: Update on primary sclerosing cholangitis. Dig Liver Dis 42:390-400, 2010 15. Dave M, Elmunzer BJ, Dwamena BA, et al: Primary sclerosing cholangitis: meta-analysis of diagnostic performance of MR cholangiopancreatography. Radiology 256:387-396, 2010 16. Ito K, Mitchell DG, Outwater EK, et al: Primary sclerosing cholangitis: MR imaging features. Am J Roentgenol 172:1527-1533, 1999 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 226:675-685, 2003 18. Leyendecker JR, Tchelepi H: Gallbladder and bile ducts. in Dalrymple NC, Leyendecker JR, Oliphant M (eds.), Philadelphia, PA: Mosby Elsevier, 340-366, 2009 19. Lim JH, Park CK: Pathology of cholangiocarcinoma. Abdom Imaging 29:540-547, 2004 20. Masselli G, Gualdi G: Hilar cholangiocarcinoma: MRI/MRCP in staging and treatment planning. Abdom Imaging 33:444-451, 2008 21. Choi BI, Lee JM, Han JK: Imaging of intrahepatic and hilar cholangiocarcinoma. Abdom Imaging 29:548-557, 2004 22. Ayuso JR, Pages M, Darnell A: Imaging bile duct tumors: Staging. Abdom Imaging 38:1071-1081, 2013 23. Lim JH: Cholangiocarcinoma: Recent advances in imaging and intervention. Abdom Imaging 29:538-539, 2004 24. Chung YE, Kim MJ, Park YN, et al: Varying appearances of cholangiocarcinoma: Radiologic-pathologic correlation. Radiographics 29:683-700, 2009 25. Abdallah AA, Krige JE, Bornman PC: Biliary tract obstruction in chronic pancreatitis. HPB (Oxford) 9:421-428, 2007 26. Kamisawa T, Funata N, Hayshi Y, et al: A new clinicopatholological entity of IgG4-related autoimmune disease. J Gastroenterol 38: 982-984, 2003 27. Hedgire SS, McDermott S, Borczuk D, et al: The spectrum of IgG4related disease in the abdomen and pelvis. Am J Roentgenol 201: 14-22, 2013
196 28. Tokala A, Khalili K, Menezes R, et al: Comparative MRI analysis of morphologic patterns of bile duct disease in IgG4-related systemic disease versus primary sclerosing cholangitis. Am J Roentgenol 202:536-543, 2014 29. Ohara H, Okazaki K, Tsubouchi H, et al: Clinical diagnostic criteria of IgG4-related sclerosing cholangitis 2012. J Hepatobiliary Pancreat Sci 19:536-542, 2012 30. Buis CI, Hoekstra H, Verdonk RC, et al: Causes and consequences of ischemic-type biliary lesions after liver transplantation. J Hepatobiliary Pancreat Surg 13:517-524, 2006 31. Valls C, Alba E, Cruz M, et al: Biliary complications after liver transplantation: Diagnosis with MR cholangiopancreatography. Am J Roentgenol 184:812-820, 2005 32. Sandrasegaran K, Alazmi WM, Tann M, et al: Chemotherapyinduced sclerosing cholangitis. Clin Radiol 61:670-678, 2006
M.K. Feldman and C. Coppa 33. Abdalian R, Heathcote EJ: Sclerosing cholangitis: A focus on secondary causes. Hepatology 44:1063-1074, 2006 34. Tonolini M, Bianco R: HIV-related/AIDS cholangiopathy: Pictorial review with emphasis on MRCP findings and differential diagnosis. Clin Imaging 37:219-226, 2013 35. Kim SW, Shin HC, Kim HC, et al: Diagnostic performance of multidetector CT for acute cholangitis: Evaluation of a CT scoring method. Br J Radiol 85:770-777, 2012 36. Patel NB, Oto A, Thomas S: Multidetector CT of emergent biliary pathologic conditions. Radiographics 33:1867-1888, 2013 37. Melamud K, LeBedis CA, Anderson SW, et al: Biliary imaging: Multimodality approach to imaging of biliary injuries and their complications. Radiographics 34:613-623, 2014 38. Ragozzino A, De Ritis R, Mosca A, et al: Value of MR cholangiography in patients with iatrogenic bile duct injury after cholecystectomy. Am J Roentgenol 183:1567-1572, 2004
Introduction Biliary obstruction may be suspected in a patient who presents with colicky right upper quadrant abdominal pain, abnormal liver and bile chemistries, or jaundice. Initial imaging studies are typically obtained to establish the presence or absence of biliary obstruction. When biliary obstruction is confirmed, imaging studies must then be scrutinized to determine the level, and if possible, the cause of obstruction. Bile duct stones and benign and malignant strictures are the most commonly encountered sources of biliary obstruction. Interventional procedures aimed at alleviating or bypassing biliary obstructions can offer symptomatic relief, treat complications of obstruction, or act as a bridge before definitive surgery or intervention. Biliary leak may be iatrogenic or result from trauma. Patients with biliary leak typically present with significant abdominal pain, anorexia, and malaise. Initial imaging studies may show the presence of free fluid or a fluid collection in the abdomen. Advanced imaging can confirm biliary leak and in some instances can show the location of
Section of Abdominal Imaging, Imaging Institute, Cleveland Clinic, Cleveland, OH. Address reprint requests to Myra K. Feldman, MD, Section of Abdominal Imaging, Imaging Institute, Cleveland Clinic, 9500 Euclid Ave A-21, Cleveland, OH 44195. E-mail: [email protected]
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the leak. Interventional procedures can then be used to confirm the diagnosis and control or bypass the leak. In this article, common causes of biliary obstruction (including stone disease and benign and malignant strictures) and biliary leaks are reviewed. Emphasis is placed on using a multimodality approach to assess the imaging findings of biliary pathology frequently encountered by the interventional radiologist.
Imaging Ultrasound (US) is often the first imaging study ordered in a patient with suspected biliary disease. Compared with other imaging modalities, US is less expensive, is widely available, does not use ionizing radiation, and is well tolerated by patients. US is widely regarded as a highly sensitive study for the detection of biliary obstruction. Studies have shown that for the evaluation of patients with acute right upper quadrant pain, US is more effective than computed tomography (CT) because of its superior sensitivity for the detection of cholelithiasis, a common cause of these symptoms.1 US is also useful for establishing the level of biliary obstruction, with a reported accuracy of more than 90%.2 This modality falls short when it comes to identifying the cause of obstruction, with accuracy rates ranging from 30%-70%.3 US may also be technically compromised in individuals with large body habitus, limited scanning window, or excessive bowel gas.
1089-2516/15/$ - see front matter & 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2015.07.001
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CT and magnetic resonance (MR) imaging with or without MR cholangiopancreatography (MRCP) can also be used to evaluate the biliary tract. Both modalities allow visualization of the bile ducts beyond an obstruction, as well as sources of extrinsic duct narrowing. In addition, both modalities image a large field of view and may reveal abnormalities outside the biliary tract contributing to a patient’s symptoms. Advantages of CT include quicker scanning and fewer image artifacts as compared with MR. MR offers imaging without ionizing radiation and improved identification of stones. Ultimately, the choice of which modality to use may rely on preference or local expertise.4 Unenhanced CT imaging plays a limited role in evaluation of the biliary tract but can potentially add value as some biliary stones cause high attenuation and may be more conspicuous on CT scans performed without contrast (Fig. 1). Dilated bile ducts can be seen with standard portal venous phase contrast-enhanced CT obtained 70-80
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seconds after intravenous contrast administration. Arterial phase imaging can be helpful when pancreatic, hepatic, or other hypervascular malignancies are suspected. When cholangiocarcinoma is suspected, imaging performed 1020 minutes after contrast administration may be helpful owing to delayed enhancement of the fibrous stroma within these tumors (Fig. 1). Positive enteric contrast should be avoided in patients with suspected biliary pathology, as this contrast may obscure pathology at the ampulla. Administration of a neutral contrast agent such as VoLumen (Bracco Diagnostics, Monroe Township, NJ) immediately before the scan distends the duodenum and improves visualization (Fig. 1). Coronal and sagittal reconstructions and 3-dimensionally (3D) rendered postprocessing techniques may also be helpful in evaluation of the biliary tree. Direct CT cholangiography can be performed with contrast injected into the biliary system via the percutaneous or endoscopic retrograde cholangiopancreatography approach. Indirect CT cholangiography can be
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Figure 1 Coronal reformatted contrast-enhanced CT image (A) shows dilated CBD with abrupt cutoff. Highattenuation material in the lumen of the distal CBD (white arrowhead) could be a stone or a mass. Axial unenhanced CT image (B) from the same patient shows that the filling defect is a well-defined, round, highattenuation stone (white arrow). Axial contrast-enhanced CT (C) performed during the portal venous phase in a different patient shows an intrahepatic cholangiocarcinoma with heterogeneous enhancement and indistinct borders (black arrows). Axial contrast-enhanced CT (D) performed 10 minutes after contrast administration shows the same lesion with homogeneous delayed enhancement (dashed black arrows). Coronal contrast-enhanced CT (E) performed during the arterial phase of contrast enhancement with neutral enteric contrast agent shows a hypervascular carcinoid tumor in the second portion of the duodenum (dashed white arrow). The duodenum is well distended by the neutral oral contrast agent, allowing excellent visualization of this tumor. There is no associated biliary obstruction in this case.
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186 performed with agents that are excreted into the biliary system. This practice is not widespread and has the potential for increased risk of allergy.4,5 The biliary system can be evaluated by standard MR sequences with and without contrast enhancement. MRCP imaging can be performed using 2D or 3D heavily T2weighted techniques. The 2D “thick-slab” MRCP technique is a useful way to evaluate the entire biliary system. These thick-section images are often obtained in coronal and oblique views and include the entire pancreaticobiliary tree in a single image. The 3D MRCP technique typically covers the biliary tree in 15-20 images. These thinner sections are helpful for identifying filling defects such as stones and are not compromised by intersection gaps. A maximum intensity projection image can be created from the 3D data sets to obtain a similar overall view of the biliary tree as seen in the 2D technique (Fig. 2). The main disadvantage of the 3D technique is increased time for image acquisition compared with the 2D technique.4 Newer hepatocyte-specific contrast agents such as gadoxetate (gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid [Gd-EOBDTPA], Eovist; Bayer HealthCare,
Berlin, Germany) are excreted via the biliary system (in addition to the urinary system) and can be used to create an MR cholangiogram by opacifying the bile ducts. This is accomplished by acquiring 3D gradient echo T1-weighted images 20-40 minutes after injection, at which time the bile ducts are opacified with contrast. These agents have the potential to delineate bile duct anatomy and morphology and to assess for bile duct leaks (Fig. 2).6
Biliary Obstruction There is variability in the literature regarding the normal size of the common bile duct (CBD). In general, the common hepatic duct and CBD should measure less than 7 mm by US (luminal diameter measurement) or less than 8-10 mm by CT and MR (measurements inclusive of biliary walls). Intrahepatic bile ducts are considered dilated by CT or MR when they measure greater than 2 mm or greater than 40% of the adjacent portal vein diameter.7 When dilated bile ducts are identified by any modality, the next step is to identify the level of obstruction.
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Figure 2 Thick-slab 2D MRCP image (A) in a patient with PSC shows multiple segmental strictures (white arrowheads). Coronal maximum intensity projection (MIP) MRCP image (B) acquired from the same patient on the same day shows more branches and strictures (white arrows) of the biliary tree compared with the 2D technique. MIP MRCP image (C) in a different patient with acute cholecystitis shows dilated intrahepatic bile ducts but fails to show the cystic duct (dashed white arrow) and gallbladder stones (white arrowheads) that were identified on the 3D MRCP image (D). These stones were not seen on the MIP image, which displays only the maximum-intensity signal. MIP image from 3D MRCP (E) in a potential living donor for hepatic transplant shows that the CBD is normal in course and caliber. The intrahepatic ducts are not seen. Coronal T1-weighted image (F) obtained during the hepatobiliary phase after intravenous administration of gadoxetate in the same patient as seen in (B). The bile ducts are now well visualized as hyperintense branching structures. The right hepatic duct joins the CBD (black arrow). This variant anatomy was not seen with the standard MRCP technique; knowledge about this anatomy is crucial for surgical planning.
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Figure 3 Transabdominal US image of the CBD in the sagittal plane (A) shows echogenic shadowing stone in the CBD (white arrow). Smaller stones more distally in the CBD are echogenic but do not shadow (dashed white arrow). Axial contrast-enhanced CT image (B) in a different patient shows a high-attenuation stone in the CBD (white arrowhead). The stone in the gallbladder is of peripherally high attenuation but centrally has attenuation similar to that of bile (black arrow). Thick-slab MRCP image (C) shows T2 hypointense filling defect in the CBD compatible with a stone (curved dashed white arrow). Unenhanced T1-weighted gradient echo image (D) shows that this stone is T1 hyperintense (curved white arrow).
Different disease processes affect characteristic portions of the biliary tree, so defining the level of the obstruction can be a clue to the underlying etiology. The presence or absence of intraductal filling defects should be established. Bile duct wall thickness, enhancement, and texture (smooth vs irregular) should be scrutinized. Peribiliary tissues should be evaluated for edema or masses. If present, stricture morphology and length can also help determine the cause of obstruction. Commonly encountered causes of biliary obstruction include choledocholithisis, iatrogenic injury, primary sclerosing cholangitis (PSC), neoplasm, and secondary forms of cholangitis such as chronic pancreatitis, autoimmune-mediated disease, and ischemic cholangitis.
Choledocholithasis Choledocholithasis is the most common cause of biliary obstruction. It is possible to detect CBD stones by US when a suitable imaging window is present. The CBD is often identified at the hepatic hilum on US but may be obscured by the ampulla because of shadowing by bowel gas. Imaging the patient in the left lateral decubitus position can improve visualization of this region, as the gallbladder serves as an acoustic window. Biliary stones appear as echogenic structures within the duct with
posterior acoustic shadowing. Stones smaller than 3 mm may not produce an acoustic shadow (Fig. 3). On MR and CT, stones lie in the dependent portion of the bile ducts. Stones have a variable appearance on CT based on their composition. Biliary stones may be of high attenuation on CT because of calcium content or low attenuation because of nitrogen gas content. Stones with cholesterol content may be isoattenuating to bile and thus difficult to see on CT (Fig. 3).4 The overall sensitivity for detection of choledocholithiasis by multidetector CT is modest, ranging from 72%-78%, whereas specificity is high, ranging from 95%-96%.8 MRCP is both highly sensitive (95%) and highly specific (90%) for the detection of CBD stones.9 On MR, calculi are best seen on T2-weighted images, where they stand out as hypointense filling defects against a background of hyperintense bile. The T1 signal characteristics of stones vary with composition. Some pigmented stones show mild T1 hyperintense signal, whereas cholesterol stones classically demonstrate T1 hypointense signal (Fig. 3).10 It is important to confirm the presence of a filling identified on an MRCP image in more than a single sequence or plane to avoid a potential misdiagnosis. Pneumobilia also appears as a T2 hypointense filling defect on MR but can be differentiated from stones by its nondependent position in the ducts. Occasionally, the hepatic artery may simulate a filling defect on MRCP images where it
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Figure 4 Thick-slab 2D MRCP image (A) shows an apparent filling defect in the common hepatic duct, which could be mistaken for a stone (white arrow). Sagittal half-Fourier acquisition single-shot turbo spin echo (HASTE) image (B) in the same patient shows flow void from the hepatic artery (dashed white arrow) adjacent to the T2 hyperintense common hepatic duct. There is no stone or filling defect in the CBD.
crosses the CBD (Fig. 4). Surgical clips may also cause apparent filling defects on MRCP. In this case, a comparison with CT (if available) can be helpful. Choledocholithiasis is usually managed endoscopically, but there is a role for percutaneous transhepatic
management for patients with altered anatomy (eg, patients with Roux-en-Y gastric bypass or biliary enteric anastomosis) or for patients in whom the endoscopic approach fails.11 Transhepatic techniques can also be used in patients with hepatolithiasis.
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Figure 5 Thick-slab MRCP (A) and coronal HASTE (B) images in a patient with prior hepaticojejunostomy show marked intrahepatic biliary duct dilation with stricture of the duct at the hepaticojejunostomy (white arrow). Images from percutaneous transhepatic cholangiogram during placement of external-internal biliary catheter show the smooth stricture (black arrow) (C) and the external-internal biliary catheter positioned across the stricture (D).
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Figure 6 MIP 3D MRCP image (A) shows multiple strictures (white arrows) of the intrahepatic bile ducts with intervening normal-caliber bile ducts in a patient with PSC and prior choledochoduodenostomy. Thick-slab 2D MRCP image (B) in a different patient shows more conspicuous changes of PSC with innumerable focal intrahepatic bile duct strictures alternating with mildly dilated ducts, creating a “string of beads” appearance. Axial T1 contrast-enhanced MR image (C) from a different patient with PSC shows multiple focally dilated bile ducts with circumferential wall thickening and increased enhancement (black arrows). Coronal contrast-enhanced CT image (D) from a different patient with PSC shows circumferential wall thickening involving the common hepatic duct (dashed white arrows). Axial contrast-enhanced CT image (E) in a different patient with PSC-associated cirrhosis. The lateral lobe (white arrowhead) is atrophic and the caudate is hypertrophied (dashed black arrows), giving the liver a round, macrolobulated shape.
Iatrogenic Stricture Iatrogenic injury is the most common cause of benign biliary stricture. Iatrogenic biliary strictures occur after upper gastrointestinal tract surgeries (cholecystectomy, orthotopic liver transplantation [OLT], choledochocyst repair, and choledochojejunostomy) or endoscopic procedures.3 Operative injuries following cholecystectomy can
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be attributed to variant anatomy or technical failure and tend to involve the common hepatic duct or CBD.12 Biliary strictures are the most common complication after OLT, with strictures most commonly identified at the biliary anastomosis due to fibrosis. Biliary strictures proximal to the anastomosis in patients who have undergone OLT are usually secondary to ischemic injury, described later in
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Figure 7 Thick-slab MRCP image (A) shows markedly dilated bile ducts (dashed white arrows) and pancreatic duct (white arrowhead) with abrupt cutoff at the level of the pancreatic head (white star). This is the “double-duct sign,” indicative of pancreatic adenocarcinoma, the diagnosis in this patient. Coronal HASTE image (B) in a different patient with long-segment CBD stricture (white arrow). Axial T1 contrast-enhanced MR image (C) in the same patient as in (B) shows enhancing carcinomatosis in the porta hepatis at the level of obstruction (curved arrows).
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Figure 8 Transabdominal US image of the left lobe (A) shows dilated intrahepatic bile ducts (dashed white arrow). MRCP image (B) in the same patient shows markedly dilated left intrahepatic ducts (dashed white arrow) and mildly dilated right intrahepatic ducts (solid white arrow). The right and left ducts do not communicate because of a Klatskin tumor involving the biliary confluence. Axial unenhanced T1 MR image (C) from a different patient with intrahepatic mass-forming cholangiocarcinoma and overlying hepatic capsular retraction (white arrowheads). Axial T1 contrast-enhanced MR performed during the arterial (D) and venous (E) phase of contrast enhancement shows early peripheral enhancement (black arrow) and delayed central enhancement (dashed black arrow) of the tumor. Images also show capsular retraction and vascular encasement. Axial contrast-enhanced CT (F and G) from a different patient with peribiliary cholangiocarcinoma (black star), which extends along the right hepatic duct (F) and CBD (G).
this article.3,13 In general, iatrogenic strictures are identified on imaging by their location at the surgical site and smooth, tapered appearance (Fig. 5). Although these features may suggest iatrogenic injury as the underlying cause of a stricture, tissue diagnosis is often required to exclude underlying malignancy.
Primary Sclerosing Cholangitis PSC is a chronic disorder characterized by inflammation and fibrosis of the bile ducts. In patients of Northern European descent, 62%-83% of those with PSC also have
inflammatory bowel disease, typically ulcerative colitis.14 MRCP is highly sensitive and specific for the diagnosis of PSC.15 The disorder can involve the intrahepatic and extrahepatic bile ducts. Isolated intrahepatic involvement occurs in roughly 28% of patients; isolated extrahepatic involvement is rare.14 Imaging findings of PSC vary based on the stage or severity of disease. Initially, focal biliary strictures alternating with segments of normal-caliber ducts are identified. When focal strictures are accompanied by mildly dilated bile ducts, the biliary tree is likened to a “string of beads” on MRCP images (Fig. 6). Imaging in patients with
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Figure 9 Coronal contrast-enhanced CT image (A) shows smooth distal CBD stricture (white arrowheads) with upstream dilation of CBD in a patient with chronic pancreatitis. Coronal contrast-enhanced CT through the pancreatic head (B) shows multiple pancreatic calcifications (black arrows) with no associated mass, a characteristic finding of chronic pancreatitis.
more advanced disease may demonstrate longer strictures with obliteration of ducts. When the peripheral ducts become obliterated, the biliary tree may have a “pruned tree” appearance on MRCP. The degree of duct dilation in patients with PSC is usually not marked due to peribiliary fibrosis. Circumferential bile duct wall thickening with increased enhancement may be seen on contrast-enhanced CT or MR (Fig. 6). Patients with PSC may also develop biliary stones (hepatolithiasis).13,16 Many patients with PSC go on to develop cirrhosis. Caudate hypertrophy occurs more commonly in patients with PSC-associated cirrhosis than in those with other forms of cirrhosis. Macronodular cirrhotic liver morphology, peripheral atrophy, and peripheral wedge or bandlike areas of parenchymal fibrosis are also seen in patients with PSC cirrhosis (Fig. 6).17 Patients with PSC are at increased risk for the development of cholangiocarcinoma, which can be difficult to detect. Recognition of a new mass, a dominant stricture, or dilated bile ducts in a segment of the liver out of proportion to the degree of dilation in other portions
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of the liver should raise suspicion for underlying cholangiocarcinoma.18
Neoplasm Malignant obstruction of the bile ducts can be caused by primary malignancy of the bile ducts (cholangiocarcinoma), malignant tumor invasion of the biliary tree, or external compression. Compared with benign strictures, neoplastic biliary strictures tend to cause abrupt duct cutoff. The degree of upstream dilation may be greater than with a benign obstruction. Extrinsic tumors can displace or encase the bile ducts, causing narrowing or complete obstruction. Pancreatic adenocarcinoma located in the pancreatic head can obstruct both the CBD and pancreatic duct, causing the “double-duct sign” (Fig. 7). Other local primary malignancies (gallbladder, duodenal, and gastric adenocarcinomas) and metastatic disease (nodal or carcinomatosis) may obstruct the biliary tree in a similar manner (Fig. 7). Hepatocellular carcinoma can extrinsically compress or
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Figure 10 Coronal MRCP image (A) from a patient with a clinical diagnosis of ISD shows multiple focal intrahepatic strictures (white arrows). There is also a stricture of the common hepatic duct (dashed white arrow). Axial contrastenhanced T1-weighted MR images (B and C) show circumferential wall thickening of the intrahepatic bile ducts (B) (solid black arrow) and extrahepatic common hepatic duct (C) (dashed black arrow). The degree of wall thickening is greater than is typically seen with PSC.
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Figure 11 Axial arterial phase contrast-enhanced CT image (A) in a patient who has undergone OLT shows thrombosis of the hepatic artery (white arrow). Axial portal venous phase contrast-enhanced CT image (B and C) shows irregular fluid attenuation tracks in a biliary or peribiliary distribution (black arrows), compatible with biliary necrosis from ischemic injury.
invade the biliary tree. Lymphoma can surround the ducts without causing obstruction.7 Cholangiocarcinoma is a primary malignant neoplasm of the bile ducts. Chronic inflammation of the bile ducts due to a variety of underlying etiologies leads to an increased risk for cholangiocarcinoma. In Western countries, PSC is a leading risk factor. Cholangiocarcinoma can involve the intrahepatic or extrahepatic bile ducts and is classified into 3 distinct morphologic forms: periductal infiltrating, mass forming, and intraductal. In the periductal infiltrating form of cholangiocarcinoma, the tumor grows along the bile duct without forming a distinct mass. This form is most often seen at the hepatic hilum (Klatskin tumor).19,20 On contrast-enhanced MR and CT, this type of tumor causes irregular increased enhancement along the ducts. Dilated bile ducts in the right and left lobes that do not communicate at the confluence should raise suspicion for a hilar cholangiocarcinoma (Fig. 8). The mass-forming subtype of cholangiocarcinoma most commonly involves the intrahepatic bile ducts.21 On imaging, these lesions show peripheral enhancement early on with gradual central enhancement on delayed imaging obtained 10-15 minutes after contrast administration. The center of the tumor may enhance less than the background liver on delayed images when necrosis or mucin is present. Capsular retraction, satellite nodules, vascular encasement, and hepatic atrophy may also be observed. On unenhanced MR images, the lesions are typically T1 hypointense and T2 hyperintense.22 The signal within the lesions centrally on T2-weighted imaging is variable based on the amount of fibrous tissue, mucin, or necrosis (Fig. 8). The intraductal form of cholangiocarcinoma tends to be a slow-growing malignancy with a better prognosis.23 This form of cholangiocarcinoma has a varied appearance on imaging, including sessile or polypoid intraductal masses, cast-like intraductal mass, and stricture.24
Chronic Pancreatitis Patients with chronic pancreatitis may develop strictures in the distal pancreatic portion of the CBD because of repeated episodes of inflammation and subsequent
fibrosis. The reported incidence of benign biliary strictures in patients with chronic pancreatitis varies widely in the literature, ranging from 3%-46%. Clinically, patients with this condition may present with abdominal pain, jaundice, and biochemical abnormalities. Some individuals are asymptomatic, with strictures discovered incidentally.25 In addition to distal CBD strictures, other imaging manifestations of chronic pancreatitis, including pancreatic calcifications, pancreatic atrophy, and an irregularly dilated pancreatic duct, may be seen on imaging studies (Fig. 9).
Autoimmune-Mediated Disease IgG4 systemic disease (ISD) was first recognized as a disease with effects on the biliary system in 2003.26 The
Figure 12 Coronal MR HASTE image in a patient with AIDSrelated cholangiopathy shows dominant distal CBD stricture to the level of the ampulla (dashed white arrow). Extrahepatic strictures are commonly seen in AIDS-related cholangiopathy, with papillary stenosis occurring in up to 75% of patients. The intrahepatic ducts are irregular, with focal intrahepatic strictures (white arrows) and a dilated, beaded appearance. Intrahepatic imaging findings of HIV cholangiopathy are identical to those seen with PSC. This rare disorder is typically seen in severely immunocompromised patients (CD4 less than 100).34
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Figure 13 Patient with a history of biliary ischemia and multifocal biliary strictures and leaks presented to the emergency department with new-onset abdominal pain and fever. Axial contrast-enhanced CT image (A) shows multiple dilated bile ducts with internal high-attenuation material (white arrow). T2 MR image (B) in the same patient shows T2 hypointense material centrally within the duct with surrounding T2 hyperintense bile (dashed white arrows). The material did not enhance on postcontrast imaging (not shown). Subsequent ERCP revealed pus and blood products within the ducts. Contrast-enhanced CT image (C and D) from a different patient with chronic biliary obstruction from PSC and new-onset cholangitis shows dilated bile ducts in the left lobe (C) and new left portal vein thrombosis (black arrow) (D). Contrast-enhanced T1 MR image (E) in the same patient shows smooth, circumferential bile duct wall thickening with increased enhancement (curved white arrow) and peripheral areas of transient increased hepatic signal (white arrowheads).
disease is characterized by inflammation, fibrosis, and a lymphoplasmacytic infiltrate rich in IgG4 plasma cells. The biliary system is the second most common site of ISD outside the pancreas. MR with MRCP imaging is the preferred imaging modality for the evaluation of patients with suspected ISD affecting the bile ducts. Imaging in these patients shows bile duct wall thickening with postcontrast enhancement and luminal narrowing (Fig. 10). There is overlap between the imaging appearance of ISD-related biliary disease and that of PSC; distinguishing between the 2 conditions on imaging can be difficult.27 A study by Tokala et al28 showed that CBD wall thickness greater than 2.5 mm, continuous biliary tree involvement, gallbladder involvement, and absence of liver parenchyma abnormalities can be used to predict a diagnosis of ISD as opposed to PSC. Imaging findings of other extrabiliary forms of ISD (pancreatic, renal, or retroperitoneal) may also help narrow the diagnosis. Ultimately, the diagnosis is made based on a combination of elevated serum IgG4 levels, typical imaging findings of ISD involving the biliary
system or other characteristic locations, and typical features on histopathology.29 It is important that this condition be diagnosed correctly, as patients with ISD-related strictures may respond to treatment with steroids, potentially obviating the need for invasive interventions.
Ischemic Cholangiopathy Unlike the hepatic parenchyma, which receives its vascular supply from both the portal venous system and the hepatic arteries, the bile ducts are supplied solely by the hepatic artery. Ischemic bile duct injuries were originally described in the setting of hepatic artery thrombosis, but in patients who have undergone OLT, this pattern of injury has also been identified in those without hepatic artery thrombosis. Studies have shown that in the OLT population, ischemictype biliary injuries may also arise from prolonged ischemia time, reperfusion injury, preservation solutions, or immunologic injury.30 When biliary ischemia leads to necrosis, dilated bile ducts and bilomas are identified on
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Figure 14 Axial contrast-enhanced CT image (A) in a patient with increasing abdominal pain and leukocytosis 2 days after cholecystectomy shows free fluid (white arrows) surrounding the liver. Image from CT-guided aspiration and drain placement (B) shows needle tip within the fluid (dashed white arrow). The diagnosis of biliary leak was confirmed by percutaneous aspiration. Image from hepatobiliary iminodiacetic acid (HIDA) scan performed 90 minutes after radiotracer injection (C) in a different patient with bile leak from a perforated gallbladder. Leaked radiotracer has accumulated along the right lateral surface of the liver (black arrow). Axial T1weighted MR image obtained during the hepatobiliary phase (D) after gadoxetate disodium injection in a different patient with prior hepaticojejunostomy shows excreted T1 hyperintense contrast in the biliary tree (curved white arrow). T1-weighted MIP image (E) obtained during the hepatobiliary phase of contrast enhancement shows bile leak at the level of the hepaticojejunostomy with extra luminal contrast accumulated anteriorly (black arrowheads).
imaging. This pattern is usually seen in conjunction with arterial thrombosis (Fig. 11). Hilar strictures, dilated bile ducts, and biliary casts can be seen in cases of biliary ischemia with or without arterial thrombosis.31 Chemotherapy-induced cholangitis after hepatic arterial chemotherapy is also an ischemic type of secondary cholangiopathy. This form of cholangitis causes segmental or diffuse biliary strictures. The cystic duct and common hepatic duct may be involved, but the intrapancreatic segment of the CBD is spared, likely due to a separate vascular supply by the gastroduodenal artery.32
Secondary Sclerosing Cholangitis Secondary sclerosing cholangiopathies may have imaging features that overlap with those of PSC, but these conditions arise from a known underlying pathologic process. In addition to some of the more commonly encountered causes of secondary cholangitis previously described (eg, chronic pancreatitis, autoimmune sclerosing disease, and
ischemic cholangiopathy), there are many other causes, including AIDS-related cholangiopathy (Fig. 12), portal biliopathy, eosinophilic cholangitis, inflammatory pseudotumor, and recurrent pyogenic cholangitis.33,34 These are rarely encountered and beyond the scope of this review.
Ascending Cholangitis Acute (ascending) cholangitis is a complication of biliary obstruction but may also arise as a complication after transhepatic or endoscopic biliary procedures. Patients with this condition commonly present with Charcot’s triad of symptoms, including right upper quadrant abdominal pain, fever, and jaundice. Imaging should be performed to evaluate the site and cause of obstruction so that an approach to biliary decompression can be planned. Imaging by any modality may show dilated bile ducts. Purulent material may cause the bile to have a complex appearance with increased attenuation on CT (Fig. 13). The bile duct walls may also appear thickened with increased
Noninvasive imaging of the biliary tree enhancement (Fig. 13).7 Areas of transient hepatic attenuation difference are often identified during the arterial phase of contrast-enhanced CT imaging in patients with acute cholangitis.35 Scans should also be evaluated for complications of acute cholangitis, including hepatic abscess, bile peritonitis, portal vein thrombus, and biliary strictures (Fig. 13).36
Biliary Leak Bile leaks may occur after trauma or as an iatrogenic injury after surgery (cholecystectomy, OLT, liver resection, or biliary enteric anastomosis), liver biopsy, liver ablation procedures, or biliary stent manipulation. Clinically, patients may present with significant abdominal pain, anorexia, and malaise.37 Bile duct leaks appear as intrahepatic or extrahepatic fluid on all imaging modalities (US, CT, and MR). This appearance is nonspecific, as other low-attenuation abdominal fluid such as seroma, leak from another source, or ascites can have a similar appearance. Although the location of fluid and clinical context may suggest the diagnosis, confirmatory imaging or aspiration to confirm the location may be warranted. Hepatobiliary scintigraphy can be used to confirm the presence of a biliary leak (Fig. 14). In these studies, the radiotracer is taken up by hepatocytes and excreted into the biliary system. Identification of radiotracer in the peritoneum that does not conform to the bowel is evidence of a leak. These studies can confirm the presence of a leak but do not reveal the source or site of the leak. In recent years, MR imaging with hepatobiliary contrast agents has been shown to be a powerful diagnostic option for the detection and characterization of bile leaks. As discussed earlier, these agents are taken up by hepatocytes and partially excreted in bile. Imaging during the hepatobiliary phase may not only show a leak as extravasated contrast but also identify the precise location of the injury (Fig. 14). If hepatocyte function is impaired, biliary excretion is diminished, which could decrease diagnostic sensitivity. Standard MRCP imaging is also helpful in the evaluation of bile duct trauma. These sequences may show the injury as a stricture or disruption of the duct. Free fluid adjacent to the duct may also be seen.38 Image-guided aspiration may be required to confirm the diagnosis. Smaller leaks may resolve without intervention. Larger leaks may require percutaneous drainage, stent placement, or surgical repair.37
Conclusion Patients with suspected biliary disease can pose a diagnostic challenge because of nonspecific clinical symptoms, physical findings, and laboratory abnormalities. A specific diagnosis can often be made when key imaging findings are assessed in the context of pertinent clinical information. Diagnostic imaging plays a crucial role in the initial evaluation and surveillance of patients with biliary disease.
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