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More Than Just Stones: A Pictorial Review of Common and Less Common Gallbladder Pathologies
More Than Just Stones: A Pictorial Review of Common and Less Common Gallbladder Pathologies Janice Ash-Miles, FRCR, Huw Roach, FRCR, Jim Virjee, FRCR, and Mark Callaway, FRCR
Although stone disease is by far the most commonly encountered pathology of the gallbladder, there are several other important disease processes affecting it. These include adenomyomatosis, cholesterolosis, polyps, porcelain gallbladder, acalculous cholecystitis, xanthogranulomatous cholecystitis, emphysematous cholecystitis, gallbladder cancer, and gallbladder hemorrhage. The purpose of this article was to review the different gallbladder pathologies encountered in everyday radiological practice and to describe their features in the standard imaging modalities.
In an imaging setting, the most frequently encountered gallbladder pathology is stone disease. There are several other less common abnormalities and anomalies of the gallbladder, both symptomatic and asymptomatic. The purpose of this article was to provide a pictorial review of the imaging features of the various gallbladder pathologies and relevant radiological interventions.
Congenital Variations Agenesis of the gallbladder occurs in less than 0.1% of the population.1 It can be associated with other congenital anomalies of the gastrointestinal tract and other systems. Hypoplastic gallbladder can be congenital or associated with cystic fibrosis. There can be variation in gallbladder location. The most common sites for ectopic gallbladder are under the left lobe of liver, intrahepatic or retrohepatic.1 From the Department of Radiology, Bristol Royal Infirmary, Bristol, United Kingdom. Reprint requests: Huw Roach, FRCR, Department of Radiology, Bristol Royal Infirmary, Marlborough Street, Bristol BS2 8HW, UK. E-mail: [email protected]. Curr Probl Diagn Radiol 2008;37:189-202. © 2008 Mosby, Inc. All rights reserved. 0363-0188/2008/$34.00 ⫹ 0 doi:10.1067/j.cpradiol.2007.12.001
Curr Probl Diagn Radiol, September/October 2008
“Floating” gallbladder describes a gallbladder with loose peritoneal reflections, which makes it more mobile than normal and prone to torsion. Septation of the gallbladder may be transverse or longitudinal, single or multiple. The most common is a “Phrygian cap,” which is a folding between the fundus and body of the gallbladder associated with a transverse septum (Fig 1). It is not clinically important but may be mistaken for a calculus on ultrasound.
Gallstones Gallstone disease is a frequent problem in developed countries and represents a major health burden. An estimated 20 to 25 million adults in the USA are afflicted with gallstones2 with prevalences in Europe similarly ranging from 5.9 to 21.9%.3 Females have an increased risk of gallstone disease but this additional risk diminishes after the menopause. Postmenopausal women on estrogen replacement show a continued increase in risk, however.4 Obesity is also an established major risk factor for developing gallstones due to the increased hepatic secretion of cholesterol. Ethnicity is an important risk factor with higher rates in Native Americans, and those of Hispanic and Northern European descent. Ethnicity can also determine the type and position in the biliary tract of stones. In developed countries, 80 to 85% of calculi contain cholesterol, either on its own or mixed with calcium compounds. In East Asia, brown pigment stones are predominant. These more readily form in bile ducts, usually in association with infection. This accounts for the higher prevalence of intrahepatic duct stones.5 Bile salt malabsorption leads to bile salt depletion and results in hepatic secretions that are saturated in
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FIG 1. Ultrasound image showing gallbladder septation (arrow).
cholesterol. As a result, patients with terminal ileal disease, eg, in Crohn’s disease, have an increased risk of developing gallstones. Other predisposing factors include diabetes, hemolytic disorders, eg, hereditary spherocytosis and sickle cell disease, cystic fibrosis, and cholestatic disorders. Conventional radiography is relatively insensitive for the detection of gallstones, but approximately 10% of calculi can be seen on X-rays (Fig 2). Computed tomography (CT) and magnetic resonance imaging (MRI) (especially magnetic resonance cholangiopancreatography (MRCP)) are more sensitive (Fig 3). Ultrasound, however, is usually the primary diagnostic imaging tool as it is noninvasive and widely available and has sensitivity and specificity greater than 95% for gallstones larger than 1.5 mm6 (Fig 4). Endoscopic ultrasound is able to detect stones too small to be seen on transabdominal ultrasound and has sensitivities in the range of 94 to 98%.7 Many gallstones are asymptomatic and 60 to 80% of patients with gallstones do not develop symptoms.8 However, they may be associated with pain, nausea, and intolerance of fatty food. Complications include cholecystitis (Fig 5), gallbladder perforation (Fig 6), abscess formation (Fig 7), biliary obstruction (Fig 8), pancreatitis, and fistulation into the gastrointestinal tract. Gallbladder cancer is also associated with chronic inflammation from gallstones. Percutaneous imaging-guided cholecystostomy can sometimes be used as a temporizing measure in patients with acute cholecystitis not responding to medical treatment and in whom surgical cholecystectomy is unsafe. Percutaneous cholecystostomy can
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FIG 2. (A) Radiograph demonstrating gallbladder calculi (arrow). Large calculus impacted at gallbladder neck is also demonstrated (arrowhead). (B) Radiograph showing multiple small calcified stones (arrows). This morphology suggests that they are pigment stones.
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FIG 3. (A) CT scan showing calcified gallbladder stone (arrow). (B) CT demonstrating noncalcified stones containing gas (arrows). (C) CT demonstrating tiny noncalcified stones (arrow). (D) T2-weighted MR showing small gallbladder calculi (arrow). (E) T2 MRCP image showing gallbladder calculi (arrows).
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FIG 4. Classical ultrasound appearance of gallbladder calculi (arrow) with acoustic shadowing.
also be utilized to achieve biliary decompression in patients with common bile duct obstruction (Fig 9). This is as a rapid alternative to the more commonly employed techniques of endoscopic retrograde cholangiopancreatography or percutaneous transhepatic cholangiopancreatography. When performing percutaneous gallbladder drainage, a transhepatic route is generally favored as this will anchor the drain and reduce the risk of leakage of bile around the drain. Other imaging-guided treatments for gallstones include lithotripsy and percutaneous extraction.
Adenomyomatosis Adenomyomatosis of the gallbladder is one of the so-called “hyperplastic cholecystoses.”9 It is characterized by hyperplasia of the gallbladder mucosa and muscularis propria10 with out-pouching of the mucosa into or through the muscularis forming diverticula known as Rokitansky–Aschoff sinuses.11 These sinuses may be filled with bile, cholesterol crystals, sludge, or calculi.10 The condition occurs in as many as 8.7% of cholecystectomy specimens12 and there is an apparent female predilection. Most diagnoses are made in middle-aged patients,10 but cases have been reported in pediatric patients.10,13 Adenomyomatosis may be generalized, localized (usually affecting the fundus), or segmental (typically an annular constriction in the body giving an “hourglass” configuration).
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FIG 5. (A) Ultrasound image illustrating thickened gallbladder wall (arrow) and pericholecystic fluid (arrowhead) in keeping with gallstone-related cholecystitis. (B) T2-weighted MR image showing pericholecystic fluid and inflammatory change (arrows) due to cholecystitis. (C) Pericholecystic inflammatory change (arrow) on CT.
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FIG 6. CT image in a patient with gallbladder perforation secondary to gallstone-related cholecystitis. Gallbladder wall defect is seen (arrow). FIG 8. MRCP image showing a “Mirizzi” type proximal biliary obstruction due to large gallbladder neck calculus (arrow). A further calculus is seen in the gallbladder body.
FIG 7. Ultrasound image showing inflamed gallbladder and associated abscess collection.
Adenomyomatosis is rarely apparent on conventional radiography. It can be demonstrated on oral cholecystography (Fig 10), but this is now rarely performed. Ultrasound is usually the primary imaging modality used for assessing the gallbladder in current practice and adenomyomatosis usually appears as focal or generalized gallbladder wall thickening (Fig 11). Rokitansky–Aschoff sinuses may appear as anechoic spaces or may give the characteristic “ringdown” artifact from cholesterol-rich material within them (Fig 12). CT appearance is similar to ultrasound but is less specific as it cannot demonstrate the
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FIG 9. Contrast injection through percutaneous cholecystostomy drainage tube, showing drain entrance into gallbladder (arrow) and obstructing common bile duct calculi (arrowhead).
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FIG 10. Oral cholecystogram showing Rokitansky–Aschoff sinuses (arrows).
“ring-down” artifact and the small cystic spaces.11,14 MRI typically demonstrates gallbladder wall thickening but can also demonstrate the Rokitansky–Aschoff sinuses. These are typically low signal on T1-weighted images and high signal on T2-weighted images. Single-shot heavily T2-weighted MRCP images is probably the most effective sequence and is specific for adenomyomatosis when it demonstrates the classical “Pearl necklace” appearance of the Rokitansky– Aschoff sinuses15 (Fig 13). This is analogous to the classical appearance seen at oral cholecystography. The demonstration of the Rokitansky–Aschoff sinuses is vital for a confident diagnosis of adenomyomatosis to be made. Where these are not visible, the thickening of the gallbladder wall and enhancement pattern are relatively nonspecific, making it difficult to distinguish from other conditions, including gallbladder cancer. This can be particularly difficult when
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FIG 11. (A) Diffuse gallbladder wall thickening of adenomyosis seen on ultrasound. Rokitansky–Aschoff sinus is shown (arrow). (B) Thickened gallbladder wall (arrow) on CT.
adenomyomatosis is focal, giving rise to a focal “mass” or adenomyoma (Fig 14).
Cholesterolosis Cholesterolosis is the other main “hyperplastic cholecystosis.” This is characterized by the deposition of triglycerides and cholesterol esters in the gallbladder wall. The combination of these deposits with mucosal hyperemia gives the appearance of “strawberry gallbladder” macroscopically. This is not demonstrable radiologically. Cholesterol deposition can also give rise to polypoid lesions (Fig 15).
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FIG 12. Cholesterol-rich material within Rokitansky–Aschoff sinuses seen on ultrasound (arrow) with associated “ring down.”
FIG 13. T2-weighted MR image showing the high signal Rokitansky– Aschoff sinuses of adenomyomatosis (arrow) aligned perpendicularly to the gallbladder lumen. (Image courtesy of Dr. Paul Burn).
Gallbladder Polyps Cholesterol polyps account for approximately 50% of polypoid lesions seen in the gallbladder.14 They are more common in women. They can be solitary or multiple and are usually small. They are often discovered incidentally at ultrasound scanning for suspected gallstones. Their typical ultrasound appearance is of a hyperechoic nonshadowing structure with a delicate stalk. Where the stalk is not visible, the polyps are difficult to distinguish from
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FIG 14. Focal adenomyosis of gallbladder fundus seen on (A) ultrasound (arrow), (B) CT (arrow), and (C) pathological specimen. (Color version of figure is available online.)
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FIG 15. “Ring down” from small cholesterol polyp (arrow) seen on ultrasound. FIG 17. Large polypoid adenoma (arrow) in gallbladder seen at ultrasound.
include patient age ⬎50 years; broad based, solitary, or enlarging polyp; and coexistent gallstones.17-19 The ultrasound appearances are of a fixed, nonshadowing sessile or pedunculated mass, which is homogeneously hyperechoic (Fig 16). They may be lobulated (Fig 17). On CT, adenomas tend to be soft-tissue intraluminal masses with attenuation close to liver. Other polypoid lesions in the gallbladder include carcinomas, metastases, inflammatory polyps, neurofibromas, and heterotopia. Endoscopic ultrasound has been suggested as a useful imaging modality in differentiating between neoplastic and nonneoplastic polypoid gallbladder lesions.20 FIG 16. Nonshadowing gallbladder filling defects on ultrasound (arrows) consistent with polyps.
Gallbladder “Sludge” nonshadowing adherent calculi. They are difficult to see at CT but may enhance with contrast.16 Gallbladder adenomas are usually intraluminal polypoid lesions. They occur more commonly in women and may be associated with Peutz–Jeghers or familial polyposis syndromes. Pathologically, adenomas are subdivided into tubular, papillary, or tubulopapillary, with tubular being the most common.14 There is a potential adenoma-carcinoma sequence and polyps over 10 mm are considered suspicious. Other potential predictors of malignancy
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Gallbladder “sludge” is echogenic material often seen after prolonged fasting or cholecystitis. It can appear mass-like but can be differentiated from solid lesions by its mobile nature (Fig 18).
Milk of Calcium Bile Milk of calcium bile is caused by the precipitation of calcium-rich material in the gallbladder. The appearance is intermediate between sludge and stones.
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FIG 18. Thick bile/sludge in gallbladder (arrows) seen at ultrasound. Echogenicity is similar to liver.
Porcelain Gallbladder Porcelain gallbladder is characterized by calcium deposition in the gallbladder wall. The pattern of calcification can be complete intramural or selective mucosal. It is due to chronic inflammation, usually associated with gallstones, although it gives rise to few symptoms per se. It is more common in females. It was believed that there was a significant link between porcelain gallbladder and gallbladder carcinoma. This is now thought less than previously and possibly only associated with the selective mucosal pattern of calcification.21 Some authors recognize no relationship with gallbladder carcinoma.22 On ultrasound, porcelain gallbladder appears as curvilinear hyperechoic gallbladder wall with acoustic shadowing (Fig 19B). There can be some diagnostic difficulty differentiating porcelain gallbladder from emphysematous cholecystitis, milk of calcium bile, or contracted gallbladder containing calculi. The calcification in the gallbladder wall can be better demonstrated on conventional radiographs or CT (Fig 19A and C).
Acalculous Cholecystitis Up to approximately 10% of cases of acute cholecystitis occur in the absence of stones23—so-called acalculous cholecystitis. It tends to occur in debilitated
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FIG 19. Calcified porcelain gallbladder (arrow) seen at (A) X-ray, (B) ultrasound, and (C) CT.
patients, eg, the critically ill on mechanical ventilation and parenteral nutrition, or following severe trauma, burns, or major surgery. It has also been described in the immunocompromised and in certain infections, eg,
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FIG 20. Gallbladder perforation (arrow) due to acalculous cholecystitis seen at CT. FIG 21. Mural gallbladder gas of emphysematous cholecystitis seen on plain X-ray.
salmonella strains. Bile stasis, cystic duct obstruction, gallbladder ischemia, and systemic infection are thought to be pathogenetic factors.23,24 Mortality rates vary, but figures as high as 65% have been reported.25 Thickening of the gallbladder wall, gallbladder distension, pericholecystic fluid, and an absence of calculi are the typical features seen at ultrasound. CT appearances are similarly nonspecific. Early diagnosis and intervention is important as perforation and gangrene can occur rapidly (Fig 20). Treatment is normally by surgical cholecystectomy, but this can be associated with significant risk in critically ill or elderly patients. Imaging-guided percutaneous cholecystostomy is increasingly being used as a temporizing measure in high-risk patients.
Xanthogranulomatous Cholecystitis Xanthogranulomatous cholecystitis (XGC) is a rare inflammatory process affecting the gallbladder, characterized by nodules or streaks in the gallbladder wall, mainly due to lipid-laden macrophages.26 Its etiology is uncertain but is thought to result from extravasation of bile into the gallbladder wall in the presence of gallstones, obstruction, and cholestasis. There is inflammation followed by a granulomatous reaction (analogous to the development of xanthogranulomatous pyelonephritis in the kidney).27 Some authors have proposed an association between XGC and tumors of the gallbladder and biliary tree.26
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XGC appears as nonspecific thickening of the gallbladder wall on ultrasound, CT, and MRI. Where visible, the characteristic features at ultrasound are the presence of hypoechoic nodules and bands.26 CT may demonstrate nonenhancing hypoattenuating nodules, which may be focal or diffuse.26,28 A hypoattenuating band around the gallbladder may also be visible.26,29 MRI may demonstrate focal or diffuse areas of high signal on T2-weighted sequences. These areas are low signal on T1-weighted sequences and show delayed enhancement with gadolinium.28 Foci of very high T2 signal are likely to represent abscess or necrosis. In/out-of-phase gradient-echo MR may demonstrate foci of signal dropout in the gallbladder wall in XGC due to the presence of fat.30
Emphysematous Cholecystitis Emphysematous cholecystitis is a variant of acute cholecystitis characterized by the presence of gas in the gallbladder wall, lumen, and pericholecystic tissue in the absence of an abnormal connection between the gallbladder and gastrointestinal tract.31 It is more common in male patients and in patients with diabetes mellitus.31,32 Initially emphysematous cholecystitis is indistinguishable from uncomplicated acute cholecystitis but can rapidly progress to ischemia, gangrene, and perforation. As such, it has
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FIG 23. CT image of focal gallbladder cancer (arrow) invading adjacent liver. FIG 22. Pathologically confirmed focal gallbladder cancer seen at ultrasound (arrow).
a higher mortality, although there may be a spectrum of severity with some patients able to be treated conservatively rather than by emergency intervention.31 Gas-forming anaerobic bacteria such as Clostridium species and Escherichia coli are often implicated. The radiological diagnosis depends on the demonstration of the gas in or around the gallbladder. Conventional radiographs may be sufficient (Fig 21). Ultrasound appearances depend on the amount of gas present.33 The presence of rising bubbles in the gallbladder is termed “effervescent gallbladder.”34 More commonly, ultrasound shows echogenic foci with posterior acoustic shadowing or ring-down artifact. With a large amount of gas, a wide band of acoustic shadowing from the gallbladder is seen.33 In these cases the gallbladder can be difficult to assess and it may be difficult to differentiate emphysematous cholecystitis from porcelain gallbladder or a contracted gallbladder full of stones. CT is probably the most sensitive modality (approaching 100%31) for diagnosing emphysematous cholecystitis and can also demonstrate the exact location of the gas. It is not usually the primary modality employed in acute cholecystitis, however. T2weighted MR shows a gas/fluid level in the gallbladder, low signal rim around the gallbladder indicating mural gas, and pericholecystic low signal, indicating gallbladder perforation.32
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FIG 24. CT image showing diffuse gallbladder cancer invading liver. Calculus is seen within (arrow).
Gallbladder Cancer It is estimated that there will be over 9000 new cases of gallbladder and other biliary cancers in the USA in 2007, most of which will be gallbladder tumors.35 Approximately 500 new cases of gallbladder cancer are diagnosed each year in the UK.36 Most cases are adenocarcinomas, but squamous cell and other types can occur. Gallbladder metastases may occur and melanoma is the most common. Risk factors postulated include female sex, cholelithiasis, porcelain gallbladder, choledochal cyst and other anatomical anomalies, smoking, chronic salmonella typhi infection, primary sclerosing cholangitis, and certain industrial
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FIG 25. Axial CT images showing gallbladder cancer and lymphadenopathy infiltrating around biliary stent (arrow). Vascular invasion is also present (arrowhead).
FIG 26. Large gallbladder cancer (arrow) invading liver and with liver metastasis (arrowheads) seen on CT.
chemicals.37 There are also ethnic and geographical variations. Clinical features are often nonspecific and include weight loss, abdominal pain, anorexia, and jaundice. Most tumors are advanced by the time they present clinically, but many early gallbladder cancers are incidental findings at cholecystectomy. Radiologically, there are three main morphological types of gallbladder cancer: a mass replacing the gallbladder; focal or diffuse gallbladder wall thickening; and intraluminal polypoid tumor. These features can be demonstrated on ultrasound and CT (Figs 22 and 23). As described previously, gallbladder wall thickening is seen in several other conditions. Features suspi-
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FIG 27. Gallbladder hematoma demonstrated on (A) ultrasound and (B) CT. Calculus is seen within (arrows).
cious for malignancy are severe thickening (eg, ⬎10 mm), marked asymmetry, and mucosal irregularity.37 MR is often not the primary imaging modality employed but may have a problem-solving role, eg, differentiating suspected malignancy from adenomyomatosis. As well as demonstrating the primary tumor, imaging can also demonstrate associated features such as pericholecystic infiltration, direct invasion of adjacent structures (most commonly liver, but also colon, duodenum, and pancreas), bile duct infiltration/obstruction, vascular involvement, malignant nodes, and metastases—most commonly to liver and peritoneum (Figs 24-26). Distant metastases are uncommon. With the increased availability of multidetector-row CT,
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surgical resectability can be accurately assessed38 and vascular anatomy can be demonstrated. Positron emission tomography–CT may also improve diagnostic accuracy.39
Gallbladder Hemorrhage Hemorrhage into the gallbladder is uncommon. It can be secondary to excessive anticoagulation, trauma, acute cholecystitis, gallbladder ischemia, infection, aneurysm/fistula, or gastric/pancreatic heterotopia. The appearance of gallbladder hematoma can be very similar to empyema or carcinoma (Fig 27).
Other Conditions The gallbladder wall can be thickened in several other conditions including acquired immune deficiency syndrome, acute hepatitis, portal hypertension, and congestive cardiac failure.
Conclusion Although stone disease is by far the most commonly encountered pathology of the gallbladder, there are several other important disease processes affecting it. There is a certain amount of overlap between the imaging features of the different conditions, but there are some more specific radiological findings that can point toward the correct diagnosis.
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9. Jutras JA, Longtin JM, Levesque MD. Hyperplastic cholecystoses. Hickey lecture. AJR 1960;83:795-827. 10. Boscak AR, Al-Hawary M, Ramsburgh SR. Best cases from the AFIP adenomyomatosis of the gallbladder. Radiographics 2006;26:941-6. 11. Hwang JI, Chou YH, Tsay SH, et al. Radiologic and pathologic correlation of adenomyomatosis of the gallbladder. Abdom Imaging 1998;23:73-7. 12. Ootani T, Shirai Y, Tsudakada K, et al. Relationship between gallbladder carcinoma and the segmental type of adenomyomatosis of the gallbladder. Cancer 1992;69:2647-52. 13. Zani A, Pacilli M, Conforti A, et al. Adenomyomatosis of the gallbladder in childhood: report of a case and review of the literature. Pediatr Dev Pathol 2005;8:577-80. 14. Levy AD, Murakata LA, Abbott RM, et al. From the archives of the AFIP benign tumors and tumorlike lesions of the gallbladder and extrahepatic bile ducts: radiologic-pathologic correlation. Radiographics 2002;22:387-413. 15. Haradome H, Ichikawa T, Sou H, et al. The pearl necklace sign: an imaging sign of adenomyomatosis of the gallbladder at MR cholangiopancreatography. Radiology 2003;227:80-8. 16. Furukawa H, Takayasu K, Mukai K, et al. CT evaluation of small polypoid lesions of the gallbladder. Hepatogastroenterology 1995;42:800-10. 17. Lee KF, Wong J, Li JC, et al. Polypoid lesions of the gallbladder. Am J Surg 2004;188:186-90. 18. Sun XJ, Shi JS, Han Y, et al. Diagnosis and treatment of polypoid lesions of the gallbladder: report of 194 cases. Hepatobil Pancreatic Dis Int 2004;3:591-4. 19. Myers RP, Shaffer EA, Beck PL. Gallbladder polyps: epidemiology, natural history and management. Can J Gastroenterol 2002;16:187-94. 20. Sadamoto Y, Oda S, Tanaka M, et al. A useful approach to the differential diagnosis of small polypoid lesions of the gallbladder, utilising an endoscopic ultrasound scoring system. Endoscopy 2002;34:959-65. 21. Stephen AE, Berger DL. Carcinoma in the porcelain gallbladder: a relationship revisited. Surgery 2001;129:699-703. 22. Towfigh S, McFadden DW, Cortina GR, et al. Porcelain gallbladder is not associated with gallbladder carcinoma. Am Surg 2001;67:7-10. 23. Wang AJ, Wang TE, Lin CC, et al. Clinical predictors of severe gallbladder complications in acute acalculous cholecystitis. World J Gastroenterol 2003;9:2821-3. 24. Barie PS, Fischer E. Acute acalculous cholecystitis. J Am Coll Surg 1995;180:232-44. 25. Flancbaum L, Choban PS. Use of morphine cholescintigraphy in the diagnosis of acute cholecystitis in critically ill patients. Intensive Care Med 1995;21:120-4. 26. Parra JA, Acinas O, Bueno J, et al. Xanthogranulomatous cholecystitis: clinical, sonographic and CT findings in 26 patients. AJR 2000;174:979-83. 27. Spinelli A, Schumacher G, Pascher A, et al. Extended surgical resection for xanthogranulomatous cholecystitis mimicking advanced gallbladder carcinoma: a case report and review of literature. World J Gastroenterol 2006;12:2293-6. 28. Shuto R, Kiyosue H, Komatsu E, et al. CT and MR imaging findings of xanthogranulomatous cholecystitis: correlation with pathologic findings. Eur Radiol 2004;14:440-6.
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29. Chun KAC, Ha HK, Yu ES, et al. Xanthogranulomatous cholecystitis: CT features with emphasis on differentiation from gallbladder carcinoma. Radiology 1997;203:93-7. 30. Hatakenaka M, Adachi T, Matsuyama A, et al. Xanthogranulomatous cholecystitis: importance of chemical-shift gradientecho MR imaging. Eur Radiol 2003;13:2233-5. 31. Gill KS, Chapman AH, Weston MJ. The changing face of emphysematous cholecystitis. Br J Radiol 1997;70:986-91. 32. Koenig T, Tamm EP, Kawashima A. Magnetic resonance imaging findings in emphysematous cholecystitis. Clin Radiol 2004;59:455-8. 33. Konno K, Ishida H, Naganuma H, et al. Emphysematous cholecystitis: sonographic findings. Abdom Imaging 2002;27: 191-5. 34. Nemcek AAJ, Gore RM, Vogelzang RL, et al. The effervescent gallbladder: a sonographic sign of emphysematous cholecystitis. Am J Radiol 1988;150:575-7.
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35. National Cancer Institute, US National Institutes of Health: Gallbladder Cancer Home Page. http://www.cancer.gov/ cancertopics/types/gallbladder/. Accessed April 23, 2007. 36. Cancerbackup: Gallbladder cancer. http://www.cancerbackup. org.uk/Cancertype/Gallbladder/Gallbladdercancer. Accessed April 23, 2007. 37. Levy AD, Murakata LA, Rohrmann CA. Gallbladder carcinoma: radiologic-pathologic correlation. Radiographics 2001;21:295-314. 38. Kalra N, Suri S, Gupta R, et al. MDCT in the staging of gallbladder carcinoma. AJR 2006;186:758-62. 39. Rodriguez-Fernandez A, Gomez-Rio M, Medina-Benitez A, et al. Application of modern imaging methods in diagnosis of gallbladder cancer. J Surg Oncol 2006;93:650-4.
Curr Probl Diagn Radiol, September/October 2008
Although stone disease is by far the most commonly encountered pathology of the gallbladder, there are several other important disease processes affecting it. These include adenomyomatosis, cholesterolosis, polyps, porcelain gallbladder, acalculous cholecystitis, xanthogranulomatous cholecystitis, emphysematous cholecystitis, gallbladder cancer, and gallbladder hemorrhage. The purpose of this article was to review the different gallbladder pathologies encountered in everyday radiological practice and to describe their features in the standard imaging modalities.
In an imaging setting, the most frequently encountered gallbladder pathology is stone disease. There are several other less common abnormalities and anomalies of the gallbladder, both symptomatic and asymptomatic. The purpose of this article was to provide a pictorial review of the imaging features of the various gallbladder pathologies and relevant radiological interventions.
Congenital Variations Agenesis of the gallbladder occurs in less than 0.1% of the population.1 It can be associated with other congenital anomalies of the gastrointestinal tract and other systems. Hypoplastic gallbladder can be congenital or associated with cystic fibrosis. There can be variation in gallbladder location. The most common sites for ectopic gallbladder are under the left lobe of liver, intrahepatic or retrohepatic.1 From the Department of Radiology, Bristol Royal Infirmary, Bristol, United Kingdom. Reprint requests: Huw Roach, FRCR, Department of Radiology, Bristol Royal Infirmary, Marlborough Street, Bristol BS2 8HW, UK. E-mail: [email protected]. Curr Probl Diagn Radiol 2008;37:189-202. © 2008 Mosby, Inc. All rights reserved. 0363-0188/2008/$34.00 ⫹ 0 doi:10.1067/j.cpradiol.2007.12.001
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“Floating” gallbladder describes a gallbladder with loose peritoneal reflections, which makes it more mobile than normal and prone to torsion. Septation of the gallbladder may be transverse or longitudinal, single or multiple. The most common is a “Phrygian cap,” which is a folding between the fundus and body of the gallbladder associated with a transverse septum (Fig 1). It is not clinically important but may be mistaken for a calculus on ultrasound.
Gallstones Gallstone disease is a frequent problem in developed countries and represents a major health burden. An estimated 20 to 25 million adults in the USA are afflicted with gallstones2 with prevalences in Europe similarly ranging from 5.9 to 21.9%.3 Females have an increased risk of gallstone disease but this additional risk diminishes after the menopause. Postmenopausal women on estrogen replacement show a continued increase in risk, however.4 Obesity is also an established major risk factor for developing gallstones due to the increased hepatic secretion of cholesterol. Ethnicity is an important risk factor with higher rates in Native Americans, and those of Hispanic and Northern European descent. Ethnicity can also determine the type and position in the biliary tract of stones. In developed countries, 80 to 85% of calculi contain cholesterol, either on its own or mixed with calcium compounds. In East Asia, brown pigment stones are predominant. These more readily form in bile ducts, usually in association with infection. This accounts for the higher prevalence of intrahepatic duct stones.5 Bile salt malabsorption leads to bile salt depletion and results in hepatic secretions that are saturated in
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FIG 1. Ultrasound image showing gallbladder septation (arrow).
cholesterol. As a result, patients with terminal ileal disease, eg, in Crohn’s disease, have an increased risk of developing gallstones. Other predisposing factors include diabetes, hemolytic disorders, eg, hereditary spherocytosis and sickle cell disease, cystic fibrosis, and cholestatic disorders. Conventional radiography is relatively insensitive for the detection of gallstones, but approximately 10% of calculi can be seen on X-rays (Fig 2). Computed tomography (CT) and magnetic resonance imaging (MRI) (especially magnetic resonance cholangiopancreatography (MRCP)) are more sensitive (Fig 3). Ultrasound, however, is usually the primary diagnostic imaging tool as it is noninvasive and widely available and has sensitivity and specificity greater than 95% for gallstones larger than 1.5 mm6 (Fig 4). Endoscopic ultrasound is able to detect stones too small to be seen on transabdominal ultrasound and has sensitivities in the range of 94 to 98%.7 Many gallstones are asymptomatic and 60 to 80% of patients with gallstones do not develop symptoms.8 However, they may be associated with pain, nausea, and intolerance of fatty food. Complications include cholecystitis (Fig 5), gallbladder perforation (Fig 6), abscess formation (Fig 7), biliary obstruction (Fig 8), pancreatitis, and fistulation into the gastrointestinal tract. Gallbladder cancer is also associated with chronic inflammation from gallstones. Percutaneous imaging-guided cholecystostomy can sometimes be used as a temporizing measure in patients with acute cholecystitis not responding to medical treatment and in whom surgical cholecystectomy is unsafe. Percutaneous cholecystostomy can
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FIG 2. (A) Radiograph demonstrating gallbladder calculi (arrow). Large calculus impacted at gallbladder neck is also demonstrated (arrowhead). (B) Radiograph showing multiple small calcified stones (arrows). This morphology suggests that they are pigment stones.
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FIG 3. (A) CT scan showing calcified gallbladder stone (arrow). (B) CT demonstrating noncalcified stones containing gas (arrows). (C) CT demonstrating tiny noncalcified stones (arrow). (D) T2-weighted MR showing small gallbladder calculi (arrow). (E) T2 MRCP image showing gallbladder calculi (arrows).
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FIG 4. Classical ultrasound appearance of gallbladder calculi (arrow) with acoustic shadowing.
also be utilized to achieve biliary decompression in patients with common bile duct obstruction (Fig 9). This is as a rapid alternative to the more commonly employed techniques of endoscopic retrograde cholangiopancreatography or percutaneous transhepatic cholangiopancreatography. When performing percutaneous gallbladder drainage, a transhepatic route is generally favored as this will anchor the drain and reduce the risk of leakage of bile around the drain. Other imaging-guided treatments for gallstones include lithotripsy and percutaneous extraction.
Adenomyomatosis Adenomyomatosis of the gallbladder is one of the so-called “hyperplastic cholecystoses.”9 It is characterized by hyperplasia of the gallbladder mucosa and muscularis propria10 with out-pouching of the mucosa into or through the muscularis forming diverticula known as Rokitansky–Aschoff sinuses.11 These sinuses may be filled with bile, cholesterol crystals, sludge, or calculi.10 The condition occurs in as many as 8.7% of cholecystectomy specimens12 and there is an apparent female predilection. Most diagnoses are made in middle-aged patients,10 but cases have been reported in pediatric patients.10,13 Adenomyomatosis may be generalized, localized (usually affecting the fundus), or segmental (typically an annular constriction in the body giving an “hourglass” configuration).
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FIG 5. (A) Ultrasound image illustrating thickened gallbladder wall (arrow) and pericholecystic fluid (arrowhead) in keeping with gallstone-related cholecystitis. (B) T2-weighted MR image showing pericholecystic fluid and inflammatory change (arrows) due to cholecystitis. (C) Pericholecystic inflammatory change (arrow) on CT.
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FIG 6. CT image in a patient with gallbladder perforation secondary to gallstone-related cholecystitis. Gallbladder wall defect is seen (arrow). FIG 8. MRCP image showing a “Mirizzi” type proximal biliary obstruction due to large gallbladder neck calculus (arrow). A further calculus is seen in the gallbladder body.
FIG 7. Ultrasound image showing inflamed gallbladder and associated abscess collection.
Adenomyomatosis is rarely apparent on conventional radiography. It can be demonstrated on oral cholecystography (Fig 10), but this is now rarely performed. Ultrasound is usually the primary imaging modality used for assessing the gallbladder in current practice and adenomyomatosis usually appears as focal or generalized gallbladder wall thickening (Fig 11). Rokitansky–Aschoff sinuses may appear as anechoic spaces or may give the characteristic “ringdown” artifact from cholesterol-rich material within them (Fig 12). CT appearance is similar to ultrasound but is less specific as it cannot demonstrate the
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FIG 9. Contrast injection through percutaneous cholecystostomy drainage tube, showing drain entrance into gallbladder (arrow) and obstructing common bile duct calculi (arrowhead).
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FIG 10. Oral cholecystogram showing Rokitansky–Aschoff sinuses (arrows).
“ring-down” artifact and the small cystic spaces.11,14 MRI typically demonstrates gallbladder wall thickening but can also demonstrate the Rokitansky–Aschoff sinuses. These are typically low signal on T1-weighted images and high signal on T2-weighted images. Single-shot heavily T2-weighted MRCP images is probably the most effective sequence and is specific for adenomyomatosis when it demonstrates the classical “Pearl necklace” appearance of the Rokitansky– Aschoff sinuses15 (Fig 13). This is analogous to the classical appearance seen at oral cholecystography. The demonstration of the Rokitansky–Aschoff sinuses is vital for a confident diagnosis of adenomyomatosis to be made. Where these are not visible, the thickening of the gallbladder wall and enhancement pattern are relatively nonspecific, making it difficult to distinguish from other conditions, including gallbladder cancer. This can be particularly difficult when
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FIG 11. (A) Diffuse gallbladder wall thickening of adenomyosis seen on ultrasound. Rokitansky–Aschoff sinus is shown (arrow). (B) Thickened gallbladder wall (arrow) on CT.
adenomyomatosis is focal, giving rise to a focal “mass” or adenomyoma (Fig 14).
Cholesterolosis Cholesterolosis is the other main “hyperplastic cholecystosis.” This is characterized by the deposition of triglycerides and cholesterol esters in the gallbladder wall. The combination of these deposits with mucosal hyperemia gives the appearance of “strawberry gallbladder” macroscopically. This is not demonstrable radiologically. Cholesterol deposition can also give rise to polypoid lesions (Fig 15).
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FIG 12. Cholesterol-rich material within Rokitansky–Aschoff sinuses seen on ultrasound (arrow) with associated “ring down.”
FIG 13. T2-weighted MR image showing the high signal Rokitansky– Aschoff sinuses of adenomyomatosis (arrow) aligned perpendicularly to the gallbladder lumen. (Image courtesy of Dr. Paul Burn).
Gallbladder Polyps Cholesterol polyps account for approximately 50% of polypoid lesions seen in the gallbladder.14 They are more common in women. They can be solitary or multiple and are usually small. They are often discovered incidentally at ultrasound scanning for suspected gallstones. Their typical ultrasound appearance is of a hyperechoic nonshadowing structure with a delicate stalk. Where the stalk is not visible, the polyps are difficult to distinguish from
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FIG 14. Focal adenomyosis of gallbladder fundus seen on (A) ultrasound (arrow), (B) CT (arrow), and (C) pathological specimen. (Color version of figure is available online.)
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FIG 15. “Ring down” from small cholesterol polyp (arrow) seen on ultrasound. FIG 17. Large polypoid adenoma (arrow) in gallbladder seen at ultrasound.
include patient age ⬎50 years; broad based, solitary, or enlarging polyp; and coexistent gallstones.17-19 The ultrasound appearances are of a fixed, nonshadowing sessile or pedunculated mass, which is homogeneously hyperechoic (Fig 16). They may be lobulated (Fig 17). On CT, adenomas tend to be soft-tissue intraluminal masses with attenuation close to liver. Other polypoid lesions in the gallbladder include carcinomas, metastases, inflammatory polyps, neurofibromas, and heterotopia. Endoscopic ultrasound has been suggested as a useful imaging modality in differentiating between neoplastic and nonneoplastic polypoid gallbladder lesions.20 FIG 16. Nonshadowing gallbladder filling defects on ultrasound (arrows) consistent with polyps.
Gallbladder “Sludge” nonshadowing adherent calculi. They are difficult to see at CT but may enhance with contrast.16 Gallbladder adenomas are usually intraluminal polypoid lesions. They occur more commonly in women and may be associated with Peutz–Jeghers or familial polyposis syndromes. Pathologically, adenomas are subdivided into tubular, papillary, or tubulopapillary, with tubular being the most common.14 There is a potential adenoma-carcinoma sequence and polyps over 10 mm are considered suspicious. Other potential predictors of malignancy
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Gallbladder “sludge” is echogenic material often seen after prolonged fasting or cholecystitis. It can appear mass-like but can be differentiated from solid lesions by its mobile nature (Fig 18).
Milk of Calcium Bile Milk of calcium bile is caused by the precipitation of calcium-rich material in the gallbladder. The appearance is intermediate between sludge and stones.
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FIG 18. Thick bile/sludge in gallbladder (arrows) seen at ultrasound. Echogenicity is similar to liver.
Porcelain Gallbladder Porcelain gallbladder is characterized by calcium deposition in the gallbladder wall. The pattern of calcification can be complete intramural or selective mucosal. It is due to chronic inflammation, usually associated with gallstones, although it gives rise to few symptoms per se. It is more common in females. It was believed that there was a significant link between porcelain gallbladder and gallbladder carcinoma. This is now thought less than previously and possibly only associated with the selective mucosal pattern of calcification.21 Some authors recognize no relationship with gallbladder carcinoma.22 On ultrasound, porcelain gallbladder appears as curvilinear hyperechoic gallbladder wall with acoustic shadowing (Fig 19B). There can be some diagnostic difficulty differentiating porcelain gallbladder from emphysematous cholecystitis, milk of calcium bile, or contracted gallbladder containing calculi. The calcification in the gallbladder wall can be better demonstrated on conventional radiographs or CT (Fig 19A and C).
Acalculous Cholecystitis Up to approximately 10% of cases of acute cholecystitis occur in the absence of stones23—so-called acalculous cholecystitis. It tends to occur in debilitated
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FIG 19. Calcified porcelain gallbladder (arrow) seen at (A) X-ray, (B) ultrasound, and (C) CT.
patients, eg, the critically ill on mechanical ventilation and parenteral nutrition, or following severe trauma, burns, or major surgery. It has also been described in the immunocompromised and in certain infections, eg,
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FIG 20. Gallbladder perforation (arrow) due to acalculous cholecystitis seen at CT. FIG 21. Mural gallbladder gas of emphysematous cholecystitis seen on plain X-ray.
salmonella strains. Bile stasis, cystic duct obstruction, gallbladder ischemia, and systemic infection are thought to be pathogenetic factors.23,24 Mortality rates vary, but figures as high as 65% have been reported.25 Thickening of the gallbladder wall, gallbladder distension, pericholecystic fluid, and an absence of calculi are the typical features seen at ultrasound. CT appearances are similarly nonspecific. Early diagnosis and intervention is important as perforation and gangrene can occur rapidly (Fig 20). Treatment is normally by surgical cholecystectomy, but this can be associated with significant risk in critically ill or elderly patients. Imaging-guided percutaneous cholecystostomy is increasingly being used as a temporizing measure in high-risk patients.
Xanthogranulomatous Cholecystitis Xanthogranulomatous cholecystitis (XGC) is a rare inflammatory process affecting the gallbladder, characterized by nodules or streaks in the gallbladder wall, mainly due to lipid-laden macrophages.26 Its etiology is uncertain but is thought to result from extravasation of bile into the gallbladder wall in the presence of gallstones, obstruction, and cholestasis. There is inflammation followed by a granulomatous reaction (analogous to the development of xanthogranulomatous pyelonephritis in the kidney).27 Some authors have proposed an association between XGC and tumors of the gallbladder and biliary tree.26
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XGC appears as nonspecific thickening of the gallbladder wall on ultrasound, CT, and MRI. Where visible, the characteristic features at ultrasound are the presence of hypoechoic nodules and bands.26 CT may demonstrate nonenhancing hypoattenuating nodules, which may be focal or diffuse.26,28 A hypoattenuating band around the gallbladder may also be visible.26,29 MRI may demonstrate focal or diffuse areas of high signal on T2-weighted sequences. These areas are low signal on T1-weighted sequences and show delayed enhancement with gadolinium.28 Foci of very high T2 signal are likely to represent abscess or necrosis. In/out-of-phase gradient-echo MR may demonstrate foci of signal dropout in the gallbladder wall in XGC due to the presence of fat.30
Emphysematous Cholecystitis Emphysematous cholecystitis is a variant of acute cholecystitis characterized by the presence of gas in the gallbladder wall, lumen, and pericholecystic tissue in the absence of an abnormal connection between the gallbladder and gastrointestinal tract.31 It is more common in male patients and in patients with diabetes mellitus.31,32 Initially emphysematous cholecystitis is indistinguishable from uncomplicated acute cholecystitis but can rapidly progress to ischemia, gangrene, and perforation. As such, it has
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FIG 23. CT image of focal gallbladder cancer (arrow) invading adjacent liver. FIG 22. Pathologically confirmed focal gallbladder cancer seen at ultrasound (arrow).
a higher mortality, although there may be a spectrum of severity with some patients able to be treated conservatively rather than by emergency intervention.31 Gas-forming anaerobic bacteria such as Clostridium species and Escherichia coli are often implicated. The radiological diagnosis depends on the demonstration of the gas in or around the gallbladder. Conventional radiographs may be sufficient (Fig 21). Ultrasound appearances depend on the amount of gas present.33 The presence of rising bubbles in the gallbladder is termed “effervescent gallbladder.”34 More commonly, ultrasound shows echogenic foci with posterior acoustic shadowing or ring-down artifact. With a large amount of gas, a wide band of acoustic shadowing from the gallbladder is seen.33 In these cases the gallbladder can be difficult to assess and it may be difficult to differentiate emphysematous cholecystitis from porcelain gallbladder or a contracted gallbladder full of stones. CT is probably the most sensitive modality (approaching 100%31) for diagnosing emphysematous cholecystitis and can also demonstrate the exact location of the gas. It is not usually the primary modality employed in acute cholecystitis, however. T2weighted MR shows a gas/fluid level in the gallbladder, low signal rim around the gallbladder indicating mural gas, and pericholecystic low signal, indicating gallbladder perforation.32
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FIG 24. CT image showing diffuse gallbladder cancer invading liver. Calculus is seen within (arrow).
Gallbladder Cancer It is estimated that there will be over 9000 new cases of gallbladder and other biliary cancers in the USA in 2007, most of which will be gallbladder tumors.35 Approximately 500 new cases of gallbladder cancer are diagnosed each year in the UK.36 Most cases are adenocarcinomas, but squamous cell and other types can occur. Gallbladder metastases may occur and melanoma is the most common. Risk factors postulated include female sex, cholelithiasis, porcelain gallbladder, choledochal cyst and other anatomical anomalies, smoking, chronic salmonella typhi infection, primary sclerosing cholangitis, and certain industrial
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FIG 25. Axial CT images showing gallbladder cancer and lymphadenopathy infiltrating around biliary stent (arrow). Vascular invasion is also present (arrowhead).
FIG 26. Large gallbladder cancer (arrow) invading liver and with liver metastasis (arrowheads) seen on CT.
chemicals.37 There are also ethnic and geographical variations. Clinical features are often nonspecific and include weight loss, abdominal pain, anorexia, and jaundice. Most tumors are advanced by the time they present clinically, but many early gallbladder cancers are incidental findings at cholecystectomy. Radiologically, there are three main morphological types of gallbladder cancer: a mass replacing the gallbladder; focal or diffuse gallbladder wall thickening; and intraluminal polypoid tumor. These features can be demonstrated on ultrasound and CT (Figs 22 and 23). As described previously, gallbladder wall thickening is seen in several other conditions. Features suspi-
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FIG 27. Gallbladder hematoma demonstrated on (A) ultrasound and (B) CT. Calculus is seen within (arrows).
cious for malignancy are severe thickening (eg, ⬎10 mm), marked asymmetry, and mucosal irregularity.37 MR is often not the primary imaging modality employed but may have a problem-solving role, eg, differentiating suspected malignancy from adenomyomatosis. As well as demonstrating the primary tumor, imaging can also demonstrate associated features such as pericholecystic infiltration, direct invasion of adjacent structures (most commonly liver, but also colon, duodenum, and pancreas), bile duct infiltration/obstruction, vascular involvement, malignant nodes, and metastases—most commonly to liver and peritoneum (Figs 24-26). Distant metastases are uncommon. With the increased availability of multidetector-row CT,
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surgical resectability can be accurately assessed38 and vascular anatomy can be demonstrated. Positron emission tomography–CT may also improve diagnostic accuracy.39
Gallbladder Hemorrhage Hemorrhage into the gallbladder is uncommon. It can be secondary to excessive anticoagulation, trauma, acute cholecystitis, gallbladder ischemia, infection, aneurysm/fistula, or gastric/pancreatic heterotopia. The appearance of gallbladder hematoma can be very similar to empyema or carcinoma (Fig 27).
Other Conditions The gallbladder wall can be thickened in several other conditions including acquired immune deficiency syndrome, acute hepatitis, portal hypertension, and congestive cardiac failure.
Conclusion Although stone disease is by far the most commonly encountered pathology of the gallbladder, there are several other important disease processes affecting it. There is a certain amount of overlap between the imaging features of the different conditions, but there are some more specific radiological findings that can point toward the correct diagnosis.
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