Gastrointest Radiol 16:143-148 (1991)


Radiology 9 Springer-VerlagNewYorkInc. 1991

Primary Gallbladder Carcinoma: Imaging Findings in 50 Patients with Pathologic Correlation T. Franquet, 1 M. Montes, z Y. Ruiz de Azua, 2 F.J. Jimenez, 1 and R. Cozcolluela 1 Departments of 1Radiology and 2Pathology, Hospital "Virgen del Camino," Pamplona, Spain

Abstract. Different diagnostic imaging modalities [contrast cholangiography, ultrasonography, and computed tomography (CT)] in a large group of patients with proven gallbladder carcinoma are reviewed. Noninvasive cross-sectional imaging methods strongly correlated with the different gross pathologic types of gallbladder carcinoma. The most common observed type was a mass replacing the gallbladder (39%). Other types observed either by sonography and/or CT were a focal/diffuse gallbladder wall thickening and the presence of an intraluminal polypoid mass. Despite the improvement in several imaging modalities, most of the preoperatively diagnosed gallbladder carcinomas were in advanced stage (84%). A combined approach using noninvasive diagnostic methods and percutaneous aspirative biopsies may reduce the number of explorative laparotomies in the final diagnosis of gallbladder carcinoma. Key words: Gallbladder, carcinoma - Ultrasonography, diagnosis - Computed tomography, diagnosis.

imaging modalities were used, emphasizing the roles and limitations of noninvasive cross-sectional imaging methods in the diagnosis.

Subjects and Methods During the 10-year period from 1979-1989, 50 patients with gallbladder carcinoma were seen at our institution. There were 40 women and 10 men, aged from 54 to 89 years (mean, 72 years). The most common presenting symptom was pain in the right upper quadrant or epigastrum (45 cases). Sixteen patients had jaundice, three patients reported weight loss, and two remained asymptomatic. On physical examination, a palpable mass in the right upper quadrant was noted in 10 patients. Fifteen patients were examined by sonography, 10 patients were examined by sonography and computed tomography (CT), six were examined by sonography and contrast cholangiography (percutaneous transhepatic cholangiography, intravenous cholangiography, and oral gallbladder series), and 19 were examined by contrast studies alone. The sonographic and CT studies were evaluated specifically for (a) intraluminal mass, (b) mass filling or replacing gallbladder, (c) focal or diffuse wall thickening, (d) direct liver invasion by tumor, and (e) regional lymphadenopathy. Forty-six cases had histologic confirmation either by surgery, percutaneous biopsy, laparoscopy, or autopsy. In four patients there was no histologic proof of the diagnosis, but the imaging findings were considered to be diagnostic.

Results Primary carcinoma of the gallbladder is the most common malignancy of the biliary system, and it represents the fifth most common malignant disease of the gastrointestinal tract [1, 2]. The preoperative diagnosis of gallbladder carcinoma remains very difficult because of the nonspecificity of its clinical manifestations. We present a series of 50 proven cases of gallbladder carcinoma in which different diagnostic Address offprint requests to: T. Franquet, M.D., Department of Radiology, Hospital "Virgen del Camino," c/Irunlarrea s/n, Pamplona 31008, Spain

The ultrasonographic and CT findings in patients with gallbladder carcinoma are summarized in Table 1. The most common sonographic finding in our series, as seen in 12 patients, was an inhomogeneous mass replacing the gallbladder (Fig. 1). On CT scans, six of these 12 patients showed a lowdensity mass with peripheral enhancement after intravenous contrast administration. Focal or diffuse thickening of the gallbladder wall was sonographically noted in six patients (Fig. 2); CT was performed in two of these patients and confirmed the sonographic findings (Fig. 3). In three cases sonog-


T. Franqnet et al. : Primary Gallbladder Carcinoma

Fig. 1. A Sonography demonstrates a large hypoechoic mass replacing almost entirely the gallbladder lumen (arrowheads). Note a gallstone with shadowing in the infundibulum (arrow). B Unenhanced CT confirms the presence of a solid mass in the gallbladder area. A gallstone is engulfed within the tumoral mass. Slight intrahepatic biliary dilatation is a/so visible.


Sonography (31 cases)

CT (10 cases)

Fig. 2. A A longitudinal sonogram of the gallbladder demonstrates a diffuse wall thickening. The intraluminal echoes associated with shadowing represent gallstones. B The corresponding gross specimen shows diffuse thickening of the gallbladder wall from infiltrating adenocarcinoma.

Mass filling or replacing gallbladder Asymmetric thickening of gallbladder wall





Intraluminal mass 3 Normal gallbladder 2 Cholelithiasis 6 Nonvisualized 2 gallbladder Direct invasion 10 of the liver Lymphadenopathy 2


r a p h y s h o w e d an i n t r a l u m i n a l m a s s (Fig. 4); two o f these i n t r a l u m i n a l masses were also d o c u m e n t e d by C T (Fig. 5). Cholelithiasis was the only s o n o graphic finding in six patients with p r o v e n gallb l a d d e r c a r c i n o m a . I n two a u t o p s i e d patients, the available previous gallbladder s o n o g r a m s were n o r m a l (Fig. 6). T h e gallbladder was n o t visualized s o n o g r a p h i c a l l y in two cases. A direct invasion o f the liver was d e m o n s t r a t e d by s o n o g r a p h y in 10 patients; seven o f these patients also h a d C T d e m o n s t r a t i o n o f direct liver invasion (Fig. 7). I n t r a ductal spread o f gallbladder c a r c i n o m a was s h o w n by C T in one patient. S o n o g r a p h y s h o w e d regional l y m p h n o d e e n l a r g e m e n t in two patients, whereas

Table 1. Imaging findings in gallbladder carcinoma


Contrast studies (19 cases)


7 5

C T p r o v e d the existence o f l y m p h a d e n o p a t h y in five cases. A diagnosis o f gallbladder c a r c i n o m a was initially suggested in 6 1 % o f patients studied by son o g r a p h y a n d / o r C T a n d was u n e x p e c t e d in 3 8 %

T. Franquet et al. : Primary Gallbladder Carcinoma


Fig. 3. A A transverse sonogram of the gallbladder shows a focal wall thickening (arrows). Intraluminal gallstones with acoustic shadows are also visible. B Enhanced CT confirms the sonographic findings. A focal and irregular thickening of the gallbladder wall is demonstrated (arrow). C The gross specimen shows focal tumoral infiltration of the gallbladder wall. Two gallstones are present in the gallbladder infundibulum (white arrows).

Fig. 4. A Sonography in the transverse plane shows an echogenic intraluminal gallbladder mass (arrows). B CT scan demonstrates an homogeneous enhancement of the intraluminal fungating gallbladder mass. Two adjacent gallstones are also visible. C The cut gross specimen shows the tumor located at the gallbladder fundus. A large lymphadenopathy, not visible on sonography and CT, is demonstrated in the cystic area (arrow).

of cases. Of the entire group of patients, including those studied by cholangiographic methods, the diagnosis of gallbladder carcinoma was missed or unexpected in 31 cases (62%). Cholangiographic studies performed in 19 cases provided less information than cross-sectional imaging methods. The pathologic diagnosis of gallbladder carcinoma was made by surgery (N = 37), percutaneous biopsy (N=6), autopsy (N=2), and laparoscopy ( N = I ) . In four patients there was no histologic diagnosis because the imaging findings were considered to be diagnostic. The most common type of primary gallbladder carcinoma was adenocarci-

noma (N= 44), and, of these, three were papillary adenocarcinoma. There was one case of squamous cell carcinoma, and there were five cases classified as undifferentiated carcinoma. Tumoral extension was graded following three pathologic stages [3]: stage I, carcinoma invading no further than the muscle coat of the gallbladder, with or without extension along Rokitansky-Aschoff sinuses in the subserosa (N=2); stage II, carcinoma extending to the subserosal fibroadipose tissue of the gallbladder (N= 6); and stage III, carcinoma invading the adjacent organs with or without associated distant metastases (N= 42).


Fig. 5. A A longitudinal sonogram of the gallbladder shows a fixed hypoechoic mass in the infundibulum. B Enhanced CT scan shows an inhomogeneous enhancement of the mass (ar-

row). Fig. 6. " I n situ" gallbladder carcinoma. Histologic examination reveals a cauliflower-like intraluminal projection composed microscoically of coarse connective tissue stalks covered by columnar epithelium. " I n situ" adenocarcinoma (arrows) is present. (Hematoxylin & eosin, original magnification x 2.5).

T. Franquet et al. : Primary Gallbladder Carcinoma

Fig. 7. A Sonography demonstrates a diffuse gallbladder wall thickening associated with tumoral infiltration of the adjacent hepatic parenchyma (arrows). Biliary sludge and gallstones are also sonographically demonstrated. B Percutaneous transhepatic cholangiography shows a complete obstruction of the common hepatic duct secondary to tumoral liver invasion.

T. Franquet et al. : Primary Gallbladder Carcinoma

Discussion Gallbladder carcinoma accounts for 1-2% of all gastrointestinal malignancies [1, 2]. W o m e n are more commonly affected than men with a preponderance at a ratio of 4:1. Its incidence is more c o m m o n in advanced ages with a mean of 72 years in our series. The clinical presentation of gallbladder carcinoma may be indistinguishable from those of chronic cholecystitis and/or cholelithiasis [2]. Currently, a significant number of gallbladder carcinomas are still misdiagnosed preoperatively and represent an incidental surgical finding with a reported frequency of 1.1% among all cholecystectomies [4]. In addition, in large autopsy series, the incidence of an unexpected gallbladder carcinoma has been reported for 0.5-2.4% of cases [5]. Prior to the advent of ultrasound and CT, contrast cholangiographic studies were used in the diagnosis of the diseases of the gallbladder and biliary tract [6]. Two thirds of patients with gallbladder carcinoma examined by oral cholecystography had a nonvisualized gallbladder, probably due to cystic duct obstruction [7]. In our series, 10 of 19 patients studied by cholangiographic methods showed a nonvisualized gallbladder and three had associated biliary obstruction. Conventional radiographic methods do not provide an accurate diagnosis of gallbladder carcinoma because of the nonspecificity of the radiologic findings. A diagnosis of gallbladder carcinoma was not suspected in any of our patients studied by cholangiographic methods alone. Sonography and CT have been shown superior to conventional radiographic studies in the diagnosis of gallbladder carcinoma [8-13]. The different sonographic and CT findings strongly correlate with the gross pathologic appearance of gallbladder carcinoma. Three different patterns have been pathologically described [14]. The most c o m m o n observed pattern in our series, seen in 12 cases (39%), was a mass replacing gallbladder. Focal/ diffuse thickening of the gallbladder wall was noted by sonography and/or CT in 19% of our cases. Thickening of the gallbladder wall due to infiltration by carcinoma is extremely difficult to differentiate from cholecystitis because both entities may have the same imaging findings [15, 16]. Similarly, those cases presenting an associated mass in the gallbladder area are difficult to differentiate from complicated cholecystitis. In this regard, the presence of a curvilinear low-attentuation " h a l o " around the gallbladder wall on CT studies has been described by Smathers et al. as a specific sign of complicated cholecystitis [17]. In our series, two


cases of gallbladder carcinoma were sonographically diagnosed as complicated cholecystitis and no further examinations were done. We believe that CT may be helpful, as a complementary diagnostic method, in evaluating those elderly patients with sonographic findings suggestive of complicated cholecystitis, to rule out gallbladder carcinoma. The presence of an intraluminal gallbladder mass was noted in three of our cases. Several conditions may sonographically simulate polypoid gallbladder carcinoma. Biliary sludge is the most frequently observed condition that may be confused with an intraluminal gallbladder mass. Decubitus views of the gallbladder may be helpful in demonstrating sludge movement to the most dependent part of the gallbladder when the patient's position is changed. Several patterns of spread have been reported in gallbladder carcinoma [18]. Direct extension into the liver, the most commonly reported pattern, was demonstrated either by sonography and/ or CT in 10 of our patients. Other modes of spread include lymphatic and hematogenous pathways. Lymph node enlargement around the distal comm o n bile duct and in the region of the head of the pancreas may be confused by sonography and CT with pancreatic carcinoma [19]. In two of our patients, lymph node enlargement was demonstrated by sonography, whereas CT demonstrated lymphadenopathies in five patients. An accurate sonographic examination of the periduodenal and peripancreatic area is sometimes made difficult by the presence of a large amount of abdominal gas. On the basis of our data, lymph node enlargement was more easily demonstrated by CT than sonography. Intraductal spread has been reported in at least 4% of cases of gallbladder carcinoma [17]. In our series, only one patient presented intraductal spread visible on CT scans. Biliary obstruction secondary to gallbladder carcinoma was demonstrated in 32% of our patients. In the elderly population, jaundiced patients should be carefully examined by cross-sectional imaging methods to rule out gallbladder carcinoma. Unfortunately, most of the preoperatively diagnosed gallbladder carcinomas are in advanced stage [2]. Eighty-four percent of cases in our series, were in stage III, and only two cases (4%) were incidentally diagnosed in stage I. Carcinoma of the gallbladder is very difficult to diagnose clinically in the early stages because the great majority of patients are often free of symptoms. However, with the wide use of sonography, the diagnosis of gallbladder carcinoma will be more frequently made


in routine abdominal examinations, especially in the elderly population. In those advanced cases with suspicion of gallbladder malignancy, the use of percutaneous aspirative biopsy may avoid unnecessary laparotomies. In summary, improvement in the diagnosis of gallbladder carcinoma has increased using noninvasive cross-sectional imaging methods. Our results and previous reports indicate that sonography and CT must be used as complementary diagnostic methods in those patients at risk of gallbladder carcinoma. A combined approach using noninvasive diagnostic methods and percutaneous aspirative biopsies may reduce the number of explorative laparotomies in the final diagnosis of gallbladder carcinoma. References 1. Klein JB, Finck FM. Primary carcinoma of the gallbladder: review of 28 cases. Arch Surg 1972; 104:769-772 2. Hamrick RE Jr, Liner F J, Hastings PR, Cohn I Jr. Primary carcinoma of the gallbladder. Ann Surg 1982; 195:270-273 3. Yamaguchi K, Enjoji M. Carcinoma of the gallbladder. A clinicopathologic study of 103 patients and a newly proposed staging. Cancer 1988; 62:1425-1432 4. Oertli D, Herzog V, Mihatsch M J, Tondelli P. Long-term results following surgery of gallbladder carcinoma. Schweiz Med Woehenschr 1989; 119 : 282-286 5. Kimura W, Nagai H, Kuroda A, Morioka Y. Clinicopathologic study of asymptomatic gallbladder carcinoma found at autopsy. Cancer 1989; 64:98-103 6. Graham EA, Cole WH, Copher GH. Visualizing the gallbladder by the sodium salt of tetrabromphenophtalein. JAMA 1924; 82:1077-1078 7. Shieh CJ, Dunn E, Standard JE. Primary carcinoma of the

T. Franquet et al. : Primary Gallbladder Carcinoma gallbladder. A review of a 16-year experience at the Waterbury Hospital Health Center. Cancer 1981; 47:996-1004 8. Yeh HC. Ultrasonography and computed tomography of carcinoma of the gallbladder. Radiology 1979; 133 : 167-173 9. Itai Y, Araki T, Yoshikawa K, Furui S, Tasaka A. Computed tomography of gallbladder carcinoma. Radiology 1980; 137:713-718 10. Weiner SN, Koenigsberg M, Morehouse H, Hoffman J. Sonography and computed tomography in the diagnosis of carcinoma of the gallbladder. A JR 1984; 142: 735-739 11. Soiva M, Aro K, Pamilo M, P~iiv~insaloM, Suramo I, Taavitsainen M. Ultrasonography in carcinoma of the gallbladder. Aeta Radiol 1987; 28:711-714 12. Frank W, Graf O, Jantsch H, Lechner G, Maier A, Pichler W. Sonography of gallbladder carcinoma. Correlation with surgical findings in 60 cases. ROFO 1989; 150:556-561 13. Nilsson P, Ekberg O, Aspelin P, Sigurjonsson SV, Genell S. Ultrasonography in the diagnosis of gallbladder carcinoma. ROFO 1989; 150:171-175 14. Lane J, Buck JL, Zeman RK. Primary carcinoma of the gallbladder: a pictorial essay. Radiographics 1989; 2:209228 15. Solomon A, Kreel L, Pinto D. Contrast computed tomography in the diagnosis of acute cholecystitis. J Comput Assist Tomogr 1979; 3:585-588 16. Pedrosa CS, Rodriguez R. CT findings in subacute perforation of the gallbladder: report of 5 cases. Eur J Radio11981 ; 1:137-142 17. Smathers RL, Lee JKT, Heiken JP. Differentiation of complicated cholecystitis from gallbladder carcinoma by computed tomography. A JR 1984; 143 : 255-259 18. Albores-Saavedra J, Henson DE. Tumors of the gallbladder and extrahepatic bile ducts. In: Atlas of tumor pathology. Fasc 22. Washington, DC: Armed Forces Institute of Pathology, 1986:65 19. Baker ME, Silverman PM, Halvorsen RA Jr, Cohan RH. Computed tomography of masses in periportal/hepatoduodenal ligament. J Comput Assist Tomogr 1987; 11 : 258-263 Received: May 31, 1990; accepted: June 30, 1990

Primary gallbladder carcinoma: imaging findings in 50 patients with pathologic correlation.

Different diagnostic imaging modalities [contrast cholangiography, ultrasonography, and computed tomography (CT)] in a large group of patients with pr...
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