Double Intrahepatic and Extrahepatic Cholangiocarcinomas Arising from Biliary Papillomatosis: A Case Report
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1 Korean Journal of HBP Surgery 증 례 Vol. 14, No. 1, March 2010 Double Intrahepatic and Extrahepatic Cholangiocarcinomas Arising from Biliary Papillomatosis: A Case Report Biliary papillomatosis is a rare disease entity characterized by multiple papillary adenomas along the bile duct mucosa. It is widely accepted that the adenoma-carcinoma sequence represents the process by which most, if not all, cholangiocarcinomas of an intraductal-growing type arise. Interestingly, friable papillary projections easily detached from the primary site can be implanted into the other sites in the bile duct in suitable animal models, resulting in multiple tumors. A 76-year-old male was referred to our hospital due to intermittent abdominal discomfort. Imaging workups revealed two lesions: wall thickening in the proximal portion of the left interhepatic duct and abrupt narrowing of the distal common bile duct. A hepatopancreaticoduodenectomy was carried out and pathological analysis demonstrated a well-differentiated adenocarcinoma of the left hepatic duct and carcinoma in situ of the distal common bile duct on a background of biliary papillomatosis. Six days after the operation, the patient received a re-exploration due to ruptured mesenteric vessels. Unfortunately, 3 months after the initial operation, the patient died of aspiration pneumonia. Biliary papillomatosis can present with a broad spectrum of disease characteristics ranging from adenoma to, usually, low-grade adenocarcinoma. If there is a complete excision, and a favorable postoperative course is secured, excellent survival can be expected after surgery. Say June Kim, M.D., Jung Uee Lee, M.D. 1 Departments of Surgery and 1 Pathology, Deajeon St. Mary s Hospital, The Catholic University of Korea College of Medicine Corresponding Author Say June Kim Department of Surgery, Deajeon St. Mary s Hospital, The Catholic University of Korea College of Medicine, 520-2, Daeheung-dong, Jung-gu, Daejeon, , Korea Tel: Fax: sejoonkim@hanmail.net Key Words : Biliary papillomatosis, Cholangiocarcinoma Received: Accepted: Introduction Biliary papillomatosis (BP) is characterized by the occurrence of multiple papillary adenomas in the biliary tract with significant risk of malignant transformation. Because BP is a scare entity, our knowledge about its clinical course, prognosis and treatment strategies are largely limited. It is known to have a tendency to spread superficially alone the bile duct mucosa. Certain subtype of BP can produce mucin, which can raise the incidences of biliary obstruction causing jaundice. Malignant transformation of BP is usually less invasive and grows slowly. Reports regarding incidences of malignant transformation have showed variable differences from %. 1-3 The Liver Cancer Study Group of Japan 4 has proposed a new classification of cholangiocarcinoma based on its growth characteristics: mass-forming, periductal-infiltrating, and intraductal-growing types. Depending on each type, they show substantial differences in the gross appearance, the way of spreading, prognosis and operative strategy. Malignancy arising from BP corresponds to intraductal-growing type of cholangiocarcinoma. As a result, intraductal-growing cholangiocarcinoma has a tendency to spread super- 57
2 한국간담췌외과학회지 : 제 14 권 1 호 2010 ficially within mucosa. In addition, its intraluminal papillary projections may slough spontaneously so that the detached tumor implanted at a different level of the bile duct, giving rise to multiple tumors. We herein report a case with unusual finding of a malignant transformation of BP which has two distinct lesions - hilar and distal bile ducts- far apart from each other. Case Report A 76-year-old male was admitted with intermittent abdominal discomfort in the right upper quadrant of the abdomen for 2 months. In his past history, he received an abdominoperineal resection of the rectum due to rectal cancer about 20 years ago. His recent follow-up examination revealed no evidence of the tumor recurrence. He had been taking oral hypoglycemic agents for 10 years owing to type II diabetes mellitus. No weight loss was addressed. He had history of intermittent drinking of alcohol about 2 3 bottles per week for 20 years. He was not a smoker. Physical examination was unremarkable except for an end-colostomy in left lower quadrant of the abdomen; No tenderness, palpable mass or icteric sclera was demonstrated. The levels of major laboratory results were as follows: white blood cells /L, hemoglobin 12 g/dl, platelets /L, AST/ALT/Alkaline phosphatase 17/12/107 IU/L, total bilirubin 0.9 mg/dl and albumin 4.7 g/dl. Serum CEA was within normal limits but serum CA19-9 was increased up to U/mL. Abdominal ultrasonography showed an irregular cystic or dilated lesion in first confluence of the left bile duct. Liver dynamic computed tomography (CT) demonstrated the markedly enlarged left intrahepatic duct with certain lymph nodes with variable sizes in porta hepatis (Fig. 1). Magnetic resonance cholangiopancreatography (MRCP) revealed a focal short segmental stenosis and mild wall thickening in the proximal portion of the left interhepatic duct resulting marked dilatation of the distal ducts and abrupt narrowing and shouldering of the distal common bile duct (CBD) (Fig. 2). The result of PET CT was unremarkable. Under the impression of cholangiocarcinomas located in two different sites- left primary pedicle from the hepatic hilum and distal CBD, we performed hepatopancreatodudenectomy, which included a left hemihepactecomy combined with pylorus-preserving pancreaticoduodenectomy (PPPD). During the operation, the extent of resected hepatic duct was determined after confirmation of the negative cut margin by frozen sections: we made 4 frozen sections, three of which showed atypical cells, so we connected the jejunal limb with the right intrahepatic duct Fig. 1. Abdominal CT finding demonstrating the dilated left hepatic duct (A) and the dilated distal common bile duct with thickened wall (B). 58
3 Say June Kim and Jung Uee Lee:Double Cholangiocarcinomas Fig. 2. Magnetic resonance cholangiopancreatography showing two separate narrowed lesions in the primary pedicle of left intrahepatic duct and the distal portion of common bile duct. Fig. 3. Gross specimen of the resected left hepatic and caudate lobes. Dilated left intrahepatic duct was noted. A white arrow indicates the first pedicle of left intrahepatic duct. after acquiring negative cut margin. On the specimens, explanted left hepatic lobe contained markedly dilated left intrahepatic duct, however the lesion could not be localized (Fig. 3). And, certain mucosal change - elevation and faint color - was noted on the distal CBD (Fig. 4). Histologically, the lesions - the liver and Fig. 4. Gross specimen of the distal common bile duct combined with the pancreatic head and duodenum. A white arrow indicates the probable lesion in distal common bile duct. distal CBD - showed papillary growing nature; proliferations of columnar epithelial cells comprised innumerous papillary infoldings. The lesion located in primary pedicle of left hepatic duct was mainly papillary adenocarcinoma in situ with focal well-differentiated adenocarcinoma (Fig. 5). And, another lesion in distal CBD was also composed of mainly adenocarcinoma in situ with adenoma and dysplasia (Fig. 6). No lymphovascular or perineural invasion was demonstrated on both specimens. No lymph node metastasis was observed. Six days after the operation, bleeding from ruptured mesenteric vessels prompted us to perform reexploration and bleeding control. Twenty days after initial operation, an enterocutaneous fistula was detected on the mid portion of an incision site. Unfortunately, the patient was expired due to aspiration pneumonia 3 months after initial operation. Discussion Biliary papillomatosis (BP) is defined as papillary proliferation of the lining epithelium of the bile duct. It can involve the intrahepatic duct and/or extrahepatic biliary tree with a tendency of superficially spreading along the bile duct mucosa. 3 Although it is basically a collection of benign 59
4 한국간담췌외과학회지 : 제 14 권 1 호 2010 Fig. 5. Microscopic finding of an intrahepatic duct bearing biliary papillomatosis (A; H&E stain, 40). Picture B (H&E stain, 100) is the enlargement of the black boxed area of the picture A. Neoplastic cells are placed along the epithelium of intraductal bile ducts and these cells invade to the periductal stroma (B). Fig. 6. Microscopic finding of resection margin of common bile duct (H&E, 200). Neoplastic cells (an arrow) are placed along the surface epithelium but no stromal invasion is noted demonstrating adenocarcinoma in situ. papillary adenomas, papillary adenocarcinoma can develop within these lesions. 3,5 It is a rare disease entity and occurs most often in ederly male. 2,3 Untill now, the pathogenesis of this disease remains to be elucidated. The main cause is thought to be the proceeding periductal inflammatory change which is initiated by bile stasis and recurrent infection in the background of hepatolithiasis or clonorchiasis. 6,7 High incidence of BP in patients with biliary stones or clornorchiasis suggests us such an association. 6-8 Lee et al 3 proposed, after analysis of 58 patients with BP, a classification of BP into mucin-hypersecreting or nonmucin-producing types depending on the presence of mucobilia. These two types showed similar histological features, except for mucin hypersecretion. However, clinically, patients with mucin hypersecretion experienced more frequent episodes of acute cholangitis and exhibited higher CA 19-9 level than patients without mucin hyersecretion. Therefore, thick mucin secretion is thought to be the cause of more frequent episodes of bile duct obstruction resulting in acute cholangitis and cholestasis. Focally dilated intrahepatic and/or extrahepatic bile duct with concomitant multiple ill-defined filling defects are usually demonstrated as a basic finding of BP in ultrasonography (US), computed tomography (CT) and cholangiopancreatography (Magnetic resonance [MRCP] or Endoscopic retrograde [ERCP]). 9,10 The accuracy of US or CT in detecting mucinous papillomatosis was not so high, estimating about %. 3 Excessive mucous discharge from the ampulla of Vater observed during ERCP provides the high credit in making a diagnosis of BP but, in certain patients, a large amount of mucin can interfere direct visualization of the bile duct. Therefore, certain authors prefer to percutaneous transhepatic cholangioscopy (PTCS) owing to its merit of full direct visualization. 3 In addition, MRCP is useful in follow-up examination because of its 60
5 Say June Kim and Jung Uee Lee:Double Cholangiocarcinomas noninvasiveness. 10 As mentioned, BP has significant risk of malignant transformation. 1-3 Occasional coexistance of papillary adenocarcinoma in the background of papillary adenoma suggests that BP is not fixed pathologic entity, but represents a continuous histologic spectrum from adenoma, by way of dysplasia and carcinoma in situ, to carcinoma. 1,3,6 BP is frequently compared with intraductal papillary mucinous neoplasm of the pancreas (IPMN) because they share similar findings 6,11 ; they belong to intraductal tumor hypersecreting mucin which can result in inflammation - cholangitis and/or pancreatitis- secondary to ductal obstruction. In addition, they hold malignant potential in common which is characterized by slowly growing nature. As a result, patients with cholangiocarcinoma originated from BP usually have a prolonged survival than those with usual cholangiocarcinoma. 12 Recently these two desease entities -BP and IPMN- have been termed as a same category, that is, intrapapillary neoplasm of the liver (IPNL). 13,14 The location of cholangiocarcinoma is intrahepatic and/or extrahepatic throughout the bile duct. And irrespective of its location, cholangiocarcinoma can be stratified into mass-forming, periductal-infiltrating, and intraductalgrowing types according to its growth characteristics. 4 Mass-forming type indicates the nodular or exophytic nature of cholangiocarcinomas and after its growing into the lumen, it penestrates the bile duct wall and grows outward to form a nodular mass. Because of its high incidences of metastasis to the regional lymph node(s) 15 and poorly-differentiated histology, 16 resection of the primary tumor combined with lymph node dissection should be performed. Periductal-infiltrating type exhibits infiltrating or sclerosing morphology, and spreads longitudinally along the axis of the bile duct wall. Therefore, it is difficult to delineate the margin. Most hilar cholangiocarcinomas belong to the periductal infiltrating type, whereas most peripheral cholangiocarcinomas are of mass-forming type. 17 Its frequent metastasis to lymph nodes and distal organs necessitates more radical surgery as a treatment. The polypoid or papillary morphology of cholangiocarcinoma matches the intraductal-growing type. Malignant transformation of BP corresponds to this type of cholangiocarcinoma. 18 Intraductal-growing type is a low-grade malignancy and has a tendency to spread superficially within mucosa. Its intraluminal papillary projections are prone to be detached spontaneously and implanted apart so that multiple tumors involving many different locations within intra- and/or extrahepatic bile duct can be developed. 15,19,20 Because an intrahepatic growing cholangiocarcinoma invades the bile duct wall in the later phase and shows more favorable histology 16 than other types, tumor resection with a tumor-free margin suffices adequate treatment. Survival rates following curative resection is reported to be over 80%. 3 In such extensive cases of bilobar and multiple tumors, only liver transplantation can salvage the patients. 20,21 In short, BP is a rare disease entity predominantly affecting elderly males. It can be presented with biliary obstructing symptom such as acute cholangitis or cholestasis, especially in mucin-hypersecrtion type. BP grows along the mucosa and forms easily detachable papillary projections. It can also spread within the lumen detached from the primary site and implanted into another sites, resulting in multiple tumors. Malignant transformation of BP corresponds to the intraductal-growing type of cholangiocarcinoma expressing low-grade malignant potential. Tumor-free resection is sufficient as a treatment. Therefore, special attention should be paid to acquire R0 resection during operation because BP has a tendency of multiplicity and diffuse involvement. References 1. Taguchi J, Yasunaga M, Kojiro M, Arita T, Nakayama T, Simokobe T. Intrahepatic and extrahepatic biliary papillomatosis. Arch Pathol Lab Med 1993;117: Yeung YP, AhChong K, Chung CK, Chun AY. Biliary papillomatosis: report of seven cases and review of English 61
6 한국간담췌외과학회지 : 제 14 권 1 호 2010 literature. J Hepatobiliary Pancreat Surg 2003;10: Lee SS, Kim MH, Lee SK, et al. Clinicopathologic review of 58 patients with biliary papillomatosis. Cancer 2004;100: The general rules for the clinical and pathological study of primary liver cancer. Liver Cancer Study Group of Japan. Jpn J Surg 1989;19: Okulski EG, Dolin BJ, Kandawalla NM. Intrahepatic biliary papillomatosis. Arch Pathol Lab Med 1979;103: Nakanuma Y, Sasaki M, Ishikawa A, Tsui W, Chen TC, Huang SF. Biliary papillary neoplasm of the liver. Histol Histopathol 2002;17: Kim YI, Yu ES, Kim ST. Intraductal variant of peripheral cholangiocarcinoma of the liver with Clonorchis sinensis infection. Cancer 1989;63: Suh KS, Roh HR, Koh YT, Lee KU, Park YH, Kim SW. Clinicopathologic features of the intraductal growth type of peripheral cholangiocarcinoma. Hepatology 2000;31: Ma KF, Iu PP, Chau LF, Chong AK, Lam HS. Clinical and radiological features of biliary papillomatosis. Australas Radiol 2000;44: Chung DJ, Lee SK, Ha HK, Kim PN, Lee MG. Multiple biliary papillomatosis: comparison of MR cholangiography with endoscopic retrograde cholangiography. J Comput Assist Tomogr 2002;26: Kim HJ, Kim MH, Lee SK, et al. Mucin-hypersecreting bile duct tumor characterized by a striking homology with an intraductal papillary mucinous tumor (IPMT) of the pancreas. Endoscopy 2000;32: Chen MF, Jan YY, Chen TC. Clinical studies of mucin- producing cholangiocellular carcinoma: a study of 22 histopathology-proven cases. Ann Surg 1998;227: Shimonishi T, Zen Y, Chen TC, et al. Increasing expression of gastrointestinal phenotypes and p53 along with histologic progression of intraductal papillary neoplasia of the liver. Hum Pathol 2002;33: Chen TC, Nakanuma Y, Zen Y, et al. Intraductal papillary neoplasia of the liver associated with hepatolithiasis. Hepatology 2001;34: Lim JH, Park CK. Pathology of cholangiocarcinoma. Abdom Imaging 2004;29: Sasaki A, Aramaki M, Kawano K, et al. Intrahepatic peripheral cholangiocarcinoma: mode of spread and choice of surgical treatment. Br J Surg 1998;85: Choi BI, Lee JH, Han MC, Kim SH, Yi JG, Kim CW. Hilar cholangiocarcinoma: comparative study with sonography and CT. Radiology 1989;172: Güllüoglu MG, Ozden I, Poyanli A, Cevikbas U, Ariogul O. Intraductal growth-type mucin-producing peripheral cholangiocarcinoma associated with biliary papillomatosis. Ann Diagn Pathol 2007;11: Lim JH. Cholangiocarcinoma: morphologic classification according to growth pattern and imaging findings. AJR Am J Roentgenol 2003;181: Dumortier J, Scoazec JY, Valette PJ, Ponchon T, Boillot O. Successful liver transplantation for diffuse biliary papillomatosis. J Hepatol 2001;35: Beavers KL, Fried MW, Johnson MW, et al. Orthotopic liver transplantation for biliary papillomatosis. Liver Transpl 2001; 7:
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