Variations of the Union between the Terminal Bile Duct and the Pancreatic Duct in Patients with Pancreaticobiliary Maljunction

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1 Yamanashi Med. J. 18(4), 67~ 75, 2003 Review Variations of the Union between the Terminal Bile Duct and the Pancreatic Duct in Patients with Pancreaticobiliary Maljunction Hideki FUJII 1) 1) Department of Surgery, School of Medicine, Yamanashi University, Tamaho, Nakakoma, Yamanashi, , Japan Abstract: Background and Purpose: Pancreaticobiliary maljunction (PBM) is an anomaly with an extramural location of the union between the bile duct and the pancreatic duct system in the duodenum, and is probably caused by disarrangement of the embryonic connection between the two duct systems that presents varied clinical manifestations. The aim of this study was to analyze and categorize various patterns of connection between the two duct systems in PBM patients in order to improve the precision of the diagnosis of PBM and to establish safe surgical procedures to treat it. Materials and Methods: We made group classifications of the patterns of connection between the two duct systems in 226 PBM patients based on radiologic or/and anatomical examinations. Results: The 226 cases of PBM were divided into three groups: Group A, 2 patients with a complicated connection pattern, Group B, 176 patients with a notch or a small duct segment distal to the terminal bile duct, Group C, 48 patients without a notch or the segment at the terminal bile duct. Conclusion: In Group A, the terminal bile duct was probably connected to one of the multi-branched main ducts of the ventral pancreas, while in Group B, it was probably connected to a second branch of the ventral pancreas, and in Group C, directly to the main pancreatic duct. Key words: pancreaticobiliary maljunction, choledochal cyst, embryology INTRODUCTION The origin of a narrow duct segment distal to the enlarged common bile duct in congenital choledochal cysts is controversial. In 1936, Yotuyanagi described this duct system and termed it ductus pancreaticobiliosis based on the anatomical findings of autopsy cases 1). Babbitt detected the narrow duct system using direct cholangiography in 3 children with congenital cystic dilatation of the bile duct (CCBD, Received October 28, 2003 Accepted October 29, 2003 Alonso-Lej Type I 3) ) and described the narrow duct as a long common channel, defining it as an anomalous arrangement of the pancreaticobiliary ductal system 2). Both of those authors suspected that the narrow duct system was a predisposing factor in the occurrence of CCBD, and subsequently this hypothesis became well known throughout the world. Since Babbitt s report, further investigations of pancreaticobiliary maljunction (PBM) have been done. The Japanese Study Group on Pancreaticobiliary Maljunction presented extramural location of the union of the terminal bile

2 68 Hideki FUJII duct and the pancreatic duct in the duodenum as a definition of PBM 4). However, how PBM arises during embryogenesis remains unclear. Recently we proposed an hypothesis, based on radiological and anatomical analyses of PBM, that the narrow duct system was neither a narrowed bile duct nor a common channel of the two duct systems, but was rather part of the pancreatic duct system 5). That is, the development of PBM during embryogenesis is probably caused by disarrangement of the embryonic connection between the biliary and pancreatic ducts in an early period of gestation 5). However, this connection may occur at various locations of the duct system of the ventral pancreas 5), and moreover, PBM is often accompanied by other malformations of the hepatobiliary system and pancreas such as CCBD 2), congenital stricture of the intrahepatic bile duct 6) and pancreas divisum 7,8). Consequently, the connection pattern between the two duct systems may be extremely complicated, and making a precise diagnosis of PBM will continue to be very difficult in PBM patients with a short common duct 5) if the embryo genetic etiology of PBM is not clarified. The aim of this study was to analyze the anatomical variations in the location of the union and in the patterns of connection of the terminal bile duct with the pancreatic duct system in patients with PBM, in order to improve the precision of the diagnosis of PBM and to establish safe surgical procedures. We believe that making a precise diagnosis of PBM, which carries a high risk of bile duct cancer, is important for preventing the development of bile duct cancer 9,10). PATIENTS AND METHODS Patients Of 2,613 patients who underwent ERCP in our institute, 226 had PBM. The 226 PBM patients consisted of 70 males and 156 females, 158 of whom had benign biliary or/and pancreatic diseases and 68 who had a malignant tumor of the biliary system, while 146 patients had CCBD and 80 did not. The age of the 226 patients ranged from 6 to 81 years and the mean age of the patients with benign biliary disease was years in 54 males and years in 104 females. The mean age of the PBM patients with biliary malignancy was years in 16 males and years in 52 females. DIAGNOSTIC CRITERIA AND PBM DETECTION The Japanese Study Group on Pancreaticobiliary Maljunction has defined PBM as a congenital anomaly in which the junction of the pancreatic and biliary ducts is radiologically and/or anatomically detected outside of the duodenal wall (extramural location)[4]. We made a diagnosis of PBM by means of ERCP, PTC, and/or anatomical confirmation based on operative findings during transduodenal papilloplasty or examination of pancreatoduodenectomized specimens or autopsy materials. Radiological detection of the extramural location of the union of the two ducts in the duodenum was performed according to the methods described previously 5). RESULTS The 226 PBM patients were classified into three groups according to whether or not they had the following characteristics: 1) a compli-

3 Variations of Pancreaticobiliary Union 69 cated connection of the terminal bile duct or the cystic dilatation of the bile duct with the pancreatic duct system, 2) evidence of a notch or a small duct distal to the bile duct (narrow duct segment 11) ), and 3) no evidence of a notch or small duct at the union of the bile duct with the ventral pancreas duct on direct cholangiopancreatograms. Here notch means a v- shaped indentation on the terminal bile duct near the union of the bile duct and the main pancreatic duct seen on the cholangiopancreatogram, and a small duct means a much narrower duct distal to the terminal bile duct or to the biliary cyst. PBM was frequently associated with pancreas divisum, especially partial pancreas divisum 7) in which there was only communication between a small branch of the ventral pancreas and one of the dorsal pancreas. We encountered no case in which there was a union of the bile duct and the dorsal pancreatic duct. 1. Group A: PBM patients in whom the connection of the terminal bile duct (or the bottom of the biliary cyst) with the pancreatic duct showed a complicated pattern. Two of the 226 patients were classified into this group. In these patients, ERCP revealed multi-branching of the main pancreatic duct of the ventral pancreas and communication of the biliary cyst with one of the branches, as shown in Fig. 1a and 1b. 2. Group B: PBM patients in whom a notch or a small duct distal to the terminal bile duct was detected at the point of union between the two duct systems. Of the 226 patients, 176 were classified into this group. Direct cholangiograms of patients in Fig. 1. ERCP of a 37-year-old woman with Group A PBM, CCBD, pancreas divisum, and a biliary cyst, discovered by AUS in a mass survey screening. a) The terminal bile duct can be seen to join with a pancreatic duct (long thin arrow). However, the main pancreatic duct branches away into at least three branches, and one of them is connected with the biliary cyst at the bottom of the cyst. b) The dorsal pancreatic duct (arrow) is visualized by the flow of contrast medium through the major papilla. These images show multi-branching of the main duct of the ventral pancreas and the connection between the ventral and the dorsal pancreatic duct (partial pancreas divisum).

4 70 Hideki FUJII Fig. 2. T-tube cholangiogram of a 31-year-old woman with Group B PBM, after cholecystectomy. The terminal bile duct is seen to join with a small radicle (2 small thin arrows) arising from the main pancreatic duct (arrow) near the duodenal wall and a notch is formed in the distal portion of the bile duct. The terminal bile duct is seen to be suddenly reduced in diameter, showing an irregular shape at the distal end and connecting with the small radicle arising from the main pancreatic duct. This small radicle was a second branch of the ventral pancreatic duct. this group showed a notch or a small duct segment in the distal portion of the terminal bile duct (or the biliary cyst). In Fig. 2, a T-tube cholangio-pancreatogram shows a notch in the distal portion of the terminal bile duct, and this finding is thought to imply that a second branch of the pancreatic duct is interposed between the bile duct and the main pancreatic duct. Figure 3 reveals a small duct distal to the biliary cyst and a smaller pancreatic duct that arises from the small duct (narrow duct segment 11) ). Figure 4 shows the ERCP image after Fig. 3. ERCP of a 65-year-old woman with Group B PBM, CCBD and gallbladder cancer. A narrowed duct segment (2 small thin arrows) distal to the biliary cyst ca be seen. This segment is joined with the main pancreatic duct (long thin arrow). A small radicle (arrowhead) arising from the narrow duct segment can be seen. The narrowed duct segment is thought to be a second branch of the ventral pancreatic duct. resection of a biliary cyst in a case of CCBD. The main pancreatic duct appears to enter a large U-shaped duct, which seems to be the intrapancreatic portion of the common bile duct. But the U-shaped duct is considered to correspond to the common duct which occurs in PBM patients and consists of a narrow duct segment and part of the main pancreatic duct. This type of connection is considered to indicate that the bile duct is anatomically joined with the main duct of the ventral pancreas, accompanied by an interposition of the second or third branch of the ventral pancreatic duct between the two ducts. 3. Group C: PBM patients in whom a notch or

5 Variations of Pancreaticobiliary Union 71 Fig. 4. ERCP after resection of the bile duct cyst in a 20-year-old woman with Group B PBM and CCBD. The main pancreatic duct (long thin arrow) enters to a U-shaped large duct, which seems to be the intrapancreatic portion of the common bile duct at the point indicated by an asterisk, of which the top (indicated by an arrow) corresponds to the proximal end of the narrow duct segment distal to the resected biliary cyst. Small pancreatic duct radicles (arrowhead) arising from the U- shaped large duct can also be seen. Although the diameter of the U-shaped large duct and the main pancreatic duct are different, the duct from the major papilla (large arrow) to the tail of the pancreas corresponded to the main pancreatic duct, and the segment of the U-shaped large duct from the asterisk to the arrow was the second branch of the pancreatic duct. Fig. 5. ERCP of a 41-year-old woman with Group C PBM and acute cholecystitis. The terminal bile duct is joined to the main pancreatic duct near the duodenal wall (arrow) without a notch or a small duct. a small duct distal to the terminal bile duct was not detected at the union of the two ducts. Group C consisted of 48 patients with PBM. An ERCP (Fig. 5) of a representative PBM patient in this group demonstrated that the terminal bile duct was joined with the main pancreatic duct near the duodenal wall, without a notch or a small duct on the terminal bile duct. Figure 6 shows that the terminal bile duct was Fig. 6. Operative cholangiogram of a 7-year-old boy with Group C PBM, CCBD and bile duct stone. The terminal bile duct is joined (large arrow) to the main pancreatic duct far from the duodenal wall without a notch or a small duct.

6 72 Hideki FUJII Fig. 7. ERCP of a 55-year-old woman with Group C PBM, partial pancreas divisum and gallbladder cancer. The whole extrahepatic bile duct, part of the intrahepatic ducts, and the dorsal pancreatic duct (via the small duct indicated by a small arrow) were revealed by the flow of contrast medium through the major papilla. The terminal bile duct was directly joined (arrow) with the proximal end of the main duct of the ventral pancreas and a small pancreatic radicle (the high density line is indicated by a small arrow) was connected with the large duct from the major papilla (ventral pancreatic duct) and the dorsal pancreatic duct from the minor papilla to the pancreatic tail (partial pancreas divisum). Small pancreatic radicles (arrowhead) arose from the large duct from the major papilla, which is thought to be the main duct of the ventral pancreas.

7 Variations of Pancreaticobiliary Union 73 joined with the main pancreatic duct far from the duodenal wall without a notch or a small duct segment. Figure 7 shows that the extrahepatic bile duct and the dorsal pancreatic duct via a small duct arising from the main duct of the ventral pancreas (partial pancreas divisum 7,8) ). In this case, the terminal bile duct was considered to be joined directly with the proximal end of the main duct of the ventral pancreas. DISCUSSION Extramural location of the union of the terminal bile duct and the pancreatic duct in the duodenum was not recognized in the past as an anomaly in the pancreaticobiliary ductal system, but was rather thought to be a normal variations 9,12 14). However, in several reports that described detailed analyses of the location of the junction of the terminal bile duct and the pancreatic duct based on anatomical and/or radiological examinations, a long common channel 15) or extramural location of the union in the duodenum 15 17) was not found in normal cases, but was found in cases of CCBD, congenital biliary atresia (CBA) 18) or acute pancreatitis 12,19). Since Babbitt s key report about PBM 2), our knowledge about a long common channel has increased, and diagnostic criteria for PBM were presented by the Japanese Study Group on Pancreaticobiliary Maljunction 4). However, the mechanism of embryonic development of PBM was not clarified ay that time. We hope that our hypothesis about the mechanism of PBM development will aid progress in making a precise diagnosis of PBM and the establishment of safe surgical procedures for PBM. In this report, we presented various cholangiopancreatograms of PBM patients with various locations or/and anomalous connections due to an embryonic disarrangement between the bile duct and the pancreatic duct, and investigated the essential patterns of the disarrangement with the aim of establishing safe and appropriate surgical procedures for this disease. Moreover, a notch or a small duct segment was noted to be a key point of detecting PBM. We showed that the anatomical location of the union could exist at any site in the duct system of the ventral pancreas. In our series, 136 of the 226 PBM patients had a short common duct less than 1 cm in length, and these 136 patients consisted of 113 patients in Group B and 23 in Group C. The remaining 90 of the 226 patients had a long common duct over 1 cm in length, and they consisted of the 2 patients in Group A, 63 patients in Group B and 25 patients in Group C. A short common duct was apparently formed due to the location of the union near the duodenal wall in Group C patients and also in patients with a notch (not a small duct) in Group B. On the other hand, a long common duct was seen in Group B patients with a small duct segment and in Group C patients with the location of the union far from the duodenal wall, and also in Group A patients. Figure 8 shows a schematic diagram showing the possible anatomical points of the union. Clinical manifestations in PBM patients, such as acute pancreatitis 12,19), intermittent abdominal pain, obstructive jaundice, acute cholangitis, primary bile duct stones 20) and bile duct cancer 21,22) did not correlate with the presence of a long or a short common duct, with accompanying CCBD 5) or the connection patterns. These clinical features do not correlate with the length of the common duct in PBM patients, so it is difficult to detect the extramural location of the union in the duodenum, especially in patients with a short common duct. Concerning the relationship between PBM

8 74 Hideki FUJII Fig. 8. Schematic diagram showing possible anatomical points of the union between the terminal bile duct and the ventral pancreatic duct, indicated by numbers corresponding to those of Figs D: a small pancreatic duct connecting the dorsal and the ventral pancreatic duct in partial pancreas divisum. N: normal connection of the bile duct and pancreatic duct. and the development of gallbladder cancer, PBM was found in 45 of 112 patients with gallbladder cancer treated in our institute during the study period. Since PBM is considered to be a high risk condition for the development of gallbladder cancer 23), we make it a rule that PBM patients receive cholecystectomy as soon as possible even if the patients have no clinical manifestations, in order to prevent the development of gallbladder cancer 21 23). Moreover, since CCBD with PBM is also known to be associated with a high-risk condition for the development of bile duct cancer, preventive surgery is recommended when the disease is discovered. It is well known that an extirpation of the biliary cyst is the most appropriate procedure, but details of the optimal approach for the intrapancreatic portion of the biliary cyst, as well as those for the proximal portion of the cyst, remain controversial. It is important to establish a practical and safe procedure for treatment of the anomaly with the goals of avoiding intraoperative injury of the main pancreatic duct and preventing the development of cancer originating from a remnant cyst wall. The classification of the patterns of connection between the bile duct and the pancreatic duct into the groups described here should be helpful for the optimization of the surgical approach. A complete resection of the bile duct or the biliary cyst is possible only for patients with a small duct segment in Groups A and B. Resection of the terminal bile duct or the biliary cyst in patients with a notch in Group B and in patients in Group C must be performed in a manner that retains part of the terminal bile duct in order to avoid injury of the main pancreatic duct. REFERENCES 1) Yotuyanagi S. Contributions to the etiology and pathogeny of idiopathic cystic dilatation of the common bile duct with report of three cases: a new etiological theory based on supposed unequal epithelial proliferation at the stage of

9 Variations of Pancreaticobiliary Union 75 the physiological epithelial occlusion of the primitive choledochus. GANN 30: , ) Babbitt DP. Congenital choledochal cyst: new etiological concept based on anomalous relationships of common bile duct and pancreatic duct. Ann Radiol 12: , ) Alonso-Lej F, Rever WB, Pessagno DJ. Congenital choledochal cyst with a report of two and analysis of 94 cases. Int Abstr Surg 108: 1 23, ) The Japanese Study Group on Pancreaticobiliary Maljunction: Diagnostic criteria of pancreaticobiliary maljunction. J Hepatobiliary Pancreat Surg 1: , ) Matsumoto Y, Fujii H, Itakura J, Mogaki M, Matsuda M, et al. Pancreaticobiliary Maljunction: etiologic concepts based on radiologic aspects. Gastrointest Endosc 53: , ) Matsumoto Y, Fujii H, Yoshioka M, Sekikawa T, Wada T, et al. Biliary strictures as a cause of primary intrahepatic bile duct stone. World J Surg 10: , ) Douglas CW, Michael VS. Partial pancreas divisum. Cleveland Clin J Med 54: 33 37, ) Itakura J, Fujii H, Matsumoto Y, Suda K. Clinicopathological studies of anomalous arrangement of the pancreaticobiliary ductal system with pancreas divisum. J Hepatobiliary Pancreat Surg 1: , ) Kimura K, Ohto M, Saisho H, Unogawa T, Tsuchiya Y, et al. Association of gallbladder carcinoma and anomalous pancreaticobiliary ductal union. Gastroenterol 89: , ) Kinoshita H, Nagata E, Hirohashi K, Sakai K, Kobayoshi Y. Carcinoma of the gallbladder with an anomalous connection between the choledochus and the pancreatic duct: report of 10 cases and review of the literature in Japan. Cancer 54: , ) Suda K, Matsumoto Y, Miyano T. Narrow duct segment distal to choledochal cyst. Am J Gastroenterol 86: , ) Hicken NF, McAllister AJ. Is the reflux of bile into the pancreatic ducts a normal or abnormal physiologic process? Am J Surg 89: , ) Dowdy GS, Waldron GW, Brown WG. Surgical anatomy of the pancreatobiliary ductal system. Arch Surg 84: , ) Misra SP, Gulati P, Thorat VK, VIJ JC, Anand BS. Pancreaticobiliary ductal union in biliary diseases; An endoscopic retrograde cholangiopancreatographic study. Gastroenterol 96: , ) Jones GM, Caylor HD. Anomalous termination of common duct Am J Surg 93: , ) Hand BH. An anatomical study of choledochoduodenal area. British J Surg 50: , ) Suda K, Miyano T, Hashimato K. The choledocho pancreatico-ductal junction in infantile obstructive jaundice disease. Acta Pathol Jpn 30: , ) Arima E, Akita H. Congenital biliary tract dilation and anomalous junction of the pancreaticobiliary ductal system J Pediatr Surg 14: 9 15, ) Schweiger P, Schweiger M. Pancreaticobiliary long common channel syndrome and congenital anomalous dilatation of the choledochal duct study of 46 patients. Eur J Pediatr Surg 3: 15 21, ) Matsumoto Y, Uchida K, Nakase A, Honjo I. Congenital cystic dilatation of the common bile duct as a cause of primary bile duct stone. Am J Surg 134: , ) Tanno S, Obara T, Fujii T, Mizukami Y, Shuda R, et al. Proliferative potential and K-ras mutation in epithelial hyperplasia of the gallbladder in patient with anomalous pancreaticobiliary ductal union. Cancer 83: , ) Hanada K, Itoh M, Fujii K, Tsuchida A, Ooishi H, et al. K-ras and P53 mutations in Stage gallbladder carcinoma with an anomalous junction of the pancreaticobiliary duct. Cancer 77: , ) Matsumoto Y, Fujii H, Itakura J, Matsuda M, Suda K. Recent advances in pancreaticobiliary maljunction: clinical significance and carcinogenesis. J Hepatobiliary Pancreat Surg 9: 45 54, 2002.

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