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Published in: Journal of Gastrointestinal Surgery 2/2010

01-02-2010 | Original Article

Surgical Management of Infrahilar/Suprapancreatic Cholangiocarcinoma: an Analysis of the Surgical Procedures, Surgical Margins, and Survivals of 77 Patients

Authors: Yoshihiro Sakamoto, Kazuaki Shimada, Satoshi Nara, Minoru Esaki, Hidenori Ojima, Tsuyoshi Sano, Junji Yamamoto, Tomoo Kosuge

Published in: Journal of Gastrointestinal Surgery | Issue 2/2010

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Abstract

Background

Optical surgical management of infrahilar/suprapancreatic cholangiocarcinoma remains controversial.

Methods

Between 1988 and 2006, 77 patients with infrahilar/suprapancreatic cholangiocarcinoma underwent curative surgical resections following our intention-to-treat strategy. The clinicopathological factors affecting survival were evaluated using univariate and multivariate analyses with regard to the surgical procedures and surgical margins.

Results

The surgical procedure included extrahepatic bile duct resection alone (EHBD; n = 17), major hepatectomy combined with extrahepatic bile duct resection (MHx; n = 26), pancreaticoduodenectomy (PD; n = 28), and MHx and concomitant PD (HPD; n = 6). Performance of MHx and/or PD in addition to EHBD increased surgical morbidity (p = 0.001). Among patients undergoing the four surgical procedures (EHBD, MHx, PD, and HPD), no significant difference was found in the incidence of positive overall surgical margins (53%, 65%, 46%, and 67%, p = 0.51) or long-term survivals (median survival time, 51, 27, 41, and 22 months, p = 0.60). A multivariate analysis revealed that perineural invasion (95% confidence interval, 1.1–12.3, p = 0.009), nodal metastasis (1.6–6.8, p = 0.001), and blood transfusion (1.1–3.9, p = 0.02) were independent predictors of a poor outcome. Perineural invasion was associated with positive radial margins (p = 0.045) and submucosal ductal infiltration (p = 0.03).

Conclusion

Perineural invasion, rather than the type of surgical procedure, had a significant impact on surgical curability and survival of patients with infrahilar/suprapancreatic cholangiocarcinoma treated according to our intention-to-treat strategy.
Literature
1.
go back to reference Kosuge T, Yamamoto J, Shimada K, Yamasaki S, Makuuchi M. Improved surgical results for hilar cholangiocarcinoma with procedures including major hepatic resection. Ann Surg 1999;230:663–671.CrossRefPubMed Kosuge T, Yamamoto J, Shimada K, Yamasaki S, Makuuchi M. Improved surgical results for hilar cholangiocarcinoma with procedures including major hepatic resection. Ann Surg 1999;230:663–671.CrossRefPubMed
2.
go back to reference Neuhaus P, Jonas S, Bechstein WO, Lohmann R, Radke C, Kling N, Wex C, Lobeck H, Hintze R. Extended resections for hilar cholangiocarcinoma. Ann Surg 1999;230:808–818.CrossRefPubMed Neuhaus P, Jonas S, Bechstein WO, Lohmann R, Radke C, Kling N, Wex C, Lobeck H, Hintze R. Extended resections for hilar cholangiocarcinoma. Ann Surg 1999;230:808–818.CrossRefPubMed
3.
go back to reference Kawasaki S, Imamura H, Kobayashi A, Noike T, Miwa S, Miyagawa S. Results of surgical resection for patients with hilar bile duct cancer. Application of extended hepatectomy after biliary drainage and hemihepatic portal vein embolization. Ann Surg 2003;238:84–92.CrossRefPubMed Kawasaki S, Imamura H, Kobayashi A, Noike T, Miwa S, Miyagawa S. Results of surgical resection for patients with hilar bile duct cancer. Application of extended hepatectomy after biliary drainage and hemihepatic portal vein embolization. Ann Surg 2003;238:84–92.CrossRefPubMed
4.
go back to reference Seyama Y, Kubota K, Sano K, Noie T, Takayama T, Kosuge T, Makuuchi M. Long-term outcome of extended hemihepatectomy for hilar bile duct cancer with no mortality and high survival rate. Ann Surg 2003;238:73–83.CrossRefPubMed Seyama Y, Kubota K, Sano K, Noie T, Takayama T, Kosuge T, Makuuchi M. Long-term outcome of extended hemihepatectomy for hilar bile duct cancer with no mortality and high survival rate. Ann Surg 2003;238:73–83.CrossRefPubMed
5.
go back to reference Kondo S, Hirano S, Ambo Y, Tanaka E, Okushiba S, Morikawa T, Katoh H. Forty consecutive resection of hilar cholangiocarcinoma with no postoperative mortality and no positive ductal margins. Results of a prospective study. Ann Surg 2004;240:95–101.CrossRefPubMed Kondo S, Hirano S, Ambo Y, Tanaka E, Okushiba S, Morikawa T, Katoh H. Forty consecutive resection of hilar cholangiocarcinoma with no postoperative mortality and no positive ductal margins. Results of a prospective study. Ann Surg 2004;240:95–101.CrossRefPubMed
6.
go back to reference Hemming AW, Reed AI, Fujita S, Foley DP, Howard RJ. Surgical management of hilar cholangiocarcinoma. Ann Surg 2005;241:693–702.CrossRefPubMed Hemming AW, Reed AI, Fujita S, Foley DP, Howard RJ. Surgical management of hilar cholangiocarcinoma. Ann Surg 2005;241:693–702.CrossRefPubMed
7.
go back to reference Sano T, Shimada K, Sakamoto Y, Yamamoto J, Yamasaki S, Kosuge T. One hundred two consecutive hepatobiliary resections for perihilar cholangiocarcinoma with zero mortality. Ann Surg 2006;244:240–247.CrossRefPubMed Sano T, Shimada K, Sakamoto Y, Yamamoto J, Yamasaki S, Kosuge T. One hundred two consecutive hepatobiliary resections for perihilar cholangiocarcinoma with zero mortality. Ann Surg 2006;244:240–247.CrossRefPubMed
8.
go back to reference Bhuiya MR, Nimura Y, Kamiya J, Kondo S, Nagino M, Hayakawa N. Clinicopathologic factors influencing survival of patients with bile duct carcinoma: multivariate statistical analysis. World J Surg 1993;17:653–657.CrossRefPubMed Bhuiya MR, Nimura Y, Kamiya J, Kondo S, Nagino M, Hayakawa N. Clinicopathologic factors influencing survival of patients with bile duct carcinoma: multivariate statistical analysis. World J Surg 1993;17:653–657.CrossRefPubMed
9.
go back to reference Ogura Y, Takahashi K, Tabata M, Mizumoto R. Clinicopathological study on carcinoma of the extrahepatic bile duct with special focus on cancer invasion on the surgical margins. World J Surg 1994;18:778–784.CrossRefPubMed Ogura Y, Takahashi K, Tabata M, Mizumoto R. Clinicopathological study on carcinoma of the extrahepatic bile duct with special focus on cancer invasion on the surgical margins. World J Surg 1994;18:778–784.CrossRefPubMed
10.
go back to reference Fong Y, Blumgart LH, Lin E, Fortner JG, Brennan MF. Outcome of treatment for distal bile duct cancer. Br J Surg 1996;83:1712–1715.CrossRefPubMed Fong Y, Blumgart LH, Lin E, Fortner JG, Brennan MF. Outcome of treatment for distal bile duct cancer. Br J Surg 1996;83:1712–1715.CrossRefPubMed
11.
go back to reference Kayahara M, Nagakawa T, Ohta T, Kitagawa H, Tajima H, Miwa K. Role of nodal involvement and the periductal soft-tissue margin in middle and distal bile duct cancer. Ann Surg 1999;229:76–83.CrossRefPubMed Kayahara M, Nagakawa T, Ohta T, Kitagawa H, Tajima H, Miwa K. Role of nodal involvement and the periductal soft-tissue margin in middle and distal bile duct cancer. Ann Surg 1999;229:76–83.CrossRefPubMed
12.
go back to reference Sasaki R, Takahashi M, Funato O, Nitta H, Murakami M, Kawamura H, Suto T, Kanno S, Saito K. Prognostic significance of lymph node involvement in middle and distal bile duct cancer. Surgery 2001;129:677–683.CrossRefPubMed Sasaki R, Takahashi M, Funato O, Nitta H, Murakami M, Kawamura H, Suto T, Kanno S, Saito K. Prognostic significance of lymph node involvement in middle and distal bile duct cancer. Surgery 2001;129:677–683.CrossRefPubMed
13.
go back to reference Todoroki T, Kawamoto T, Koike N, Fukao K, Shoda J, Takahashi H. Treatment strategy for patients with middle and lower third bile duct cancer. Br J Surg 2001;88:364–370.CrossRefPubMed Todoroki T, Kawamoto T, Koike N, Fukao K, Shoda J, Takahashi H. Treatment strategy for patients with middle and lower third bile duct cancer. Br J Surg 2001;88:364–370.CrossRefPubMed
14.
go back to reference Yoshida T, Matsumoto T, Sasaki A, Morii Y, Aramaki M, Kitano S. Prognostic factors after pancreatoduodenectomy with extended lymphadenectomy for distal bile duct cancer. Arch Surg 2002;137:69–73.CrossRefPubMed Yoshida T, Matsumoto T, Sasaki A, Morii Y, Aramaki M, Kitano S. Prognostic factors after pancreatoduodenectomy with extended lymphadenectomy for distal bile duct cancer. Arch Surg 2002;137:69–73.CrossRefPubMed
15.
go back to reference Sakamoto Y, Kosuge T, Shimada K, Sano T, Ojima H, Yamamoto J, Yamasaki S, Takayama T, Makuuchi M. Prognostic factors of surgical resection in middle and distal bile duct cancer—an analysis of 55 patients concerning the significance of ductal and excisional margins. Surgery 2005;137:396–402.CrossRefPubMed Sakamoto Y, Kosuge T, Shimada K, Sano T, Ojima H, Yamamoto J, Yamasaki S, Takayama T, Makuuchi M. Prognostic factors of surgical resection in middle and distal bile duct cancer—an analysis of 55 patients concerning the significance of ductal and excisional margins. Surgery 2005;137:396–402.CrossRefPubMed
16.
go back to reference Japanese Society of Biliary Surgery (JSBC). General Rules for Surgical and Pathological Studies on Cancer of the Biliary Tract. 5th ed. Tokyo: Kanehara, 2003. Japanese Society of Biliary Surgery (JSBC). General Rules for Surgical and Pathological Studies on Cancer of the Biliary Tract. 5th ed. Tokyo: Kanehara, 2003.
17.
go back to reference Bismuth H, Corlette MB. Intrahepatic cholangioenteric anastomosis in carcinoma of the hilus of the liver. Surg Gynecol Obstet 1975;140:170–178.PubMed Bismuth H, Corlette MB. Intrahepatic cholangioenteric anastomosis in carcinoma of the hilus of the liver. Surg Gynecol Obstet 1975;140:170–178.PubMed
18.
go back to reference Tompkins RK, Saunders K, Roslyn JJ, Longmire WP Jr. Changing patterns in diagnosis and management of bile duct cancer. Ann Surg 1990;211:614–620.PubMed Tompkins RK, Saunders K, Roslyn JJ, Longmire WP Jr. Changing patterns in diagnosis and management of bile duct cancer. Ann Surg 1990;211:614–620.PubMed
19.
go back to reference Reding R, Buard JL, Lebeau G, Launois B. Surgical management of 552 carcinomas of the extrahepatic bile ducts (gallbladder and periampullary tumors excluded). Results of the French surgical association survey. Ann Surg 1991;213:236–241.CrossRefPubMed Reding R, Buard JL, Lebeau G, Launois B. Surgical management of 552 carcinomas of the extrahepatic bile ducts (gallbladder and periampullary tumors excluded). Results of the French surgical association survey. Ann Surg 1991;213:236–241.CrossRefPubMed
20.
go back to reference Sakamoto E, Nimura Y, Hayakawa N, Kamiya J, Kondo S, Nagino M, Kanai M, Miyachi M, Uesaka K. The pattern of infiltration at the proximal border of hilar bile duct carcinoma. Ann Surg 1998;227:405–411.CrossRefPubMed Sakamoto E, Nimura Y, Hayakawa N, Kamiya J, Kondo S, Nagino M, Kanai M, Miyachi M, Uesaka K. The pattern of infiltration at the proximal border of hilar bile duct carcinoma. Ann Surg 1998;227:405–411.CrossRefPubMed
21.
go back to reference Ikeyama T, Nagino M, Oda K, Ebata T, Nishio H, Nimura Y. Surgical approach to Bismuth type I and II hilar cholangiocarcinomas: audit of 54 consecutive cases. Ann Surg 2007;246:1052–1057.CrossRefPubMed Ikeyama T, Nagino M, Oda K, Ebata T, Nishio H, Nimura Y. Surgical approach to Bismuth type I and II hilar cholangiocarcinomas: audit of 54 consecutive cases. Ann Surg 2007;246:1052–1057.CrossRefPubMed
22.
go back to reference Ito F, Agni R, Rettammel RJ, Been MJ, Cho CS, Mahvi DM, Rikkers LF, Weber SM. Resection of hilar cholangiocarcinoma: concomitant liver resection decreases hepatic recurrence. Ann Surg 2008;248:273–279.CrossRefPubMed Ito F, Agni R, Rettammel RJ, Been MJ, Cho CS, Mahvi DM, Rikkers LF, Weber SM. Resection of hilar cholangiocarcinoma: concomitant liver resection decreases hepatic recurrence. Ann Surg 2008;248:273–279.CrossRefPubMed
23.
go back to reference Sakamoto Y, Sano T, Shimada K, Kosuge T, Kimata Y, Sakuraba M, Yamamoto J, Ojima H. Clinical significance of reconstruction of the right hepatic artery for biliary malignancy. Langenbecks Arch Surg 2006;391:203–208.CrossRefPubMed Sakamoto Y, Sano T, Shimada K, Kosuge T, Kimata Y, Sakuraba M, Yamamoto J, Ojima H. Clinical significance of reconstruction of the right hepatic artery for biliary malignancy. Langenbecks Arch Surg 2006;391:203–208.CrossRefPubMed
24.
go back to reference Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M. International study group on pancreatic fistula definition. International study group on pancreatic fistula definition. Postoperative pancreatic fistula: an International Study Group (ISGPF) definition. Surgery 2005;138:8–13.CrossRefPubMed Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M. International study group on pancreatic fistula definition. International study group on pancreatic fistula definition. Postoperative pancreatic fistula: an International Study Group (ISGPF) definition. Surgery 2005;138:8–13.CrossRefPubMed
25.
go back to reference Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Büchler MW. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142:761–768.CrossRefPubMed Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Büchler MW. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142:761–768.CrossRefPubMed
26.
go back to reference International Union Against Cancer (UICC). TNM classification of malignant tumours. In Sobin LH, Wittekind CH, eds. 6th ed. New York: Wiley-Liss, 2002. International Union Against Cancer (UICC). TNM classification of malignant tumours. In Sobin LH, Wittekind CH, eds. 6th ed. New York: Wiley-Liss, 2002.
27.
go back to reference Bhuiya MR, Nimura Y, Kamiya J, Kondo S, Fukata S, Hayakawa N, Shionoya S. Clinicopathologic studies on perineural invasion of bile duct carcinoma. Ann Surg 1992;215:344–349.PubMedCrossRef Bhuiya MR, Nimura Y, Kamiya J, Kondo S, Fukata S, Hayakawa N, Shionoya S. Clinicopathologic studies on perineural invasion of bile duct carcinoma. Ann Surg 1992;215:344–349.PubMedCrossRef
28.
go back to reference Yamaguchi R, Nagino M, Oda K, Kamiya J, Uesaka K, Nimura Y. Perineural invasion has a negative impact on survival of patients with gallbladder carcinoma. Br J Surg 2002;89:1130–1136.CrossRefPubMed Yamaguchi R, Nagino M, Oda K, Kamiya J, Uesaka K, Nimura Y. Perineural invasion has a negative impact on survival of patients with gallbladder carcinoma. Br J Surg 2002;89:1130–1136.CrossRefPubMed
29.
go back to reference Sakamoto Y, Kosuge T, Shimada K, Sano T, Hibi T, Yamamoto J, Takayama T, Makuuchi M. Clinical significance of extrahepatic bile duct resection for advanced gallbladder cancer. J Surg Oncol 2006;94:298–306.CrossRefPubMed Sakamoto Y, Kosuge T, Shimada K, Sano T, Hibi T, Yamamoto J, Takayama T, Makuuchi M. Clinical significance of extrahepatic bile duct resection for advanced gallbladder cancer. J Surg Oncol 2006;94:298–306.CrossRefPubMed
30.
go back to reference Makuuchi M, Thai BL, Takayasu K, Takayama T, Kosuge T, Gunvén P, Yamazaki S, Hasegawa H, Ozaki H. Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery 1990;107:521–527.PubMed Makuuchi M, Thai BL, Takayasu K, Takayama T, Kosuge T, Gunvén P, Yamazaki S, Hasegawa H, Ozaki H. Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery 1990;107:521–527.PubMed
31.
go back to reference Seyama Y, Kubota K, Kobayashi T, Hirata Y, Itoh A, Makuuchi M. Two-staged pancreatoduodenectomy with external drainage of pancreatic juice and omental graft technique. J Am Coll Surg 1998;187:103–105.CrossRefPubMed Seyama Y, Kubota K, Kobayashi T, Hirata Y, Itoh A, Makuuchi M. Two-staged pancreatoduodenectomy with external drainage of pancreatic juice and omental graft technique. J Am Coll Surg 1998;187:103–105.CrossRefPubMed
32.
go back to reference Sakamoto Y, Shimada K, Esaki M, Kajiwara T, Sano T, Kosuge T. Wrapping the stump of the gastroduodenal artery using the falciform ligament during pancreaticoduodenectomy. J Am Coll Surg 2007;204:334–336.CrossRefPubMed Sakamoto Y, Shimada K, Esaki M, Kajiwara T, Sano T, Kosuge T. Wrapping the stump of the gastroduodenal artery using the falciform ligament during pancreaticoduodenectomy. J Am Coll Surg 2007;204:334–336.CrossRefPubMed
33.
go back to reference Foster RS Jr, Costanza MC, Foster JC, Wanner MC, Foster CB. Adverse relationship between blood transfusions and survival after colectomy for colon cancer. Cancer. 1985;55:1195–1201.CrossRefPubMed Foster RS Jr, Costanza MC, Foster JC, Wanner MC, Foster CB. Adverse relationship between blood transfusions and survival after colectomy for colon cancer. Cancer. 1985;55:1195–1201.CrossRefPubMed
34.
go back to reference Nowak MM, Ponsky JL. Blood transfusion and disease-free survival in carcinoma of the breast. J Surg Oncol 1984;27:124–130.CrossRefPubMed Nowak MM, Ponsky JL. Blood transfusion and disease-free survival in carcinoma of the breast. J Surg Oncol 1984;27:124–130.CrossRefPubMed
35.
go back to reference Sugezawa A, Kaibara N, Sumi K, Ohta M, Kimura O, Nishidoi H, Koga S. Blood transfusion and the prognosis of patients with gastric cancer. J Surg Oncol. 1989;42:113–116.CrossRefPubMed Sugezawa A, Kaibara N, Sumi K, Ohta M, Kimura O, Nishidoi H, Koga S. Blood transfusion and the prognosis of patients with gastric cancer. J Surg Oncol. 1989;42:113–116.CrossRefPubMed
36.
go back to reference Park SJ, Kim SW, Jang JY, Lee KU, Park YH. Intraoperative transfusion: is it a real prognostic factor of periampullary cancer following pancreatoduodenectomy? World J Surg 2002;26:487–492.CrossRefPubMed Park SJ, Kim SW, Jang JY, Lee KU, Park YH. Intraoperative transfusion: is it a real prognostic factor of periampullary cancer following pancreatoduodenectomy? World J Surg 2002;26:487–492.CrossRefPubMed
37.
go back to reference Yamamoto J, Kosuge T, Takayama T, Shimada K, Yamasaki S, Ozaki H, Yamaguchi N, Mizuno S, Makuuchi M. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy. Surgery 1994;115:303–309.PubMed Yamamoto J, Kosuge T, Takayama T, Shimada K, Yamasaki S, Ozaki H, Yamaguchi N, Mizuno S, Makuuchi M. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy. Surgery 1994;115:303–309.PubMed
38.
go back to reference Blajchman MA, Bardossy L, Carmen R, Sastry A, Singal DP. Allogeneic blood transfusion-induced enhancement of tumor growth: two animal models showing amelioration by leukodepletion and passive transfer using spleen cells. Blood 1993;81:1880–1882.PubMed Blajchman MA, Bardossy L, Carmen R, Sastry A, Singal DP. Allogeneic blood transfusion-induced enhancement of tumor growth: two animal models showing amelioration by leukodepletion and passive transfer using spleen cells. Blood 1993;81:1880–1882.PubMed
Metadata
Title
Surgical Management of Infrahilar/Suprapancreatic Cholangiocarcinoma: an Analysis of the Surgical Procedures, Surgical Margins, and Survivals of 77 Patients
Authors
Yoshihiro Sakamoto
Kazuaki Shimada
Satoshi Nara
Minoru Esaki
Hidenori Ojima
Tsuyoshi Sano
Junji Yamamoto
Tomoo Kosuge
Publication date
01-02-2010
Publisher
Springer-Verlag
Published in
Journal of Gastrointestinal Surgery / Issue 2/2010
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-009-1072-7

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