World Journal of Surgery

, Volume 38, Issue 5, pp 1164–1176

Surgical Treatment of 144 Cases of Hilar Cholangiocarcinoma Without Liver-Related Mortality

  • Norihiko Furusawa
  • Akira Kobayashi
  • Takahide Yokoyama
  • Akira Shimizu
  • Hiroaki Motoyama
  • Sin-ichi Miyagawa



The present study evaluated whether the short- and long-term outcomes improved during our 23 years of experience treating 144 consecutive patients with hilar cholangiocarcinoma.


Patients treated between 1990 and 2000 (period 1; n = 70) were retrospectively compared with those treated between 2001 and 2012 (period 2; n = 74). Mortality and major complications were defined as any death occurring within 90 days of surgery and a grade III–IV complication according to the Clavien classification, respectively.


The mortality and major complication rates decreased from 1.2 and 34 % during period 1–0 and 24 % during period 2, respectively. Although the surgical procedure was comparable between the two periods, the median blood loss was significantly reduced from 1,020 mL during period 1–745 mL during period 2 (P = 0.003), and blood loss was the only significant predictor of postoperative morbidity in a multivariable analysis. The R0 resection rate (70 vs. 78 %, P = 0.250) and the 5-year survival rate (33 vs. 35 %, P = 0.529) were similar for the two periods. A multivariable analysis identified positive nodal involvement and R1–2 resection as independent prognostic factors for survival.


The perioperative outcomes after surgical treatment for hilar cholangiocarcinoma have steadily improved through the accumulation of experience and meticulous surgical techniques to reduce blood loss. Further improvement of the R0 resection rate could prolong patient survival.


  1. 1.
    Hadjis NS, Blenkharn JI, Alexander N et al (1990) Outcome of radical surgery in hilar cholangiocarcinoma. Surgery 107:597–604PubMedGoogle Scholar
  2. 2.
    Baer HU, Stain SC, Dennison AR et al (1993) Improvements in survival by aggressive resections of hilar cholangiocarcinoma. Ann Surg 217:20–27PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Pichlmayr R, Weimann A, Klempnauer J et al (1996) Surgical treatment in proximal bile duct cancer. A single-center experience. Ann Surg 224:628–638PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Mizumoto R, Kawarada Y, Suzuki H (1986) Surgical treatment of hilar carcinoma of the bile duct. Surg Gynecol Obstet 162:153–158PubMedGoogle Scholar
  5. 5.
    Klempnauer J, Ridder GJ, von Wasielewski R et al (1997) Resectional surgery of hilar cholangiocarcinoma: a multivariate analysis of prognostic factors. J Clin Oncol 15:947–954PubMedGoogle Scholar
  6. 6.
    Nimura Y, Hayakawa N, Kamiya J et al (1990) Hepatic segmentectomy with caudate lobe resection for bile duct carcinoma of the hepatic hilus. World J Surg 14:535–543 (discussion 544)PubMedCrossRefGoogle Scholar
  7. 7.
    Neuhaus P, Jonas S, Bechstein WO et al (1999) Extended resections for hilar cholangiocarcinoma. Ann Surg 230:808–818 (discussion 819)PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Jarnagin WR, Fong Y, DeMatteo RP et al (2001) Staging, resectability, and outcome in 225 patients with hilar cholangiocarcinoma. Ann Surg 234:507–517 (discussion 517–509)PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Kawasaki S, Imamura H, Kobayashi A et al (2003) 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 238:84–92PubMedCentralPubMedGoogle Scholar
  10. 10.
    Burke EC, Jarnagin WR, Hochwald SN et al (1998) Hilar cholangiocarcinoma: patterns of spread, the importance of hepatic resection for curative operation, and a presurgical clinical staging system. Ann Surg 228:385–394PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Launois B, Terblanche J, Lakehal M et al (1999) Proximal bile duct cancer: high resectability rate and 5-year survival. Ann Surg 230:266–275PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Kawasaki S, Makuuchi M, Miyagawa S et al (1994) Radical operation after portal embolization for tumor of hilar bile duct. J Am Coll Surg 178:480–486PubMedGoogle Scholar
  13. 13.
    Makuuchi M, Thai BL, Takayasu K et al (1990) Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery 107:521–527PubMedGoogle Scholar
  14. 14.
    Makuuchi M, Bandai Y, Ito T et al (1980) Ultrasonically guided percutaneous transhepatic bile drainage: a single-step procedure without cholangiography. Radiology 136:165–169PubMedGoogle Scholar
  15. 15.
    Kobayashi A, Miwa S, Nakata T et al (2010) Disease recurrence patterns after R0 resection of hilar cholangiocarcinoma. Br J Surg 97:56–64PubMedCrossRefGoogle Scholar
  16. 16.
    Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (eds) (2010) Perihilar bile ducts. In: AJCC Cancer Staging Manual, 7th edition. New York: Springer, pp 219–222Google Scholar
  17. 17.
    Pringle JH (1908) Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg 48:541–549PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Rahbari NN, Garden OJ, Padbury R et al (2011) Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149:713–724PubMedCrossRefGoogle Scholar
  20. 20.
    Kosuge T, Yamamoto J, Shimada K et al (1999) Improved surgical results for hilar cholangiocarcinoma with procedures including major hepatic resection. Ann Surg 230:663–671PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Kondo S, Hirano S, Ambo Y et al (2004) Forty consecutive resections of hilar cholangiocarcinoma with no postoperative mortality and no positive ductal margins: results of a prospective study. Ann Surg 240:95–101PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Nuzzo G, Giuliante F, Ardito F et al (2012) Improvement in perioperative and long-term outcome after surgical treatment of hilar cholangiocarcinoma: results of an Italian multicenter analysis of 440 patients. Arch Surg 147:26–34PubMedCrossRefGoogle Scholar
  23. 23.
    Farges O, Regimbeau JM, Fuks D et al (2013) Multicentre European study of preoperative biliary drainage for hilar cholangiocarcinoma. Br J Surg 100:274–283PubMedCrossRefGoogle Scholar
  24. 24.
    Seyama Y, Kubota K, Sano K et al (2003) Long-term outcome of extended hemihepatectomy for hilar bile duct cancer with no mortality and high survival rate. Ann Surg 238:73–83PubMedCentralPubMedGoogle Scholar
  25. 25.
    Ozawa K, Yamada T, Ida T et al (1974) Primary cause of decreased functional reserve in the liver of icteric patients and rats. Surg Gynecol Obstet 139:358–362PubMedGoogle Scholar
  26. 26.
    Bailey ME (1976) Endotoxin, bile salts and renal function in obstructive jaundice. Br J Surg 63:774–778PubMedCrossRefGoogle Scholar
  27. 27.
    Zimmermann H, Reichen J, Zimmermann A et al (1992) Reversibility of secondary biliary fibrosis by biliodigestive anastomosis in the rat. Gastroenterology 103:579–589PubMedGoogle Scholar
  28. 28.
    Lang C, Berardi S, Schafer M et al (2002) Impaired ketogenesis is a major mechanism for disturbed hepatic fatty acid metabolism in rats with long-term cholestasis and after relief of biliary obstruction. J Hepatol 37:564–571PubMedCrossRefGoogle Scholar
  29. 29.
    McPherson GA, Benjamin IS, Hodgson HJ et al (1984) Pre-operative percutaneous transhepatic biliary drainage: the results of a controlled trial. Br J Surg 71:371–375PubMedCrossRefGoogle Scholar
  30. 30.
    Hochwald SN, Burke EC, Jarnagin WR et al (1999) Association of preoperative biliary stenting with increased postoperative infectious complications in proximal cholangiocarcinoma. Arch Surg 134:261–266PubMedCrossRefGoogle Scholar
  31. 31.
    Cherqui D, Benoist S, Malassagne B et al (2000) Major liver resection for carcinoma in jaundiced patients without preoperative biliary drainage. Arch Surg 135:302–308PubMedCrossRefGoogle Scholar
  32. 32.
    Sano T, Shimada K, Sakamoto Y et al (2006) One hundred two consecutive hepatobiliary resections for perihilar cholangiocarcinoma with zero mortality. Ann Surg 244:240–247PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Chauhan A, House MG, Pitt HA et al (2011) Post-operative morbidity results in decreased long-term survival after resection for hilar cholangiocarcinoma. HPB (Oxford) 13:139–147CrossRefGoogle Scholar
  34. 34.
    D’Angelica M, Martin RC 2nd, Jarnagin WR et al (2004) Major hepatectomy with simultaneous pancreatectomy for advanced hepatobiliary cancer. J Am Coll Surg 198:570–576PubMedCrossRefGoogle Scholar
  35. 35.
    Gerhards MF, van Gulik TM, de Wit LT et al (2000) Evaluation of morbidity and mortality after resection for hilar cholangiocarcinoma: a single center experience. Surgery 127:395–404PubMedCrossRefGoogle Scholar
  36. 36.
    Ebata T, Nagino M, Kamiya J et al (2003) Hepatectomy with portal vein resection for hilar cholangiocarcinoma: audit of 52 consecutive cases. Ann Surg 238:720–727PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Miyazaki M, Kato A, Ito H et al (2007) Combined vascular resection in operative resection for hilar cholangiocarcinoma: does it work or not? Surgery 141:581–588PubMedCrossRefGoogle Scholar
  38. 38.
    Nagino M, Kamiya J, Arai T et al (2005) One hundred consecutive hepatobiliary resections for biliary hilar malignancy: preoperative blood donation, blood loss, transfusion, and outcome. Surgery 137:148–155PubMedCrossRefGoogle Scholar
  39. 39.
    Jarnagin WR, Gonen M, Fong Y et al (2002) Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg 236:397–406 (discussion 406–407)PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Imamura H, Seyama Y, Kokudo N et al (2003) One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 138:1198–1206 (discussion 1206)PubMedCrossRefGoogle Scholar
  41. 41.
    Rea DJ, Munoz-Juarez M, Farnell MB et al (2004) Major hepatic resection for hilar cholangiocarcinoma: analysis of 46 patients. Arch Surg 139:514–523 discussion 523–525PubMedCrossRefGoogle Scholar
  42. 42.
    Dinant S, Gerhards MF, Rauws EA et al (2006) Improved outcome of resection of hilar cholangiocarcinoma (Klatskin tumor). Ann Surg Oncol 13:872–880PubMedCrossRefGoogle Scholar
  43. 43.
    Shimada K, Sano T, Sakamoto Y et al (2005) Safety and effectiveness of left hepatic trisegmentectomy for hilar cholangiocarcinoma. World J Surg 29:723–727. doi:10.1007/s00268-005-7704-5 PubMedCrossRefGoogle Scholar
  44. 44.
    Nagino M, Kamiya J, Arai T et al (2006) “Anatomic” right hepatic trisectionectomy (extended right hepatectomy) with caudate lobectomy for hilar cholangiocarcinoma. Ann Surg 243:28–32PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Miyazaki M, Ito H, Nakagawa K et al (1999) Parenchyma-preserving hepatectomy in the surgical treatment of hilar cholangiocarcinoma. J Am Coll Surg 189:575–583PubMedCrossRefGoogle Scholar
  46. 46.
    Wakai T, Shirai Y, Moroda T et al (2005) Impact of ductal resection margin status on long-term survival in patients undergoing resection for extrahepatic cholangiocarcinoma. Cancer 103:1210–1216PubMedCrossRefGoogle Scholar
  47. 47.
    Igami T, Nagino M, Oda K et al (2009) Clinicopathologic study of cholangiocarcinoma with superficial spread. Ann Surg 249:296–302PubMedCrossRefGoogle Scholar
  48. 48.
    Higuchi R, Ota T, Araida T et al (2010) Prognostic relevance of ductal margins in operative resection of bile duct cancer. Surgery 148:7–14PubMedCrossRefGoogle Scholar
  49. 49.
    Hemming AW, Reed AI, Fujita S et al (2005) Surgical management of hilar cholangiocarcinoma. Ann Surg 241:693–699 (discussion 699–702)PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Lee SG, Song GW, Hwang S et al (2010) Surgical treatment of hilar cholangiocarcinoma in the new era: the Asan experience. J Hepatobiliary Pancreat Sci 17:476–489PubMedCrossRefGoogle Scholar
  51. 51.
    Cannon RM, Brock G, Buell JF (2012) Surgical resection for hilar cholangiocarcinoma: experience improves resectability. HPB (Oxford) 14:142–149CrossRefGoogle Scholar
  52. 52.
    Nagino M, Ebata T, Yokoyama Y et al (2013) Evolution of surgical treatment for perihilar cholangiocarcinoma: a single-center 34-year review of 574 consecutive resections. Ann Surg 258:129–140PubMedCrossRefGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2013

Authors and Affiliations

  • Norihiko Furusawa
    • 1
  • Akira Kobayashi
    • 1
  • Takahide Yokoyama
    • 1
  • Akira Shimizu
    • 1
  • Hiroaki Motoyama
    • 1
  • Sin-ichi Miyagawa
    • 1
  1. 1.First Department of SurgeryShinshu University School of MedicineMatsumotoJapan

Personalised recommendations