Skip to main content
Log in

Safety and Oncological Benefit of Hepatopancreatoduodenectomy for Advanced Extrahepatic Cholangiocarcinoma with Horizontal Tumor Spread: Shinshu University Experience

  • Hepatobiliary Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Although hepatopancreatoduodenectomy (HPD) is the only means of achieving R0 resection of widespread extrahepatic cholangiocarcinoma, its safety and oncological benefit remain controversial because of its inherent high risk of mortality and morbidity.

Objective

The aim of this study was to retrospectively analyze short- and long-term outcomes and evaluate the safety and oncological benefit of this advanced procedure.

Methods

The study cohort comprised 37 consecutive patients who had undergone major HPD. Portal vein embolization was performed before surgery in 20 (54%) patients with future remnant liver volume < 35%.

Results

The median operative time and blood loss were 866 min and 1000 mL, respectively. Concomitant vascular resection was performed in five patients (14%). The overall morbidity and mortality rates were 100% and 5.4% (n = 2), respectively. Nineteen patients (51%) had major (Clavien–Dindo grade III or higher) complications, the most common being intra-abdominal infection (49%) and post-hepatectomy liver failure (46%, grade B/C: 32%/5%), followed by postoperative pancreatic fistula (30%, grade B/C). R0 resection was achieved in 31 patients (84%). The 1-, 3-, and 5-year overall survival (OS) rates were 83%, 48%, and 37%, respectively. In patients with R0 resection, 5-year OS was comparable between patients who had undergone major HPD and major hepatectomy alone (41% vs. 40%, p = non-significant).

Conclusions

HPD is a valid treatment option for extensive cholangiocarcinoma, offering long-term survival benefit at the cost of relatively high but acceptable morbidity and mortality rates. HPD is advocated in selected patients provided that it is considered possible to achieve R0 resection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Klempnauer J, Ridder GJ, Werner M, Weimann A, Pichlmayr R. What constitutes long-term survival after surgery for hilar cholangiocarcinoma? Cancer. 1997;79(1):26–34.

    Article  CAS  PubMed  Google Scholar 

  2. Bartlett DL, Fong Y, Fortner JG, Brennan MF, Blumgart LH. Long-term results after resection for gallbladder cancer. Implications for staging and management. Ann Surg. 1996;224(5):639–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 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(1):84–92.

    PubMed  PubMed Central  Google Scholar 

  4. Takasaki K, Kobayashi S, Mutoh H, et al. Our experiences (5 cases) of extended right lobectomy combined with pancreato-duodenectony for the carcinoma of the gallbladder [in Japanese]. Tan to Sui. 1980;1(7):923–32.

    Google Scholar 

  5. Nimura Y, Hayakawa N, Kamiya J, et al. Hepatopancreatoduodenectomy for advanced carcinoma of the biliary tract. Hepatogastroenterology. 1991;38(2):170–75.

    CAS  PubMed  Google Scholar 

  6. Nakamura S, Nishiyama R, Yokoi Y, et al. Hepatopancreatoduodenectomy for advanced gallbladder carcinoma. Arch Surg. 1994;129(6):625–29.

    Article  CAS  PubMed  Google Scholar 

  7. Tsukada K, Yoshida K, Aono T, et al. Major hepatectomy and pancreatoduodenectomy for advanced carcinoma of the biliary tract. Br J Surg. 1994;81(1):108–10.

    Article  CAS  PubMed  Google Scholar 

  8. Shirai Y, Ohtani T, Tsukada K, Hatakeyama K. Combined pancreaticoduodenectomy and hepatectomy for patients with locally advanced gallbladder carcinoma: long term results. Cancer. 1997;80(10):1904–909.

    Article  CAS  PubMed  Google Scholar 

  9. Ota T, Araida T, Yamamoto M, Takasaki K. Operative outcome and problems of right hepatic lobectomy with pancreatoduodenectomy for advanced carcinoma of the biliary tract. J Hepatobiliary Pancreat Surg. 2007;14(2):155–58.

    Article  PubMed  Google Scholar 

  10. D’Angelica M, Martin RC 2nd, Jarnagin WR, Fong Y, DeMatteo RP, Blumgart LH. Major hepatectomy with simultaneous pancreatectomy for advanced hepatobiliary cancer. J Am Coll Surg. 2004;198(4):570–76.

    Article  PubMed  Google Scholar 

  11. Wakai T, Shirai Y, Tsuchiya Y, Nomura T, Akazawa K, Hatakeyama K. Combined major hepatectomy and pancreaticoduodenectomy for locally advanced biliary carcinoma: long-term results. World J Surg. 2008;32(6):1067–1074.

    Article  PubMed  Google Scholar 

  12. Fernandes Ede S, Mello FT, Ribeiro-Filho J, et al. The Largest Western Experience with Hepatopancreatoduodenectomy: Lessons Learned with 35 Cases. Arq Bras Cir Dig. 2016;29(1):17–20.

    Article  PubMed  Google Scholar 

  13. Dai WC, Chok KS, Cheung TT, Chan AC, Chan SC, Lo CM. Hepatopancreatoduodenectomy for advanced hepatobiliary malignancies: a single-center experience. Hepatobiliary Pancreat Dis Int. 2017;16(4):382–86.

    Article  PubMed  Google Scholar 

  14. Kawasaki S, Makuuchi M, Miyagawa S, Kakazu T. Radical operation after portal embolization for tumor of hilar bile duct. J Am Coll Surg. 1994;178(5):480–86.

    CAS  PubMed  Google Scholar 

  15. Miyagawa S, Makuuchi M, Kawasaki S, et al. Outcome of major hepatectomy with pancreatoduodenectomy for advanced biliary malignancies. World J Surg. 1996;20(1):77–80.

    Article  CAS  PubMed  Google Scholar 

  16. Makuuchi M, Thai BL, Takayasu K, et al. Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery. 1990;107(5):521–27.

    CAS  PubMed  Google Scholar 

  17. Miwa S, Kobayashi A, Akahane Y, et al. Is major hepatectomy with pancreatoduodenectomy justified for advanced biliary malignancy? J Hepatobiliary Pancreat Surg. 2007;14(2):136–41.

    Article  PubMed  Google Scholar 

  18. Imamura H, Seyama Y, Kokudo N, et al. One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg. 2003;138(11):1198–206; discussion 1206.

    Article  PubMed  Google Scholar 

  19. Miyagawa S, Makuuchi M, Lygidakis NJ, et al. A retrospective comparative study of reconstructive methods following pancreaticoduodenectomy: pancreaticojejunostomy vs. pancreaticogastrostomy. Hepatogastroenterology 1992;39(5):381–84.

    CAS  PubMed  Google Scholar 

  20. Miyagawa S, Makuuchi M, Kawasaki S, Ogiwara M. Second-stage pancreatojejunostomy following pancreatoduodenectomy in high-risk patients. Am J Surg. 1994;168(1):66–68.

    Article  CAS  PubMed  Google Scholar 

  21. Fukami Y, Kaneoka Y, Maeda A, Takayama Y, Onoe S. Major hepatopancreatoduodenectomy with simultaneous resection of the hepatic artery for advanced biliary cancer. Langenbecks Arch Surg. 2016;401(4):471–78.

    Article  PubMed  Google Scholar 

  22. Akashi K, Ebata T, Mizuno T, et al. Surgery for perihilar cholangiocarcinoma from a viewpoint of age: Is it beneficial to octogenarians in an aging society? Surgery. 2018;164(5):1023–1029.

    Article  PubMed  Google Scholar 

  23. Nakanishi Y, Okamura K, Tsuchikawa T, et al. Time to recurrence after surgical resection and survival after recurrence among patients with perihilar and distal cholangiocarcinomas. Ann Surg Oncol. 2020;27(11):4171–180.

    Article  PubMed  Google Scholar 

  24. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti AI (eds). AJCC cancer staging manual, 7th Edition. New York, NY: Springer; 2010.

    Google Scholar 

  25. Rahbari NN, Garden OJ, Padbury R, et al. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery. 2011;149(5):713–24.

    Article  PubMed  Google Scholar 

  26. Koch M, Garden OJ, Padbury R, et al. Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery. 2011;149(5):680–88.

    Article  PubMed  Google Scholar 

  27. Bassi C, Marchegiani G, Dervenis C, et al. The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery. 2017;161(3):584–91.

    Article  PubMed  Google Scholar 

  28. Yokoyama Y, Ebata T, Igami T, et al. The predictive value of indocyanine green clearance in future liver remnant for posthepatectomy liver failure following hepatectomy with extrahepatic bile duct resection. World J Surg. 2016;40(6):1440–447.

    Article  PubMed  Google Scholar 

  29. Nagino M, Kamiya J, Nishio H, Ebata T, Arai T, Nimura Y. Two hundred forty consecutive portal vein embolizations before extended hepatectomy for biliary cancer: surgical outcome and long-term follow-up. Ann Surg. 2006;243(3):364–72.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205–213.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kaneoka Y, Yamaguchi A, Isogai M. Hepatopancreatoduodenectomy: its suitability for bile duct cancer versus gallbladder cancer. J Hepatobiliary Pancreat Surg. 2007;14(2):142–48.

    Article  PubMed  Google Scholar 

  32. Kaneoka Y, Yamaguchi A, Isogai M, Kumada T. Survival benefit of hepatopancreatoduodenectomy for cholangiocarcinoma in comparison to hepatectomy or pancreatoduodenectomy. World J Surg. 2010;34(11):2662–670.

    Article  PubMed  Google Scholar 

  33. Hochwald SN, Burke EC, Jarnagin WR, Fong Y, Blumgart LH. Association of preoperative biliary stenting with increased postoperative infectious complications in proximal cholangiocarcinoma. Arch Surg. 1999;134(3):261–66.

    Article  CAS  PubMed  Google Scholar 

  34. Ferrero A, Lo Tesoriere R, Vigano L, Caggiano L, Sgotto E, Capussotti L. Preoperative biliary drainage increases infectious complications after hepatectomy for proximal bile duct tumor obstruction. World J Surg. 2009;33(2):318–25.

    Article  PubMed  Google Scholar 

  35. Sugawara G, Ebata T, Yokoyama Y, et al. The effect of preoperative biliary drainage on infectious complications after hepatobiliary resection with cholangiojejunostomy. Surgery. 2013;153(2):200–210.

    Article  PubMed  Google Scholar 

  36. Longbotham D, Young A, Nana G, et al. The impact of age on post-operative liver function following right hepatectomy: a retrospective, single centre experience. HPB (Oxford). 2020;22(1):151–160.

    Article  Google Scholar 

  37. Mathur AK, Ghaferi AA, Osborne NH, et al. Body mass index and adverse perioperative outcomes following hepatic resection. J Gastrointest Surg. 2010;14(8):1285–291.

    Article  PubMed  PubMed Central  Google Scholar 

  38. El Nakeeb A, Hamed H, Shehta A, et al. Impact of obesity on surgical outcomes post-pancreaticoduodenectomy: a case-control study. Int J Surg. 2014;12(5):488–93.

    Article  PubMed  Google Scholar 

  39. Global Health Observatory data repository | by category. Mean body mass index trends among adults, crude (kg/m2)—Estimates by WHO region. Geneva: World Health Organization. Available at: https://apps.who.int/gho/data/view.main.BMIMEANADULTCREGv?lang=en Accessed 19 Jun 2020.

  40. Hemming AW, Magliocca JF, Fujita S, et al. Combined resection of the liver and pancreas for malignancy. J Am Coll Surg. 2010;210(5):808–14, 814–6.

  41. Ebata T, Yokoyama Y, Igami T, et al. Hepatopancreatoduodenectomy for cholangiocarcinoma: a single-center review of 85 consecutive patients. Ann Surg. 2012;256(2):297–305.

    Article  PubMed  Google Scholar 

  42. Lim CS, Jang JY, Lee SE, Kang MJ, Kim SW. Reappraisal of hepatopancreatoduodenectomy as a treatment modality for bile duct and gallbladder cancer. J Gastrointest Surg. 2012;16(5):1012–1018.

    Article  PubMed  Google Scholar 

  43. Sakamoto Y, Nara S, Kishi Y, et al. Is extended hemihepatectomy plus pancreaticoduodenectomy justified for advanced bile duct cancer and gallbladder cancer? Surgery. 2013;153(6):794–800.

    Article  PubMed  Google Scholar 

  44. D’Souza MA, Valdimarsson VT, Campagnaro T, et al. Hepatopancreatoduodenectomy: a controversial treatment for bile duct and gallbladder cancer from a European perspective. HPB (Oxford). 2020;22(9):1339–1348.

    Article  Google Scholar 

Download references

Acknowledgment

The authors thank Rebecca Tollefson, DVM, from Edanz Group (https://en-author-services.edanzgroup.com/) for editing a draft of this manuscript.

Funding

No funding was received specifically for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Shimizu MD, PhD.

Ethics declarations

Disclosures

Akira Shimizu, Hiroaki Motoyama, Koji Kubota, Tsuyoshi Notake, Kentaro Fukushima, Tomohiko Ikehara, Hikaru Hayashi, Koya Yasukawa, Akira Kobayashi, and Yuji Soejima have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shimizu, A., Motoyama, H., Kubota, K. et al. Safety and Oncological Benefit of Hepatopancreatoduodenectomy for Advanced Extrahepatic Cholangiocarcinoma with Horizontal Tumor Spread: Shinshu University Experience. Ann Surg Oncol 28, 2012–2025 (2021). https://doi.org/10.1245/s10434-020-09209-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-020-09209-8

Navigation