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Transhepatic Direct Approach to the “Limit of the Division of the Hepatic Ducts” Leads to a High R0 Resection Rate in Perihilar Cholangiocarcinoma

  • Original Article
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Journal of Gastrointestinal Surgery

Abstract

Background

Previous studies have shown that curative resection (R0 resection) was among the most crucial factors for the long-term survival of patients with PHCC. To achieve R0 resection, we performed the transhepatic direct approach and resection on the limits of division of the hepatic ducts. Although a recent report showed that the resection margin (RM) status impacted PHCC patients’ survival, it is still unclear whether RM is an important clinical factor.

Objective

To describe a technique of transhepatic direct approach and resection on the limit of division of hepatic ducts, investigate its short-term surgical outcome, and validate whether the radial margin (RM) would have a clinical impact on long-term survival of perihilar cholangiocarcinoma (PHCC) patients.

Methods

Consecutive PHCC patients (n = 211) who had undergone major hepatectomy with extrahepatic bile duct resection, without pancreaticoduodenectomy, in our department were retrospectively evaluated.

Results

R0 resection rate was 92% and 86% for invasive cancer-free and both invasive cancer-free and high-grade dysplasia-free resection, respectively. Overall 5-year survival rate was 46.9%. Univariate analysis showed that preoperative serum carcinoembryonic antigen level (> 7.0 mg/dl), pathological lymph node metastasis, and portal vein invasion were independent risk factors, but R status on both resection margin and bile duct margin was not an independent risk factor for survival.

Conclusion

The transhepatic direct approach to the limits of division of the bile ducts leads to the highest R0 resection rate in the horizontal margin of PHCC. Further examination will be needed to determine the adjuvant therapy for PHCC to improve patient survival.

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References

  1. Kondo S, Hirano S, Ambo Y, Tanaka E, Okushiba S, Morikawa T et al. Forty consecutive resections of hilar cholangiocarcinoma with no postoperative mortality and no positive ductal margins: results of a prospective study. Ann Surg. 2004;240(1):95-101.

    Article  Google Scholar 

  2. Shinohara K, Ebata T, Shimoyama Y, Mizuno T, Yokoyama Y, Yamaguchi J et al. A Study on Radial Margin Status in Resected Perihilar Cholangiocarcinoma. Ann Surg. 2019. doi:https://doi.org/10.1097/SLA.0000000000003305.

  3. Lee SG, Song GW, Hwang S, Ha TY, Moon DB, Jung DH et al. Surgical treatment of hilar cholangiocarcinoma in the new era: the Asan experience. J Hepatobiliary Pancreat Sci. 2010;17(4):476-89. doi:https://doi.org/10.1007/s00534-009-0204-5.

    Article  PubMed  Google Scholar 

  4. Shimizu H, Kimura F, Yoshidome H, Ohtsuka M, Kato A, Yoshitomi H et al. Aggressive surgical resection for hilar cholangiocarcinoma of the left-side predominance: radicality and safety of left-sided hepatectomy. Ann Surg. 2010;251(2):281-6. doi:https://doi.org/10.1097/SLA.0b013e3181be0085.

    Article  PubMed  Google Scholar 

  5. Matsuo K, Rocha FG, Ito K, D'Angelica MI, Allen PJ, Fong Y et al. The Blumgart preoperative staging system for hilar cholangiocarcinoma: analysis of resectability and outcomes in 380 patients. J Am Coll Surg. 2012;215(3):343-55. doi:https://doi.org/10.1016/j.jamcollsurg.2012.05.025.

    Article  PubMed  Google Scholar 

  6. Cheng QB, Yi B, Wang JH, Jiang XQ, Luo XJ, Liu C et al. Resection with total caudate lobectomy confers survival benefit in hilar cholangiocarcinoma of Bismuth type III and IV. Eur J Surg Oncol. 2012;38(12):1197-203. doi:https://doi.org/10.1016/j.ejso.2012.08.009.

    Article  PubMed  Google Scholar 

  7. Song SC, Choi DW, Kow AW, Choi SH, Heo JS, Kim WS et al. Surgical outcomes of 230 resected hilar cholangiocarcinoma in a single centre. ANZ J Surg. 2013;83(4):268-74. doi:https://doi.org/10.1111/j.1445-2197.2012.06195.x.

    Article  PubMed  Google Scholar 

  8. Furusawa N, Kobayashi A, Yokoyama T, Shimizu A, Motoyama H, Miyagawa S. Surgical treatment of 144 cases of hilar cholangiocarcinoma without liver-related mortality. World J Surg. 2014;38(5):1164-76. doi:https://doi.org/10.1007/s00268-013-2394-x.

    Article  PubMed  Google Scholar 

  9. Higuchi R, Yazawa T, Uemura S, Izumo W, Ota T, Kiyohara K et al. Surgical Outcomes for Perihilar Cholangiocarcinoma with Vascular Invasion. J Gastrointest Surg. 2019;23(7):1443-53. doi:https://doi.org/10.1007/s11605-018-3948-x.

    Article  PubMed  Google Scholar 

  10. Matsuyama R, Morioka D, Mori R, Yabushita Y, Hiratani S, Ota Y et al. Our Rationale of Initiating Neoadjuvant Chemotherapy for Hilar Cholangiocarcinoma: A Proposal of Criteria for "Borderline Resectable" in the Field of Surgery for Hilar Cholangiocarcinoma. World J Surg. 2019;43(4):1094-104. doi:https://doi.org/10.1007/s00268-018-04883-y.

    Article  PubMed  Google Scholar 

  11. Olthof PB, Miyasaka M, Koerkamp BG, Wiggers JK, Jarnagin WR, Noji T et al. A comparison of treatment and outcomes of perihilar cholangiocarcinoma between Eastern and Western centers. HPB (Oxford). 2019;21(3):345-51. doi:https://doi.org/10.1016/j.hpb.2018.07.014.

    Article  PubMed  Google Scholar 

  12. Tran TB, Ethun CG, Pawlik TM, Schmidt C, Beal EW, Fields RC et al. Actual 5-Year Survivors After Surgical Resection of Hilar Cholangiocarcinoma. Ann Surg Oncol. 2019;26(2):611-8. doi:https://doi.org/10.1245/s10434-018-7075-4.

    Article  PubMed  Google Scholar 

  13. Hirano S, Tanaka E, Shichinohe T, Suzuki O, Hazama K, Kitagami H et al. Treatment strategy for hilar cholangiocarcinoma, with special reference to the limits of ductal resection in right-sided hepatectomies. J Hepatobiliary Pancreat Surg. 2007;14(5):429-33. doi:https://doi.org/10.1007/s00534-006-1190-5.

    Article  PubMed  Google Scholar 

  14. De Lu C, Huang J, Wu SD, Hua YF, Javed AA, Fang JZ et al. Total Hilar En Bloc Resection with Left Hemihepatectomy and Caudate Lobectomy: a Novel Approach for Treatment of Left-Sided Perihilar Cholangiocarcinoma (with Video). J Gastrointest Surg. 2017;21(11):1906-14. doi:https://doi.org/10.1007/s11605-017-3561-4.

    Article  PubMed  Google Scholar 

  15. Kamachi H, Kamiyama T, Tsuruga Y, Orimo T, Wakayama K, Shimada S et al. Transparenchymal glissonean approach: a novel surgical technique for advanced perihilar bile duct cancer. Langenbecks Arch Surg. 2018;403(3):387-94. doi:https://doi.org/10.1007/s00423-017-1633-2.

    Article  PubMed  Google Scholar 

  16. Kuriyama N, Isaji S, Tanemura A, Iizawa Y, Kato H, Murata Y et al. Transhepatic Hilar Approach for Perihilar Cholangiocarcinoma: Significance of Early Judgment of Resectability and Safe Vascular Reconstruction. J Gastrointest Surg. 2017;21(3):590-9. doi:https://doi.org/10.1007/s11605-016-3332-7.

    Article  PubMed  Google Scholar 

  17. Nagino M, Kamiya J, Arai T, Nishio H, Ebata T, Nimura Y. "Anatomic" right hepatic trisectionectomy (extended right hepatectomy) with caudate lobectomy for hilar cholangiocarcinoma. Ann Surg. 2006;243(1):28-32. doi:https://doi.org/10.1097/01.sla.0000193604.72436.63.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Uesaka K. Left hepatectomy or left trisectionectomy with resection of the caudate lobe and extrahepatic bile duct for hilar cholangiocarcinoma (with video). J Hepatobiliary Pancreat Sci. 2012;19(3):195-202. doi:https://doi.org/10.1007/s00534-011-0474-6.

    Article  PubMed  Google Scholar 

  19. Govil S, Reddy MS, Rela M. Surgical resection techniques for locally advanced hilar cholangiocarcinoma. Langenbecks Arch Surg. 2014;399(6):707-16. doi:https://doi.org/10.1007/s00423-014-1216-4.

    Article  PubMed  Google Scholar 

  20. Noji T, Okamura K, Tanaka K, Nakanishi Y, Asano T, Nakamura T et al. Surgical technique and results of intrapancreatic bile duct resection for hilar malignancy (with video). HPB (Oxford). 2018;20(12):1145-9. doi:https://doi.org/10.1016/j.hpb.2018.05.010.

    Article  PubMed  Google Scholar 

  21. Nakanishi Y, Tsuchikawa T, Okamura K, Nakamura T, Tamoto E, Murakami S et al. Prognostic impact of the site of portal vein invasion in patients with surgically resected perihilar cholangiocarcinoma. Surgery. 2016;159(6):1511-9. doi:https://doi.org/10.1016/j.surg.2016.01.012.

    Article  PubMed  Google Scholar 

  22. Noji T, Tsuchikawa T, Okamura K, Tanaka K, Nakanishi Y, Asano T et al. Concomitant hepatic artery resection for advanced perihilar cholangiocarcinoma: a case-control study with propensity score matching. J Hepatobiliary Pancreat Sci. 2016;23(7):442-8. doi:https://doi.org/10.1002/jhbp.363.

    Article  PubMed  Google Scholar 

  23. Kawamura T, Noji T, Okamura K, Tanaka K, Nakanishi Y, Asano T et al. Postoperative Liver Failure Criteria for Predicting Mortality after Major Hepatectomy with Extrahepatic Bile Duct Resection. Dig Surg. 2019;36(2):158-65. doi:https://doi.org/10.1159/000486906.

    Article  CAS  PubMed  Google Scholar 

  24. Hirano S, Kondo S, Tanaka E, Shichinohe T, Tsuchikawa T, Kato K et al. Outcome of surgical treatment of hilar cholangiocarcinoma: a special reference to postoperative morbidity and mortality. J Hepatobiliary Pancreat Sci. 2010;17(4):455-62. doi:https://doi.org/10.1007/s00534-009-0208-1.

    Article  PubMed  Google Scholar 

  25. Kawakami H, Kuwatani M, Onodera M, Haba S, Eto K, Ehira N et al. Endoscopic nasobiliary drainage is the most suitable preoperative biliary drainage method in the management of patients with hilar cholangiocarcinoma. J Gastroenterol. 2011;46(2):242-8. doi:https://doi.org/10.1007/s00535-010-0298-1.

    Article  PubMed  Google Scholar 

  26. Yokoyama Y, Nishio H, Ebata T, Igami T, Sugawara G, Nagino M. Value of indocyanine green clearance of the future liver remnant in predicting outcome after resection for biliary cancer. Br J Surg. 2010;97(8):1260-8. doi:https://doi.org/10.1002/bjs.7084.

    Article  CAS  PubMed  Google Scholar 

  27. 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(6):1052-7. doi:https://doi.org/10.1097/SLA.0b013e318142d97e.

    Article  PubMed  Google Scholar 

  28. Ebata T, Mizuno T, Yokoyama Y, Igami T, Sugawara G, Nagino M. Surgical resection for Bismuth type IV perihilar cholangiocarcinoma. Br J Surg. 2017. doi:https://doi.org/10.1002/bjs.10556.

  29. Noji T, Hirano S. Surgical indication and procedure for perihilar cholangiocarcinoma with Bismuth type III or IV. Geka. 2017;79(8):714-9.

    Google Scholar 

  30. Natsume S, Ebata T, Yokoyama Y, Igami T, Sugawara G, Shimoyama Y et al. Clinical significance of left trisectionectomy for perihilar cholangiocarcinoma: an appraisal and comparison with left hepatectomy. Ann Surg. 2012;255(4):754-62. doi:https://doi.org/10.1097/SLA.0b013e31824a8d82.

    Article  PubMed  Google Scholar 

  31. Clavien PA, Strasberg SM. Severity grading of surgical complications. Ann Surg. 2009;250(2):197-8. doi:https://doi.org/10.1097/SLA.0b013e3181b6dcab.

    Article  PubMed  Google Scholar 

  32. Primrose JN, Fox RP, Palmer DH, Malik HZ, Prasad R, Mirza D et al. Capecitabine compared with observation in resected biliary tract cancer (BILCAP): a randomised, controlled, multicentre, phase 3 study. Lancet Oncol. 2019;20(5):663-73. doi:https://doi.org/10.1016/s1470-2045(18)30915-x.

    Article  CAS  PubMed  Google Scholar 

  33. Ebata T, Hirano S, Konishi M, Uesaka K, Tsuchiya Y, Ohtsuka M et al. Randomized clinical trial of adjuvant gemcitabine chemotherapy versus observation in resected bile duct cancer. Br J Surg. 2018;105(3):192-202. doi:https://doi.org/10.1002/bjs.10776.

    Article  CAS  PubMed  Google Scholar 

  34. Saito H, Noji T, Okamura K, Tsuchikawa T, Shichinohe T, Hirano S. A new prognostic scoring system using factors available preoperatively to predict survival after operative resection of perihilar cholangiocarcinoma. Surgery. 2016;159(3):842-51. doi:https://doi.org/10.1016/j.surg.2015.10.027.

    Article  PubMed  Google Scholar 

  35. Ferrone CR, Marchegiani G, Hong TS, Ryan DP, Deshpande V, McDonnell EI et al. Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann Surg. 2015;261(1):12-7. doi:https://doi.org/10.1097/SLA.0000000000000867.

    Article  PubMed  Google Scholar 

  36. Khushman M, Dempsey N, Maldonado JC, Loaiza-Bonilla A, Velez M, Carcas L et al. Full dose neoadjuvant FOLFIRINOX is associated with prolonged survival in patients with locally advanced pancreatic adenocarcinoma. Pancreatology. 2015;15(6):667-73. doi:https://doi.org/10.1016/j.pan.2015.08.010.

    Article  CAS  PubMed  Google Scholar 

  37. Noji T, Kondo S, Hirano S, Tanaka E, Ambo Y, Kawarada Y et al. CT evaluation of paraaortic lymph node metastasis in patients with biliary cancer. J Gastroenterol. 2005;40(7):739-43. doi:https://doi.org/10.1007/s00535-005-1618-8.

    Article  PubMed  Google Scholar 

  38. Noji T, Kondo S, Hirano S, Tanaka E, Suzuki O, Shichinohe T. Computed tomography evaluation of regional lymph node metastases in patients with biliary cancer. Br J Surg. 2008;95(1):92-6. doi:https://doi.org/10.1002/bjs.5920.

    Article  CAS  PubMed  Google Scholar 

  39. Kobayashi S, Nagano H, Hoshino H, Wada H, Marubashi S, Eguchi H et al. Diagnostic value of FDG-PET for lymph node metastasis and outcome of surgery for biliary cancer. J Surg Oncol. 2011;103(3):223-9. doi:https://doi.org/10.1002/jso.21811.

    Article  PubMed  Google Scholar 

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Correspondence to Takehiro Noji.

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Noji, T., Tanaka, K., Matsui, A. et al. Transhepatic Direct Approach to the “Limit of the Division of the Hepatic Ducts” Leads to a High R0 Resection Rate in Perihilar Cholangiocarcinoma. J Gastrointest Surg 25, 2358–2367 (2021). https://doi.org/10.1007/s11605-020-04891-1

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