Cholangiographic Tumor Classification for Simple Patient Selection Prior to Hepatopancreatoduodenectomy for Cholangiocarcinoma

  • Yoshitaka Toyoda
  • Tomoki EbataEmail author
  • Takashi Mizuno
  • Yukihiro Yokoyama
  • Tsuyoshi Igami
  • Junpei Yamaguchi
  • Shunsuke Onoe
  • Nobuyuki Watanabe
  • Masato Nagino
Hepatobiliary Tumors



Hepatopancreatoduodenectomy (HPD) is employed for patients with laterally advanced cholangiocarcinoma. However, the survival benefit of this extended approach remains controversial. The aim of this study is to identify a tumor feature benefiting from HPD from the standpoint of long-term survival.

Patients and Methods

Patients with cholangiocarcinoma who underwent HPD with curative intent between 2001 and 2017 were retrospectively analyzed. Tumors were radiologically classified by preoperative cholangiogram. Diffuse type was defined as significant tumor/stricture located from the hilar to intrapancreatic duct; localized type was defined as tumor otherwise. Univariable and multivariable analyses were performed to identify prognostic indicators.


Of 100 study patients, 28 (28%) patients had diffuse tumor type, while the remaining 72 (72%) patients had localized tumors. The former group showed significantly longer lateral length (43 versus 22 mm, P < 0.001) and more frequent pancreatic invasion (50% versus 32%, P = 0.110), advanced T classification (64% versus 49%, P = 0.185), and nodal metastasis (57% versus 47%, P = 0.504), compared with the latter group. The survival for patients with diffuse tumor type was significantly worse than that for patients with localized tumor type, with 5-year survival rates of 59.0% versus 26.3%, respectively (P = 0.003). Multivariable analysis identified four independent factors deteriorating long-term survival: cholangiographic diffuse tumor (P = 0.021), higher age (P = 0.020), percutaneous biliary drainage (P = 0.007), and portal vein resection (P = 0.007).


Presurgical cholangiographic classification, diffuse or localized type, is a tumor-related factor closely associated with survival probability; therefore, it may be a useful feature for patient selection prior to HPD for cholangiocarcinoma.



The authors declare that they have no conflict of interest of this work.

Supplementary material

10434_2019_7457_MOESM1_ESM.tif (100 kb)
Supplemental Fig. 1. Diagram showing the patients who underwent hepatopancreatoduodenectomy for cholangiocarcinoma. HPD, hepatopancreatoduodenectomy; Hx, hepatectomy; PD, pancreatoduodenectomy (TIFF 100 kb)


  1. 1.
    Ebata T, Yokoyama Y, Igami T, et al. Review of hepatopancreatoduodenectomy for biliary cancer: an extended radical approach of Japanese origin. J Hepatobiliary Pancreat Sci. 2014;21:550–5.CrossRefGoogle Scholar
  2. 2.
    Ebata T, Yokoyama Y, Igami T, et al. Hepatopancreatoduodenectomy for cholangiocarcinoma: a single-center review of 85 consecutive patients. Ann Surg. 2012;256:297–305.CrossRefGoogle Scholar
  3. 3.
    Nimura Y, Hayakawa N, Kamiya J, et al. Hepatopancreatoduodenectomy for advanced carcinoma of the biliary tract. Hepatogastroenterology. 1991;38:170–5.Google Scholar
  4. 4.
    Tsukada K, Yoshida K, Aono T, et al. Major hepatectomy and pancreatoduodenectomy for advanced carcinoma of the biliary tract. Br J Surg. 1994;81:108–10.CrossRefGoogle Scholar
  5. 5.
    Ebata T, Nagino M, Nishio H, et al. Right hepatopancreatoduodenectomy: improvements over 23 years to attain acceptability. J Hepatobiliary Pancreat Surg. 2007;14:131–5.CrossRefGoogle Scholar
  6. 6.
    Aoki T, Sakamoto Y, Kohno Y, et al. Hepatopancreaticoduodenectomy for biliary cancer: strategies for near-zero operative mortality and acceptable long-term outcome. Ann Surg. 2018;267:332–7.CrossRefGoogle Scholar
  7. 7.
    Otsubo T, Kobayashi S, Sano K, et al. Safety-related outcomes of the Japanese Society of Hepato-Biliary-Pancreatic Surgery board certification system for expert surgeons. J Hepatobiliary Pancreat Sci. 2017;24:252–61.CrossRefGoogle Scholar
  8. 8.
    Tran TB, Dua MM, Spain DA, et al. Hepato-pancreatectomy: how morbid? Results from the national surgical quality improvement project. HPB (Oxford). 2015;17:763–9.CrossRefGoogle Scholar
  9. 9.
    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;29:17–20.CrossRefGoogle Scholar
  10. 10.
    Kaneoka Y, Yamaguchi A, Isogai M. Hepatopancreatoduodenectomy: its suitability for bile duct cancer versus gallbladder cancer. J Hepatobiliary Pancreat Surg. 2007;14:142–8.CrossRefGoogle Scholar
  11. 11.
    Sakamoto Y, Nara S, Kishi Y, et al. Is extended hemihepatectomy plus pancreaticoduodenectomy justified for advanced bile duct cancer and gallbladder cancer? Surgery. 2013;153:794–800.CrossRefGoogle Scholar
  12. 12.
    Kawashima H, Itoh A, Ohno E, et al. Preoperative endoscopic nasobiliary drainage in 164 consecutive patients with suspected perihilar cholangiocarcinoma: a retrospective study of efficacy and risk factors related to complications. Ann Surg. 2013;257:121–7.CrossRefGoogle Scholar
  13. 13.
    Kawashima H, Itoh A, Ohno E, et al. Diagnostic and prognostic value of immunohistochemical expression of S100P and IMP3 in transpapillary biliary forceps biopsy samples of extrahepatic bile duct carcinoma. J Hepatobiliary Pancreat Sci. 2013;20:441–7.CrossRefGoogle Scholar
  14. 14.
    Edgemen SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.CrossRefGoogle Scholar
  15. 15.
    Ebata T, Nagino M, Kamiya J, et al. Hepatectomy with portal vein resection for hilar cholangiocarcinoma: audit of 52 consecutive cases. Ann Surg. 2003;238:720–7.CrossRefGoogle Scholar
  16. 16.
    Nagino M, Nimura Y, Nishio H, et al. Hepatectomy with simultaneous resection of the portal vein and hepatic artery for advanced perihilar cholangiocarcinoma: an audit of 50 consecutive cases. Ann Surg. 2010;252:115–23.CrossRefGoogle Scholar
  17. 17.
    Ebata T, Mizuno T, Yokoyama Y, et al. Surgical resection for Bismuth type IV perihilar cholangiocarcinoma. Br J Surg. 2018;105:829–38.CrossRefGoogle Scholar
  18. 18.
    Mizuno T, Ebata T, Yokoyama Y, et al. Adjuvant gemcitabine monotherapy for resectable perihilar cholangiocarcinoma with lymph node involvement: a propensity score matching analysis. Surg Today. 2017;47:182–92.CrossRefGoogle Scholar
  19. 19.
    Ebata T, Watanabe H, Ajioka Y, et al. Pathological appraisal of lines of resection for bile duct carcinoma. Br J Surg. 2002;89:1260–7.CrossRefGoogle Scholar
  20. 20.
    Igami T, Nagino M, Oda K, et al. Clinicopathologic study of cholangiocarcinoma with superficial spread. Ann Surg. 2009;249:296–302.CrossRefGoogle Scholar
  21. 21.
    Onoe S, Shimoyama Y, Ebata T, et al. Prognostic delineation of papillary cholangiocarcinoma based on the invasive proportion: a single-institution study with 184 patients. Surgery. 2014;155:280–91.CrossRefGoogle Scholar
  22. 22.
    Sakamoto E, Nimura Y, Hayakawa N, et al. The pattern of infiltration at the proximal border of hilar bile duct carcinoma: a histologic analysis of 62 resected cases. Ann Surg. 1998;227:405–11.CrossRefGoogle Scholar
  23. 23.
    Wakai T, Shirai Y, Moroda T, et al. Impact of ductal resection margin status on long-term survival in patients undergoing resection for extrahepatic cholangiocarcinoma. Cancer. 2005;103:1210–6.CrossRefGoogle Scholar
  24. 24.
    Wakai T, Shirai Y, Tsuchiya Y, et al. Combined major hepatectomy and pancreaticoduodenectomy for locally advanced biliary carcinoma: long-term results. World J Surg. 2008;32:1067–74.CrossRefGoogle Scholar
  25. 25.
    Hirano S, Tanaka E, Tsuchikawa T, et al. Oncological benefit of preoperative endoscopic biliary drainage in patients with hilar cholangiocarcinoma. J Hepatobiliary Pancreat Sci. 2014;21:533–40.CrossRefGoogle Scholar
  26. 26.
    Komaya K, Ebata T, Fukami Y, et al. Percutaneous biliary drainage is oncologically inferior to endoscopic drainage: a propensity score matching analysis in resectable distal cholangiocarcinoma. J Gastroenterol. 2016;51:608–19.CrossRefGoogle Scholar
  27. 27.
    Komaya K, Ebata T, Yokoyama Y, et al. Verification of the oncologic inferiority of percutaneous biliary drainage to endoscopic drainage: a propensity score matching analysis of resectable perihilar cholangiocarcinoma. Surgery. 2017;161:394–404.CrossRefGoogle Scholar
  28. 28.
    Park MS, Kim TK, Kim KW, et al. Differentiation of extrahepatic bile duct cholangiocarcinoma from benign stricture: findings at MRCP versus ERCP. Radiology. 2004;233:234–40.CrossRefGoogle Scholar
  29. 29.
    Masselli G, Gualdi G. Hilar cholangiocarcinoma: MRI/MRCP in staging and treatment planning. Abdom Imaging. 2008;33:444–51.CrossRefGoogle Scholar
  30. 30.
    McGahan JP, Phillips HE, Cox KL. Sonography of the normal pediatric gallbladder and biliary tract. Radiology. 1982;144:873–5.CrossRefGoogle Scholar
  31. 31.
    Khan SA, Davidson BR, Goldin RD, et al. Guidelines for the diagnosis and treatment of cholangiocarcinoma: an update. Gut. 2012;61:1657–69.CrossRefGoogle Scholar
  32. 32.
    Noji T, Kondo S, Hirano S, et al. Computed tomography evaluation of regional lymph node metastases in patients with biliary cancer. Br J Surg. 2008;95:92–6.CrossRefGoogle Scholar
  33. 33.
    Sugiura T, Nishio H, Nagino M, et al. Value of multidetector-row computed tomography in diagnosis of portal vein invasion by perihilar cholangiocarcinoma. World J Surg. 2008;32:1478–84.CrossRefGoogle Scholar
  34. 34.
    Valle J, Wasan H, Palmer DH, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–81.CrossRefGoogle Scholar
  35. 35.
    Bridgewater J, Lopes A, Wasan H, et al. Prognostic factors for progression-free and overall survival in advanced biliary tract cancer. Ann Oncol. 2016;27:134–40.CrossRefGoogle Scholar
  36. 36.
    Nagino M, Ebata T, Yokoyama Y, et al. Evolution of surgical treatment for perihilar cholangiocarcinoma: a single-center 34-year review of 574 consecutive resections. Ann Surg. 2013;258:129–40.CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2019

Authors and Affiliations

  • Yoshitaka Toyoda
    • 1
  • Tomoki Ebata
    • 1
    Email author
  • Takashi Mizuno
    • 1
  • Yukihiro Yokoyama
    • 1
  • Tsuyoshi Igami
    • 1
  • Junpei Yamaguchi
    • 1
  • Shunsuke Onoe
    • 1
  • Nobuyuki Watanabe
    • 1
  • Masato Nagino
    • 1
  1. 1.Division of Surgical Oncology, Department of SurgeryNagoya University Graduate School of MedicineNagoyaJapan

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