Albumin–Indocyanine Green Evaluation (ALICE) grade predicts bile leakage after hepatic resection

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We investigated the predictors of bile leakage after hepatic resection.


The data of 270 consecutive patients who underwent curative hepatic resection in our institute between January, 2016 and April, 2019 were reviewed retrospectively. The patients were assigned to one of two groups according to the presence of bile leakage and the clinicopathological and surgical outcomes were analyzed. Bile leakage was defined by the International Study Group of Liver Surgery (ISGLS) grade.


There were no hospital deaths. The median intraoperative blood loss volume was 167 ml. Bile leakage occurred in 12 patients (4.4%), as ISGLS grade A leakage in 1 and as ISGLS grade B leakage in 11. The mean hospital stay was significantly longer for patients with bile leakage. High-risk procedures, hepatocellular carcinoma, and Albumin–Indocyanine Green Evaluation (ALICE) grade 3 were independent predictors of ISGLS grade B or C postoperative bile leakage. In patients with three high-risk factors, the incidence of bile leakage was 53.9%.


Based on this retrospective analysis, high-risk procedures, hepatocellular carcinoma, and ALICE grade 3 were independent predictors of bile leakage in patients undergoing hepatic resection. Thus, special care must be taken during surgery to prevent bile leakage in patients with these risk factors.

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  1. 1.

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

  2. 2.

    Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Tahara M, Yamashita K, et al. Perioperative management of hepatic resection toward zero mortality and morbidity: analysis of 793 consecutive cases in a single institution. J Am Coll Surg. 2010;211(4):443–9.

  3. 3.

    Fan ST, Lo CM, Liu CL, Lam CM, Yuen WK, Yeung C, et al. Hepatectomy for hepatocellular carcinoma: toward zero hospital deaths. Ann Surg. 1999;229(3):322–30.

  4. 4.

    Taketomi A, Kitagawa D, Itoh S, Harimoto N, Yamashita Y, Gion T, et al. Trends in morbidity and mortality after hepatic resection for hepatocellular carcinoma: an institute's experience with 625 patients. J Am Coll Surg. 2007;204(4):580–7.

  5. 5.

    Harimoto N, Shirabe K, Ikegami T, Yoshizumi T, Maeda T, Kajiyama K, et al. Postoperative complications are predictive of poor prognosis in hepatocellular carcinoma. J Surg Res. 2015;199(2):470–7.

  6. 6.

    Harimoto N, Hoshino H, Muranushi R, Hagiwara K, Yamanaka T, Ishii N, et al. Skeletal muscle volume and intramuscular adipose tissue are prognostic predictors of postoperative complications after hepatic resection. Anticancer Res. 2018;38(8):4933–9.

  7. 7.

    Kokudo T, Hasegawa K, Amikura K, Uldry E, Shirata C, Yamaguchi T, et al. Assessment of Preoperative Liver Function in Patients with Hepatocellular Carcinoma - The Albumin-Indocyanine Green Evaluation (ALICE) Grade. PLoS ONE. 2016;11(7):e0159530.

  8. 8.

    Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, 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):680–8.

  9. 9.

    Johnson PJ, Berhane S, Kagebayashi C, Satomura S, Teng M, Reeves HL, et al. Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J Clin Oncol. 2015;33(6):550–8.

  10. 10.

    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):205–13.

  11. 11.

    Araki K, Harimoto N, Kubo N, Watanabe A, Igarashi T, Tsukagoshi M, et al. Functional liver volumetry using Gd-EOB-DTPA-enhanced magnetic resonance imaging (MRI) predicts post-hepatectomy liver failure in resection of more than one segment. HPB. 2019;S1365(19):20687–92.

  12. 12.

    Rahbari NN, Koch M, Mehabi A, Weidmann K, Motschall E, Kahlert C, et al. Portal triad clamping versus vascular exclusion for vascular control during hepatic resection: a systematic review and meta-analysis. J Gastrointest Surg. 2009;13:558–68.

  13. 13.

    Ishii H, Ochiai T, Murayama Y, Komatsu S, Shiozaki A, Kuriu Y, et al. Risk factors and management of postoperative bile leakage after hepatectomy without bilioenteric anastomosis. Dig Surg. 2011;28(3):198–204.

  14. 14.

    Sadamori H, Yagi T, Shinoura S, Umeda Y, Yoshida R, Satoh D, et al. Risk factors for major morbidity after liver resection for hepatocellular carcinoma. Br J Surg. 2013;100(1):122–9.

  15. 15.

    Nakagawa K, Tanaka K, Nojiri K, Sawada Y, Kumamoto T, Ueda M, et al. Predictive factors for bile leakage after hepatectomy for hepatic tumors: a retrospective multicenter study with 631 cases at Yokohama Clinical Oncology Group (YCOG). J Hepatobiliary Pancreat Sci. 2017;24(1):33–41.

  16. 16.

    Yamashita Y, Hamatsu T, Rikimaru T, Tanaka S, Shirabe K, Shimada M, et al. Bile leakage after hepatic resection. Ann Surg. 2001;233(1):45–50.

  17. 17.

    Panaro F, Hacina L, Bouyabrine H, Al-Hashmi AW, Herrero A, Navarro F. Risk factors for postoperative bile leakage: a retrospective single-center analysis of 411 hepatectomies. Hepatobiliary Pancreat Dis Int. 2016;15(1):81–6.

  18. 18.

    Nakano R, Ohira M, Kobayashi T, Imaoka Y, Mashima H, Yamaguchi M, et al. Independent risk factors that predict bile leakage after hepatectomy for hepatocellular carcinoma: Cohort study. Int J Surg. 2018;57:1–7.

  19. 19.

    Russolillo N, Forchino F, Conci S, Mele C, Langella S, Ruzzenente A, et al. Validation of the albumin-indocyanine green evaluation model in patients with resected hepatocellular carcinoma and comparison with the albumin-bilirubin score. J Hepatobiliary Pancreat Sci. 2019;26(1):51–7.

  20. 20.

    Miyazaki Y, Kokudo T, Amikura K, Takahashi A, Ohkohchi N, Sakamoto H. Albumin-indocyanine green evaluation grading system predicts post-hepatectomy liver failure for biliary tract cancer. Dig Surg. 2019;36(1):13–9.

  21. 21.

    Honmyo N, Kobayashi T, Hamaoka M, Kohashi T, Abe T, Oishi K, et al. Comparison of new prognostic systems for patients with resectable hepatocellular carcinoma: Albumin–Bilirubin grade and Albumin-Indocyanine Green Evaluation grade. Hepatol Res. 2019;49(10):1218–26.

  22. 22.

    Shirata C, Kokudo T, Arita J, Akamatsu N, Kaneko J, Sakamoto Y, et al. Albumin-Indocyanine Green Evaluation (ALICE) grade combined with portal hypertension to predict post-hepatectomy liver failure. Hepatol Res. 2019;49(8):942–9.

  23. 23.

    Strücker B, Stockmann M, Denecke T, Neuhaus P, Seehofer D. Intraoperative placement of external biliary drains for prevention and treatment of bile leaks after extended liver resection without bilioenteric anastomosis. World J Surg. 2013;37(11):2629–34.

  24. 24.

    Nanashima A, Abo T, Shibuya A, Tominaga T, Matsumoto A, Tou K, et al. Does the placement of a cystic duct tube after a hepatic resection help reduce the incidence of post-operative bile leak? HPB (Oxford). 2013;15(7):517–22.

  25. 25.

    Ishii T, Hatano E, Furuyama H, Manaka D, Terajima H, Uemoto S. Preventive measures for postoperative bile leakage after central hepatectomy: a multicenter, prospective, observational study of 101 patients. World J Surg. 2016;40(7):1720–8.

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Correspondence to Norifumi Harimoto.

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Harimoto, N., Muranushi, R., Hoshino, K. et al. Albumin–Indocyanine Green Evaluation (ALICE) grade predicts bile leakage after hepatic resection. Surg Today (2020).

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  • Bile leakage
  • Hepatic resection
  • Liver function
  • ALICE grade