Advertisement

Prospective validation of the Eastern Staging in predicting survival after surgical resection for patients with hepatocellular carcinoma: a multicenter study from China

  • Shun-Chao Yang
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China

    Graduate School, Hebei North University, Hebei, China
    Search for articles by this author
  • Lei Liang
    Affiliations
    Department of General Surgery, Cancer Center, Division of Hepatobiliary and Pancreatic Surgery, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, Hangzhou, Zhejiang, China
    Search for articles by this author
  • Ming-Da Wang
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China
    Search for articles by this author
  • Xian-Ming Wang
    Affiliations
    Department of General Surgery, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong, China
    Search for articles by this author
  • Li-Hui Gu
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China
    Search for articles by this author
  • Kong-Ying Lin
    Affiliations
    Department of Hepatobiliary Surgery, Mengchao Hepatobiliary Hospital, Fujian Medical University, Fujian, China
    Search for articles by this author
  • Ya-Hao Zhou
    Affiliations
    Department of Hepatobiliary Surgery, Pu'er People's Hospital, Yunnan, China
    Search for articles by this author
  • Ting-Hao Chen
    Affiliations
    Department of General Surgery, Ziyang First People's Hospital, Sichuan, China
    Search for articles by this author
  • Wei-Min Gu
    Affiliations
    The First Department of General Surgery, The Fourth Hospital of Harbin, Heilongjiang, China
    Search for articles by this author
  • Jie Li
    Affiliations
    Department of Hepatobiliary Surgery, Fuyang People's Hospital, Anhui, China
    Search for articles by this author
  • Hong Wang
    Affiliations
    Department of General Surgery, Liuyang People's Hospital, Hunan, China
    Search for articles by this author
  • Zhong Chen
    Affiliations
    Department of Hepatobiliary Surgery, Affiliated Hospital of Nantong University, Nantong, Jiangsu, China
    Search for articles by this author
  • Chao Li
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China
    Search for articles by this author
  • Lan-Qing Yao
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China
    Search for articles by this author
  • Yong-Kang Diao
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China
    Search for articles by this author
  • Li-Yang Sun
    Affiliations
    Department of General Surgery, Cancer Center, Division of Hepatobiliary and Pancreatic Surgery, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, Hangzhou, Zhejiang, China
    Search for articles by this author
  • Cheng-Wu Zhang
    Affiliations
    Department of General Surgery, Cancer Center, Division of Hepatobiliary and Pancreatic Surgery, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, Hangzhou, Zhejiang, China
    Search for articles by this author
  • Yong-Yi Zeng
    Affiliations
    Department of Hepatobiliary Surgery, Mengchao Hepatobiliary Hospital, Fujian Medical University, Fujian, China
    Search for articles by this author
  • Wan Yee Lau
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China

    Faculty of Medicine, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR, China
    Search for articles by this author
  • Dong-Sheng Huang
    Affiliations
    Department of General Surgery, Cancer Center, Division of Hepatobiliary and Pancreatic Surgery, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, Hangzhou, Zhejiang, China

    School of Public Health, Hangzhou Medical College, Hangzhou, Zhejiang, China
    Search for articles by this author
  • Feng Shen
    Correspondence
    Correspondence: Feng Shen, Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University, Shanghai, China.
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China

    Eastern Hepatobiliary Clinical Research Institute, Third Affiliated Hospital of Navy Medical University, Shanghai, China
    Search for articles by this author
  • Tian Yang
    Correspondence
    Correspondence: Tian Yang, Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University, Shanghai, China.
    Affiliations
    Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery Hospital, Navy Medical University (Second Military Medical University), Shanghai, China

    Department of General Surgery, Cancer Center, Division of Hepatobiliary and Pancreatic Surgery, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, Hangzhou, Zhejiang, China

    School of Public Health, Hangzhou Medical College, Hangzhou, Zhejiang, China

    Eastern Hepatobiliary Clinical Research Institute, Third Affiliated Hospital of Navy Medical University, Shanghai, China
    Search for articles by this author
Published:September 09, 2022DOI:https://doi.org/10.1016/j.hpb.2022.09.002

      Abstract

      Background

      The Eastern Staging System, which was specially developed for patients undergoing surgical resection for hepatocellular carcinoma (HCC), has been proposed for more than ten years. To prospectively validate the predictive accuracy of the Eastern staging on long-term survival after HCC resection.

      Methods

      Patients who underwent hepatectomy for HCC from 2011 to 2020 at 10 Chinese hospitals were identified from a prospectively collected database. The survival predictive accuracy was evaluated and compared between the Eastern Staging with six other staging systems, including the JIS, BCLC, Okuda, CLIP, 8th AJCC TNM, and HKLC staging.

      Results

      Among 2365 patients, the 1-, 3-, and 5-year overall survival rates were 84.2%, 64.5%, and 52.6%, respectively. Among these seven staging systems, the Eastern staging was associated with the best monotonicity of gradients (linear trend χ2: 408.5) and homogeneity (likelihood ratio χ2: 447.3), and the highest discriminatory ability (the areas under curves for 1-, 3-, and 5-year mortality: 0.776, 0.787, and 0.768, respectively). In addition, the Eastern staging was the most informative staging system in predicting survival (Akaike information criterion: 2982.33).

      Conclusion

      Using a large multicenter prospectively collected database, the Eastern Staging was found to show the best predictive accuracy on long-term overall survival in patients with resectable HCC than the other 6 commonly-used staging systems.

      Graphical abstract

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to HPB
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Chapiro J.
        • Geschwind J.F.
        Hepatocellular carcinoma: have we finally found the ultimate staging system for HCC.
        Nat Rev Gastroenterol Hepatol. 2014; 11: 334-336
        • Bruix J.
        • Reig M.
        • Sherman M.
        Evidence-based diagnosis, staging, and treatment of patients with hepatocellular carcinoma.
        Gastroenterology. 2016; 150: 835-853
        • Sherman M.
        Staging for hepatocellular carcinoma: an embarrassment of riches.
        J Hepatol. 2016; 64: 535-536
        • Llovet J.M.
        • Brú C.
        • Bruix J.
        Prognosis of hepatocellular carcinoma: the BCLC staging classification.
        Semin Liver Dis. 1999; 19: 329-338
        • Yau T.
        • Tang V.Y.
        • Yao T.J.
        • Fan S.T.
        • Lo C.M.
        • Poon R.T.
        Development of Hong Kong Liver Cancer staging system with treatment stratification for patients with hepatocellular carcinoma.
        Gastroenterology. 2014; 146: 1691-1700.e3
        • Xu X.
        • Lau W.Y.
        • Yang T.
        The updated BCLC staging system needs further refinement: a surgeon's perspective.
        J Hepatol. 2022; 76: 1239-1240
        • Yang T.
        • Zhang J.
        • Lu J.H.
        • Yang L.Q.
        • Yang G.S.
        • Wu M.C.
        • et al.
        A new staging system for resectable hepatocellular carcinoma: comparison with six existing staging systems in a large Chinese cohort.
        J Cancer Res Clin Oncol. 2011; 137: 739-750
        • Okuda K.
        • Ohtsuki T.
        • Obata H.
        • Tomimatsu M.
        • Okazaki N.
        • Hasegawa H.
        • et al.
        Natural history of hepatocellular carcinoma and prognosis in relation to treatment. Study of 850 patients.
        Cancer. 1985; 56: 918-928
        • Edge S.B.
        • Byrd D.R.
        • Compton C.C.
        • Fritz A.G.
        • Greene F.L.
        • Trotti A.
        AJCC cancer staging manual.
        7th ed. Springer, New York2010: 191-200
        • investigators C.
        A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients: the Cancer of the Liver Italian Program (CLIP) investigators.
        Hepatology. 1998; 28: 751-755
        • Leung T.W.
        • Tang A.M.
        • Zee B.
        • Lau W.Y.
        • Lai P.B.
        • Leung K.L.
        • et al.
        Construction of the Chinese University Prognostic Index for hepatocellular carcinoma and comparison with the TNM staging system, the Okuda staging system, and the Cancer of the Liver Italian Program staging system: a study based on 926 patients.
        Cancer. 2002; 94: 1760-1769
        • Kudo M.
        • Chung H.
        • Osaki Y.
        Prognostic staging system for hepatocellular carcinoma (CLIP score): its value and limitations, and a proposal for a new staging system, the Japan Integrated Staging Score (JIS score).
        J Gastroenterol. 2003; 38: 207-215
        • Maida M.
        • Orlando E.
        • Cammà C.
        • Cabibbo G.
        Staging systems of hepatocellular carcinoma: a review of literature.
        World J Gastroenterol. 2014; 20: 4141-4150
        • Yang J.D.
        • Hainaut P.
        • Gores G.J.
        • Amadou A.
        • Plymoth A.
        • Roberts L.R.
        A global view of hepatocellular carcinoma: trends, risk, prevention and management.
        Nat Rev Gastroenterol Hepatol. 2019; 16: 589-604
      1. Hepatocellular carcinoma.
        Nat Rev Dis Prim. 2021; 7: 7
        • Akateh C.
        • Black S.M.
        • Conteh L.
        • Miller E.D.
        • Noonan A.
        • Elliott E.
        • et al.
        Neoadjuvant and adjuvant treatment strategies for hepatocellular carcinoma.
        World J Gastroenterol. 2019; 25: 3704-3721
        • Pinato D.J.
        • Fessas P.
        • Sapisochin G.
        • Marron T.U.
        Perspectives on the neoadjuvant use of immunotherapy in hepatocellular carcinoma.
        Hepatology. 2021; 74: 483-490
        • Su Y.Y.
        • Li C.C.
        • Lin Y.J.
        • Hsu C.
        Adjuvant versus neoadjuvant immunotherapy for hepatocellular carcinoma: clinical and immunologic perspectives.
        Semin Liver Dis. 2021; 41: 263-276
        • Amin M.B.
        • Greene F.L.
        • Edge S.B.
        • Compton C.C.
        • Gershenwald J.E.
        • Brookland R.K.
        • et al.
        The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging.
        CA A Cancer J Clin. 2017; 67: 93-99
        • Reig M.
        • Forner A.
        • Rimola J.
        • Ferrer-Fàbrega J.
        • Burrel M.
        • Garcia-Criado Á
        • et al.
        BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update.
        J Hepatol. 2022; 76: 681-693
        • Ueno S.
        • Tanabe G.
        • Sako K.
        • Hiwaki T.
        • Hokotate H.
        • Fukukura Y.
        • et al.
        Discrimination value of the new western prognostic system (CLIP score) for hepatocellular carcinoma in 662 Japanese patients. Cancer of the Liver Italian Program.
        Hepatology. 2001; 34: 529-534
        • Cillo U.
        • Bassanello M.
        • Vitale A.
        • Grigoletto F.A.
        • Burra P.
        • Fagiuoli S.
        • et al.
        The critical issue of hepatocellular carcinoma prognostic classification: which is the best tool available.
        J Hepatol. 2004; 40: 124-131
        • Feinstein A.R.
        Clinical biostatistics. XVI. The process of prognostic stratification. 2.
        Clin Pharmacol Ther. 1972; 13: 609-624
        • Hanley J.A.
        • McNeil B.J.
        The meaning and use of the area under a receiver operating characteristic (ROC) curve.
        Radiology. 1982; 143: 29-36
        • Liu P.H.
        • Hsu C.Y.
        • Hsia C.Y.
        • Lee Y.H.
        • Su C.W.
        • Huang Y.H.
        • et al.
        Prognosis of hepatocellular carcinoma: assessment of eleven staging systems.
        J Hepatol. 2016; 64: 601-608
        • Borzio M.
        • Dionigi E.
        • Rossini A.
        • Marignani M.
        • Sacco R.
        • De Sio I.
        • et al.
        External validation of the ITA.LI.CA prognostic system for patients with hepatocellular carcinoma: a multicenter cohort study.
        Hepatology. 2018; 67: 2215-2225
        • Benson A.B.
        • D’, Angelica M.I.
        • Abbott D.E.
        • Anaya D.A.
        • Anders R.
        • Are C.
        • et al.
        Hepatobiliary cancers, version 2.2021, NCCN clinical practice Guidelines in Oncology.
        J Natl Compr Cancer Netw. 2021; 19: 541-565
        • Chun Y.S.
        • Pawlik T.M.
        • Vauthey J.N.
        8th edition of the AJCC cancer staging manual: pancreas and hepatobiliary cancers.
        Ann Surg Oncol. 2018; 25: 845-847
        • Xu X.
        • Zhang H.L.
        • Liu Q.P.
        • Sun S.W.
        • Zhang J.
        • Zhu F.P.
        • et al.
        Radiomic analysis of contrast-enhanced CT predicts microvascular invasion and outcome in hepatocellular carcinoma.
        J Hepatol. 2019; 70: 1133-1144
        • Lee S.
        • Kim S.H.
        • Lee J.E.
        • Sinn D.H.
        • Park C.K.
        Preoperative gadoxetic acid-enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma.
        J Hepatol. 2017; 67: 526-534
        • Xu X.F.
        • Yu J.J.
        • Xing H.
        • Shen F.
        • Yang T.
        How to better predict microvascular invasion and recurrence of hepatocellular carcinoma.
        J Hepatol. 2017; 67: 1119-1120
        • Lei Z.
        • Li J.
        • Wu D.
        • Xia Y.
        • Wang Q.
        • Si A.
        • et al.
        Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the milan criteria.
        JAMA Surg. 2016; 151: 356-363
        • Hong S.B.
        • Choi S.H.
        • Kim S.Y.
        • Shim J.H.
        • Lee S.S.
        • Byun J.H.
        • et al.
        MRI features for predicting microvascular invasion of hepatocellular carcinoma: a systematic review and meta-analysis.
        Liver Cancer. 2021; 10: 94-106
        • Chen G.
        • Wang R.
        • Zhang C.
        • Gui L.
        • Xue Y.
        • Ren X.
        • et al.
        Integration of pre-surgical blood test results predict microvascular invasion risk in hepatocellular carcinoma.
        Comput Struct Biotechnol J. 2021; 19: 826-834
        • Adhoute X.
        • Penaranda G.
        • Raoul J.L.
        • Bourlière M.
        Hepatocellular carcinoma scoring and staging systems. Do we need new tools.
        J Hepatol. 2016; 64: 1449-1450
        • Yuan Y.
        • Yang F.
        • Wang Y.
        • Guo Y.
        Factors associated with liver cancer prognosis after hepatectomy: a retrospective cohort study.
        Medicine (Baltim). 2021; 100e27378
        • Hsu C.Y.
        • Lee Y.H.
        • Hsia C.Y.
        • Huang Y.H.
        • Su C.W.
        • Lin H.C.
        • et al.
        Performance status in patients with hepatocellular carcinoma: determinants, prognostic impact, and ability to improve the Barcelona Clinic Liver Cancer system.
        Hepatology. 2013; 57: 112-119
        • Wu H.
        • Xing H.
        • Liang L.
        • Huang B.
        • Li C.
        • Lau W.Y.
        • et al.
        Real-world role of performance status in surgical resection for hepatocellular carcinoma: a multicenter study.
        Eur J Surg Oncol. 2019; 45: 2360-2368
        • Hsu C.Y.
        • Lee Y.H.
        • Hsia C.Y.
        • Huang Y.H.
        • Su C.W.
        • Lin H.C.
        • et al.
        Performance status enhances the selection of treatment for patients with hepatocellular carcinoma within the milan criteria.
        Ann Surg Oncol. 2013; 20: 2035-2042
        • Moris D.
        • Burkhart R.A.
        • Beal E.W.
        • Pawlik T.M.
        Laparoscopic hepatectomy for hepatocellular carcinoma: are oncologic outcomes truly superior to an open approach.
        Hepatobiliary Surg Nutr. 2017; 6: 200-202
        • Han H.S.
        • Shehta A.
        • Ahn S.
        • Yoon Y.S.
        • Cho J.Y.
        • Choi Y.
        Laparoscopic versus open liver resection for hepatocellular carcinoma: case-matched study with propensity score matching.
        J Hepatol. 2015; 63: 643-650
        • Sangro B.
        • Sarobe P.
        • Hervás-Stubbs S.
        • Melero I.
        Advances in immunotherapy for hepatocellular carcinoma.
        Nat Rev Gastroenterol Hepatol. 2021; 18: 525-543
        • Brown Z.J.
        • Greten T.F.
        • Heinrich B.
        Adjuvant treatment of hepatocellular carcinoma: prospect of immunotherapy.
        Hepatology. 2019; 70: 1437-1442
        • Yang T.
        • Tabrizian P.
        • Zhang H.
        • Lau W.Y.
        • Han J.
        • Li Z.L.
        • et al.
        Comparison of patterns and outcomes of liver resection for hepatocellular carcinoma: East vs west.
        Clin Gastroenterol Hepatol. 2017; 15: 1972-1974
        • Kokudo T.
        • Hasegawa K.
        • Kokudo N.
        • Kokudo T.
        • Uldry E.
        • Demartines N.
        • et al.
        Hepatocellular carcinoma: the gap between Eastern and western clinical practice.
        Ann Surg. 2018; 267: e27-e28