Journal of Gastrointestinal Surgery

, Volume 23, Issue 2, pp 288–296 | Cite as

Identification of Actual 10-Year Survival After Hepatectomy of HBV-Related Hepatocellular Carcinoma: a Multicenter Study

  • Zhen-Li Li
  • Wen-Tao Yan
  • Jin Zhang
  • Yi-Jun Zhao
  • Wan Yee Lau
  • Xian-Hai Mao
  • Yong-Yi Zeng
  • Ya-Hao Zhou
  • Wei-Min Gu
  • Hong Wang
  • Ting-Hao Chen
  • Jun Han
  • Hao Xing
  • Han Wu
  • Chao Li
  • Ming-Da Wang
  • Meng-Chao Wu
  • Feng ShenEmail author
  • Tian YangEmail author
Original Article



Hepatitis B virus (HBV) infection is the leading cause of hepatocellular carcinoma (HCC) worldwide. The aim of the study was to identify the incidence and predictive factors of actual 10-year survival following liver resection of HBV-related HCC.


A Chinese multicenter database of patients undergoing curative hepatectomy of HBV-related HCC was reviewed. Patients who survived ≥ 10 years and patients who died < 10 years after surgery were compared and analyzed. Univariable and multivariable regression analyses were performed to identify predictive factors associated with 10-year survival.


Among all enrolled 1016 patients, the actuarial 10-year survival rate was 24.1%, while the actual 10-year survival rate was 16.6%. There were 169 patients who survived at least 10 years after surgery and 688 who died within 10 years from surgery. These patients constituted the study population of this study. Multivariable regression analysis revealed that cirrhosis, preoperative HBV viral load > 104 copies/mL, maximum tumor size > 5 cm, multiple tumors, macroscopic and microscopic vascular invasion, postoperative HBV reactivation, and early recurrence (< 2 years after surgery) were independent risk factors associated with actual 10-year survival, while postoperative antiviral therapy, regular recurrence surveillance, and curative treatments for initial recurrence were independent protective factors.


The actual 10-year survival after curative resection of HBV-related HCC was calculated to be 16.6%. Postoperative antiviral therapy and regular recurrence surveillance were independent protective factors associated with actual 10-year survival after liver resection of HBV-related HCC.


Hepatocellular carcinoma Hepatectomy Overall survival Hepatitis B virus 



Hepatocellular carcinoma


Hepatitis B virus


Hepatitis C virus


Body mass index


American Society of Anesthesiologists


Aspartate transaminase


Alanine aminotransferase




Computed tomography


Magnetic resonance imaging


Transcatheter arterial chemoembolization


Standard deviation


Odds ratios

95% CI

95% confidence interval


Financial Support

This work was supported in part by the National Natural Science Foundation of China (No. 81472284 and 81672699) and Shanghai Pujiang Program (No. 16PJD004).

Authors’ Contributions

Conception: Tian Yang, Feng Shen; study design: Tian Yang, Zhen-Li Li, Wen-Tao Yan, Jin Zhang, Xian-Hai Mao, Hao Xing, Jun Han; administrative support: Meng-Chao Wu, Feng Shen; data collection and acquisition: Chao Li, Ming-Da Wang, Ya-Hao Zhou, Ting-Hao Chen, Wei-Min Gu, Hong Wang, Yong-Yi Zeng; data analysis: Zhen-Li Li, Yi-Jun Zhao, Jun Han, Han Wu, Tian Yang; manuscript preparation: Zhen-Li Li, Wen-Tao Yan, Jin Zhang, Yi-Jun Zhao, Xian-Hai Mao, Tian Yang; critical revision: Feng Shen, Tian Yang, Wan Yee Lau; final approval of manuscript: all authors.

Compliance with Ethical Standards

Informed consent for the data to be used for clinical researches was obtained from all enrolled patients. This study was performed in accordance with the Declaration of Helsinki and the Ethical Guidelines for Clinical Studies of all the seven enrolled hospitals.

Conflict of Interest

The authors declare that they have no conflicts of interest.


  1. 1.
    Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin, 2014, 64:9–29.CrossRefGoogle Scholar
  2. 2.
    Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet, 2015, 385:117–171.Google Scholar
  3. 3.
    Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66:115–132.CrossRefGoogle Scholar
  4. 4.
    Nguyen VT, Law MG, Dore GJ. Hepatitis B-related hepatocellular carcinoma: epidemiological characteristics and disease burden. J Viral Hepat, 2009, 16:453–463.CrossRefGoogle Scholar
  5. 5.
    Yang T, Lu JH, Zhai J, Lin C, Yang GS, Zhao RH, Shen F, Wu MC. High viral load is associated with poor overall and recurrence-free survival of hepatitis B virus-related hepatocellular carcinoma after curative resection: a prospective cohort study. Eur J Surg Oncol, 2012, 38:683–691.CrossRefGoogle Scholar
  6. 6.
    Llovet JM, Fuster J, Bruix J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology, 1999, 30:1434–1440.CrossRefGoogle Scholar
  7. 7.
    Takayama T, Makuuchi M, Hirohashi S, Sakamoto M, Yamamoto J, Shimada K, Kosuge T, Okada S, Takayasu K, Yamasaki S. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology, 1998, 28:1241–1246.CrossRefGoogle Scholar
  8. 8.
    Cunningham SC, Tsai S, Marques HP, Mira P, Cameron A, Barroso E, Philosophe B, Pawlik TM. Management of early hepatocellular carcinoma in patients with well-compensated cirrhosis. Ann Surg Oncol, 2009, 16:1820–1831.CrossRefGoogle Scholar
  9. 9.
    Nathan H, Bridges JF, Schulick RD, Cameron AM, Hirose K, Edil BH, Wolfgang CL, Segev DL, Choti MA, Pawlik TM. Understanding surgical decision making in early hepatocellular carcinoma. J Clin Oncol, 2011, 29:619–625.CrossRefGoogle Scholar
  10. 10.
    Dhir M, Melin AA, Douaiher J, Lin C, Zhen WK, Hussain SM, Geschwind JF, Doyle MB, Abou-Alfa GK, Are C. A review and update of treatment options and controversies in the management of hepatocellular carcinoma. Ann Surg, 2016, 263:1112–1125.CrossRefGoogle Scholar
  11. 11.
    Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XP, Peng T, Xie GS, Li LQ. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg, 2014, 260:329–340.CrossRefGoogle Scholar
  12. 12.
    Yau T, Tang VY, Yao TJ, Fan ST, Lo CM, Poon RT. Development of Hong Kong Liver Cancer staging system with treatment stratification for patients with hepatocellular carcinoma. Gastroenterology, 2014, 146:1691–1700.e3.CrossRefGoogle Scholar
  13. 13.
    Vitale A, Burra P, Frigo AC, Trevisani F, Farinati F, Spolverato G, Volk M, Giannini EG, Ciccarese F, Piscaglia F, Rapaccini GL, Di MM, Caturelli E, Zoli M, Borzio F, Cabibbo G, Felder M, Gasbarrini A, Sacco R, Foschi FG, Missale G, Morisco F, Svegliati BG, Virdone R, Cillo U. Survival benefit of liver resection for patients with hepatocellular carcinoma across different Barcelona Clinic Liver Cancer stages: a multicentre study. J Hepatol, 2015, 62:617–624.CrossRefGoogle Scholar
  14. 14.
    Yang T, Lu JH, Lau WY, Zhang TY, Zhang H, Shen YN, Alshebeeb K, Wu MC, Schwartz M, Shen F. Perioperative blood transfusion does not influence recurrence-free and overall survivals after curative resection for hepatocellular carcinoma: a Propensity Score Matching Analysis. J Hepatol, 2016, 64:583–593.CrossRefGoogle Scholar
  15. 15.
    Hyun MH, Lee YS, Kim JH, Lee CU, Jung YK, Seo YS, Yim HJ, Yeon JE, Byun KS. Hepatic resection compared to chemoembolization in intermediate- to advanced-stage hepatocellular carcinoma: a meta-analysis of high-quality studies. Hepatology, 2018. DOI:
  16. 16.
    Trevisani F, Bucci L, Garuti F. Is it time to extend criteria for hepatic resection in the treatment of hepatocellular carcinoma. Hepatology, 2016, 64:2257–2258.CrossRefGoogle Scholar
  17. 17.
    Gluer AM, Cocco N, Laurence JM, Johnston ES, Hollands MJ, Pleass HC, Richardson AJ, Lam VW. Systematic review of actual 10-year survival following resection for hepatocellular carcinoma. HPB (Oxford), 2012, 14:285–290.CrossRefGoogle Scholar
  18. 18.
    Zheng J, Kuk D, Gönen M, Balachandran VP, Kingham TP, Allen PJ, D’Angelica MI, Jarnagin WR, DeMatteo RP. Actual 10-Year Survivors After Resection of Hepatocellular Carcinoma. Ann Surg Oncol, 2017, 24:1358–1366.CrossRefGoogle Scholar
  19. 19.
    Shimada K, Sano T, Sakamoto Y, Kosuge T. A long-term follow-up and management study of hepatocellular carcinoma patients surviving for 10 years or longer after curative hepatectomy. Cancer, 2005, 104:1939–1947.CrossRefGoogle Scholar
  20. 20.
    Wu KT, Wang CC, Lu LG, Zhang WD, Zhang FJ, Shi F, Li CX. Hepatocellular carcinoma: clinical study of long-term survival and choice of treatment modalities. World J Gastroenterol, 2013, 19:3649–3657.CrossRefGoogle Scholar
  21. 21.
    Zhou XD, Tang ZY, Ma ZC, Fan J, Wu ZQ, Qin LX, Zhou J, Yu Y, Sun HC, Qiu SJ. Twenty-year survivors after resection for hepatocellular carcinoma-analysis of 53 cases. J Cancer Res Clin Oncol, 2009, 135:1067–1072.CrossRefGoogle Scholar
  22. 22.
    Zhou XD, Tang ZY, Yang BH, Lin ZY, Ma ZC, Ye SL, Wu ZQ, Fan J, Qin LX, Zheng BH. Experience of 1000 patients who underwent hepatectomy for small hepatocellular carcinoma. Cancer, 2001, 91:1479–1486.CrossRefGoogle Scholar
  23. 23.
    Zhu Y, Wen L, Shao S, Tan Y, Meng T, Yang X, Liu Y, Liu X, Yuan H, Hu F. Inhibition of tumor-promoting stroma to enforce subsequently targeting AT1R on tumor cells by pathological inspired micelles. Biomaterials, 2018, 161:33–46.CrossRefGoogle Scholar
  24. 24.
    Strasberg SM, Phillips C. Use and dissemination of the brisbane 2000 nomenclature of liver anatomy and resections. Ann Surg, 2013, 257:377–382.CrossRefGoogle Scholar
  25. 25.
    Franssen B, Jibara G, Tabrizian P, Schwartz ME, Roayaie S. Actual 10-year survival following hepatectomy for hepatocellular carcinoma. HPB (Oxford), 2014, 16:830–835.CrossRefGoogle Scholar
  26. 26.
    Huang G, Li PP, Lau WY, Pan ZY, Zhao LH, Wang ZG, Wang MC, Zhou WP. Antiviral therapy reduces hepatocellular carcinoma recurrence in patients with low HBV-DNA levels: a randomized controlled trial. Ann Surg, 2018. DOI:
  27. 27.
    Huang G, Lau WY, Wang ZG, Pan ZY, Yuan SX, Shen F, Zhou WP, Wu MC. Antiviral therapy improves postoperative survival in patients with hepatocellular carcinoma: a randomized controlled trial. Ann Surg, 2015, 261:56–66.CrossRefGoogle Scholar
  28. 28.
    Huang G, Lai EC, Lau WY, Zhou WP, Shen F, Pan ZY, Fu SY, Wu MC. Posthepatectomy HBV reactivation in hepatitis B-related hepatocellular carcinoma influences postoperative survival in patients with preoperative low HBV-DNA levels. Ann Surg, 2013, 257:490–505.CrossRefGoogle Scholar
  29. 29.
    Yamamoto Y, Ikoma H, Morimura R, Konishi H, Murayama Y, Komatsu S, Shiozaki A, Kuriu Y, Kubota T, Nakanishi M, Ichikawa D, Fujiwara H, Okamoto K, Sakakura C, Ochiai T, Otsuji E. Optimal duration of the early and late recurrence of hepatocellular carcinoma after hepatectomy. World J Gastroenterol, 2015, 21:1207–1215.CrossRefGoogle Scholar
  30. 30.
    Mittal S, Kanwal F, Ying J, Chung R, Sada YH, Temple S, Davila JA, El-Serag HB. Effectiveness of surveillance for hepatocellular carcinoma in clinical practice: a United States cohort. J Hepatol, 2016, 65:1148–1154.CrossRefGoogle Scholar
  31. 31.
    Khalaf N, Ying J, Mittal S, Temple S, Kanwal F, Davila J, El-Serag HB. Natural history of untreated hepatocellular carcinoma in a US cohort and the role of cancer surveillance. Clin Gastroenterol Hepatol, 2017, 15:273–281.e1.CrossRefGoogle Scholar
  32. 32.
    Zheng J, Chou JF, Gönen M, Vachharajani N, Chapman WC, Majella DMB, Turcotte S, Vandenbroucke-Menu F, Lapointe R, Buettner S, Groot KB, JNM I, Chan CY, BKP G, Teo JY, Kam JH, Jeyaraj PR, Cheow PC, AYF C, PKH C, LLPJ O, Balachandran VP, Kingham TP, Allen PJ, D’Angelica MI, DeMatteo RP, Jarnagin WR, Lee SY. Prediction of hepatocellular carcinoma recurrence beyond Milan criteria after resection: validation of a clinical risk score in an international cohort. Ann Surg, 2017, 266:693–701.CrossRefGoogle Scholar
  33. 33.
    Poon RT. Differentiating early and late recurrences after resection of HCC in cirrhotic patients: implications on surveillance, prevention, and treatment strategies. Ann Surg Oncol, 2009, 16:792–794.CrossRefGoogle Scholar
  34. 34.
    Du ZG, Wei YG, Chen KF, Li B. Risk factors associated with early and late recurrence after curative resection of hepatocellular carcinoma: a single institution’s experience with 398 consecutive patients. Hepatobiliary Pancreat Dis Int, 2014, 13:153–161.CrossRefGoogle Scholar
  35. 35.
    Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer, 2000, 89:500–507.CrossRefGoogle Scholar
  36. 36.
    Portolani N, Coniglio A, Ghidoni S, Giovanelli M, Benetti A, Tiberio GA, Giulini SM. Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann Surg, 2006, 243:229–235CrossRefGoogle Scholar
  37. 37.
    Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, Sugawara Y, Minagawa M, Takayama T, Kawasaki S, Makuuchi M. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol, 2003, 38:200–207.CrossRefGoogle Scholar
  38. 38.
    Bagante F, Spolverato G, Weiss M, Alexandrescu S, Marques HP, Aldrighetti L, Maithel SK, Pulitano C, Bauer TW, Shen F, Poultsides GA, Soubrane O, Martel G, Groot KB, Guglielmi A, Itaru E, Pawlik TM. Defining long-term survivors following resection of intrahepatic cholangiocarcinoma. J Gastrointest Surg, 2017, 21:1888–1897CrossRefGoogle Scholar
  39. 39.
    Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, Kemeny N, Brennan MF, Blumgart LH, D’Angelica M. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol, 2007, 25:4575–4580.CrossRefGoogle Scholar
  40. 40.
    Tran TB, Postlewait LM, Maithel SK, Prescott JD, Wang TS, Glenn J, Phay JE, Keplinger K, Fields RC, Jin LX, Weber SM, Salem A, Sicklick JK, Gad S, Yopp AC, Mansour JC, Duh QY, Seiser N, Solorzano CC, Kiernan CM, Votanopoulos KI, Levine EA, Hatzaras I, Shenoy R, Pawlik TM, Norton JA, Poultsides GA. Actual 10-year survivors following resection of adrenocortical carcinoma. J Surg Oncol, 2016, 114:971–976.CrossRefGoogle Scholar
  41. 41.
    Creasy JM, Sadot E, Koerkamp BG, Chou JF, Gonen M, Kemeny NE, Balachandran VP, Kingham TP, DeMatteo RP, Allen PJ, Blumgart LH, Jarnagin WR, D’Angelica MI. Actual 10-year survival after hepatic resection of colorectal liver metastases: what factors preclude cure. Surgery, 2018, 163:1238–1244.CrossRefGoogle Scholar
  42. 42.
    Chua TC, Saxena A, Chu F, Zhao J, Morris DL. Predictors of cure after hepatic resection of colorectal liver metastases: an analysis of actual 5- and 10-year survivors. J Surg Oncol, 2011, 103:796–800.CrossRefGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  • Zhen-Li Li
    • 1
  • Wen-Tao Yan
    • 1
    • 2
  • Jin Zhang
    • 1
  • Yi-Jun Zhao
    • 1
  • Wan Yee Lau
    • 1
    • 3
  • Xian-Hai Mao
    • 4
  • Yong-Yi Zeng
    • 5
  • Ya-Hao Zhou
    • 6
  • Wei-Min Gu
    • 7
  • Hong Wang
    • 8
  • Ting-Hao Chen
    • 9
  • Jun Han
    • 1
  • Hao Xing
    • 1
  • Han Wu
    • 1
  • Chao Li
    • 1
  • Ming-Da Wang
    • 1
  • Meng-Chao Wu
    • 1
  • Feng Shen
    • 1
    Email author
  • Tian Yang
    • 1
    Email author
  1. 1.Department of Hepatobiliary Surgery, Eastern Hepatobiliary Surgery HospitalSecond Military Medical UniversityShanghaiChina
  2. 2.Department of Clinical MedicineSecond Military Medical UniversityShanghaiChina
  3. 3.Faculty of MedicineThe Chinese University of Hong KongShatinHong Kong SAR
  4. 4.Department of Hepatobiliary SurgeryThe People’s Hospital of Hunan ProvinceChangshaChina
  5. 5.Department of Hepatobiliary Surgery, Mengchao Hepatobiliary HospitalFujian Medical UniversityFuzhouChina
  6. 6.Department of Hepatobiliary SurgeryPu’er People’s HospitalPu’erChina
  7. 7.The First Department of General SurgeryThe Fourth Hospital of HarbinHarbinChina
  8. 8.Department of General SurgeryLiuyang People’s HospitalLiuyangChina
  9. 9.Department of General SurgeryZiyang First People’s HospitalZiyangChina

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