Surgical and oncological outcomes of hepatic resection for BCLC-B hepatocellular carcinoma: a retrospective multicenter analysis among 474 consecutive cases

  • Stefano Di SandroEmail author
  • Leonardo Centonze
  • Enrico Pinotti
  • Andrea Lauterio
  • Riccardo De Carlis
  • Fabrizio Romano
  • Luca Gianotti
  • Luciano De Carlis
  • The NTF Research Group
Original Article


The Barcelona clinic liver cancer (BCLC) algorithm is the most widely accepted staging system form hepatocellular carcinoma (HCC). Liver resection is traditionally proposed to early stage HCC (BCLC-0/A), even if recent reports have shown that surgical resection could provide a safe and effective treatment also for intermediate-stage HCC (BCLC-B). In this study, we focused on surgical and oncological outcomes of hepatic resection in BLCB-B patients. Patients who received hepatic resection for early- (BCLC-0/A) or intermediate-stage (BCLC-B) HCC in two tertiary hepatobiliary centers between January 2003 and December 2016 were included in study. Four-hundred and twenty-nine patients were included in the analysis. At the time of resection, 298 patients were classified as BCLC-A/0 and 131 as BCLC-B. Despite a higher complication rate in BCLC-B group (49.6% vs 32.9%; p = 0.001), the incidence of clinically relevant complications did not differ significantly between the two groups (16.0% vs 10.1%; p = 0.079); moreover, postoperative mortality (4.6% vs 2.7%; p = 0.309) and relapse-free survival (RFS) were similar between BCLC-0/A and BCLC-B group (1-, 3-, and 5-year RFS: 74, 43, and 31% vs 59, 38, and 34%; p = 0.180). Overall survival was slightly worse in BCLC-B group (1-, 3-, and 5-year overall survival of 89, 70, and 52% vs. 77, 51, and 44%; p = 0.004). Focusing on BCLC-B group, a Child–Pugh score B (HR 2.47; p = 0.003), growing number of nodules (HR 3.04; p = 0.003), and R1 resection (HR 2.43; p = 0.005) beard a higher risk of tumor recurrence, while overall survival was negatively affected by the presence of more than two nodules (HR 3.66; p = 0.0001) and R1 resection (HR 3.06; p = 0.0001); patients presenting single-large HCC experienced a better overall survival (HR 0.53; p = 0.014) and lower recurrence-rate (HR 0.60; p = 0.046). Hepatic resection for intermediate-stage HCC shows acceptable results in terms of perioperative morbidity and mortality, with better oncological outcomes in patients with lower number of lesions despite of their size.


Hepatocellular carcinoma BCLC Liver resection Liver surgery 



Barcelona clinic liver cancer


Hepatocellular carcinoma


Transarterial chemoembolization


Liver transplantation


Hepatic resection


Radiofrequency ablation


Computed tomography


Magnetic resonance imaging


Odds ratio


Hazard ratio



We thank the NTF Research Group, Enrico Pinotti MD [MONZA], Laura Benuzzi MD [MILANO], Isabella Pezzoli MD [MILANO], Maria Danieli MD [MILANO], Arianna Ciravegna MD [MONZA]) for its efforts in data managing and statistical analysis. The members of the NTF Research Group are: Tiziana Cena [NOVARA], Vincenzo Bagnardi PhD [MILANO], Laura Benuzzi MD [MILANO], Isabella Pezzoli MD [MILANO], Maria Danieli MD [MILANO], and Arianna Ciravegna MD [MONZA].

Compliance with ethical standards

Conflict of interest

The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.

Ethical approval

Ethical approval was no necessary because of the retrospective nature of this study.

Informed consent

Informed consent was obtained for all the patients enrolled in clinical research studies.


  1. 1.
    Bray F, Ferlay J, Soerjomataram I et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424CrossRefGoogle Scholar
  2. 2.
    Lafaro KJ, Demirjian AN, Pawlik TM (2015) Epidemiology of hepatocellular carcinoma. Surg Oncol Clin N Am 24:1–17CrossRefGoogle Scholar
  3. 3.
    Forner A, Reig M, Bruix J (2018) Hepatocellular carcinoma. Lancet 391:1301–1314CrossRefGoogle Scholar
  4. 4.
    Ruzzenente A, Guglielmi A, Sandri M et al (2012) Surgical resection versus local ablation for HCC on cirrhosis: results from a propensity case-matched study. J Gastrointest Surg 16:301–311 (discussion 311) CrossRefGoogle Scholar
  5. 5.
    Qi X, Tang Y, An D et al (2014) Radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma. J Clin Gastroenterol 48(5):450–457Google Scholar
  6. 6.
    De Carlis L, Di Sandro S, Centonze L et al (2016) Liver-allocation policies for patients affected by HCC in Europe. Curr Transplant Rep 3:313–318CrossRefGoogle Scholar
  7. 7.
    Ota K, Teraoka S, Kawai T (1995) Donor difficulties in Japan and Asian countries. Transplant Proc 27:83–86Google Scholar
  8. 8.
    Ho M-C, Huang G-T, Tsang Y-M et al (2009) Liver resection improves the survival of patients with multiple hepatocellular carcinomas. Ann Surg Oncol 16:848–855CrossRefGoogle Scholar
  9. 9.
    Garancini M, Pinotti E, Nespoli S et al (2016) Hepatic resection beyond Barcelona clinic liver cancer indication: when and how. World J Hepatol 8:513–519CrossRefGoogle Scholar
  10. 10.
    Forner A, Gilabert M, Bruix J, Raoul J-L (2014) Treatment of intermediate-stage hepatocellular carcinoma. Nat Rev Clin Oncol 11:525–535CrossRefGoogle Scholar
  11. 11.
    Kapitanov T, Neumann UP, Schmeding M (2015) Hepatocellular carcinoma in liver cirrhosis: surgical resection versus transarterial chemoembolization—a meta-analysis. Gastroenterol Res Pract 2015:696120CrossRefGoogle Scholar
  12. 12.
    Jianyong L, Lunan Y, Wentao W et al (2014) Barcelona clinic liver cancer stage B hepatocellular carcinoma: transarterial chemoembolization or hepatic resection? Medicine 93:e180CrossRefGoogle Scholar
  13. 13.
    Lin C-T, Hsu K-F, Chen T-W et al (2010) Comparing hepatic resection and transarterial chemoembolization for barcelona clinic liver cancer (BCLC) stage B hepatocellular carcinoma: change for treatment of choice? World J Surg 34:2155–2161CrossRefGoogle Scholar
  14. 14.
    von Elm E, Altman DG, Egger M et al (2007) Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ 335:806–808CrossRefGoogle Scholar
  15. 15.
    Llovet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362:1907–1917CrossRefGoogle Scholar
  16. 16.
    Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefGoogle Scholar
  17. 17.
    European Association For The Study Of The Liver, European Organisation For Research And Treatment Of Cancer (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56:908–943CrossRefGoogle Scholar
  18. 18.
    Mazzaferro V, Llovet JM, Miceli R et al (2009) Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 10:35–43CrossRefGoogle Scholar
  19. 19.
    Verslype C, Rosmorduc O, Rougier P, ESMO Guidelines Working Group (2012) Hepatocellular carcinoma: ESMO-ESDO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 23(Suppl 7):vii41–vii48CrossRefGoogle Scholar
  20. 20.
    Guerrini GP, Gerunda GE, Montalti R et al (2014) Results of salvage liver transplantation. Liver Int 34:e96–e104CrossRefGoogle Scholar
  21. 21.
    Felli E, Cillo U, Pinna AD et al (2015) Salvage liver transplantation after laparoscopic resection for hepatocellular carcinoma: a multicenter experience. Updates Surg 67:215–222CrossRefGoogle Scholar
  22. 22.
    Di Sandro S, Bagnardi V, Najjar M et al (2018) Minor laparoscopic liver resection for hepatocellular carcinoma is safer than minor open resection, especially for less compensated cirrhotic patients: propensity score analysis. Surg Oncol 27:722–729CrossRefGoogle Scholar
  23. 23.
    Sharma R, Gibbs JF (2010) Recent advances in the management of primary hepatic tumors refinement of surgical techniques and effect on outcome. J Surg Oncol 101:745–754CrossRefGoogle Scholar
  24. 24.
    Day RW, Brudvik KW, Vauthey J-N et al (2016) Advances in hepatectomy technique: toward zero transfusions in the modern era of liver surgery. Surgery 159:793–801CrossRefGoogle Scholar
  25. 25.
    Torzilli G, Belghiti J, Kokudo N et al (2013) A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers. Ann Surg 257:929–937CrossRefGoogle Scholar
  26. 26.
    Kim H, Ahn SW, Hong SK et al (2017) Survival benefit of liver resection for Barcelona clinic liver cancer stage B hepatocellular carcinoma. Br J Surg 104:1045–1052CrossRefGoogle Scholar
  27. 27.
    Cucchetti A, Djulbegovic B, Tsalatsanis A et al (2015) When to perform hepatic resection for intermediate-stage hepatocellular carcinoma. Hepatology 61:905–914CrossRefGoogle Scholar
  28. 28.
    Shah SA, Cleary SP, Wei AC et al (2007) Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery 141:330–339CrossRefGoogle Scholar
  29. 29.
    Lafaro K, Grandhi MS, Herman JM, Pawlik TM (2016) The importance of surgical margins in primary malignancies of the liver. J Surg Oncol 113:296–303CrossRefGoogle Scholar
  30. 30.
    Di Sandro S, Sposito C, Lauterio A et al (2018) Proposal of prognostic survival models before and after liver resection for hepatocellular carcinoma in potentially transplantable patients. J Am Coll Surg 226:1147–1159CrossRefGoogle Scholar

Copyright information

© Italian Society of Surgery (SIC) 2019

Authors and Affiliations

  • Stefano Di Sandro
    • 1
    Email author
  • Leonardo Centonze
    • 1
  • Enrico Pinotti
    • 2
  • Andrea Lauterio
    • 1
  • Riccardo De Carlis
    • 1
    • 3
  • Fabrizio Romano
    • 2
  • Luca Gianotti
    • 2
  • Luciano De Carlis
    • 1
    • 2
  • The NTF Research Group
  1. 1.Department of General Surgery and TransplantationNiguarda Ca’ Granda HospitalMilanItaly
  2. 2.School of Medicine and SurgeryUniversity of Milano-BicoccaMilanItaly
  3. 3.Department of Surgical SciencesUniversity of PaviaPaviaItaly

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