Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Updates in Surgery Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

BCLC:

Barcelona clinic liver cancer

HCC:

Hepatocellular carcinoma

TACE:

Transarterial chemoembolization

LT:

Liver transplantation

HR:

Hepatic resection

RFA:

Radiofrequency ablation

CT:

Computed tomography

MRI:

Magnetic resonance imaging

OR:

Odds ratio

HRs:

Hazard ratio

References

  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 68:394–424

    Article  Google Scholar 

  2. Lafaro KJ, Demirjian AN, Pawlik TM (2015) Epidemiology of hepatocellular carcinoma. Surg Oncol Clin N Am 24:1–17

    Article  PubMed  Google Scholar 

  3. Forner A, Reig M, Bruix J (2018) Hepatocellular carcinoma. Lancet 391:1301–1314

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  5. Qi X, Tang Y, An D et al (2014) Radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma. J Clin Gastroenterol 48(5):450–457

    Article  PubMed  Google Scholar 

  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 3:313–318

    Article  PubMed  PubMed Central  Google Scholar 

  7. Ota K, Teraoka S, Kawai T (1995) Donor difficulties in Japan and Asian countries. Transplant Proc 27:83–86

    CAS  PubMed  Google Scholar 

  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 16:848–855

    Article  PubMed  Google Scholar 

  9. Garancini M, Pinotti E, Nespoli S et al (2016) Hepatic resection beyond Barcelona clinic liver cancer indication: when and how. World J Hepatol 8:513–519

    Article  PubMed  PubMed Central  Google Scholar 

  10. Forner A, Gilabert M, Bruix J, Raoul J-L (2014) Treatment of intermediate-stage hepatocellular carcinoma. Nat Rev Clin Oncol 11:525–535

    Article  CAS  Google Scholar 

  11. Kapitanov T, Neumann UP, Schmeding M (2015) Hepatocellular carcinoma in liver cirrhosis: surgical resection versus transarterial chemoembolization—a meta-analysis. Gastroenterol Res Pract 2015:696120

    Article  PubMed  PubMed Central  Google Scholar 

  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:e180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 34:2155–2161

    Article  PubMed  Google Scholar 

  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 335:806–808

    Article  Google Scholar 

  15. Llovet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362:1907–1917

    Article  PubMed  Google Scholar 

  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 240:205–213

    Article  PubMed  PubMed Central  Google Scholar 

  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 56:908–943

    Article  Google Scholar 

  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 10:35–43

    Article  Google Scholar 

  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–vii48

    Article  PubMed  Google Scholar 

  20. Guerrini GP, Gerunda GE, Montalti R et al (2014) Results of salvage liver transplantation. Liver Int 34:e96–e104

    Article  PubMed  Google Scholar 

  21. Felli E, Cillo U, Pinna AD et al (2015) Salvage liver transplantation after laparoscopic resection for hepatocellular carcinoma: a multicenter experience. Updates Surg 67:215–222

    Article  PubMed  Google Scholar 

  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 27:722–729

    Article  PubMed  Google Scholar 

  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 101:745–754

    Article  PubMed  Google Scholar 

  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 159:793–801

    Article  PubMed  Google Scholar 

  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 257:929–937

    Article  PubMed  Google Scholar 

  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 104:1045–1052

    Article  CAS  PubMed  Google Scholar 

  27. Cucchetti A, Djulbegovic B, Tsalatsanis A et al (2015) When to perform hepatic resection for intermediate-stage hepatocellular carcinoma. Hepatology 61:905–914

    Article  PubMed  Google Scholar 

  28. Shah SA, Cleary SP, Wei AC et al (2007) Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery 141:330–339

    Article  PubMed  Google Scholar 

  29. Lafaro K, Grandhi MS, Herman JM, Pawlik TM (2016) The importance of surgical margins in primary malignancies of the liver. J Surg Oncol 113:296–303

    Article  PubMed  Google Scholar 

  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 226:1147–1159

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

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].

Author information

Authors and Affiliations

  1. Department of General Surgery and Transplantation, Niguarda Ca’ Granda Hospital, Piazza Ospedale Maggiore 3, 20162, Milan, Italy

    Stefano Di Sandro, Leonardo Centonze, Andrea Lauterio, Riccardo De Carlis & Luciano De Carlis

  2. School of Medicine and Surgery, University of Milano-Bicocca, Milan, Italy

    Enrico Pinotti, Fabrizio Romano, Luca Gianotti & Luciano De Carlis

  3. Department of Surgical Sciences, University of Pavia, Pavia, Italy

    Riccardo De Carlis

Authors
  1. Stefano Di Sandro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonardo Centonze
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrico Pinotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea Lauterio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Riccardo De Carlis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabrizio Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luca Gianotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Luciano De Carlis
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The NTF Research Group

  • Tiziana Cena
  • , Vincenzo Bagnardi
  • , Laura Benuzzi
  • , Isabella Pezzoli
  • , Maria Danieli
  •  & Arianna Ciravegna

Corresponding author

Correspondence to Stefano Di Sandro.

Ethics declarations

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.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

NTF (Niguarda Transplant Foundation) Research Group has contributed to the study by data management and statistical analysis.

The members of the NTF Research Group are listed in acknowledgements.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Di Sandro, S., Centonze, L., Pinotti, E. et al. Surgical and oncological outcomes of hepatic resection for BCLC-B hepatocellular carcinoma: a retrospective multicenter analysis among 474 consecutive cases. Updates Surg 71, 285–293 (2019). https://doi.org/10.1007/s13304-019-00649-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13304-019-00649-w

Keywords

Search

Navigation