Several investigators have advocated for extending the Barcelona Clinic Liver Cancer (BCLC) resection criteria to select patients with BCLC-B and even BCLC-C hepatocellular carcinoma (HCC). The objective of the current study was to define the outcomes and recurrence patterns after resection within and beyond the current resection criteria.
Patients and Methods
Patients who underwent resection for HCC within (i.e., BCLC 0/A) and beyond (i.e. BCLC B/C) the current resection criteria between 2005 and 2017 were identified from an international multi-institutional database. Overall survival (OS), disease-free survival (DFS), as well as patterns of recurrence of patients undergoing HCC resection within and beyond the BCLC guidelines were examined.
Among 756 patients, 602 (79.6%) patients were BCLC 0/A and 154 (20.4%) were BCLC B/C. Recurrences were mostly intrahepatic (within BCLC: 74.3% versus beyond BCLC: 70.8%, p = 0.80), with BCLC B/C patients more often having multiple tumors at relapse (69.6% versus 49.4%, p = 0.001) and higher rates of early (< 2 years) recurrence (88.0% versus 75.5%, p = 0.011). During the first postoperative year, annual recurrence was 38.3% and 21.3% among BCLC B/C and BCLC 0/A patients, respectively; 5-year OS among BCLC 0/A and BCLC B/C patients was 76.9% versus 51.6% (p = 0.003). On multivariable analysis, only a-fetoprotein (AFP) > 400 ng/mL (HR = 1.84, 95% CI 1.07–3.15) and R1 resection (HR = 2.36, 95% CI 1.32–4.23) were associated with higher risk of recurrence among BCLC B/C patients.
Surgery can provide acceptable outcomes among select patients with BCLC B/C HCC. The data emphasize the need to further refine the BCLC treatment algorithm as well as highlight the need for surveillance protocols with a particular focus on the liver, especially for patients undergoing resection outside the BCLC criteria.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Beal EW, Tumin D, Kabir A, et al. Trends in the mortality of hepatocellular carcinoma in the United States. J Gastrointest Surg. 2017; 21(12): 2033–8.
Lafaro KJ, Demirjian AN, Pawlik TM. Epidemiology of hepatocellular carcinoma. Surg Oncol Clin N Am. 2015; 24(1): 1–17.
Vietti Violi N, Duran R, Guiu B, et al. Efficacy of microwave ablation versus radiofrequency ablation for the treatment of hepatocellular carcinoma in patients with chronic liver disease: a randomised controlled phase 2 trial. Lancet Gastroenterol Hepatol. 2018; 3(5): 317–25.
European Association for the Study of the Liver. Electronic address eee, European Association for the study of the L. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018; 69(1): 182–236.
Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018; 68(2): 723–50.
Marrero JA, Fontana RJ, Barrat A, et al. Prognosis of hepatocellular carcinoma: comparison of 7 staging systems in an American cohort. Hepatology. 2005; 41(4): 707–16.
O’Neil BH, Venook AP. Hepatocellular carcinoma: the role of the North American GI Steering Committee Hepatobiliary Task Force and the advent of effective drug therapy. Oncologist. 2007; 12(12): 1425–32.
Cillo U, Vitale A, Grigoletto F, et al. Prospective validation of the Barcelona clinic liver cancer staging system. J Hepatol. 2006; 44(4): 723–31.
Wada H, Eguchi H, Noda T, et al. Selection criteria for hepatic resection in intermediate-stage (BCLC stage B) multiple hepatocellular carcinoma. Surgery 2016; 160(5): 1227–35.
Bhandare MS, Patkar S, Shetty N, et al. Liver resection for HCC outside the BCLC criteria. Langenbecks Arch Surg. 2018; 403(1): 37–44.
Moris D, Felekouras E. Ignore reality but not the consequences of its ignorance: Broaden guidelines in surgery of hepatocellular carcinoma. Hepatology. 2017; 65(5): 1772–3.
Guo H, Wu T, Lu Q, et al. Surgical resection improves long-term survival of patients with hepatocellular carcinoma across different Barcelona Clinic Liver Cancer stages. Cancer Manag Res. 2018; 10: 361–9.
Tsilimigras DI, Bagante F, Moris D, Merath K, Paredes AZ, Sahara K, Ratti F, Marques HP, Soubrane O, Lam V, Poultsides GA. Defining the chance of cure after resection for hepatocellular carcinoma within and beyond the Barcelona clinic liver cancer guidelines: A multi-institutional analysis of 1,010 patients. Surgery. 2019;166(6):967–74.
Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg. 2005; 12(5): 351–5.
Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009; 250(2): 187–96.
Clavien PA, Vetter D, Staiger RD, et al. The comprehensive complication index (CCI(R)): added value and clinical perspectives 3 years “down the line”. Ann Surg. 2017; 265(6): 1045–50.
Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien PA. The comprehensive complication index: a novel continuous scale to measure surgical morbidity. Ann Surg. 2013; 258(1): 1–7.
Ng KK, Vauthey JN, Pawlik TM, et al. Is hepatic resection for large or multinodular hepatocellular carcinoma justified? results from a multi-institutional database. Ann Surg Oncol. 2005; 12(5): 364–73.
Pawlik TM, Poon RT, Abdalla EK, et al. Critical appraisal of the clinical and pathologic predictors of survival after resection of large hepatocellular carcinoma. Arch Surg. 2005; 140(5): 450–7; discussion 7–8.
Pandey D, Lee KH, Wai CT, Wagholikar G, Tan KC. Long term outcome and prognostic factors for large hepatocellular carcinoma (10 cm or more) after surgical resection. Ann Surg Oncol. 2007; 14(10): 2817–23.
Tsilimigras DI, Bagante F, Sahara K, et al. Prognosis after resection of barcelona clinic liver cancer (BCLC) stage 0, A, and B hepatocellular carcinoma: a comprehensive assessment of the current BCLC classification. Ann Surg Oncol. 2019.
Moris D, Tsilimigras DI, Kostakis ID, et al. Anatomic versus non-anatomic resection for hepatocellular carcinoma: A systematic review and meta-analysis. Eur J Surg Oncol. 2018; 44(7): 927–38.
Hyun MH, Lee YS, Kim JH, et al. Hepatic resection compared to chemoembolization in intermediate- to advanced-stage hepatocellular carcinoma: a meta-analysis of high-quality studies. Hepatology 2018; 68(3): 977–93.
Lim C, Salloum C, Osseis M, et al. Short-term outcomes following hepatectomy for hepatocellular carcinoma within and beyond the BCLC guidelines: a prospective study. HPB (Oxford), 2018; 20(3): 222–30.
Moris D, Ronnekleiv-Kelly S, Kostakis ID, et al. Operative Results and oncologic outcomes of associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) versus two-stage hepatectomy (TSH) in patients with unresectable colorectal liver metastases: A systematic review and meta-analysis. World J Surg. 2018; 42(3): 806–15.
She WH, Chok K. Strategies to increase the resectability of hepatocellular carcinoma. World J Hepatol. 2015; 7(18): 2147–54.
European Association For The Study Of The L, European Organisation For R, Treatment Of C. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2012; 56(4): 908–43.
Kim H, Ahn SW, Hong SK, et al. Survival benefit of liver resection for Barcelona Clinic Liver Cancer stage B hepatocellular carcinoma. Br J Surg. 2017; 104(8): 1045-52.
Labgaa I, Demartines N, Melloul E. Surgical resection versus transarterial chemoembolization for intermediate stage hepatocellular carcinoma (BCLC-B): an unsolved question. Hepatology. 2019; 69(2): 923.
Mo DC, Jia RR, Zhong JH. Hepatic resection compared to chemoembolization in intermediate to advanced-stage HCC: a comment for moving forward. Hepatolog.y 2018.
Chang WT, Kao WY, Chau GY, et al. Hepatic resection can provide long-term survival of patients with non-early-stage hepatocellular carcinoma: extending the indication for resection? Surgery. 2012; 152(5): 809–20.
Torzilli G, Belghiti J, Kokudo N, et al. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: is it adherent to the EASL/AASLD recommendations?: an observational study of the HCC East-West study group. Ann Surg 2013; 257(5): 929–37.
Xu XF, Xing H, Han J, et al. Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: A multicenter study from China. JAMA Surg 2019; 154(3): 209–17.
Tsilimigras DI, Sahara K, Moris D, et al. Effect of surgical margin width on patterns of recurrence among patients undergoing R0 hepatectomy for T1 hepatocellular carcinoma: An international multi-institutional analysis. J Gastrointest Surg. 2019.
Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg. 2015; 261(5): 947–55.
Xu XF, Xing H, Han J, et al. Risk factors, patterns, and outcomes of late recurrence after liver resection for hepatocellular carcinoma: a multicenter study from China. JAMA Surg. 2018.154(3), 209-217
Imamura H, Matsuyama Y, Tanaka E, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003; 38(2): 200–7.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Tsilimigras, D.I., Bagante, F., Moris, D. et al. Recurrence Patterns and Outcomes after Resection of Hepatocellular Carcinoma within and beyond the Barcelona Clinic Liver Cancer Criteria. Ann Surg Oncol 27, 2321–2331 (2020). https://doi.org/10.1245/s10434-020-08452-3