The role of resection in hepatocellular carcinoma BCLC stage B: A multi-institutional patient-level meta-analysis and systematic review.


Journal

Langenbeck's archives of surgery
ISSN: 1435-2451
Titre abrégé: Langenbecks Arch Surg
Pays: Germany
ID NLM: 9808285

Informations de publication

Date de publication:
13 Sep 2024
Historique:
received: 18 03 2024
accepted: 01 09 2024
medline: 13 9 2024
pubmed: 13 9 2024
entrez: 13 9 2024
Statut: epublish

Résumé

The Barcelona Clinic Liver Cancer (BCLC) staging schema is widely used for hepatocellular carcinoma (HCC) treatment. In the updated recommendations, HCC BCLC stage B can become candidates for transplantation. In contrast, hepatectomy is currently not recommended. This systematic review includes a multi-institutional meta-analysis of patient-level data. Survival, postoperative mortality, morbidity and patient selection criteria for liver resection and transplantation in BCLC stage B are explored. All clinical studies reporting HCC patients with BCLC stage B undergoing liver resection or transplantation were included. A total of 31 studies with 3163 patients were included. Patient level data was available for 580 patients from 9 studies (423 after resection and 157 after transplantation). The overall survival following resection was 50 months and recurrence-free survival was 15 months. Overall survival after transplantation was not reached and recurrence-free survival was 45 months. The major complication rate after resection was 0.11 (95%-CI, 0.0-0.17) with the 90-day mortality rate of 0.03 (95%-CI, 0.03-0.08). Child-Pugh A (93%), minor resection (60%), alpha protein level less than 400 (64%) were common in resected patients. Resected patients were mostly outside the Milan criteria (99%) with mean tumour number of 2.9. Studies reporting liver transplantation in BCLC stage B were scarce. Liver resection can be performed safely in selected patients with HCC BCLC stage B, particularly if patients present with preserved liver function. No conclusion can done on liver transplantation due to scarcity of reported studies.

Identifiants

pubmed: 39269544
doi: 10.1007/s00423-024-03466-x
pii: 10.1007/s00423-024-03466-x
doi:

Types de publication

Journal Article Systematic Review Meta-Analysis

Langues

eng

Sous-ensembles de citation

IM

Pagination

277

Informations de copyright

© 2024. The Author(s).

Références

El-Serag HB, Mason AC (1999) Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340(10):745–750
pubmed: 10072408 doi: 10.1056/NEJM199903113401001
Hyun MH, Lee YS, Kim JH, Lee CU, Jung YK, Seo YS et al (2018) Hepatic resection compared to chemoembolization in intermediate- to advanced-stage hepatocellular carcinoma: a meta-analysis of high-quality studies. Hepatology 68(3):977–993
pubmed: 29543988 doi: 10.1002/hep.29883
Reig M, Forner A, Rimola J, Ferrer-Fabrega J, Burrel M, Garcia-Criado A et al (2022) BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol 76(3):681–693
pubmed: 34801630 doi: 10.1016/j.jhep.2021.11.018
Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM et al (2018) Diagnosis, staging, and management of Hepatocellular Carcinoma: 2018 Practice Guidance by the American Association for the study of Liver diseases. Hepatology 68(2):723–750
pubmed: 29624699 doi: 10.1002/hep.29913
European Association for the Study of the Liver (2018) Electronic address eee, European Association for the study of the L. EASL Clinical Practice guidelines: management of hepatocellular carcinoma. J Hepatol 69(1):182–236
doi: 10.1016/j.jhep.2018.03.019
Tschuor C, Ferrarese A, Kuemmerli C, Dutkowski P, Burra P, Clavien PA (2019) Liver allocation study G. Allocation of liver grafts worldwide - is there a best system? J Hepatol 71(4):707–718
pubmed: 31199941 doi: 10.1016/j.jhep.2019.05.025
Peng Z, Fan W, Zhu B, Wang G, Sun J, Xiao C et al (2022) Lenvatinib Combined with Transarterial Chemoembolization as First-Line treatment for Advanced Hepatocellular Carcinoma: a phase III, Randomized Clinical Trial (LAUNCH). J Clin Oncol. :JCO2200392
Kudo M, Finn RS, Qin S, Han KH, Ikeda K, Piscaglia F et al (2018) Lenvatinib versus Sorafenib in first-line treatment of patients with unresectable hepatocellular carcinoma: a randomised phase 3 non-inferiority trial. Lancet 391(10126):1163–1173
pubmed: 29433850 doi: 10.1016/S0140-6736(18)30207-1
Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XP et al (2014) Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg 260(2):329–340
pubmed: 24096763 doi: 10.1097/SLA.0000000000000236
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700
pubmed: 19622552 pmcid: 2714672 doi: 10.1136/bmj.b2700
Granholm A, Alhazzani W, Moller MH (2019) Use of the GRADE approach in systematic reviews and guidelines. Br J Anaesth 123(5):554–559
pubmed: 31558313 doi: 10.1016/j.bja.2019.08.015
The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses [updated 17.07.2024. https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
Cochrane Handbook for Systematic Reviews of Interventions (access date: 26.12.2020) [ https://training.cochrane.org/handbook/current/chapter-10
Clavien PA, Petrowsky H, DeOliveira ML, Graf R (2007) Strategies for safer liver surgery and partial liver transplantation. N Engl J Med 356(15):1545–1559
pubmed: 17429086 doi: 10.1056/NEJMra065156
Torzilli G, Belghiti J, Kokudo N, Takayama T, Capussotti L, Nuzzo G et al (2013) 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 257(5):929–937
pubmed: 23426336 doi: 10.1097/SLA.0b013e31828329b8
Mazzaferro V, Sposito C, Zhou J, Pinna AD, De Carlis L, Fan J et al (2018) Metroticket 2.0 model for analysis of competing risks of death after liver transplantation for Hepatocellular Carcinoma. Gastroenterology 154(1):128–139
pubmed: 28989060 doi: 10.1053/j.gastro.2017.09.025
Bell R, Pandanaboyana S, Lodge JPA, Prasad KR, Jones R, Hidalgo E (2017) Primary liver resection for patients with cirrhosis and hepatocellular carcinoma: the role of surgery in BCLC early (A) and intermediate stages (B). Langenbecks Arch Surg 402(4):575–583
pubmed: 27456677 doi: 10.1007/s00423-016-1475-3
Di Sandro S, Centonze L, Pinotti E, Lauterio A, De Carlis R, Romano F et al (2019) Surgical and oncological outcomes of hepatic resection for BCLC-B hepatocellular carcinoma: a retrospective multicenter analysis among 474 consecutive cases. Updates Surg 71(2):285–293
pubmed: 30941704 doi: 10.1007/s13304-019-00649-w
Fang Q, Xie QS, Chen JM, Shan SL, Xie K, Geng XP, Liu FB (2019) Long-term outcomes after hepatectomy of huge hepatocellular carcinoma: a single-center experience in China. Hepatobiliary Pancreat Dis Int 18(6):532–537
pubmed: 31543313 doi: 10.1016/j.hbpd.2019.09.001
Garancini M, Nespoli S, Romano F, Uggeri F, Degrate L, Okolicsanyi S, Gianotti L (2018) Surgical management of hepatocellular carcinoma within and beyond BCLC indications in a middle volume center. J Visc Surg 155(4):275–282
pubmed: 29606603 doi: 10.1016/j.jviscsurg.2017.12.001
Jianyong L, Lunan Y, Wentao W, Yong Z, Bo L, Tianfu W et al (2014) Barcelona clinic liver cancer stage B hepatocellular carcinoma: transarterial chemoembolization or hepatic resection? Med (Baltim) 93(26):e180
doi: 10.1097/MD.0000000000000180
Kamiyama T, Orimo T, Wakayama K, Shimada S, Nagatsu A, Yokoo H et al (2017) Survival outcomes of hepatectomy for stage B hepatocellular carcinoma in the BCLC classification. World J Surg Oncol 15(1):156
pubmed: 28830473 pmcid: 5568344 doi: 10.1186/s12957-017-1229-x
Kamo N, Kaido T, Yagi S, Okajima H, Uemoto S (2018) Liver transplantation for Intermediate-Stage Hepatocellular Carcinoma. Liver Cancer 7(2):179–189
pubmed: 29888207 pmcid: 5985555 doi: 10.1159/000487058
Kariyama K, Nouso K, Wakuta A, Oonishi A, Toyoda H, Tada T et al (2020) Treatment of Intermediate-Stage Hepatocellular Carcinoma in Japan: position of curative therapies. Liver Cancer 9(1):41–49
pubmed: 32071908 doi: 10.1159/000502479
Kim H, Ahn SW, Hong SK, Yoon KC, Kim HS, Choi YR et al (2017) Survival benefit of liver resection for Barcelona Clinic Liver Cancer stage B hepatocellular carcinoma. Br J Surg 104(8):1045–1052
pubmed: 28480964 doi: 10.1002/bjs.10541
Kim JY, Sinn DH, Gwak GY, Choi GS, Saleh AM, Joh JW et al (2016) Transarterial chemoembolization versus resection for intermediate-stage (BCLC B) hepatocellular carcinoma. Clin Mol Hepatol 22(2):250–258
pubmed: 27377909 pmcid: 4946408 doi: 10.3350/cmh.2016.0015
Lin CT, Hsu KF, Chen TW, Yu JC, Chan DC, Yu CY 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(9):2155–2161
pubmed: 20407768 doi: 10.1007/s00268-010-0598-x
Lin CW, Chen YS, Lo GH, Hsu YC, Hsu CC, Wu TC et al (2020) Comparison of overall survival on surgical resection versus transarterial chemoembolization with or without radiofrequency ablation in intermediate stage hepatocellular carcinoma: a propensity score matching analysis. BMC Gastroenterol 20(1):99
pubmed: 32272898 pmcid: 7147026 doi: 10.1186/s12876-020-01235-w
Liu YW, Lin CC, Yong CC, Wang CC, Chen CL, Wang JH, Yen YH (2020) Prognosis after resection of single large hepatocellular carcinoma: results from an Asian high-volume liver surgery center. PLoS ONE 15(3):e0230897
pubmed: 32218593 pmcid: 7100934 doi: 10.1371/journal.pone.0230897
Matsukuma S, Sakamoto K, Tokuhisa Y, Tokumitsu Y, Matsui H, Kanekiyo S et al (2018) Outcomes following liver resection for multinodular Barcelona Clinic Liver Cancer-B hepatocellular carcinoma. Oncol Lett 16(5):6383–6392
pubmed: 30344760 pmcid: 6176380
Peng Y, Liu F, Xu H, Wei Y, Li B (2020) Is laparoscopic liver resection suitable for selected patients with BCLC stage B HCC? A propensity score-matched analysis. HPB: Official J Int Hepato Pancreato Biliary Association 22(4):595–602
doi: 10.1016/j.hpb.2019.08.016
Renner P, Schuhbaum J, Kroemer A, Zeman F, Loss M, Lang SA et al (2016) Morbidity of hepatic resection for intermediate and advanced hepatocellular carcinoma. Langenbecks Arch Surg 401(1):43–53
pubmed: 26627084 doi: 10.1007/s00423-015-1359-y
Torzilli G, Donadon M, Marconi M, Palmisano A, Del Fabbro D, Spinelli A et al (2008) Hepatectomy for stage B and stage C hepatocellular carcinoma in the Barcelona Clinic Liver Cancer classification: results of a prospective analysis. Arch Surg 143(11):1082–1090
pubmed: 19015467 doi: 10.1001/archsurg.143.11.1082
Tsilimigras DI, Bagante F, Moris D, Merath K, Paredes AZ, Sahara K et al (2019) 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 166(6):967–974
pubmed: 31606196 doi: 10.1016/j.surg.2019.08.010
Wada H, Eguchi H, Noda T, Ogawa H, Yamada D, Tomimaru Y et al (2016) Selection criteria for hepatic resection in intermediate-stage (BCLC stage B) multiple hepatocellular carcinoma. Surgery 160(5):1227–1235
pubmed: 27395761 doi: 10.1016/j.surg.2016.05.023
Wang X, Wang Z, Wu L (2016) Combined measurements of tumor number and size helps estimate the outcome of resection of Barcelona clinic liver cancer stage B hepatocellular carcinoma. BMC Surg 16:22
pubmed: 27094483 pmcid: 4837634 doi: 10.1186/s12893-016-0135-4
Wei S, Hao X, Zhan D, Xiong M, Li K, Chen X, Huang Z (2011) Are surgical indications of Barcelona Clinic Liver Cancer staging classification justified? J Huazhong Univ Sci Technolog Med Sci 31(5):637
pubmed: 22038353 doi: 10.1007/s11596-011-0574-1
Wei WX, Yang ZS, Lu LH, Li J, Lei ZQ, Wang K et al (2018) Long-term survival after partial hepatectomy for sub-stage patients with intermediate stage hepatocellular carcinoma. Int J Surg 56:256–263
pubmed: 29935368 doi: 10.1016/j.ijsu.2018.06.020
Berardi G, Morise Z, Sposito C, Igarashi K, Panetta V, Simonelli I et al (2020) Development of a nomogram to predict outcome after liver resection for hepatocellular carcinoma in child-pugh B cirrhosis. J Hepatol 72(1):75–84
pubmed: 31499131 doi: 10.1016/j.jhep.2019.08.032
Di Benedetto F, Magistri P, Di Sandro S, Sposito C, Oberkofler C, Brandon E et al (2023) Safety and efficacy of robotic vs Open Liver Resection for Hepatocellular Carcinoma. JAMA Surg 158(1):46–54
pubmed: 36416833 doi: 10.1001/jamasurg.2022.5697
Lim C, Salloum C, Osseis M, Lahat E, Gomez-Gavara C, Compagnon P et al (2018) Short-term outcomes following hepatectomy for hepatocellular carcinoma within and beyond the BCLC guidelines: a prospective study. HPB: Official J Int Hepato Pancreato Biliary Association 20(3):222–230
doi: 10.1016/j.hpb.2017.08.027
Lopez-Lopez V, Brusadin R, Lopez-Conesa A, Capel A, Navarro-Barrios A, Cayuela V et al (2021) Preoperative transarterial chemoembolization for laparoscopic liver resection in child A cirrhotic patients with hepatocellular carcinoma. Langenbecks Arch Surg 406(3):763–771
pubmed: 33411038 doi: 10.1007/s00423-020-02056-x
Ramaswami R, Pinato DJ, Kubota K, Ishizuka M, Arizumi T, Kudo M et al (2016) Prognostic sub-classification of intermediate-stage hepatocellular carcinoma: a multicenter cohort study with propensity score analysis. Med Oncol 33(10):114
pubmed: 27601241 pmcid: 5013141 doi: 10.1007/s12032-016-0827-8
Villamonte M, Burdio F, Pueyo E, Andaluz A, Moll X, Berjano E et al (2022) The impact of additional margin coagulation with radiofrequency in liver resections with subcentimetric margin: can we improve the oncological results? A propensity score matching study. Eur J Surg Oncol 48(1):82–88
pubmed: 34148824 doi: 10.1016/j.ejso.2021.06.008
Weinmann A, Koch S, Sprinzl M, Kloeckner R, Schulze-Bergkamen H, Duber C et al (2015) Survival analysis of proposed BCLC-B subgroups in hepatocellular carcinoma patients. Liver Int 35(2):591–600
pubmed: 25290314 doi: 10.1111/liv.12696

Auteurs

Victor Lopez-Lopez (V)

Department of General, Visceral and Transplantation Surgery, Clinic and University Hospital Virgen de La Arrixaca, IMIB-ARRIXACA, El Palmar, Murcia, Spain.

Fabian Kalt (F)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Jian-Hong Zhong (JH)

Department of Hepatobiliary Surgery, Guangxi Medical University Cancer Hospital, Nanning, 530021, China.

Cristiano Guidetti (C)

Hepato-Pancreato-Biliary Surgery and Liver Transplantation Unit, University of Modena and Reggio Emilia, Modena, Italy.

Paolo Magistri (P)

Hepato-Pancreato-Biliary Surgery and Liver Transplantation Unit, University of Modena and Reggio Emilia, Modena, Italy.

Fabrizio Di Benedetto (F)

Hepato-Pancreato-Biliary Surgery and Liver Transplantation Unit, University of Modena and Reggio Emilia, Modena, Italy.

Arndt Weinmann (A)

Department of Internal Medicine I, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Jens Mittler (J)

Department of General, Visceral and Transplant Surgery, University Medical Center, Johannes Gutenberg-University Mainz, 55131, Mainz, Germany.

Hauke Lang (H)

Department of General, Visceral and Transplant Surgery, University Medical Center, Johannes Gutenberg-University Mainz, 55131, Mainz, Germany.

Rohini Sharma (R)

Department of Surgery and Cancer, Imperial College London, London, UK.

Vithayathil Mathew K (VM)

Department of Surgery and Cancer, Imperial College London, London, UK.

Samir Tariq (S)

Department of Surgery and Cancer, Imperial College London, London, UK.

Patricia Sánchez-Velázquez (P)

Division of Hepatobliary and pancreatic Surgery, Hospital del Mar, Universitat Pompeu Fabra, IMIM, Barcelona, Spain.

Gianluca Rompianesi (G)

Department of Clinical Medicine and Surgery, Federico II University, Naples, Italy.

Roberto Ivan Troisi (RI)

Department of Clinical Medicine and Surgery, Federico II University, Naples, Italy.

Concepción Gómez-Gavara (C)

Department HPB and Transplantation Surgery, Hospital Vall d'Hebron, Universitat Autònoma de Barcelona, Barcelona, Spain.

Mar Dalmau (M)

Department HPB and Transplantation Surgery, Hospital Vall d'Hebron, Universitat Autònoma de Barcelona, Barcelona, Spain.

Francisco Jose Sanchez-Romero (FJ)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Camilo Llamoza (C)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Christoph Tschuor (C)

Department of Surgery and Transplantation, Rigshospitalet Copenhagen University Hospital, Blegdamsvej 9 Copenhagen Ø, Copenhagen, 2100, Denmark.

Uluk Deniz (U)

Department of Surgery, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
Department of General, Visceral and Transplantation Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Georg Lurje (G)

Department of Surgery, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
Department of General, Visceral and Transplantation Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Peri Husen (P)

Department of General, Visceral and Transplantation Surgery, Heidelberg University Hospital, Heidelberg, Germany.

Sandro Hügli (S)

Department of General, Visceral and Transplantation Surgery, Clinic and University Hospital Virgen de La Arrixaca, IMIB-ARRIXACA, El Palmar, Murcia, Spain.

Jan Philipp Jonas (JP)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Fabian Rössler (F)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Philipp Kron (P)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Michaela Ramser (M)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Pablo Ramirez (P)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Kuno Lehmann (K)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland.

Ricardo Robles-Campos (R)

Department of General, Visceral and Transplantation Surgery, Clinic and University Hospital Virgen de La Arrixaca, IMIB-ARRIXACA, El Palmar, Murcia, Spain.

Dilmurodjon Eshmuminov (D)

Department of Surgery and Transplantation, University Hospital Zurich and University of Zurich, Raemistrasse 100, Zurich, CH-8091, Switzerland. Dilmurodjon.eshmuminov@usz.ch.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH