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Open Versus Laparoscopic Right Hepatectomy for Hepatocellular Carcinoma Following Sequential TACE–PVE: A Multicentric Comparative Study

  • Hepatobiliary Tumors
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Abstract

Background

Right hepatectomy (RH) for hepatocellular carcinoma (HCC) is ideally preceded by transcatheter arterial chemoembolization (TACE) and portal vein embolization (PVE). Laparoscopic approach improves short-term outcome and textbook outcome (TO), which reflects the “ideal” surgical outcome, after RH. However, laparoscopic RH on an underlying diseased liver and after TACE/PVE remains a challenging procedure. The aim of this study was to compare the outcomes in patients who underwent laparoscopic liver resection (LLR) or open liver resection (OLR) following TACE/PVE.

Patients and Methods

All patients with HCC who underwent RH after TACE/PVE in five French centers were retrospectively included. Outcomes were compared between the LLR group and the OLR group using propensity score matching (PSM). Quality of surgical care was defined by TO.

Results

Between 2005 and 2019, 117 patients were included (41 in LLR group, 76 in OLR group). Overall morbidity was comparable (51% versus 53%, p = 0.24). In LLR group, TO was completed in 66% versus 37% in OLR group (p = 0.02). LLR and absence of clamping were the only factors associated with TO completion [hazard ratio (HR) 4.27, [1.77–10.28], p = 0.001]. After PSM, 5-year overall survival (OS) and progression-free survival (PFS) were 55% in matched LLR versus 77% in matched OLR, p = 0.35, and 13% in matched LLR versus 17% in matched OLR, p = 0.97. TO completion was independently associated with a better 5-year OS (65.2% versus 42.5%, p = 0.007).

Conclusion

Major LLR after TACE/PVE should be considered as a valuable option in expert centers to increase the chance of TO, the latter being associated with a better 5-year OS.

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References

  1. Au JS, Frenette CT. Management of hepatocellular carcinoma: current status and future directions. Gut Liver juill. 2015;9(4):437–48.

    Article  CAS  Google Scholar 

  2. Llovet JM, Fuster J, Bruix J. Barcelona-Clínic liver cancer group. The Barcelona approach: diagnosis, staging, and treatment of hepatocellular carcinoma. Liver Transpl. 2004;10:S115-120.

    Article  PubMed  Google Scholar 

  3. Ogata S, Belghiti J, Farges O, Varma D, Sibert A, Vilgrain V. Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma. Br J Surg sept. 2006;93(9):1091–8.

    Article  CAS  Google Scholar 

  4. Glantzounis GK, Tokidis E, Basourakos SP, Ntzani EE, Lianos GD, Pentheroudakis G. The role of portal vein embolization in the surgical management of primary hepatobiliary cancers. A systematic review. Eur J Surg Onco. 2017;43(1):32–41.

    Article  CAS  Google Scholar 

  5. Shindoh J, Tzeng D, CW, Vauthey JN. Portal vein embolization for hepatocellular carcinoma. Liver Cancer. 2012;1(3–4):159–67.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kishi Y, Vauthey JN. Issues to be considered to address the future liver remnant prior to major hepatectomy. Surg Today. 2020;51:472–84.

    Article  PubMed  Google Scholar 

  7. Grandhi MS, Kim AK, Ronnekleiv-Kelly SM, Kamel IR, Ghasebeh MA, Pawlik TM. Hepatocellular carcinoma: from diagnosis to treatment. Surg Oncol. 2016;25(2):74–85.

    Article  PubMed  Google Scholar 

  8. Sarpel U, Hefti MM, Wisnievsky JP, Roayaie S, Schwartz ME, Labow DM. Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: case-matched analysis. Ann Surg Oncol juin. 2009;16(6):1572–7.

    Article  CAS  Google Scholar 

  9. Belli G, Limongelli P, Fantini C, D’Agostino A, Cioffi L, Belli A, et al. Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg sept. 2009;96(9):1041–8.

    Article  CAS  Google Scholar 

  10. Yoon YI, Kim KH, Cho HD, Kwon JH, Jung DH, Park GC, et al. Long-term perioperative outcomes of pure laparoscopic liver resection versus open liver resection for hepatocellular carcinoma: a retrospective study. Surg Endosc. 2020;34(2):796–805.

    Article  PubMed  Google Scholar 

  11. Hobeika C, Fuks D, Cauchy F, Goumard C, Soubrane O, Gayet B, et al. Impact of cirrhosis in patients undergoing laparoscopic liver resection in a nationwide multicentre survey. Br J Surg. 2020;107(3):268–77.

    Article  CAS  PubMed  Google Scholar 

  12. Prodeau M, Drumez E, Duhamel A, Vibert E, Farges O, Lassailly G, et al. An ordinal model to predict the risk of symptomatic liver failure in patients with cirrhosis undergoing hepatectomy. J Hepatol. 2019;71(5):920–9.

    Article  PubMed  Google Scholar 

  13. Duarte VC, Coelho FF, Valverde A, Danoussou D, Kruger JAP, Zuber K, et al. Minimally invasive versus open right hepatectomy: comparative study with propensity score matching analysis. BMC Surg. 2020;20(1):260.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, et al. The southampton consensus guidelines for laparoscopic liver surgery: From indication to implementation. Ann Surg. 2018;268(1):11–8.

    Article  PubMed  Google Scholar 

  15. Galle PR, Forner A, Llovet JM, Mazzaferro V, Piscaglia F, Raoul JL, et al. EASL clinical practice guidelines: Management of hepatocellular carcinoma. J Hepatol. 2018;69(1):182–236.

    Article  Google Scholar 

  16. Görgec B, Benedetti Cacciaguerra A, Lanari J, Russolillo N, Cipriani F, Aghayan D, et al. Assessment of textbook outcome in laparoscopic and open liver surgery. JAMA Surg. 2021;156(8):e212064.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kolfschoten NE, Kievit J, Gooiker GA, van Leersum NJ, Snijders HS, Eddes EH, et al. Focusing on desired outcomes of care after colon cancer resections; hospital variations in « textbook outcome ». Eur J Surg Oncol. 2013;39(2):156–63.

    Article  CAS  PubMed  Google Scholar 

  18. Merath K, Chen Q, Bagante F, Alexandrescu S, Marques HP, Aldrighetti L, et al. A multi-institutional international analysis of textbook outcomes among patients undergoing curative-intent resection of intrahepatic cholangiocarcinoma. JAMA Surg. 2019;154(6):e190571.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Tsilimigras DI, Mehta R, Merath K, Bagante F, Paredes AZ, Farooq A, et al. Hospital variation in textbook outcomes following curative-intent resection of hepatocellular carcinoma: an international multi-institutional analysis. HPB sept. 2020;22(9):1305–13.

    Article  Google Scholar 

  20. Hobeika C, Nault JC, Barbier L, Schwarz L, Lim C, Laurent A, et al. Influence of surgical approach and quality of resection on the probability of cure for early-stage HCC occurring in cirrhosis. JHEP Rep Innov Hepatol déc. 2020;2(6):100153.

    Article  Google Scholar 

  21. Hobeika C, Fuks D, Cauchy F, Goumard C, Gayet B, Laurent A, et al. Benchmark performance of laparoscopic left lateral sectionectomy and right hepatectomy in expert centers. J Hepatol. 2020;73(5):1100–8.

    Article  PubMed  Google Scholar 

  22. May BJ, Madoff DC. Portal vein embolization: rationale, technique, and current application. Semin Interv Radiol juin. 2012;29(2):81–9.

    Article  Google Scholar 

  23. Balzan S, Belghiti J, Farges O, Ogata S, Sauvanet A, Delefosse D, et al. The « 50–50 criteria » on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg. 2005;242(6):824–8 (Discussion 828-829).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Goumard C, Komatsu S, Brustia R, Fartoux L, Soubrane O, Scatton O. Technical feasibility and safety of laparoscopic right hepatectomy for hepatocellular carcinoma following sequential TACE-PVE: a comparative study. Surg Endosc. 2017;31(5):2340–9.

    Article  PubMed  Google Scholar 

  25. Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice guidance by the american association for the study of liver diseases. Hepatol Baltim Md août. 2018;68(2):723–50.

    Article  Google Scholar 

  26. de Franchis R, Baveno. VI faculty expanding consensus in portal hypertension: report of the Baveno VI consensus workshop: stratifying risk and individualizing care for portal hypertension. J Hepatol. 2015;63(3):743–52.

    PubMed  Google Scholar 

  27. European Association for Study of Liver. Asociacion Latinoamericana para el Estudio del Higado EASL-ALEH clinical practice guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol. 2015;63(1):237–64.

    Article  Google Scholar 

  28. Pang YY. The Brisbane 2000 terminology of liver anatomy and resections. HPB 2000; 2:333-39. HPB. 2002;4(2):99; author reply 99-100.

  29. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg août. 2004;240(2):205–13.

    Article  Google Scholar 

  30. Rahbari NN, Garden OJ, Padbury R, Brooke-Smith M, Crawford M, Adam R, et al. Posthepatectomy liver failure: a definition and grading by the international study group of liver surgery (ISGLS). Surgery mai. 2011;149(5):713–24.

    Article  Google Scholar 

  31. Rahbari NN, Garden OJ, Padbury R, Maddern G, Koch M, Hugh TJ, et al. Post-hepatectomy haemorrhage: a definition and grading by the International study group of liver surgery (ISGLS). HPB. 2011;13(8):528–35.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, et al. Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the international study group of liver surgery. Surgery mai. 2011;149(5):680–8.

    Article  Google Scholar 

  33. Merath K, Chen Q, Bagante F, Beal E, Akgul O, Dillhoff M, et al. Textbook outcomes among medicare patients undergoing hepatopancreatic surgery. Ann Surg. 2020;271(6):1116–23.

    Article  PubMed  Google Scholar 

  34. Tsilimigras DI, Sahara K, Moris D, Mehta R, Paredes AZ, Ratti F, et al. Assessing textbook outcomes following liver surgery for primary liver cancer over a 12-year time period at major hepatobiliary centers. Ann Surg Oncol. 2020;27(9):3318–27.

    Article  PubMed  Google Scholar 

  35. Goh BKP, Syn N, Lee SY, Koh YX, Teo JY, Kam JH, et al. Impact of liver cirrhosis on the difficulty of minimally-invasive liver resections: a 1:1 coarsened exact-matched controlled study. Surg Endosc [Internet]. 24 sept 2020 [cité 16 nov 2020]; Disponible sur: https://doi.org/10.1007/s00464-020-08018-0

  36. Twaij A, Pucher PH, Sodergren MH, Gall T, Darzi A, Jiao LR. Laparoscopic vs open approach to resection of hepatocellular carcinoma in patients with known cirrhosis: systematic review and meta-analysis. World J Gastroenterol. 2014;20(25):8274–81.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kluger MD, Vigano L, Barroso R, Cherqui D. The learning curve in laparoscopic major liver resection. J Hepato-Biliary-Pancreat Sci févr. 2013;20(2):131–6.

    Article  Google Scholar 

  38. Komatsu S, Scatton O, Goumard C, Sepulveda A, Brustia R, Perdigao F, et al. Development process and technical aspects of laparoscopic hepatectomy: learning curve based on 15 years of experience. J Am Coll Surg mai. 2017;224(5):841–50.

    Article  Google Scholar 

  39. Sultana A, Nightingale P, Marudanayagam R, Sutcliffe RP. Evaluating the learning curve for laparoscopic liver resection: a comparative study between standard and learning curve CUSUM. HPB. 2019;21(11):1505–12.

    Article  PubMed  Google Scholar 

  40. Pekolj J, Clariá Sánchez R, Salceda J, Maurette RJ, Schelotto PB, Pierini L, et al. Laparoscopic liver resection: a south american experience with 2887 cases. World J Surg. 2020;44(11):3868–74.

    Article  CAS  PubMed  Google Scholar 

  41. Cauchy F, Fuks D, Nomi T, Schwarz L, Barbier L, Dokmak S, et al. Risk factors and consequences of conversion in laparoscopic major liver resection. Br J Surg juin. 2015;102(7):785–95.

    Article  CAS  Google Scholar 

  42. Dokmak S, Ftériche FS, Borscheid R, Cauchy F, Farges O, Belghiti J. 2012 Liver resections in the 21st century: we are far from zero mortality. HPB. 2013;15(11):908–15.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Pan Y, Xia S, Cai J, Chen K, Cai X. Efficacy of laparoscopic hepatectomy versus open surgery for hepatocellular carcinoma with cirrhosis: a meta-analysis of case-matched studies. Front Oncol [Internet]. 7 mai 2021 [cité 3 juin 2021];11. Disponible sur: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8139628/

  44. Tsilimigras DI, Bagante F, Sahara K, Moris D, Hyer JM, Wu L, 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;26(11):3693–700.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Digestive, Hepato-Biliary and Pancreatic Surgery and Liver Transplantation, AP-HP Pitié-Salpêtrière Hospital, Paris, France

    Célia Turco MD, Tu Nguyen MD, Olivier Scatton MD, PhD & Claire Goumard MD, PhD

  2. Sorbonne Université, Centre de Recherche Saint Antoine, INSERM UMRS-938, Institute of Cardiometabolism and Nutrition (ICAN), Paris, France

    Célia Turco MD, Olivier Scatton MD, PhD & Claire Goumard MD, PhD

  3. Department of Hepato-Biliary, Liver Transplantation, and Pancreatic Surgery, Hospital Beaujon, Clichy, France

    Christian Hobeika MD, PhD, François Cauchy MD, PhD & Olivier Soubrane MD, PhD

  4. AP-HP Hôpital Paul Brousse, Centre Hépato-Biliaire, Université Paris Saclay, Inserm U 935, Villejuif, France

    Marc-Antoine Allard MD, PhD

  5. Service de Chirurgie Digestive, Oncologique, Endocrinienne et Transplantation Hépatique, CHRU Hôpital Trousseau, Chambray, Tours, France

    Nicolas Tabchouri MD, Louise Barbier MD, PhD & Ephrem Salamé MD, PhD

  6. Department of Digestive and Hepato-Pancreatico-Biliary Surgery, Henri Mondor University Hospital, APHP, Créteil, France

    Raffaele Brustia MD, PhD, Daniel Cherqui MD, PhD & Eric Vibert MD, PhD

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  1. Célia Turco MD
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Contributions

Study conception and design of the study: CG, OSc. Acquisition of data: CT, TN, CH, MAA, NT, RB. Analysis and interpretation of data: CT, CG, OSc. Drafting the article: CT, CG, OSc. Critical revision: OSc, OS, DC, ES, FC, LB Final approval of the version to be submitted: OSc., OS, DC, ES, FC, LB, CT, TN, CH, MAA, NT, RB.

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Correspondence to Claire Goumard MD, PhD.

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Turco, C., Hobeika, C., Allard, MA. et al. Open Versus Laparoscopic Right Hepatectomy for Hepatocellular Carcinoma Following Sequential TACE–PVE: A Multicentric Comparative Study. Ann Surg Oncol 30, 6615–6625 (2023). https://doi.org/10.1245/s10434-023-13752-5

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