Surgery for hepatocellular carcinoma and intrahepatic cholangiocarcinoma: milestone changes in the last two decades potentially affecting current guidelines

Abstract

The aim of this review is to describe the relevance of minimally invasive liver resection (MILR) for the treatment of most common primary liver tumors. The uptake has been slow but steady, and thus MILR has become a well-established field of hepatobiliary surgery and is considered a landmark change of the past 30 years. There is evidence that the advantage of MILR regarding specific complications of liver surgery for HCC (reduced incidence of postoperative hepatic decompensation and ascites) can be a tool to potentially expand the indications to surgical treatment. Evidence for intrahepatic cholangiocarcinoma is early and exploratory; however, it is beginning to be documented that the fundamental principles of surgical oncology for this tumor can be respected while offering patients the advantages of minimal invasiveness.

Keywords

Hepatocellular carcinoma / intrahepatic cholangiocarcinoma / minimally invasive hepatectomy / laparoscopic liver resection

References

[1] Reich H,DeCaprio J.Laparoscopic excision of benign liver lesions.Obstet Gynecol1991;78:956-8.

[2] Cipriani F,Paganelli M,Catena M.Laparoscopic or open approaches for posterosuperior and anterolateral liver resections?.HPB2019;21:1676-86

[3] Beard RE,Khan S,Tsung A.Laparoscopic liver resection for hepatocellular carcinoma in early and advanced cirrhosis.HPB2018; 20:521-529.

[4] Dagher I,Tzanis D.International experience for laparoscopic major liver resection.J Hepatobiliary Pancreat Sci2014;21:732-6

[5] Goumard C,Brustia R,Soubrane O.Technical feasibility and safety of laparoscopic right hepatectomy for hepatocellular carcinoma following sequential TACE-PVE: a comparative study.Surg Endosc2017;31:2340-9

[6] Pulitanò C,Bellio L,Ferla G.A risk score for predicting perioperative blood transfusion in liver surgery.Br J Surg2007;94:860-5

[7] Dam RM.orANGE II Study GroupOpen versus laparoscopic left lateral hepatic sectionectomy within an enhanced recovery ERAS^® programme (orANGE II-trial): study protocol for a randomised controlled trial.Trials2012;13:54 PMCID:PMC3409025

[8] Cipriani F,Fiorentini G,Paganelli M.Pure laparoscopic right hepatectomy: a risk score for conversion for the paradigm of difficult laparoscopic liver resections. a single centre case series.Int J Surg2020;82:108-15

[9] Yoh T,Kawai T.Laparoscopic right hepatectomy using the caudal approach is superior to open right hepatectomy with anterior approach and liver hanging maneuver: a comparison of short-term outcomes.Surg Endosc2020;34:636-45

[10] Ban D,Ito H.A novel difficulty scoring system for laparoscopic liver resection.J Hepatobiliary Pancreat Sci2014;21:745-53

[11] Cipriani F,Aldrighetti L.Laparoscopic liver resections at the gates of 2020: a stand-alone field of hepatobiliary surgery.Hepatobiliary Surg Nutr2020;9:371-3 PMCID:PMC7262607

[12] Reig M,Rimola J.BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update.J Hepatol2022;76:681-93 PMCID:PMC8866082

[13] Aldrighetti L,Pulitanò C.Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results.J Surg Oncol2010;102:82-6

[14] Tranchart H,Lainas P.Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study.Surg Endosc2010;24:1170-6

[15] Twaij A,Sodergren MH,Darzi A.Laparoscopic vs. open approach to resection of hepatocellular carcinoma in patients with known cirrhosis: systematic review and meta-analysis.World J Gastroenterol2014;20:8274-81 PMCID:PMC4081703

[16] Chen J,Zhang Y,Wang XB.The safety and efficacy of laparoscopic and open hepatectomy in hepatocellular carcinoma patients with liver cirrhosis: a systematic review.Int J Clin Exp Med2015;8:20679-89. PMCID:PMC4723836

[17] Coletta D,Parrino C.Laparoscopic liver surgery: what are the advantages in patients with cirrhosis and portal hypertension?.J Laparoendosc Adv Surg Tech A2020;30:1054-65

[18] Kabir T,Syn NL.Laparoscopic versus open resection of hepatocellular carcinoma in patients with cirrhosis: meta-analysis.Br J Surg2021;109:21-9

[19] Pan Y,Cai J,Cai X.Efficacy of laparoscopic hepatectomy versus open surgery for hepatocellular carcinoma with cirrhosis: a meta-analysis of case-matched studies.Front Oncol2021;11:652272 PMCID:PMC8139628

[20] Wang ZY,Sun LL.Laparoscopic versus open major liver resection for hepatocellular carcinoma: systematic review and meta-analysis of comparative cohort studies.BMC Cancer2019;19:1047 PMCID:PMC6833163

[21] Hao F,Li N,Wu H.Laparoscopic repeat hepatectomy versus conventional open repeat hepatectomy for recurrent hepatocellular carcinoma: a systematic review and meta-analysis.Front Oncol2022;12:960204 PMCID:PMC9521539

[22] Wang Q,Dai XM,Zhu Z.Laparoscopic versus open liver resection for hepatocellular carcinoma in elderly patients: systematic review and meta-analysis of propensity-score matched studies.Int J Surg2022;105:106821

[23] Guro H,Han HS,Choi Y.Current status of laparoscopic liver resection for hepatocellular carcinoma.Clin Mol Hepatol2016;22:212-8 PMCID:PMC4946407

[24] Chen K,Zhang B,Maher H.Laparoscopic versus open surgery for hepatocellular carcinoma: a meta-analysis of high-quality case-matched studies.Can J Gastroenterol Hepatol2018;2018:1746895 PMCID:PMC5852873

[25] Gaillard M,Dagher I.Laparoscopic liver resections for hepatocellular carcinoma: current role and limitations.World J Gastroenterol2014;20:4892-9 PMCID:PMC4009520

[26] Fretland AA,Postriganova N.Inflammatory response after laparoscopic versus open resection of colorectal liver metastases: data from the oslo-comet Trial.Medicine2015;94:e1786

[27] Ratti F,Fiorentini G,Paganelli M.Reappraisal of the advantages of laparoscopic liver resection for intermediate hepatocellular carcinoma within a stage migration perspective: propensity score analysis of the differential benefit.J Hepatobiliary Pancreat Sci2020;27:510-21

[28] Ciria R,Ocaña S.A systematic review and meta-analysis comparing the short- and long-term outcomes for laparoscopic and open liver resections for hepatocellular carcinoma: updated results from the european guidelines meeting on laparoscopic liver surgery, southampton, UK, 2017.Ann Surg Oncol2019;26:252-63

[29] Kasai M,Gayet B.Laparoscopic versus open major hepatectomy: a systematic review and meta-analysis of individual patient data.Surgery2018;163:985-95

[30] Ivanics T,Patel MS.Long-term outcomes of laparoscopic liver resection for hepatocellular carcinoma: a propensity score matched analysis of a high-volume North American center.Surgery2022;171:982-91

[31] Goh EL,Ma S.Laparoscopic vs. open hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a meta-analysis of the long-term survival outcomes.Int J Surg2018;50:35-42

[32] Sun Q,Gong X.Survival analysis between laparoscopic and open hepatectomy for hepatocellular carcinoma: a meta-analysis based on reconstructed time-to-event data.Hepatol Int2021;15:1215-35

[33] Cipriani F,Ratti F.Laparoscopic liver resections for hepatocellular carcinoma. can we extend the surgical indication in cirrhotic patients?.Surg Endosc2018;32:617-26

[34] Troisi RI,Morise Z.Laparoscopic and open liver resection for hepatocellular carcinoma with child-pugh B cirrhosis: multicentre propensity score-matched study.Br J Surg2021;108:196-204

[35] Molina V,Ferrer J.Benefits of laparoscopic liver resection in patients with hepatocellular carcinoma and portal hypertension: a case-matched study.Surg Endosc2018;32:2345-54

[36] Lim C,Lahat E.Safety of laparoscopic hepatectomy in patients with hepatocellular carcinoma and portal hypertension: interim analysis of an open prospective study.Surg Endosc2019;33:811-20

[37] Abu Hilal M,Dagher I.The southampton consensus guidelines for laparoscopic liver surgery: from indication to implementation.Ann Surg2018;268:11-8

[38] Mavros MN,Alexiou VG.Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: systematic review and meta-analysis.JAMA Surg2014;149:565-74

[39] Bridgewater J,Khan SA. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. J Hepatol 2014;60:1268-89.[DOI:10.1016/j.jhep.2014.01.021] Caution!

[40] Weber SM,O'Reilly EM,Miyazaki M.Intrahepatic cholangiocarcinoma: expert consensus statement.HPB2015;17:669-80 PMCID:PMC4527852

[41] Reames BN,Ejaz A.Impact of adjuvant chemotherapy on survival in patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis.HPB2017;19:901-9

[42] Spolverato G,Kim Y.Impact of complications on long-term survival after resection of intrahepatic cholangiocarcinoma.Cancer2015;121:2730-9

[43] Tsilimigras DI,Wu L.Very early recurrence after liver resection for intrahepatic cholangiocarcinoma: considering alternative treatment approaches.JAMA Surg2020;155:823-31 PMCID:PMC7344787

[44] Belfiore MP,Maggialetti N.Preliminary results in unresectable cholangiocarcinoma treated by CT percutaneous irreversible electroporation: feasibility, safety and efficacy.Med Oncol2020;37:45

[45] Uy BJ,Yoon YS.Laparoscopic liver resection for intrahepatic cholangiocarcinoma.J Laparoendosc Adv Surg Tech A2015;25:272-7

[46] Lee W,Kim JY.Comparison of perioperative and oncologic outcomes between open and laparoscopic liver resection for intrahepatic cholangiocarcinoma.Surg Endosc2016;30:4835-40

[47] Ratti F,Ariotti R.Safety and feasibility of laparoscopic liver resection with associated lymphadenectomy for intrahepatic cholangiocarcinoma: a propensity score-based case-matched analysis from a single institution.Surg Endosc2016;30:1999-2010

[48] Regmi P,Paudyal P.Is laparoscopic liver resection safe for intrahepatic cholangiocarcinoma?.Eur J Surg Oncol2021;47:979-89

[49] Machairas N,Schizas D,Nikiteas N.Meta-analysis of laparoscopic versus open liver resection for intrahepatic cholangiocarcinoma.Updates Surg2021;73:59-68

[50] Ziogas IA,Giannis D.Laparoscopic versus open hepatectomy for intrahepatic cholangiocarcinoma: an individual patient data survival meta-analysis.Am J Surg2021;222:731-8

[51] Wei F,Cai L,Liang X.Can laparoscopic liver resection provide a favorable option for patients with large or multiple intrahepatic cholangiocarcinomas?.Surg Endosc2017;31:3646-55

[52] Zhu Y,Xu X,Yang J.Safety and feasibility of laparoscopic liver resection for patients with large or multiple intrahepatic cholangiocarcinomas: a propensity score based case-matched analysis from a single institute.Medicine2019;98:e18307 PMCID:PMC6919519

[53] Martin SP,Wach MM.Laparoscopic approach to intrahepatic cholangiocarcinoma is associated with an exacerbation of inadequate nodal staging.Ann Surg Oncol2019;26:1851-7 PMCID:PMC8132107

[54] Kinoshita M,Takemura S.Indications for laparoscopic liver resection of mass-forming intrahepatic cholangiocarcinoma.Asian J Endosc Surg2020;13:46-58

[55] Kang SH,Lee W.Laparoscopic liver resection versus open liver resection for intrahepatic cholangiocarcinoma: 3-year outcomes of a cohort study with propensity score matching.Surg Oncol2020;33:63-9

[56] Haber PK,Kästner A.Laparoscopic liver resection for intrahepatic cholangiocarcinoma: a single-center experience.J Laparoendosc Adv Surg Tech A2020;30:1354-9

[57] Bertagna F,Bosio G.Diagnostic role of radiolabelled choline PET or PET/CT in hepatocellular carcinoma: a systematic review and meta-analysis.Hepatol Int2014;8:493-500

[58] Amini N,Spolverato G,Kim Y.Management of lymph nodes during resection of hepatocellular carcinoma and intrahepatic cholangiocarcinoma: a systematic review.J Gastrointest Surg2014;18:2136-48

[59] Fiorentini G,Cipriani F,Paganelli M.Challenges and technical innovations for an effective laparoscopic lymphadenectomy in liver malignancies.J Laparoendosc Adv Surg Tech A2019;29:72-5

[60] Ratti F,Cipriani F,Catena M.Perioperative and long-term outcomes of laparoscopic versus open lymphadenectomy for biliary tumors: a propensity-score-based, case-matched analysis.Ann Surg Oncol2019;26:564-75

[61] Anselmo A,Pisani G,Pirozzi B.Laparoscopic left hemihepatectomy for intrahepatic cholangiocellular carcinoma: an adequate lymphadenectomy is also possible in artery variation.Ann Surg Oncol2022:4359-60

[62] Zhang Y,Zhu J.Clinical application of indocyanine green fluorescence imaging in laparoscopic lymph node dissection for intrahepatic cholangiocarcinoma: a pilot study (with video).Surgery2022;171:1589-95

[63] Shiraiwa DK,Maeda CT.The role of minimally invasive hepatectomy for hilar and intrahepatic cholangiocarcinoma: a systematic review of the literature.J Surg Oncol2020;121:863-72

[64] Cao J,Liu S.Intrahepatic cholangiocarcinoma: genomic heterogeneity between eastern and western patients.JCO Precis Oncol2020;4 PMCID:PMC7446410

[65] Baecker A,La Vecchia C.Worldwide incidence of hepatocellular carcinoma cases attributable to major risk factors.Eur J Cancer Prev2018;27:205-12 PMCID:PMC5876122

[66] Buell JF,Geller DA.World consensus conference on laparoscopic surgeryThe international position on laparoscopic liver surgery: the louisville statement, 2008.Ann Surg2009;250:825-30

[67] Ishizawa T,Kokudo N.Laparoscopic segmentectomy of the liver: from segment I to VIII.Ann Surg2012;256:959-64

[68] Kawaguchi Y,Kokudo N.Difficulty of laparoscopic liver resection: proposal for a new classification.Ann Surg2018;267:13-7

[69] Gholami S,Lee SY.Is minimally invasive surgery of lesions in the right superior segments of the liver justified?.J Surg Oncol2020;122:1428-34 PMCID:PMC7978501

[70] Hasegawa Y,Nitta H.A novel model for prediction of pure laparoscopic liver resection surgical difficulty.Surg Endosc2017;31:5356-63

[71] Halls MC,Cipriani F.Development and validation of a difficulty score to predict intraoperative complications during laparoscopic liver resection.Br J Surg2018;105:1182-91

[72] Lin H,Yin M,Yu S.External validation of different difficulty scoring systems of laparoscopic liver resection for hepatocellular carcinoma.Surg Endosc2022;36:3732-49

[73] Lv X,Yu X.The difficulty grade of laparoscopic hepatectomy for hepatocellular carcinoma correlates with long-term outcomes.Updates Surg