The evolution of minimally invasive surgery in liver transplantation for hepatocellular carcinoma

Abstract

Hepatocellular carcinoma (HCC) is a malignant neoplasm associated with significant mortality worldwide. The most commonly applied curative options include liver resection and liver transplantation (LT). Advances in technology have led to the broader implementation of minimally invasive approaches for liver surgery, including laparoscopic, hybrid, hand-assisted, and robotic techniques. Laparoscopic liver resection for HCC or living donor hepatectomy in LT for HCC are considered to be feasible and safe. Furthermore, the combination of laparoscopy and LT is a recent impressive and promising achievement that requires further investigation. This review aims to describe the role of minimally invasive surgery techniques utilized in LT for HCC.

Keywords

Minimally invasive surgery / liver transplantation / laparoscopic hepatectomy / laparoscopic donor hepatectomy

References

[1] Ziogas IA.Evolving role of Sorafenib in the management of hepatocellular carcinoma.World J Clin Oncol2017;8:203-13 PMCID:PMC5465010

[2] Akinyemiju T,Ahmed M.Global Burden of Disease Liver Cancer CollaborationThe burden of primary liver cancer and underlying etiologies from 1990 to 2015 at the global, regional, and national level: results from the global burden of disease study 2015.JAMA Oncol2017;3:1683-91 PMCID:PMC5824275

[3] Tejeda-Maldonado J,Aguirre-Valadez J.Diagnosis and treatment of hepatocellular carcinoma: an update.World J Hepatol2015;7:362-76 PMCID:PMC4381163

[4] Cancer of the Liver Italian Program (Clip) Investigators. A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients: the Cancer of the Liver Italian Program (CLIP) investigators.Hepatology1998;28:751-5

[5] 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

[6] Wakabayashi G,Geller DA.Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka.Ann Surg2015;261:619-29

[7] Coon C,Eastwood D.Primary liver cancer: an NCDB analysis of overall survival and margins after hepatectomy.Ann Surg Oncol2020;27:1156-63

[8] Forner A,Bruix J.Hepatocellular carcinoma.Lancet2012;379:1245-55

[9] Mazzaferro V,Doci R.Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis.N Engl J Med1996;334:693-9

[10] Wong SN,Keeffe EB.Comparison of clinical outcomes in chronic hepatitis B liver transplant candidates with and without hepatocellular carcinoma.Liver Transpl2007;13:334-42

[11] Yoo HY,Geschwind JF.The outcome of liver transplantation in patients with hepatocellular carcinoma in the United States between 1988 and 2001: 5-year survival has improved significantly with time.J Clin Oncol2003;21:4329-35

[12] Felli E,Pinna AD.Salvage liver transplantation after laparoscopic resection for hepatocellular carcinoma: a multicenter experience.Updates Surg2015;67:215-22

[13] Adam R.Is primary resection and salvage transplantation for hepatocellular carcinoma a reasonable strategy?.Ann Surg2005;241:671-2 PMCID:PMC1357073

[14] Laurent A,Andréoletti M,Merle JC.Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma.J Hepatobiliary Pancreat Surg2009;16:310-4

[15] Yoshida H,Yoshioka M.Current status of laparoscopic hepatectomy.J Nippon Med Sch2019;86:201-6

[16] Otsuka Y,Maeda T.Laparoscopic hepatectomy for liver tumors: proposals for standardization.J Hepatobiliary Pancreat Surg2009;16:720-5

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

[18] Gaujoux S,Jarnagin WR,Allen PJ.Single-incision laparoscopic liver resection.Surg Endosc2011;25:1489-94

[19] Cai XJ,Liang YL,Liang X.Laparoscopic left hemihepatectomy: a safety and feasibility study of 19 cases.Surg Endosc2009;23:2556-62

[20] Koffron AJ,Auffenberg GB.Laparoscopic liver surgery for everyone: the hybrid method.Surgery2007;142:463-8; discussion 468.e1

[21] Ho CM,Nitta H,Hasegawa Y.Systematic review of robotic liver resection.Surg Endosc2013;27:732-9 PMCID:PMC3572385

[22] Panaro F,Cag M,Wolf P.Robotic liver resection as a bridge to liver transplantation.JSLS2011;15:86-9 PMCID:PMC3134704

[23] Lai EC,Yang GP.Multimodality laparoscopic liver resection for hepatic malignancy--from conventional total laparoscopic approach to robot-assisted laparoscopic approach.Int J Surg2011;9:324-8

[24] 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

[25] Xiangfei M,Yingwei P,Weidong D.Open versus laparoscopic hepatic resection for hepatocellular carcinoma: a systematic review and meta-analysis.Surg Endosc2019;33:2396-418

[26] Cai W,Xiao Y.Comparison of clinical outcomes of laparoscopic versus open surgery for recurrent hepatocellular carcinoma: a meta-analysis.Surg Endosc2019;33:3550-7

[27] Kobayashi S,Marubashi S.Hepatectomy based on the tumor hemodynamics for hepatocellular carcinoma: a comparison among the hybrid and pure laparoscopic procedures and open surgery.Surg Endosc2013;27:610-7

[28] Chen PD,Hu RH.Robotic versus open hepatectomy for hepatocellular carcinoma: a matched comparison.Ann Surg Oncol2017;24:1021-8

[29] Magistri P,Assirati G.Robotic liver resection for hepatocellular carcinoma: a systematic review.Int J Med Robot2019;15:e2004

[30] Qiu J,Chengyou D.A systematic review of robotic-assisted liver resection and meta-analysis of robotic versus laparoscopic hepatectomy for hepatic neoplasms.Surg Endosc2016;30:862-75

[31] Strong RW,Ong TH,Koido Y.Successful liver transplantation from a living donor to her son.N Engl J Med1990;322:1505-7

[32] Broelsch CE,Whitington PF,Baker AL.Application of reduced-size liver transplants as split grafts, auxiliary orthotopic grafts, and living related segmental transplants.Ann Surg1990;212:368-75; discussion 375 PMCID:PMC1358174

[33] Cherqui D,Husson E.Laparoscopic living donor hepatectomy for liver transplantation in children.Lancet2002;359:392-6

[34] Koffron AJ,Baker T,Clark L.Laparoscopic-assisted right lobe donor hepatectomy.Am J Transplant2006;6:2522-5

[35] Park JB,Kim SJ.Effect of intermittent hepatic inflow occlusion with the Pringle maneuver during donor hepatectomy in adult living donor liver transplantation with right hemiliver grafts: a prospective, randomized controlled study.Liver Transpl2012;18:129-37

[36] Poon RT.Current techniques of liver transection.HPB (Oxford)2007;9:166-73 PMCID:PMC2063596

[37] Liu Y,Chen Y.Staplers or clips?.Medicine (Baltimore)2018;97:e13116 PMCID:PMC6250510

[38] Suh KS,Lee KW.Pure laparoscopic living donor hepatectomy: Focus on 55 donors undergoing right hepatectomy.Am J Transplant2018;18:434-43

[39] Cho HD,Chaundry S.Minimally invasive donor hepatectomy, systemic review.Int J Surg2020;82S:187-91

[40] Giulianotti PC,Jeon H.Robot-assisted right lobe donor hepatectomy.Transpl Int2012;25:e5-9

[41] Ziogas IA,Quintini C,Tsoulfas G. Chapter 7 - Three-dimensional (3D) printing and liver transplantation. In: Tsoulfas G, Bangeas PI, Suri JSBT-3D PA in M and S, editors. St. Louis: Elsevier; 2020. pp. 97-116.

[42] Suh KS,Yi NJ.Pure 3-dimensional laparoscopic extended right hepatectomy in a living donor.Liver Transpl2016;22:1431-6

[43] Broering DC,El Sheikh Y,Troisi RI.Learning curve under proctorship of pure laparoscopic living donor left lateral sectionectomy for pediatric transplantation.Ann Surg2020;271:542-8

[44] Hong SK,Yoon KC.The learning curve in pure laparoscopic donor right hepatectomy: a cumulative sum analysis.Surg Endosc2019;33:3741-8

[45] Lee KW,Suh KS.One hundred fifteen cases of pure laparoscopic living donor right hepatectomy at a single center.Transplantation2018;102:1878-84

[46] Goldaracena N,Selzner M.Small-for-size syndrome in live donor liver transplantation-Pathways of injury and therapeutic strategies.Clin Transplant2017;31:e12885

[47] Soubrane O,Scatton O.Pure laparoscopic right hepatectomy in a living donor.Am J Transplant2013;13:2467-71

[48] Rotellar F,Benito A.Totally laparoscopic right-lobe hepatectomy for adult living donor liver transplantation: useful strategies to enhance safety.Am J Transplant2013;13:3269-73

[49] Troisi RI,Tomassini F.Pure laparoscopic full-left living donor hepatectomy for calculated small-for-size LDLT in adults: proof of concept.Am J Transplant2013;13:2472-8

[50] Samstein B,Rotellar F.Totally laparoscopic full left hepatectomy for living donor liver transplantation in adolescents and adults.Am J Transplant2013;13:2462-6

[51] Han HS,Yoon YS.Total laparoscopic living donor right hepatectomy.Surg Endosc2015;29:184

[52] Takahara T,Hasegawa Y.Minimally invasive donor hepatectomy: evolution from hybrid to pure laparoscopic techniques.Ann Surg2015;261:e3-4

[53] Chen KH,Siow TF.Totally laparoscopic living donor right hepatectomy in a donor with trifurcation of bile duct.Asian J Surg2016;39:51-5

[54] Li H,Li B.Total laparoscopic living donor right hemihepatectomy: first case in China mainland and literature review.Surg Endosc2016;30:4622-3

[55] Rotellar F,Benito A.Totally laparoscopic right hepatectomy for living donor liver transplantation: analysis of a preliminary experience on 5 consecutive cases.Transplantation2017;101:548-54

[56] Kim KH,Jung DH.Initial outcomes of pure laparoscopic living donor right hepatectomy in an experienced adult living donor liver transplant center.Transplantation2017;101:1106-10

[57] Han HS,Kaneko H.Expert panel statement on laparoscopic living donor hepatectomy.Dig Surg2018;35:284-8

[58] Han YS,Kwon HJ.Pure laparoscopic donor right hepatectomy in a living donor with type 3a biliary variation: a case report.Medicine (Baltimore)2017;96:e8076 PMCID:PMC5617712

[59] Hong SK,Kim HS.Pure 3D laparoscopic living donor right hemihepatectomy in a donor with separate right posterior and right anterior hepatic ducts and portal veins.Surg Endosc2017;31:4834-5

[60] Park J,Choi GS.Safety and risk factors of pure laparoscopic living donor right hepatectomy: comparison to open technique in propensity score-matched analysis.Transplantation2019;103:e308-16

[61] Samstein B,Cherqui D.Fully laparoscopic left-sided donor hepatectomy is safe and associated with shorter hospital stay and earlier return to work: a comparative study.Liver Transpl2015;21:768-73

[62] Broering DC,Shagrani M,Troisi RI.Pure laparoscopic living donor left lateral sectionectomy in pediatric transplantation: a propensity score analysis on 220 consecutive patients.Liver Transpl2018;24:1019-30

[63] Soubrane O,Scatton O.Laparoscopic left lateral sectionectomy in living donors: safety and reproducibility of the technique in a single center.Ann Surg2006;244:815-20 PMCID:PMC1856581

[64] Kim KH,Park KM.Comparison of open and laparoscopic live donor left lateral sectionectomy.Br J Surg2011;98:1302-8

[65] Scatton O,Boillot O.Pure laparoscopic left lateral sectionectomy in living donors: from innovation to development in France.Ann Surg2015;261:506-12

[66] Gautier S,Gallyamov E.Laparoscopic left lateral section procurement in living liver donors: a single center propensity score-matched study.Clin Transplant2018;32:e13374

[67] Soubrane O,Kim KH.Laparoscopic living donor left lateral sectionectomy: a new standard practice for donor hepatectomy.Ann Surg2015;262:757-61; discussion 761

[68] Nagai S,Yoshida A,Kazimi M.Mini-incision right hepatic lobectomy with or without laparoscopic assistance for living donor hepatectomy.Liver Transpl2012;18:1188-97

[69] Kitajima T,Iida T.Short-term outcomes of laparoscopy-assisted hybrid living donor hepatectomy: a comparison with the conventional open procedure.Surg Endosc2017;31:5101-10

[70] Zhang B,Chen K.Laparoscopy-assisted versus open hepatectomy for live liver donor: systematic review and meta-analysis.Can J Gastroenterol Hepatol2017;2017:2956749 PMCID:PMC5697375

[71] Safwan M,Collins K,Yoshida A.Impact of abdominal shape on living liver donor outcomes in mini-incision right hepatic lobectomy: Comparison among 3 techniques.Liver Transpl2018;24:516-27

[72] Coelho FF,Kruger JAP.Laparoscopy-assisted versus open and pure laparoscopic approach for liver resection and living donor hepatectomy: a systematic review and meta-analysis.HPB (Oxford)2018;20:687-94

[73] Park JI,Lee SG.Laparoscopic living donor hepatectomy: a review of current status.J Hepatobiliary Pancreat Sci2015;22:779-88

[74] Hori T,Iida T,Uemoto S.Comprehensive guide to laparoscope-assisted graft harvesting in live donors for living-donor liver transplantation: perspective of laparoscopic vision.Ann Gastroenterol2017;30:118-26 PMCID:PMC5198236

[75] Eguchi S,Hara T.Standardized hybrid living donor hemihepatectomy in adult-to-adult living donor liver transplantation.Liver Transpl2018;24:363-8

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

[77] Chen PD,Hu RH.Robotic liver donor right hepatectomy: a pure, minimally invasive approach.Liver Transpl2016;22:1509-18

[78] Choi GH,Han DH,Lee WJ.Robotic hepatectomy: the Korean experience and perspective.Hepatobiliary Surg Nutr2017;6:230-8 PMCID:PMC5554764

[79] Liao MH,Wu H.Robot-assisted living-donor left lateral sectionectomy.Chin Med J (Engl)2017;130:874-6 PMCID:PMC5381324

[80] Magistri P,Ballarin R,Di Benedetto F.Robotic liver donor right hepatectomy: a pure, minimally invasive approach.Liver Transpl2017;23:857-8

[81] Chen PD,Wu YM.Use of robotics in liver donor right hepatectomy.Hepatobiliary Surg Nutr2017;6:292-6 PMCID:PMC5673766

[82] Liu R,Kim HJ.International consensus statement on robotic hepatectomy surgery in 2018.World J Gastroenterol2019;25:1432-44 PMCID:PMC6441912

[83] Lee B,Han HS.Comparison of pure laparoscopic and open living donor right hepatectomy after a learning curve.Clin Transplant2019;33:e13683

[84] Eguchi S,Soyama A.Elective living donor liver transplantation by hybrid hand-assisted laparoscopic surgery and short upper midline laparotomy.Surgery2011;150:1002-5

[85] Soyama A,Hidaka M.Hybrid procedure in living donor liver transplantation.Transplant Proc2015;47:679-82

[86] Dokmak S,Sepulveda A.Laparoscopic liver transplantation: dream or reality?.Ann Surg2020;272:889-93