Skip to main content
Log in

Is minimally invasive liver surgery a reasonable option in recurrent HCC? A snapshot from the I Go MILS registry

Updates in Surgery Aims and scope Submit manuscript

Cite this article

A Correction to this article was published on 29 October 2021

This article has been updated


Laparoscopic liver resection (LLR) for Hepatocellular carcinoma (HCC) is a safe procedure. Repeat surgery is more often required, and the role of minimally invasive liver surgery (MILS) is not yet clearly defined. The present study analyzes data compiled by the Italian Group of Minimally Invasive Liver Surgery (IGoMILS) on LLR. To compare repeated LLR with the first LLR for HCC is the primary endpoint. The secondary endpoint was to evaluate the outcome of repeat LLR in the case of primary open versus primary MILS surgery. The data cohort is divided into two groups. Group 1: first liver resection and Group 2: Repeat LLR. To compare the two groups a 3:1 Propensity Score Matching is performed to analyze open versus MILS primary resection. Fifty-two centers were involved in the present study, and 1054 patients were enrolled. 80 patients underwent to a repeat LLR. The type of resection was different, with more major resections in the group 1 before matching the two groups. After propensity score matching 3:1, each group consisted of 222 and 74 patients. No difference between the two groups was observed. In the subgroup analysis, in 44 patients the first resection was performed by an open approach. The other 36 patients were resected with a MILS approach. We found no difference between these two subgroups of patients. The present study in repeat MILS for HCC using the IGoMILS Registry has observed the feasibility and safety of the MILS procedure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history


  1. Levi Sandri GB, de Werra E, Mascianà G, Colasanti M, Santoro R, D’Andrea V et al (2016) Laparoscopic and robotic approach for hepatocellular carcinoma-state of the art. Hepatobiliary Surg Nutr 5(6):478–484. 

    Article  Google Scholar 

  2. Cipriani F, Fantini C, Ratti F, Lauro R, Tranchart H, Halls M et al (2018) Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients? Surg Endosc 32(2):617–626. 

    Article  Google Scholar 

  3. 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. 

    Article  Google Scholar 

  4. Ettorre GM, Levi Sandri GB, Santoro R, Vennarecci G, Lepiane P, Colasanti M et al (2015) Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients: single center experience of 90 cases. Hepatobiliary Surg Nutr 4(5):320–324.

    PubMed  PubMed Central  Google Scholar 

  5. Levi Sandri GB, Ettorre GM, Aldrighetti L, Cillo U, Dalla Valle R, Guglielmi A et al (2019) Laparoscopic liver resection of hepatocellular carcinoma located in unfavorable segments: a propensity score-matched analysis from the I Go MILS (Italian Group of Minimally Invasive Liver Surgery) Registry. Surg Endosc 33(5):1451–1458. 

    Article  Google Scholar 

  6. Aldrighetti L, Ratti F, Cillo U, Ferrero A, Ettorre GM, Guglielmi A et al (2017) Diffusion, outcomes and implementation of minimally invasive liver surgery: a snapshot from the I Go MILS (Italian Group of Minimally Invasive Liver Surgery) Registry. Updat Surg 69(3):271–283.

    Article  Google Scholar 

  7. Yoh T, Seo S, Taura K, Iguchi K, Ogiso S, Fukumitsu K, Ishii T, Kaido T, Uemoto S. Surgery for Recurrent Hepatocellular Carcinoma: Achieving Long-term Survival. Ann Surg. 2021 Apr 1;273(4):792-799.

  8. Levi Sandri GB, Lai Q, Ravaioli M, Di Sandro S, Balzano E, Pagano D et al (2020) The role of salvage transplantation in patients initially treated with open versus minimally invasive liver surgery: an intention-to-treat analysis. Liver Transplant 26(7):878–887.

    Article  Google Scholar 

  9. Belli G, Cioffi L, Fantini C, D’Agostino A, Russo G, Limongelli P et al (2009) Laparoscopic redo surgery for recurrent hepatocellular carcinoma in cirrhotic patients: feasibility, safety, and results. Surg Endosc 23(8):1807–1811. 

    Article  Google Scholar 

  10. Hu M, Zhao G, Xu D, Liu R (2011) Laparoscopic repeat resection of recurrent hepatocellular carcinoma. World J Surg 35(3):648–655. 

    Article  Google Scholar 

  11. Kamath PS, Wiesner RH, Malinchoc M, Kremers W, Therneau TM, Kosberg CL et al (2001) A model to predict survival in patients with end-stage liver disease. Hepatology 33(2):464–470.

    Article  CAS  Google Scholar 

  12. Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213. 

    Article  Google Scholar 

  13. Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien P-A (2013) The comprehensive complication index: a novel continuous scale to measure surgical morbidity. Ann Surg 258(1):1–7. 

    Article  Google Scholar 

  14. Huang S-W, Chu P-Y, Ariizumi S, Lin CC-W, Wong HP, Chou D-A et al (2020) Anatomical versus non-anatomical resection for hepatocellular carcinoma, a propensity-matched analysis between Taiwanese and Japanese patients. In Vivo 34(5):2607–2612. 

    Article  Google Scholar 

  15. Lin Y-J, Ho C-M (2021) Is the rationale of anatomical liver resection for hepatocellular carcinoma universally adoptable? A hypothesis-driven review. Medicina (Kaunas).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Cho CW, Choi G-S, Kim JM, Kwon CHD, Joh J-W (2019) Long-term oncological outcomes of laparoscopic liver resection for solitary hepatocellular carcinoma: comparison of anatomical and nonanatomical resection using propensity score matching analysis. J Laparoendosc Adv Surg Tech A 29(6):752–758. 

    Article  Google Scholar 

  17. Shin S, Kim T-S, Lee JW, Ahn KS, Kim YH, Kang KJ (2018) Is the anatomical resection necessary for single hepatocellular carcinoma smaller than 3 cm?: single-center experience of liver resection for a small HCC. Ann Hepato-Biliary-Pancreat Surg 22(4):326–334. 

    Article  Google Scholar 

  18. Shelat VG, Serin K, Samim M, Besselink MG, Al Saati H, Gioia PD et al (2014) Outcomes of repeat laparoscopic liver resection compared to the primary resection. World J Surg 38(12):3175–3180. 

    Article  CAS  Google Scholar 

  19. Goh BKP, Syn N, Teo J-Y, Guo Y-X, Lee S-Y, Cheow P-C et al (2019) Perioperative outcomes of laparoscopic repeat liver resection for recurrent HCC: comparison with open repeat liver resection for recurrent HCC and laparoscopic resection for primary HCC. World J Surg 43(3):878–885. 

    Article  Google Scholar 

  20. Goh BKP, Teo J-Y, Chan C-Y, Lee S-Y, Cheow P-C, Chung AYF (2016) Review of 103 cases of laparoscopic repeat liver resection for recurrent hepatocellular carcinoma. J Laparoendosc Adv Surg Tech 26(11):876–881. 

    Article  Google Scholar 

  21. Onoe T, Yamaguchi M, Irei T, Ishiyama K, Sudo T, Hadano N et al (2020) Feasibility and efficacy of repeat laparoscopic liver resection for recurrent hepatocellular carcinoma. Surg Endosc 34(10):4574–4581. 

    Article  Google Scholar 

  22. Ogawa H, Nakahira S, Inoue M, Irei T, Hasegawa M, Kato K et al (2020) Our experience of repeat laparoscopic liver resection in patients with recurrent hepatocellular carcinoma. Surg Endosc 34(5):2113–2119. 

    Article  Google Scholar 

  23. Liang Y, Lin C, Zhang B, Cao J, Chen M, Shen J et al (2020) Perioperative outcomes comparing laparoscopic with open repeat liver resection for post-hepatectomy recurrent liver cancer: a systematic review and meta-analysis. Int J Surg 79:17–28. 

    Article  Google Scholar 

  24. Peng Y, Liu F, Wei Y, Li B (2019) Outcomes of laparoscopic repeat liver resection for recurrent liver cancer: a system review and meta-analysis. Medicine (Baltimore).

    Article  PubMed  PubMed Central  Google Scholar 

  25. van der Poel MJ, Barkhatov L, Fuks D, Berardi G, Cipriani F, Aljaiuossi A et al (2019) Multicentre propensity score-matched study of laparoscopic versus open repeat liver resection for colorectal liver metastases. Br J Surg 106(6):783–789. 

    Article  Google Scholar 

  26. Vennarecci G, Berardi G, Guglielmo N, Antonini M, Ettorre GM (2019) Laparoscopic resection of hepatocellular carcinoma following liver transplantation: a video case report. Laparosc Surg [Internet], 3(0). doi: 10.21037/ls.2019.02.01

  27. Morise Z, Aldrighetti L, Belli G, Ratti F, Belli A, Cherqui D et al (2020) Laparoscopic repeat liver resection for hepatocellular carcinoma: a multicentre propensity score-based study: laparoscopic repeat liver resection for hepatocellular carcinoma. Br J Surg 107(7):889–895. 

    Article  CAS  Google Scholar 

  28. Gon H, Kido M, Tanaka M, Kuramitsu K, Komatsu S, Awazu M et al (2020) Laparoscopic repeat hepatectomy is a more favorable treatment than open repeat hepatectomy for contralateral recurrent hepatocellular carcinoma cases. Surg Endosc.

    Article  PubMed  Google Scholar 

  29. Villanueva A (2019) Hepatocellular carcinoma. N Engl J Med 380(15):1450–1462.

    Article  CAS  Google Scholar 

  30. Jung S-M, Kim JM, Choi G-S, Kwon CHD, Yi N-J, Lee K-W et al (2019) Characteristics of early recurrence after curative liver resection for solitary hepatocellular carcinoma. J Gastrointest Surg 23(2):304–311.

    Article  Google Scholar 

  31. Inoue Y, Suzuki Y, Ota M, Kitada K, Kuramoto T, Fujii K et al (2021) The management of recurrence of hepatocellular carcinoma occurring within 6 months after hepatic resection: a comparative study using a propensity score matching analysis. J Gastrointest Cancer.

    Article  PubMed  Google Scholar 

  32. Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamamoto S, Yamazoe S et al (2013) Laparoscopic liver resection for treating recurrent hepatocellular carcinoma. J Hepato-Biliary-Pancreat Sci 20(5):512–517. 

    Article  Google Scholar 

  33. Chan ACY, Poon RTP, Chok KSH, Cheung TT, Chan SC, Lo CM (2014) Feasibility of laparoscopic re-resection for patients with recurrent hepatocellular carcinoma. World J Surg 38(5):1141–1146. 

    Article  Google Scholar 

  34. Zhang J, Zhou Z-G, Huang Z-X, Yang K-L, Chen J-C, Chen J-B et al (2016) Prospective, single-center cohort study analyzing the efficacy of complete laparoscopic resection on recurrent hepatocellular carcinoma. Chin J Cancer 35(1):25.

    Article  CAS  Google Scholar 

  35. Liu K, Chen Y, Wu X, Huang Z, Lin Z, Jiang J et al (2017) Laparoscopic liver re-resection is feasible for patients with posthepatectomy hepatocellular carcinoma recurrence: a propensity score matching study. Surg Endosc 31(11):4790–4798. 

    Article  Google Scholar 

Download references


Adelmo Antonucci, Policlinico di Monza, Monza;Giacomo Batignani, Università degli Studi, Firenze.Giulio Belli, Ospedale SM Loreto Nuovo, Napoli;Andrea Belli, Napoli Stefano Berti, Ospedale Civile S.Andrea, La Spezia;Ugo Boggi, AOU Pisana, Pisa;Pasquale Bonsignore, IRCCS-ISMETT, Palermo;Alberto Brolese, Ospedale S.Chiara, Trento; Fulvio Calise, Ospedale Pinetagrande, Castel Volturno;Graziano Ceccarelli, Ospedale San Donato, Arezzo;Sara Cecconi, Parma University Hospital, Parma;Michele Colledan, AO Papa Giovanni XXIII, Bergamo; Andrea Coratti, AOU Careggi, Firenze;Giorgio Ercolani, Forlì.Fabio Ferla, ASST Grande Ospedale Metropolitano Niguarda, Milan;Mauro Filauro, Genova.Antonio Floridi, AO Ospedale Maggiore, Crema; Antonio Frena, Ospedale Centrale, Bolzano;Antonio Giuliani, AO R.N. Cardarelli, Napoli;Felice Giuliante, Policlinico Gemelli, Rome;Gian Luca Grazi, Istituto Nazionale Tumori Regina Elena, Roma; Enrico Gringeri University of Padua, Padova;Guido Griseri, Ospedale San Paolo, Savona;Silvio Guerriero, Belluno.Elio Jovine, Ospedale Maggiore, Bologna;Paolo Magistri, University of Modena and Reggio Emilia; Pietro Maida, Ospedale Villa Betania, Napoli;Marco Massani, Treviso.Pietro Mezzatesta, Casa di Cura La Maddalena, Palermo;Luca Morelli,Pisa.Nadia Russolillo, Ospedale Mauriziano Umberto I, Torino; Giuseppe Navarra, AOU Policlinico G. Martino, Messina;Amilcare Parisi, AO Santa Maria di Terni, Terni;Alberto Patriti, Spoleto.Matteo Ravaioli, Policlinico Sant’Orsola Malpighi, Bologna; Francesca Ratti, IRCCS San Raffaele Hospital, Milano;Raffaele Romito, Novara.Paolo Reggiani, Policlinico di Milano, Milano;Andrea Ruzzenente, University of Verona, Verona; Roberto Santambrogio, AO San Paolo, Milano;Giammauro Berardi, San Camillo Hospital, Rome;Giovanni Sgroi, AO Treviglio-Caravaggio, Treviglio;Abdallah Slim, AO Desio e Vimercate, Vimercate; Marco Spada, OPBG, Roma.Carlo Sposito, University of Milan, Milano;Umberto Tedeschi, Verona.Giuseppe Tisone, Policlinico Tor Vergata; Roma.Guido Torzilli, Istituto Clinico Humanitas, Rozzano; Luigi Veneroni, Rimini.Leonardo Vincenti, AOU Consorziale Policlinico, Bari;Fausto Zamboni, Ospedale Brotzu, Cagliari;Giuseppe Zimmitti, Brescia.


No funding information to disclose.

Author information

Authors and Affiliations



Corresponding authors

Correspondence to Giovanni Battista Levi Sandri or Luca Aldrighetti.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest or financial ties to disclose.

Research involving human participants and/or animals

Not applicable.

Informed consent

Written informed consent was obtained from all patients in accordance with the Declaration of Helsinki.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original article has been updated: Due to co-author name update.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 14 KB)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Levi Sandri, G.B., Colasanti, M., Aldrighetti, L. et al. Is minimally invasive liver surgery a reasonable option in recurrent HCC? A snapshot from the I Go MILS registry. Updates Surg 74, 87–96 (2022).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: