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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

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Abstract

Objective

Laparoscopic liver resection (LLR) for Hepatocellular Carcinoma (HCC) is one of the most important indications for the minimally invasive approach. Our study aims to analyze the experience of the Italian Group of Minimally Invasive Liver Surgery with laparoscopic surgical treatment of HCC, with a focus on tumor location and how it affects morbidity and mortality.

Methods

38 centers participated in this study; 372 cases of LLR for HCC were prospectively enrolled. Patients were divided into two groups according to the HCC nodule location. Group 1 favorable location and group 2 unfavorable location. Perioperative outcomes were compared between the two groups before and after a propensity score match (PS) 1:1.

Results

Before PS in group 2 surgical time was longer; conversion rate was higher; postoperative transfusion and comprehensive complication index were also higher. PS was performed with a cohort of 298 patients (from 18 centers), with 66 and 232 patients with HCC in unfavorable and favorable locations, respectively. After PS matching, 62 patients from group 1 and group 2 each were compared. Operative and postoperative course were similar in patients with HCC in favorable and unfavorable LLR locations. Surgical margins were found to be identical before and after PS.

Conclusions

These results show that LLR in patients with HCC can be safely performed in all segments because of the extensive experience of all surgeons from multiple centers in performing traditional open liver surgery as well as laparoscopic surgery.

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References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90

    Article  PubMed  Google Scholar 

  2. Roayaie S, Jibara G, Tabrizian P, Park JW, Yang J, Yan L, Schwartz M, Han G, Izzo F, Chen M, Blanc JF, Johnson P, Kudo M, Roberts LR, Sherman M (2015) The role of hepatic resection in the treatment of hepatocellular cancer. Hepatology 62(2):440–451

    Article  CAS  PubMed  Google Scholar 

  3. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS, World Consensus Conference on Laparoscopic Surgery (2009) The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 250:825–830

    Article  PubMed  Google Scholar 

  4. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, OʼRourke N, Tanabe M, Koffron AJ, Tsung A, Soubrane O, Machado MA, Gayet B, Troisi RI, Pessaux P, Van Dam RM, Scatton O, Abu Hilal M, Belli G, Kwon CH, Edwin B, Choi GH, Aldrighetti LA, Cai X, Cleary S, Chen KH, Schön MR, Sugioka A, Tang CN, Herman P, Pekolj J, Chen XP, Dagher I, Jarnagin W, Yamamoto M, Strong R, Jagannath P, Lo CM, Clavien PA, Kokudo N, Barkun J, Strasberg SM (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261:619–629

    PubMed  Google Scholar 

  5. Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien PA l (2013) The comprehensive complication index: a novel continuous scale to measure surgical morbidity. Ann Surg Jul 258(1):1–7. https://doi.org/10.1097/SLA.0b013e318296c732

    Article  Google Scholar 

  6. Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, Aroori S, Belli G, Besselink M, Briceno J, Gayet B, D’Hondt M, Lesurtel M, Menon K, Lodge P, Rotellar F, Santoyo J, Scatton O, Soubrane O, Sutcliffe R, Van Dam R, White S, Halls MC, Cipriani F, Van der Poel M, Ciria R, Barkhatov L, Gomez-Luque Y, Ocana-Garcia S, Cook A, Buell J, Clavien PA, Dervenis C, Fusai G, Geller D, Lang H, Primrose J, Taylor M, Van Gulik T, Wakabayashi G, Asbun H, Cherqui D (2017) The southampton consensus guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg. https://doi.org/10.1097/SLA.0000000000002524

    Article  PubMed  Google Scholar 

  7. Gruttadauria S, Tropea A, Pagano D, Guarini A, Liotta R, Ling T, Tuzzolino F, Luca A, Vizzini G, Gridelli B (2016) Mini-invasive approach contributes to expand the indication for liver resection for hepatocellular carcinoma without increasing the incidence of posthepatectomy liver failure and other perioperative complications: a single-center analysis. J Laparoendosc Adv Surg Tech A 26(6):439–446. https://doi.org/10.1089/lap.2016.0134

    Article  PubMed  Google Scholar 

  8. Sposito C, Battiston C, Facciorusso A, Mazzola M, Muscarà C, Scotti M, Romito R, Mariani L, Mazzaferro V (2016) Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg 103(7):871–880. https://doi.org/10.1002/bjs.10137

    Article  CAS  PubMed  Google Scholar 

  9. Cheung TT, Dai WC, Tsang SH, Chan AC, Chok KS, Chan SC, Lo CM (2016) Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg 264(4):612–620. https://doi.org/10.1097/SLA.0000000000001848

    Article  PubMed  Google Scholar 

  10. Gumbs AA, Gayet B (2008) Video: the lateral laparoscopic approach to lesions in the posterior segments. J Gastrointest Surg 12(7):1154. https://doi.org/10.1007/s11605-007-0455-x

    Article  PubMed  Google Scholar 

  11. Ettorre GM, Levi Sandri GB, Santoro R, Vennarecci G, Lepiane P, Colasanti M, Felli E, de Werra E, Colace L, D’Offizi G, Montalbano M, Visco U, Maritti M, Antonini M, Santoro E (2015) Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients: single center experience of 90 cases. Hepatobiliary Surg Nutr 4(5):320–324. https://doi.org/10.3978/j.issn.2304-3881.2015.06.13

    Article  PubMed  PubMed Central  Google Scholar 

  12. Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256(6):959–964. https://doi.org/10.1097/SLA.0b013e31825ffed3

    Article  PubMed  Google Scholar 

  13. Guro H, Cho JY, Han HS, Yoon YS, Choi Y, Jang JS, Kwon SU, Kim S, Choi JK (2017) Laparoscopic liver resection of hepatocellular carcinoma located in segments 7 or 8. Surg Endosc. https://doi.org/10.1007/s00464-017-5756-x

    Article  PubMed  Google Scholar 

  14. Jang JY, Han HS, Yoon YS, Cho JY, Choi Y, Lee W, Shin HK, Choi HL (2017) Three-dimensional laparoscopic anatomical segment 8 liver resection with glissonian approach. Ann Surg Oncol 24(6):1606–1609. https://doi.org/10.1245/s10434-017-5778-6

    Article  PubMed  Google Scholar 

  15. Kirchner VA, Kim KH, Kim SH, Lee SK (2017) Pure laparoscopic right anterior sectionectomy for hepatocellular carcinoma with great vascular exposure. Surg Endosc 31(8):3349–3350. https://doi.org/10.1007/s00464-016-5349-0

    Article  PubMed  Google Scholar 

  16. Tarantino G, Magistri P, Serra V, Berardi G, Assirati G, Ballarin R, Di Benedetto F (2017) Laparoscopic liver resection of right posterior segments for hepatocellular carcinoma on cirrhosis. J Laparoendosc Adv Surg Tech A 27(6):559–563. https://doi.org/10.1089/lap.2016.0506

    Article  PubMed  Google Scholar 

  17. Levi Sandri GB, Colasanti M, Santoro R, Ettorre GM (2015) Laparoscopic right hepatectomy for hepatocellular carcinoma in cirrhotic patient. Hepatobiliary Surg Nutr 4(6):436–438. https://doi.org/10.3978/j.issn.2304-3881.2015.07.01

    Article  PubMed  Google Scholar 

  18. Krüger JA, Fonseca GM, Coelho FF, Jeismann V, Herman P (2017) Laparoscopic right hepatectomy for cirrhotic patients: Takasaki’s Hilar control and caudal approach. Ann Surg Oncol 24(2):558–559. https://doi.org/10.1245/s10434-016-5288-y

    Article  PubMed  Google Scholar 

  19. Yoon YI, Kim KH, Kang SH, Kim WJ, Shin MH, Lee SK, Jung DH, Park GC, Ahn CS, Moon DB, Ha TY, Song GW, Hwang S, Lee SG (2017) Pure laparoscopic versus open right hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score matched analysis. Ann Surg 265(5):856–863. https://doi.org/10.1097/SLA.0000000000002072

    Article  PubMed  Google Scholar 

  20. Amato B, Aprea G, De Rosa D, Milone M, di Domenico L, Amato M, Compagna R, Santoro M, Johnson LB, Sanguinetti A, Polistena A, Avenia N (2017) Laparoscopic hepatectomy for HCC in elderly patients: risks and feasibility. Aging Clin Exp Res Feb 29(Suppl 1):179–183. https://doi.org/10.1007/s40520-016-0675-6

    Article  Google Scholar 

  21. Gil E, Kwon CHD, Kim JM, Choi GS, Heo JS, Cho W, Gwak MS, Gwak GY, Joh JW (2017) Laparoscopic liver resection of hepatocellular carcinoma with a tumor size larger than 5 cm: review of 45 cases in a tertiary institution. J Laparoendosc Adv Surg Tech A. https://doi.org/10.1089/lap.2016.0575

    Article  PubMed  Google Scholar 

  22. Levi Sandri GB, de Werra E, Mascianà G, Colasanti M, Lepiane P, Vennarecci G, D’Andrea V, Ettorre GM (2016) Laparoscopic and robotic approach for hepatocellular carcinoma-state of the art. Hepatobiliary Surg Nutr Dec 5(6):478–484. https://doi.org/10.21037/hbsn.2016.05.05

    Article  Google Scholar 

  23. Levi Sandri GB, Spoletini G, Vennarecci G, Francone E, Abu Hilal M, Ettore GM (2018) Laparoscopic liver resection for large HCC: short- and long-term outcomes in relation to tumor size. Surg Endosc. https://doi.org/10.1007/s00464-018-6225-x

    Article  PubMed  Google Scholar 

  24. Cipriani F, Fantini C, Ratti F, Lauro R, Tranchart H, Halls M, Scuderi V, Barkhatov L, Edwin B, Troisi RI, Dagher I, Reggiani P, Belli G, Aldrighetti L, Abu Hilal M (2017) Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients? Surg Endosc. https://doi.org/10.1007/s00464-017-5711-x

    Article  PubMed  Google Scholar 

  25. Cheung TT, Lo CM (2015) Laparoscopic liver resection for hepatocellular carcinoma in patients with cirrhosis. Hepatobiliary Surg Nutr 4(6):406–410. https://doi.org/10.3978/j.issn.2304-3881.2015.06.12

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Collaborators of the I Go MILS Group on HCC: Adelmo Antonucci, (Policlinico di Monza, Monza); Giulio Belli, (Ospedale SM Loreto Nuovo, 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); Michele Colledan, (AO Papa Giovanni XXIII, Bergamo); Andrea Coratti, (AOU Careggi, Firenze); Fabio Ferla, (ASST Grande Ospedale Metropolitano Niguarda, Milan); 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); Maurizio Iaria, (Parma University Hospital, Parma); Elio Jovine, (Ospedale Maggiore, Bologna); Magistri Paolo, (University of Modena and Reggio Emilia); Pietro Maida, (Ospedale Villa Betania, Napoli); Pietro Mezzatesta, (Casa di Cura La Maddalena, Palermo); Nadia Russolillo, (Ospedale Mauriziano Umberto I, Torino); Giuseppe Navarra, (AOU Policlinico G. Martino, Messina); Amilcare Parisi, (AO Santa Maria di Terni, Terni); Antonio Daniele Pinna, (Policlinico Sant’Orsola Malpighi, Bologna); Francesca Ratti, (IRCCS San Raffaele Hospital, Milano); Giorgio Ettore Rossi, (Policlinico di Milano, Milano); Andrea Ruzzenente, (University of Verona, Verona); Roberto Santambrogio, (AO San Paolo, Milano); Andrea Scotti, (San Camillo Hospital, Rome); Giovanni Sgroi, (AO Treviglio-Caravaggio, Treviglio); Abdallah Slim, (AO Desio e Vimercate, Vimercate); Guido Torzilli, (Istituto Clinico Humanitas, Rozzano); Leonardo Vincenti, (AOU Consorziale Policlinico, Bari); Matteo Virdis, (University of Milan, Milano) and Fausto Zamboni, (Ospedale Brotzu, Cagliari).

Author information

Authors and Affiliations

  1. Division of General Surgery and Liver Transplantation, S. Camillo Hospital, Rome, Italy

    Giovanni Battista Levi Sandri, Giuseppe Maria Ettorre & Giovanni Vennarecci

  2. Hepatobiliary Surgery, IRCCS San Raffaele Hospital, Milan, Italy

    Luca Aldrighetti

  3. Department of Surgery, Oncology and Gastroenterology, University of Padua, Padua, Italy

    Umberto Cillo

  4. Department of Surgery, Parma University Hospital, Parma, Italy

    Raffaele Dalla Valle

  5. Department of Hepatobiliary Surgery, G.B. Rossi Hospital, University of Verona, Verona, Italy

    Alfredo Guglielmi

  6. HPB Surgery and Liver Transplantation, Department of Surgery, University of Milan, Milan, Italy

    Vincenzo Mazzaferro

  7. Department of HPB and Digestive Surgery, Ospedale Mauriziano Umberto I, Turin, Italy

    Alessandro Ferrero

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

    Fabrizio Di Benedetto

  9. Abdominal Surgery and Organ Transplant Unit, Department for the Treatment and Study of Abdominal Diseases and Abdominal Transplantation, Mediterranean Institute for Transplantation and Specialization Therapies (IRCCS-ISMETT), Palermo, Italy

    Salvatore Gruttadauria

  10. Surgical and Transplant Department, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy

    Luciano De Carlis

Authors
  1. Giovanni Battista Levi Sandri
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  2. Giuseppe Maria Ettorre
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  3. Luca Aldrighetti
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  5. Raffaele Dalla Valle
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  7. Vincenzo Mazzaferro
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  8. Alessandro Ferrero
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  9. Fabrizio Di Benedetto
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Consortia

I Go MILS Group on HCC

  • Adelmo  Antonucci
  • , Giulio Belli
  • , Stefano Berti
  • , Ugo Boggi
  • , Pasquale Bonsignore
  • , Alberto Brolese
  • , Fulvio Calise
  • , Graziano Ceccarelli
  • , Michele Colledan
  • , Andrea Coratti
  • , Fabio Ferla
  • , Antonio Floridi
  • , Antonio Frena
  • , Antonio Giuliani
  • , Felice Giuliante
  • , Gian Luca Grazi
  • , Enrico Gringeri
  • , Guido Griseri
  • , Maurizio Iaria
  • , Elio Jovine
  • , Paolo Magistri
  • , Pietro Maida
  • , Pietro Mezzatesta
  • , Nadia Russolillo
  • , Giuseppe Navarra
  • , Amilcare Parisi
  • , Antonio Daniele Pinna
  • , Francesca Ratti
  • , Giorgio Ettore Rossi
  • , Andrea Ruzzenente
  • , Roberto Santambrogio
  • , Andrea Scotti
  • , Giovanni Sgroi
  • , Abdallah Slim
  • , Guido Torzilli
  • , Leonardo Vincenti
  • , Matteo Virdis
  •  & Fausto Zamboni

Corresponding authors

Correspondence to Giovanni Battista Levi Sandri or Luca Aldrighetti.

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Disclosure

Giovanni Battista Levi Sandri Giuseppe Maria Ettorre, Luca Aldrighetti, Umberto Cillo, Raffaele Dalla Valle, Alfredo Guglielmi, Vincenzo Mazzaferro, Alessandro Ferrero, Fabrizio Di Benedetto, Salvatore Gruttadauria, Luciano De Carlis, and Giovanni Vennarecci have no conflicts of interest or financial ties to disclose.

Additional information

Collaborators of the I Go MILS Group on HCC are listed in “Acknowledgments” section.

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Levi Sandri, G.B., Ettorre, G.M., Aldrighetti, L. et al. 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, 1451–1458 (2019). https://doi.org/10.1007/s00464-018-6426-3

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  • DOI: https://doi.org/10.1007/s00464-018-6426-3

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