Surgical Endoscopy

, Volume 32, Issue 2, pp 617–626 | Cite as

Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients?

  • Federica Cipriani
  • Corrado Fantini
  • Francesca Ratti
  • Roberto Lauro
  • Hadrien Tranchart
  • Mark Halls
  • Vincenzo Scuderi
  • Leonid Barkhatov
  • Bjorn Edwin
  • Roberto I. Troisi
  • Ibrahim Dagher
  • Paolo Reggiani
  • Giulio Belli
  • Luca Aldrighetti
  • Mohammad Abu HilalEmail author



Evidence on the value of laparoscopic liver resections (LLR) for hepatocellular carcinoma (HCC) and severe cirrhosis is still lacking. The aim of this study is to assess surgical and oncological outcomes of LLR in cirrhotic HCC patients.


The analysis included 403 LLR for HCC from seven European centres. 333 cirrhotic and 70 non-cirrhotic patients were compared. A matched comparison was performed between 100 Child–Pugh A and 25 Child–Pugh B patients.


There was no difference in blood loss (250 vs. 250 mL, p 0.465) and morbidity (28.6 vs. 26.4%, p 0.473) between cirrhotics and non-cirrhotics, and liver-specific complications were similar (12.8 vs. 12%, p 0.924). The sub-analysis revealed similar perioperative outcomes in either Child–Pugh A or B patients. Noteworthy, ascitis (11 vs. 12%, p 0.562) and liver failure (3 vs. 4%, p 0.595) were not different. ASA score (OR 1.76, p 0.034) and conversion (OR 2.99, p 0.019) were risk factors for major morbidity. Despite lower recurrence-free survival in cirrhotics (43 vs. 55 months, p 0.034), overall survival was similar to non-cirrhotic patients (84 vs. 76.5, p 0.598).


LLR for HCC appear equally safe in cirrhotic and non-cirrhotic patients, and the advantages can be witnessed in those with advanced cirrhosis. Severe comorbidities and conversion should be considered risk factors for complications—rather than the severity of cirrhosis and portal hypertension—when liver resection is performed laparoscopically. Such results may be of great interest to liver surgeons and hepatologists when deciding on the management of HCC within cirrhosis.


Laparoscopic liver resection Cirrhosis Child–Pugh Hepatocellular carcinoma Portal hypertension Risk factors for major morbidity 


Compliance with ethical standards


Drs. Federica Cipriani, Corrado Fantini, Francesca Ratti, Roberto Lauro, Hadrien Tranchart, Mark Halls, Vincenzo Scuderi, Leonid Barkhatov, Bjorn Edwin, Roberto Ivan Troisi, Ibrahim Dagher, Paolo Reggiani, Giulio Belli, Luca Aldrighetti, Mohammad Abu Hilal have no conflicts of interest or financial ties to disclose.


  1. 1.
    Forner A, Reig ME, de Lope CR, Bruix J (2010) Current strategy for staging and treatment: the BCLC update and future prospects. Semin Liver Dis 30:61–74CrossRefPubMedGoogle Scholar
  2. 2.
    Cha CH, Ruo L, Fong Y, Jarnagin WR, Shia J, Blumgart LH, DeMatteo RP (2003) Resection of hepatocellular carcinoma in patients otherwise eligible for transplantation. Ann Surg 238:315–321 (discussion 321–323)PubMedPubMedCentralGoogle Scholar
  3. 3.
    Chirica M, Scatton O, Massault PP, Aloia T, Randone B, Dousset B, Legmann P, Soubrane O (2008) Treatment of stage IVA hepatocellular carcinoma. Should we reappraise the role of surgery? Arch Surg 143:538–543CrossRefPubMedGoogle Scholar
  4. 4.
    Yin L, Li H, Li AJ, Lau WY, Pan ZY, Lai EC, Wu MC, Zhou WP (2014) Partial hepatectomy vs. transcatheter arterial chemoembolization for resectable multiple hepatocellular carcinoma beyond Milan criteria: a RCT. J Hepatol 61:82e8CrossRefGoogle Scholar
  5. 5.
    Pawlik TM, Poon RT, Abdalla EK, Ikai I, Nagorney DM, Belghiti J, Kianmanesh R, Ng IO, Curley SA, Yamaoka Y, Lauwers GY, Vauthey JN (2005) Hepatectomy for hepatocellular carcinoma with major portal or hepatic vein invasion: results of a multicenter study. Surgery 137:403–410CrossRefPubMedGoogle Scholar
  6. 6.
    Ishizawa T, Hasegawa K, Kokudo N, Sano K, Imamura H, Beck Y, Sugawara Y, Makuuchi M (2009) Risk factors and management of ascites after liver resection to treat hepatocellular carcinoma. Arch Surg 144:46–51CrossRefPubMedGoogle Scholar
  7. 7.
    Fuster J, García-Valdecasas JC, Grande L, Tabet J, Bruix J, Anglada T, Taurá P, Lacy AM, González X, Vilana R, Bru C, Solé M, Visa J (1996) Hepatocellular carcinoma and cirrhosis. Results of surgical treatment in a European series. Ann Surg 223:297–302CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Belghiti J, Hiramatsu K, Benoist S, Massault P, Sauvanet A, Farges O (2000) Seven hundred forty-seven hepatectomies in the 1990s: an update to evaluate the actual risk of liver resection. J Am Coll Surg 191:38–46CrossRefPubMedGoogle Scholar
  9. 9.
    McPhail MJ, Scibelli T, Abdelaziz M, Titi A, Pearce NW, Abu Hilal M (2009) Laparoscopic versus open left lateral hepatectomy. Expert Rev Gastroenterol Hepatol 3:345–351CrossRefPubMedGoogle Scholar
  10. 10.
    Cipriani F, Shelat VG, Rawashdeh M, Francone E, Aldrighetti L, Takhar A, Armstrong T, Pearce NW, Abu Hilal M (2015) Laparoscopic parenchymal-sparing resections for nonperipheral liver lesions, the diamond technique: technical aspects, clinical outcomes and oncologic efficiency. J Am Coll Surg 221:265–272CrossRefPubMedGoogle Scholar
  11. 11.
    Ratti F, Barkhatov L, Tomassini F, Cipriani F, Kazaryan AM, Edwin B, Abu Hilal M, Troisi RI, Aldrighetti L (2016) Learning curve of self-taught laparoscopic liver surgeons in left lateral sectionectomy: results from an international multi-institutional analysis on 245 cases. Surg Endosc 30:3618–3629CrossRefPubMedGoogle Scholar
  12. 12.
    Montalti R, Tomassini F, Laurent S, Smeets P, De Man M, Geboes K, Libbrecht LJ, Troisi RI (2015) Impact of surgical margins on overall and recurrence-free survival in parenchymal-sparing laparoscopic liver resections of colorectal metastases. Surg Endosc 29:2736–2747CrossRefPubMedGoogle Scholar
  13. 13.
    Kazaryan AM, Røsok BI, Marangos IP, Rosseland AR, Edwin B (2011) Comparative evaluation of laparoscopic liver resection for posterosuperior and anterolateral segments. Surg Endosc 25:3881–3889CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Dagher I, Gayet B, Tzanis D, Tranchart H, Fuks D, Soubrane O, Han HS, Kim KH, Cherqui D, O’Rourke N, Troisi RI, Aldrighetti L, Bjorn E, Abu Hilal M, Belli G, Kaneko H, Jarnagin WR, Lin C, Pekolj J, Buell JF, Wakabayashi G (2014) International experience for laparoscopic major liver resection. J Hepatobiliary Pancreat Sci 21:732–736CrossRefPubMedGoogle Scholar
  15. 15.
    Abu Hilal M, Di Fabio F, Teng MJ, Lykoudis P, Primrose JN, Pearce NW (2011) Single-centre comparative study of laparoscopic versus open right hepatectomy. J Gastrointest Surg 15:818–823CrossRefPubMedGoogle Scholar
  16. 16.
    Aldrighetti L, Guzzetti E, Pulitanò C, Cipriani F, Catena M, Paganelli M, Ferla G (2010) Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol 102:82–86CrossRefPubMedGoogle Scholar
  17. 17.
    Belli G, Limongelli P, Fantini C, D’Agostino A, Cioffi L, Belli A, Russo G (2009) Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg 96:1041–1048CrossRefPubMedGoogle Scholar
  18. 18.
    Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N, Hatano E, Tanahashi Y, Mizuguchi T, Kamiyama T, Ikeda T, Tanaka S, Taniai N, Baba H, Tanabe M, Kokudo N, Konishi M, Uemoto S, Sugioka A, Hirata K, Taketomi A, Maehara Y, Kubo S, Uchida E, Miyata H, Nakamura M, Kaneko H, Yamaue H, Miyazaki M, Takada T (2015) Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci 22:721–727CrossRefPubMedGoogle Scholar
  19. 19.
    Tranchart H, Di Giuro G, Lainas P, Roudie J, Agostini H, Franco D, Dagher I (2010) Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc 24:1170–1176CrossRefPubMedGoogle Scholar
  20. 20.
    Cherqui D (2015) Laparoscopic liver resection: a new paradigm in the management of hepatocellular carcinoma? J Hepatol 63:540–542CrossRefPubMedGoogle Scholar
  21. 21.
    Geller DA, Tsung A (2015) Long-term outcomes and safety of laparoscopic liver resection surgery for hepatocellular carcinoma and metastatic colorectal cancer. J Hepatobiliary Pancreat Sci 22:728–730CrossRefPubMedGoogle Scholar
  22. 22.
    Abu Hilal M, Di Fabio F, Abu Salameh M, Pearce NW (2012) Oncological efficiency analysis of laparoscopic liver resection for primary and metastatic cancer: a single-center UK experience. Arch Surg 147:42–48CrossRefPubMedGoogle Scholar
  23. 23.
    Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamazoe S, Yamamoto S, Kubo S (2013) Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc 27:2592–2597CrossRefPubMedGoogle Scholar
  24. 24.
    Ker CG, Chen JS, Kuo KK, Chuang SC, Wang SJ, Chang WC, Lee KT, Chen HY, Juan CC (2011) Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol. doi: 10.4061/2011/596792 PubMedPubMedCentralGoogle Scholar
  25. 25.
    Morise Z, Ciria R, Cherqui D, Chen KH, Belli G, Wakabayashi G (2015) Can we expand the indications for laparoscopic liver resection? A systematic review and meta-analysis of laparoscopic liver resection for patients with hepatocellular carcinoma and chronic liver disease. J Hepatobiliary Pancreat Sci 22:342–352CrossRefPubMedGoogle Scholar
  26. 26.
    Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R (1973) Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 60:646e9Google Scholar
  27. 27.
    Martínez-Cecilia D, Cipriani F, Vishal S, Ratti F, Tranchart H, Barkhatov L, Tomassini F, Montalti R, Halls M, Troisi RI, Dagher I, Aldrighetti L, Edwin B, Abu Hilal M (2017) Laparoscopic versus open liver resection for colorectal metastases in elderly and octogenarian patients: a multicenter propensity score based analysis of short- and long-term outcomes. Ann Surg 265:1192–1200CrossRefPubMedGoogle Scholar
  28. 28.
    Shelat VG, Cipriani F, Basseres T, Armstrong TH, Takhar AS, Pearce NW, Abu Hilal M (2015) Pure laparoscopic liver resection for large malignant tumors: does size matter? Ann Surg Oncol 22(Suppl 3):S1601CrossRefPubMedGoogle Scholar
  29. 29.
    Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5:649–655CrossRefPubMedGoogle Scholar
  30. 30.
    Strasberg SM (2005) Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 12:351–355CrossRefPubMedGoogle Scholar
  31. 31.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Balzan S, Belghiti J, Farges O, Ogata S, Sauvanet A, Delefosse D, Durand F (2005) The “50-50 criteria” on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 242:824–828 (discussion 828-9)CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, Fan ST, Yokoyama Y, Crawford M, Makuuchi M, Christophi C, Banting S, Brooke-Smith M, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Nimura Y, Figueras J, DeMatteo RP, Büchler MW, Weitz J (2011) Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery 149:680–688CrossRefPubMedGoogle Scholar
  34. 34.
    Memeo R, de’Angelis N, Compagnon P, Salloum C, Cherqui D, Laurent A, Azoulay D (2014) Laparoscopic vs. open liver resection for hepatocellular carcinoma of cirrhotic liver: a case-control study. World J Surg 38:2919–2926CrossRefPubMedGoogle Scholar
  35. 35.
    Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S, Leteurtre E, Zerbib P, Pruvot FR (2011) Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc 25:3668–3677CrossRefPubMedGoogle Scholar
  36. 36.
    Alemi F, Kwon E, Freise C, Kang SM, Hirose R, Stewart L, Corvera CU (2010) Hepatic surgery at a VA tertiary medical center: lessons learned. Am J Surg 200:591–595CrossRefPubMedGoogle Scholar
  37. 37.
    Takahara T, Wakabayashi G, Nitta H, Hasegawa Y, Katagiri H, Takeda D, Makabe K, Sasaki A (2015) Laparoscopic liver resection for hepatocellular carcinoma with cirrhosis in a single institution. Hepatobiliary Surg Nutr 4:398–405PubMedPubMedCentralGoogle Scholar
  38. 38.
    Lee JJ, Conneely JB, Smoot RL, Gallinger S, Greig PD, Moulton CA, Wei A, McGilvray I, Cleary SP (2015) Laparoscopic versus open liver resection for hepatocellular carcinoma at a North-American Centre: a 2-to-1 matched pair analysis. HPB 17:304–310CrossRefPubMedGoogle Scholar
  39. 39.
    Shehta A, Han HS, Yoon YS, Cho JY, Choi Y (2016) Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients: 10-year single-center experience. Surg Endosc 30:638–648CrossRefPubMedGoogle Scholar
  40. 40.
    Goh BK, Chan CY, Wong JS, Lee SY, Lee VT, Cheow PC, Chow PK, Ooi LL, Chung AY (2015) Factors associated with and outcomes of open conversion after laparoscopic minor hepatectomy: initial experience at a single institution. Surg Endosc 29:2636–2642CrossRefPubMedGoogle Scholar
  41. 41.
    Cauchy F, Fuks D, Nomi T, Schwarz L, Barbier L, Dokmak S, Scatton O, Belghiti J, Soubrane O, Gayet B (2015) Risk factors and consequences of conversion in laparoscopic major liver resection. Br J Surg 102:785–795CrossRefPubMedGoogle Scholar
  42. 42.
    Ziser A, Plevak DJ, Wiesner RH, Rakela J, Offord KP, Brown DL (1999) Morbidity and mortality in cirrhotic patients undergoing anesthesia and surgery. Anesthesiology 90:42–53CrossRefPubMedGoogle Scholar
  43. 43.
    Dokmak S, Ftériche FS, Borscheid R, Cauchy F, Farges O, Belghiti J (2013) Liver resections in the 21st century: we are far from zero mortality. HPB 15:908–915CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Chen HW, Liao S, Lau WY, Wang FJ, Deng FW, Lai EC, Zhen ZJ (2015) Prognostic impact of hepatic resection for hepatocellular carcinoma: the role of the surgeon in achieving R0 resection – a retrospective cohort study. Int J Surg 13:297–301CrossRefPubMedGoogle Scholar
  45. 45.
    Fan ST, Poon RT, Yeung C, Lam CM, Lo CM, Yuen WK, Ng KK, Liu CL, Chan SC (2011) Outcome after partial hepatectomy for hepatocellular cancer within the Milan criteria. Br J Surg 98:1292–1300CrossRefPubMedGoogle Scholar
  46. 46.
    Yip VS, Gomez D, Tan CY, Staettner S, Terlizzo M, Fenwick S, Malik HZ, Ghaneh P, Poston G (2013) Tumour size and differentiation predict survival after liver resection for hepatocellular carcinoma arising from non-cirrhotic and non-fibrotic liver: a case-controlled study. Int J Surg 11:1078–1082CrossRefPubMedGoogle Scholar
  47. 47.
    Taura K, Ikai I, Hatano E, Yasuchika K, Nakajima A, Tada M, Seo S, Machimoto T, Uemoto S (2007) Influence of coexisting cirrhosis on outcomes after partial hepatic resection for hepatocellular carcinoma fulfilling the Milan criteria: an analysis of 293 patients. Surgery 142:685–694CrossRefPubMedGoogle Scholar
  48. 48.
    Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J (2000) Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer 89:500–507CrossRefPubMedGoogle Scholar
  49. 49.
    Llovet JM, Di Bisceglie AM, Bruix J, Kramer BS, Lencioni R, Zhu AX, Sherman M, Schwartz M, Lotze M, Talwalkar J, Gores GJ, Panel of Experts in HCC-Design Clinical Trials (2008) Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst 100:698–711CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Federica Cipriani
    • 1
    • 2
  • Corrado Fantini
    • 3
  • Francesca Ratti
    • 2
  • Roberto Lauro
    • 4
  • Hadrien Tranchart
    • 5
  • Mark Halls
    • 1
  • Vincenzo Scuderi
    • 6
  • Leonid Barkhatov
    • 7
  • Bjorn Edwin
    • 7
    • 8
  • Roberto I. Troisi
    • 6
  • Ibrahim Dagher
    • 5
  • Paolo Reggiani
    • 4
  • Giulio Belli
    • 3
  • Luca Aldrighetti
    • 2
  • Mohammad Abu Hilal
    • 1
    Email author
  1. 1.University Hospital Southampton NHS Foundation TrustSouthamptonUK
  2. 2.Hepatobiliary SurgeryIRCCS San Raffaele HospitalMilanItaly
  3. 3.General and Hepato-Pancreato-Biliary SurgeryLoreto Nuovo HospitalNaplesItaly
  4. 4.Hepatobiliary and Liver Transplant UnitIRCCS Foundation Policlinico Major HospitalMilanItaly
  5. 5.Department of Minimally Invasive Digestive SurgeryAntoine-Beclere HospitalClamartFrance
  6. 6.Department of General, Hepatobiliary and Liver Transplantation SurgeryGhent University Hospital Medical SchoolGhentBelgium
  7. 7.Intervention CentreOslo University Hospital, RikshospitaletOsloNorway
  8. 8.Institute of Clinical MedicineUniversity of OsloOsloNorway

Personalised recommendations