World Journal of Surgery

, Volume 43, Issue 2, pp 615–625 | Cite as

Laparoscopic Hepatectomy Versus Open Hepatectomy for the Management of Hepatocellular Carcinoma: A Comparative Study Using a Propensity Score Matching

  • Xavier Untereiner
  • Audrey Cagniet
  • Riccardo Memeo
  • Zineb Cherkaoui
  • Tullio Piardi
  • François Severac
  • Didier Mutter
  • Reza Kianmanesh
  • Taiga Wakabayashi
  • Daniele Sommacale
  • Patrick PessauxEmail author
Original Scientific Report (including Papers Presented at Surgical Conferences)



The aim of this study was to compare the results between laparoscopic hepatectomy and open hepatectomy in two French university hospitals, for the management of hepatocellular carcinoma (HCC) using a propensity score matching.

Materials and methods

A patient in the laparoscopic surgery group (LA) was randomly matched with another patient in the open approach group (OA) using a 1:1 allocated ratio with the nearest estimated propensity score. Matching criteria included age, presence of comorbidities, American Society of Anesthesiologists score, and resection type (major or minor). Patients of the LA group without matches were excluded. Intraoperative and postoperative data were compared in both groups. Survival was compared in both groups using the following matching criteria: number and size of lesions, alpha-fetoprotein rate, and cell differentiation.


From January 2012 to January 2017, a total of 447 hepatectomies were consecutively performed, 99 hepatectomies of which were performed for the management of hepatocellular carcinomas. Forty-nine resections were performed among the open approach (OA) group (49%), and 50 resections were performed among the laparoscopic surgery (LA) group (51%). Mortality rate was 2% in the LA group and 4.1% in the OA group. After propensity score matching, there was a statistical difference favorable to the LA group regarding medical complications (54.55% versus 27.27%, p = 0.04), and operating times were shorter (p = 0.03). Resection rate R0 was similar between both groups: 90.91% (n = 30) in the LA group and 84.85% (n =) in the OA group. There was no difference regarding overall survival (p = 0.98) and recurrence-free survival (p = 0.42).


Laparoscopic liver resection for the management of HCC seems to provide the same short-term and long-term results as compared to the open approach. Laparoscopic liver resections could be considered as an alternative and become the gold standard in well-selected patients.


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Cherqui D, Laurent A, Tayar C, Chang S, Van Nhieu JT, Loriau J et al (2006) Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: midterm results and perspectives. Ann Surg 243(4):499–506CrossRefGoogle Scholar
  2. 2.
    Belli G, Fantini C, Belli A, Limongelli P (2011) Laparoscopic liver resection for hepatocellular carcinoma in cirrhosis: long-term outcomes. Dig Surg 28(2):134–140CrossRefGoogle Scholar
  3. 3.
    Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917CrossRefGoogle Scholar
  4. 4.
    Are C, Fong Y, Geller DA (2005) Laparoscopic liver resections. Adv Surg 39:57–75CrossRefGoogle Scholar
  5. 5.
    Parks KR, Kuo Y-H, Davis JM, O’ Brien B, Hagopian EJ (2014) Laparoscopic versus open liver resection: a meta-analysis of long-term outcome. HPB 16(2):109–18Google Scholar
  6. 6.
    Nguyen KT, Gamblin TC, Geller DA (2008) Laparoscopic liver resection for cancer. Future Oncol Lond Engl 4(5):661–670CrossRefGoogle Scholar
  7. 7.
    Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I et al (2009) The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 250(5):825–830CrossRefGoogle Scholar
  8. 8.
    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS et al (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261(4):619–629Google Scholar
  9. 9.
    Tranchart H, Dagher I (2014) Laparoscopic liver resection: a review. J Visc Surg 151(2):107–115CrossRefGoogle Scholar
  10. 10.
    Mala T, Edwin B, Gladhaug I, Fosse E, Søreide O, Bergan A et al (2002) A comparative study of the short-term outcome following open and laparoscopic liver resection of colorectal metastases. Surg Endosc 16(7):1059–1063CrossRefGoogle Scholar
  11. 11.
    Bruix J, Sherman M (2005) Practice Guidelines Committee, American association for the study of liver diseases. Management of hepatocellular carcinoma. Hepatol Baltim Md 42(5):1208–1236Google Scholar
  12. 12.
    Bruix J, Sherman M (2011) American Association for the study of liver diseases. Management of hepatocellular carcinoma: an update. Hepatol Baltim Md 53(3):1020–1022Google Scholar
  13. 13.
    Miyagawa S, Makuuchi M, Kawasaki S, Kakazu T (1995) Criteria for safe hepatic resection. Am J Surg 169(6):589–594CrossRefGoogle Scholar
  14. 14.
    Untereiner X, Cagnet A, Memeo R, De Blasi V, Tzedakis S, Piardi T et al (2016) Short-term and middle-term evaluation of laparoscopic hepatectomies compared with open hepatectomies: a propensity score matching analysis. World J Gastrointest Surg 8:643–650CrossRefGoogle Scholar
  15. 15.
    Untereiner X, Cagniet A, Memeo R, Tzedakis S, Piardi T, Severac F et al (2016) Laparoscopic hepatectomy versus open hepatectomy for colorectal cancer liver metastases: comparative study with propensity score matching. Hepatobiliary Surg Nutr 5:290–299CrossRefGoogle Scholar
  16. 16.
    Memeo R, de Angelis N, Compagnon P, Salloum C, Cherqui D, Laurent A et al (2014) Laparoscopic vs. open liver resection for hepatocellular carcinoma of cirrhotic liver: a case-control study. World J Surg 38(11):2919–2926. CrossRefGoogle Scholar
  17. 17.
    Couinaud C (1980) Definition of hepatic anatomical regions and their value during hepatectomy (author’s transl). Chir Mem Acad Chir 106(2):103–108Google Scholar
  18. 18.
    Strasberg SM, Phillips C (2013) Use and dissemination of the brisbane 2000 nomenclature of liver anatomy and resections. Ann Surg 257(3):377–382CrossRefGoogle Scholar
  19. 19.
    Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD et al (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196CrossRefGoogle Scholar
  20. 20.
    Wong S, Huynh D, Zhang F, Nguyen NQ (2017) Use of aspartate aminotransferase to platelet ratio to reduce the need for FibroScan in the evaluation of liver fibrosis. World J Hepatol 9(17):791–796CrossRefGoogle Scholar
  21. 21.
    Hung H-H, Su C-W, Lai C-R, Chau G-Y, Chan C-C, Huang Y-H et al (2010) Fibrosis and AST to platelet ratio index predict post-operative prognosis for solitary small hepatitis B-related hepatocellular carcinoma. Hepatol Int 4(4):691–699CrossRefGoogle Scholar
  22. 22.
    Lin Z-H, Xin Y-N, Dong Q-J, Wang Q, Jiang X-J, Zhan S-H et al (2011) Performance of the aspartate aminotransferase-to-platelet ratio index for the staging of hepatitis C-related fibrosis: an updated meta-analysis. Hepatol Baltim Md 53(3):726–736CrossRefGoogle Scholar
  23. 23.
    Singh A, Le P, Peerzada MM, Lopez R, Alkhouri N (2018) The utility of noninvasive scores in assessing the prevalence of nonalcoholic fatty liver disease and advanced fibrosis in type 2 diabetic patients. J Clin Gastroenterol 52(3):268–272Google Scholar
  24. 24.
    Cheng J, Zhao P, Liu J, Liu X, Wu X (2016) Preoperative aspartate aminotransferase-to-platelet ratio index (APRI) is a predictor on postoperative outcomes of hepatocellular carcinoma. Medicine (Baltimore) 95(48):e5486CrossRefGoogle Scholar
  25. 25.
    Shen S-L, Fu S-J, Chen B, Kuang M, Li S-Q, Hua Y-P et al (2014) Preoperative aspartate aminotransferase to platelet ratio is an independent prognostic factor for hepatitis B-induced hepatocellular carcinoma after hepatic resection. Ann Surg Oncol 21(12):3802–3809CrossRefGoogle Scholar
  26. 26.
    D’Agostino RB (1998) Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med 17(19):2265–2281CrossRefGoogle Scholar
  27. 27.
    Austin PC (2010) Statistical criteria for selecting the optimal number of untreated subjects matched to each treated subject when using many-to-one matching on the propensity score. Am J Epidemiol 172(9):1092–1097CrossRefGoogle Scholar
  28. 28.
    Steiner PM, Cook TD, Shadish WR, Clark MH (2010) The importance of covariate selection in controlling for selection bias in observational studies. Psychol Methods 15:250–267CrossRefGoogle Scholar
  29. 29.
    Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F et al (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334(11):693–699CrossRefGoogle Scholar
  30. 30.
    European Association For The Study Of The Liver, European Organisation For Research And Treatment Of Cancer (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56(4):908–943CrossRefGoogle Scholar
  31. 31.
    Dagher I, O’Rourke N, Geller DA, Cherqui D, Belli G, Gamblin TC et al (2009) Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg 250(5):856–860CrossRefGoogle Scholar
  32. 32.
    Dagher I, Di Giuro G, Dubrez J, Lainas P, Smadja C, Franco D (2009) Laparoscopic versus open right hepatectomy: a comparative study. Am J Surg 198(2):173–177CrossRefGoogle Scholar
  33. 33.
    Nomi T, Fuks D, Kawaguchi Y, Mal F, Nakajima Y, Gayet B (2015) Laparoscopic major hepatectomy for colorectal liver metastases in elderly patients: a single-center, case-matched study. Surg Endosc 29(6):1368–1375CrossRefGoogle Scholar
  34. 34.
    Cheung TT, Han HS, She WH, Chen KH, Chow PKH, Yoong BK et al (2018) The Asia Pacific consensus statement on laparoscopic liver resection for hepatocellular carcinoma: a report from the 7th Asia-Pacific primary liver cancer expert meeting held in Hong Kong. Liver Cancer 7(1):28–39CrossRefGoogle Scholar
  35. 35.
    Soubrane O, Goumard C, Laurent A, Tranchart H, Truant S, Gayet B et al (2014) Laparoscopic resection of hepatocellular carcinoma: a French survey in 351 patients. HPB 16(4):357–365CrossRefGoogle Scholar
  36. 36.
    Elias D, Desruennes E, Lasser P (1991) Prolonged intermittent clamping of the portal triad during hepatectomy. Br J Surg 78(1):42–44CrossRefGoogle Scholar
  37. 37.
    Wu CC, Hwang CR, Liu TJ, P’eng FK (1996) Effects and limitations of prolonged intermittent ischaemia for hepatic resection of the cirrhotic liver. Br J Surg 83(1):121–124Google Scholar
  38. 38.
    Belghiti J, Noun R, Malafosse R, Jagot P, Sauvanet A, Pierangeli F et al (1999) Continuous versus intermittent portal triad clamping for liver resection: a controlled study. Ann Surg 229(3):369–375CrossRefGoogle Scholar
  39. 39.
    De Carlis L, Di Sandro S, Giacomoni A, Mihaylov P, Lauterio A, Mangoni I, et al. (2013) Colorectal liver metastases: hepatic pedicle clamping during hepatectomy reduces the incidence of tumor recurrence in selected patients. Case-matched analysis. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 39(7):726–733Google Scholar
  40. 40.
    Morise Z, Sugioka A, Kawabe N, Umemoto S, Nagata H, Ohshima H et al (2011) Pure laparoscopic hepatectomy for hepatocellular carcinoma patients with severe liver cirrhosis. Asian J Endosc Surg 4(3):143–146CrossRefGoogle Scholar
  41. 41.
    Belli G, Limongelli P, Fantini C, D’Agostino A, Cioffi L, Belli A et al (2009) Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg 96(9):1041–1048CrossRefGoogle Scholar
  42. 42.
    Aldrighetti L, Guzzetti E, Pulitanò C, Cipriani F, Catena M, Paganelli M, et al. (2010) Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol 102(1):82–86Google Scholar
  43. 43.
    Dagher I, Belli G, Fantini C, Laurent A, Tayar C, Lainas P et al (2010) Laparoscopic hepatectomy for hepatocellular carcinoma: a European experience. J Am Coll Surg 211(1):16–23CrossRefGoogle Scholar
  44. 44.
    Mbah NA, Brown RE, Bower MR, Scoggins CR, McMasters KM, Martin RCG (2012) Differences between bipolar compression and ultrasonic devices for parenchymal transection during laparoscopic liver resection. HPB 14(2):126–131CrossRefGoogle Scholar
  45. 45.
    Gayet B, Cavaliere D, Vibert E, Perniceni T, Levard H, Denet C et al (2007) Totally laparoscopic right hepatectomy. Am J Surg 194(5):685–689CrossRefGoogle Scholar
  46. 46.
    Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O et al (2009) Safe and feasible inflow occlusion in laparoscopic liver resection. Surg Endosc 23(4):906–908CrossRefGoogle Scholar
  47. 47.
    Troisi RI, Van Huysse J, Berrevoet F, Vandenbossche B, Sainz-Barriga M, Vinci A et al (2011) Evolution of laparoscopic left lateral sectionectomy without the Pringle maneuver: through resection of benign and malignant tumors to living liver donation. Surg Endosc 25(1):79–87CrossRefGoogle Scholar
  48. 48.
    Tranchart H, O’Rourke N, Van Dam R, Gaillard M, Lainas P, Sugioka A et al (2015) Bleeding control during laparoscopic liver resection: a review of literature. J Hepato-Biliary-Pancreat Sci 22(5):371–378CrossRefGoogle Scholar
  49. 49.
    Dagher I, Proske JM, Carloni A, Richa H, Tranchart H, Franco D (2007) Laparoscopic liver resection: results for 70 patients. Surg Endosc 21(4):619–624CrossRefGoogle Scholar
  50. 50.
    Topal B, Fieuws S, Aerts R, Vandeweyer H, Penninckx F (2008) Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of short-term results. Surg Endosc 22(10):2208–2213CrossRefGoogle Scholar
  51. 51.
    Mala T, Edwin B, Rosseland AR, Gladhaug I, Fosse E, Mathisen O (2005) Laparoscopic liver resection: experience of 53 procedures at a single center. J Hepatobiliary Pancreat Surg 12(4):298–303CrossRefGoogle Scholar
  52. 52.
    Xu H-W, Liu F, Li H-Y, Wei Y-G, Li B (2018) Outcomes following laparoscopic versus open major hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score-matched analysis. Surg Endosc 32:712–719CrossRefGoogle Scholar
  53. 53.
    Cheung TT, Dai WC, Tsang SHY, Chan ACY, Chok KSH, Chan SC et al (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):612–620CrossRefGoogle Scholar
  54. 54.
    Takahara T, Wakabayashi G, Konno H, Gotoh M, Yamaue H, Yanaga K et al (2016) Comparison of laparoscopic major hepatectomy with propensity score matched open cases from the National Clinical Database in Japan. J Hepato-Biliary-Pancreat Sci 23(11):721–734CrossRefGoogle Scholar
  55. 55.
    Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N et al (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 Hepato-Biliary-Pancreat Sci 22(10):721–727CrossRefGoogle Scholar
  56. 56.
    Sposito C, Battiston C, Facciorusso A, Mazzola M, Muscarà C, Scotti M et al (2016) Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg 103(7):871–880CrossRefGoogle Scholar
  57. 57.
    Han DH, Choi SH, Park EJ, Kang DR, Choi GH, Choi JS (2016) Surgical outcomes after laparoscopic or robotic liver resection in hepatocellular carcinoma: a propensity-score matched analysis with conventional open liver resection. Int J Med Robot Comput Assist Surg MRCAS 12(4):735–742Google Scholar
  58. 58.
    Meguro M, Mizuguchi T, Kawamoto M, Ota S, Ishii M, Nishidate T et al (2015) Clinical comparison of laparoscopic and open liver resection after propensity matching selection. Surgery 158(3):573–587CrossRefGoogle Scholar
  59. 59.
    Ahn KS, Kang KJ, Kim YH, Kim T-S, Lim TJ (2014) A propensity score-matched case-control comparative study of laparoscopic and open liver resection for hepatocellular carcinoma. J Laparoendosc Adv Surg Tech A 24(12):872–827Google Scholar
  60. 60.
    Kim H, Suh K-S, Lee K-W, Yi N-J, Hong G, Suh S-W et al (2014) Long-term outcome of laparoscopic versus open liver resection for hepatocellular carcinoma: a case-controlled study with propensity score matching. Surg Endosc 28(3):950–960CrossRefGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2018

Authors and Affiliations

  • Xavier Untereiner
    • 1
  • Audrey Cagniet
    • 2
  • Riccardo Memeo
    • 1
    • 3
    • 4
  • Zineb Cherkaoui
    • 1
  • Tullio Piardi
    • 2
  • François Severac
    • 5
  • Didier Mutter
    • 1
    • 3
    • 4
  • Reza Kianmanesh
    • 2
  • Taiga Wakabayashi
    • 1
    • 3
  • Daniele Sommacale
    • 2
  • Patrick Pessaux
    • 1
    • 3
    • 4
    • 6
    Email author
  1. 1.Digestive and Endocrine Surgery UnitNouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Université de StrasbourgStrasbourgFrance
  2. 2.General, Digestive, and Endocrine Surgery UnitHôpital Robert Debré, Centre Hospitalier Universitaire de Reims, Université de Reims Champagne-ArdenneReimsFrance
  3. 3.Research Institute Against Digestive Cancer (IRCAD)StrasbourgFrance
  4. 4.Institute of Image-Guided Surgery (IHU Mix-Surg)StrasbourgFrance
  5. 5.Laboratory of Biostatistics and Medical Computer Science, School of MedicineHôpitaux Universitaires de StrasbourgStrasbourgFrance
  6. 6.Hepatobiliary and Pancreatic Surgical UnitNouvel Hôpital Civil (NHC)StrasbourgFrance

Personalised recommendations