Journal of Gastrointestinal Surgery

, Volume 23, Issue 6, pp 1157–1165 | Cite as

Preoperative Prognosticators of Safe Laparoscopic Hepatocellular Carcinoma Resection in Advanced Cirrhosis: a Propensity Score Matching Population-Based Analysis of 1799 Western Patients

  • Eduardo A. Vega
  • Onur C. Kutlu
  • Katharina Joechle
  • Nestor De La Cruz
  • Dicken Ko
  • Claudius ConradEmail author
2018 SSAT Quick Shot Presentation



The safety and oncologic outcomes of patients with advanced cirrhosis undergoing laparoscopic liver resection (LLR) compared to open resection (OLR) for hepatocellular carcinoma (HCC) remain unclear.


Patients with HCC resection during 2010–2014 were identified from the National Cancer Database. Patients with severe fibrosis; single lesions; M0; and known grade, margin status, tumor size, length of hospital stay, 30- and 90-day mortality, 30-day readmission, surgical approach, and complete follow-up were included. A 1:1 propensity score matching analysis of LLR:OLR was performed. Prognostic effect of LLR was assessed by multivariable Cox proportional hazards model.


A total of 1799 hepatectomy patients (minor (n = 491, 27.3%); major (n = 1308, 72.7%)) were included. Of 193 (10.7%) LLR patients, 190 were eligible for matching. The LLR vs OLR did not differ for patient characteristics, resection margin status, and 30-day (p = 0.141), 90-day mortality (p = 0.121), or 30-day readmission (p = 0.784). Median hospital stay was shorter for LLR (6 vs 8 days, p = 0.001). Median overall survival (OS) was similar for LLR vs OLR (44.2 and 39.5 months, respectively, p = 0.064). Predictors of worse OS were older age (hazard ratio (HR) 1.04, p = 0.034), > 2 comorbidities (HR 1.29, p = 0.012), grade 3–4 disease (HR 1.81, p = 0.025), N1 disease (HR 1.04, p = 0.048), and R1 margins (HR 1.34, p = 0.002). After adjustment for confounders, LLR vs OLR was not a significant risk factor for OS (HR 1.14, 95% CI 0.76–1.71, p = 0.522).


While LLR in advanced cirrhosis for patients with HCC proved safe, optimal patient selection based on the preoperatively available factors comorbidities, age, degree of underlying liver disease, and high-quality oncologic surgery will determine long-term survival.


Hepatocellular carcinoma Laparoscopic Cirrhosis Propensity score 



Hepatocellular carcinoma


Hazard ratio


Laparoscopic liver resection


National Cancer Database


Open liver resection


Overall survival



The authors thank Stephanie Deming for her invaluable editorial support.

Author Contributions

Substantial contributions to:

- The conception or design of the work:

Eduardo A. Vega, MD; Onur C. Kutlu, MD; Katharina Joechle, MD; Nestor De La Cruz, MD; Dicken Ko, MD; Claudius Conrad, MD, PhD

- The acquisition, analysis, or interpretation of data for the work:

Eduardo A. Vega, MD; Onur C. Kutlu, MD; Katharina Joechle, MD; Nestor De La Cruz, MD; Dicken Ko, MD; Claudius Conrad, MD, PhD

Drafting the work or revising it critically for important intellectual content: all authors

Final approval of the version to be published: all authors

Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: all authors

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

11605_2019_4139_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 14 kb)


  1. 1.
    Ciria R, Cherqui D, Geller DA, Briceno J, Wakabayashi G. Comparative Short-term Benefits of Laparoscopic Liver Resection: 9000 Cases and Climbing. Ann Surg. 2016;263(4):761–77. Scholar
  2. 2.
    Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg. 2009;250(5):831–41. Scholar
  3. 3.
    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, O’Rourke 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, Schon 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. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261(4):619–29. Google Scholar
  4. 4.
    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. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg. 2009;250(5):825–30.CrossRefGoogle Scholar
  5. 5.
    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. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery: From Indication to Implementation. Ann Surg. 2018;268(1):11–8. Scholar
  6. 6.
    Beard RE, Wang Y, Khan S, Marsh JW, Tsung A, Geller DA. Laparoscopic liver resection for hepatocellular carcinoma in early and advanced cirrhosis. HPB (Oxford). 2018. 20(6):521–9 Scholar
  7. 7.
    Belli G, Limongelli P, Fantini C, D'Agostino A, Cioffi L, Belli A, Russo G. Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg. 2009;96(9):1041–8. Scholar
  8. 8.
    Beppu T, Wakabayashi G, Hasegawa K, Gotohda N, Mizuguchi T, Takahashi Y, Hirokawa F, Taniai N, Watanabe M, Katou M, Nagano H, Honda G, Baba H, Kokudo N, Konishi M, Hirata K, Yamamoto M, Uchiyama K, Uchida E, Kusachi S, Kubota K, Mori M, Takahashi K, Kikuchi K, Miyata H, Takahara T, Nakamura M, Kaneko H, Yamaue H, Miyazaki M, Takada T. Long-term and perioperative outcomes of laparoscopic versus open liver resection for colorectal liver metastases with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci. 2015;22(10):711–20. Scholar
  9. 9.
    Cherqui D, Laurent A, Tayar C, Chang S, Van Nhieu JT, Loriau J, Karoui M, Duvoux C, Dhumeaux D, Fagniez PL. Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: midterm results and perspectives. Ann Surg. 2006;243(4):499–506. Scholar
  10. 10.
    Cheung TT, Poon RT, Yuen WK, Chok KS, Jenkins CR, Chan SC, Fan ST, Lo CM. Long-term survival analysis of pure laparoscopic versus open hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a single-center experience. Ann Surg. 2013;257(3):506–11. Scholar
  11. 11.
    Sarpel U, Hefti MM, Wisnievsky JP, Roayaie S, Schwartz ME, Labow DM. Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: case-matched analysis. Ann Surg Oncol. 2009;16(6):1572–7. Scholar
  12. 12.
    Tranchart H, Di Giuro G, Lainas P, Roudie J, Agostini H, Franco D, Dagher I. Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc. 2010;24(5):1170–6. Scholar
  13. 13.
    Varley PR, Tohme ST, Chidi AP, Goswami J, van der Windt D, Geller DA, Tsung A. Dissemination of Minimally Invasive Liver Resection for Primary Malignancy: Reevaluating Effectiveness. Ann Surg Oncol. 2018;25(3):808–17. Scholar
  14. 14.
    Yamashita Y, Ikeda T, Kurihara T, Yoshida Y, Takeishi K, Itoh S, Harimoto N, Kawanaka H, Shirabe K, Maehara Y. Long-term favorable surgical results of laparoscopic hepatic resection for hepatocellular carcinoma in patients with cirrhosis: a single-center experience over a 10-year period. J Am Coll Surg. 2014;219(6):1117–23. Scholar
  15. 15.
    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. Pure Laparoscopic Versus Open Right Hepatectomy for Hepatocellular Carcinoma in Patients With Cirrhosis: A Propensity Score Matched Analysis. Ann Surg. 2017;265(5):856–63. Scholar
  16. 16.
    He J, Amini N, Spolverato G, Hirose K, Makary M, Wolfgang CL, Weiss MJ, Pawlik TM. National trends with a laparoscopic liver resection: results from a population-based analysis. HPB (Oxford). 2015;17(10):919–26. Scholar
  17. 17.
    Spolverato G, Ejaz A, Kim Y, Hall BL, Bilimoria K, Cohen M, Ko C, Pitt H, Pawlik TM. Patterns of care among patients undergoing hepatic resection: a query of the National Surgical Quality Improvement Program-targeted hepatectomy database. J Surg Res. 2015;196(2):221–8. Scholar
  18. 18.
    Kokudo T, Hasegawa K, Kokudo N, Kokudo T, Uldry E, Demartines N, Halkic N. Hepatocellular Carcinoma: The Gap Between Eastern and Western Clinical Practice. Ann Surg. 2018;267(2):e27-e8. Scholar
  19. 19.
    Laurent A, Tayar C, Andreoletti M, Lauzet JY, Merle JC, Cherqui D. Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg. 2009;16(3):310–4. Scholar
  20. 20.
    Sposito C, Battiston C, Facciorusso A, Mazzola M, Muscara C, Scotti M, Romito R, Mariani L, Mazzaferro V. Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg. 2016;103(7):871–80. Scholar
  21. 21.
    Belli G, Fantini C, Belli A, Limongelli P. Laparoscopic liver resection for hepatocellular carcinoma in cirrhosis: long-term outcomes. Dig Surg. 2011;28(2):134–40. Scholar
  22. 22.
    Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamazoe S, Yamamoto S, Kubo S. Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc. 2013;27(7):2592–7. Scholar
  23. 23.
    Ishak K, Baptista A, Bianchi L, Callea F, De Groote J, Gudat F, Denk H, Desmet V, Korb G, MacSween RN, et al. Histological grading and staging of chronic hepatitis. J Hepatol. 1995;22(6):696–9.CrossRefGoogle Scholar
  24. 24.
    Mise Y, Vauthey JN, Zimmitti G, Parker NH, Conrad C, Aloia TA, Lee JE, Fleming JB, Katz MH. Ninety-day Postoperative Mortality Is a Legitimate Measure of Hepatopancreatobiliary Surgical Quality. Ann Surg. 2015;262(6):1071–8. Scholar
  25. 25.
    Mise Y, Day RW, Vauthey JN, Brudvik KW, Schwarz L, Prakash L, Parker NH, Katz MH, Conrad C, Lee JE, Fleming JB, Aloia TA. After Pancreatectomy, the “90 Days from Surgery” Definition Is Superior to the “30 Days from Discharge” Definition for Capture of Clinically Relevant Readmissions. J Gastrointest Surg. 2016;20(1):77–84; discussion Scholar
  26. 26.
    Vauthey JN, Lauwers GY, Esnaola NF, Do KA, Belghiti J, Mirza N, Curley SA, Ellis LM, Regimbeau JM, Rashid A, Cleary KR, Nagorney DM. Simplified staging for hepatocellular carcinoma. J Clin Oncol. 2002;20(6):1527–36. Scholar
  27. 27.
    Shindoh J, Andreou A, Aloia TA, Zimmitti G, Lauwers GY, Laurent A, Nagorney DM, Belghiti J, Cherqui D, Poon RT, Kokudo N, Vauthey JN. Microvascular invasion does not predict long-term survival in hepatocellular carcinoma up to 2 cm: reappraisal of the staging system for solitary tumors. Ann Surg Oncol. 2013;20(4):1223–9. Scholar
  28. 28.
    Primary liver cancer in Japan. Clinicopathologic features and results of surgical treatment. Ann Surg. 1990;211(3):277–87.Google Scholar
  29. 29.
    Kaneko H, Tsuchiya M, Otsuka Y, Yajima S, Minagawa T, Watanabe M, Tamura A. Laparoscopic hepatectomy for hepatocellular carcinoma in cirrhotic patients. J Hepatobiliary Pancreat Surg. 2009;16(4):433–8. Scholar
  30. 30.
    Xu HW, Liu F, Li HY, Wei YG, Li B. Outcomes following laparoscopic versus open major hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score-matched analysis. Surg Endosc. 2018;32(2):712–9. Scholar
  31. 31.
    Komatsu S, Brustia R, Goumard C, Perdigao F, Soubrane O, Scatton O. Laparoscopic versus open major hepatectomy for hepatocellular carcinoma: a matched pair analysis. Surg Endosc. 2016;30(5):1965–74. Scholar
  32. 32.
    Nomi T, Fuks D, Kawaguchi Y, Mal F, Nakajima Y, Gayet B. Learning curve for laparoscopic major hepatectomy. Br J Surg. 2015;102(7):796–804. Scholar
  33. 33.
    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. Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients? Surg Endosc. 2018;32(2):617–26. Scholar
  34. 34.
    Wilson CB. Adoption of new surgical technology. Bmj. 2006;332(7533):112–4. Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2019

Authors and Affiliations

  1. 1.Department of Surgical OncologyThe University of Texas MD Anderson Cancer CenterHoustonUSA
  2. 2.Department of Surgery, Miller School of MedicineUniversity of MiamiMiamiUSA
  3. 3.Department of Surgery, Saint Elizabeth Medical CenterTufts University School of MedicineBrightonUSA

Personalised recommendations