Skip to main content
Log in

A Systematic Review and Meta-Analysis Comparing the Short- and Long-Term Outcomes for Laparoscopic and Open Liver Resections for Hepatocellular Carcinoma: Updated Results from the European Guidelines Meeting on Laparoscopic Liver Surgery, Southampton, UK, 2017

  • Hepatobiliary Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

The laparoscopic approach to liver resection has experienced exponential growth in recent years; however, its application is still under debate and objective, evidence-based guidelines for its safe future progression are needed.

Objective

The aim of this study was to perform a systematic review and meta-analysis comparing the short- and long-term outcomes of laparoscopic and open liver resections for hepatocellular carcinoma (HCC).

Methods

To identify all the comparative manuscripts reporting on laparoscopic and open liver resection for HCC, all published English-language studies with more than 10 cases were screened. In addition to the primary meta-analysis, four specific subgroup analyses were performed on patients with Child–Pugh A cirrhosis, resections for solitary tumors, and those undergoing minor and major resections. The quality of the studies was assessed using the Scottish Intercollegiate Guidelines Network (SIGN) methodology and the Newcastle–Ottawa Scale.

Results

From the initial 361 manuscripts, 28 were included in the meta-analysis. Five of these 28 manuscripts were specific to patients with Child–Pugh A cirrhosis (321 cases), 11 focused on solitary tumors (1003 cases), 16 focused on minor resections (1286 cases), and 3 focused on major resections (164 cases). Three manuscripts compared 1079 cases but could not be assigned to any of the above subanalyses. In general terms, short-term outcomes were favorable when using a laparoscopic approach, especially in minor resections. The only advantage seen with an open approach was reduced operative time during major liver resections. No differences in long-term outcomes were observed between the approaches.

Conclusions

Laparoscopic liver resection for HCC is feasible and offers improved short-term outcomes, with comparable long-term outcomes as the open approach.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. El-Serag HB. Hepatocellular carcinoma. N Engl J Med. 2011;365(12):1118–27.

    Article  CAS  PubMed  Google Scholar 

  2. Clavien P-A, Lesurtel M, Bossuyt PM, Gores GJ, Langer B, Perrier A. Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol. 2012;13(1):e11–e22.

    Article  PubMed  Google Scholar 

  3. Sposito C, Battiston C, Facciorusso A, Mazzola M, Muscarà C, Scotti M et al. Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg. 2016;103(7):871–80.

    Article  CAS  PubMed  Google Scholar 

  4. Ciria R, López-Cillero P, Gallardo AB, Cabrera J, Pleguezuelo M, Ayllón MD et al. Optimizing the management of patients with BCLC stage-B hepatocellular carcinoma: modern surgical resection as a feasible alternative to transarterial chemoemolization. Eur J Surg Oncol. 2015;41(9):1153–61.

    Article  CAS  PubMed  Google Scholar 

  5. Hashizume M, Takenaka K, Yanaga K, Ohta M, Kajiyama K, Shirabe K et al. Laparoscopic hepatic resection for hepatocellular carcinoma. Surg Endosc. 1995;9(12):1289–91.

    Article  CAS  PubMed  Google Scholar 

  6. Kaneko H, Takagi S, Shiba T. Laparoscopic partial hepatectomy and left lateral segmentectomy: technique and results of a clinical series. Surgery. 1996;120(3):468–75.

    Article  CAS  PubMed  Google Scholar 

  7. Ciria R, Cherqui D, Geller DA, Briceño J, Wakabayashi G. Comparative short-term benefits of laparoscopic liver resection: 9000 cases and climbing. Ann Surg. 2016;263(4):761–77.

    Article  PubMed  Google Scholar 

  8. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han H-S et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261(4):619–29.

    PubMed  Google Scholar 

  9. Chang L, Wang Y, Zhang J, Guo T. The best strategy for HCC patients at each BCLC stage: a network meta-analysis of observational studies. Oncotarget. 2017;8(12):20418–27.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Zhou Y-M, Shao W-Y, Zhao Y-F, Xu D-H, Li B. Meta-analysis of laparoscopic versus open resection for hepatocellular carcinoma. Dig Dis Sci. 2011;56(7):1937–43.

    Article  PubMed  Google Scholar 

  11. Fancellu A, Rosman AS, Sanna V, Nigri GR, Zorcolo L, Pisano M et al. Meta-analysis of trials comparing minimally-invasive and open liver resections for hepatocellular carcinoma. J Surg Res. 2011;171(1):e33–45.

    Article  PubMed  Google Scholar 

  12. Morise Z, Ciria R, Cherqui D, Chen K-H, Belli G, Wakabayashi G. 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. 2015;22(5):342–52.

    Article  PubMed  Google Scholar 

  13. Cipriani F, Fantini C, Ratti F, Lauro R, Tranchart H, Halls M et al. (2017) Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients? Surg Endosc. 30(suppl 3):61–70.

    Google Scholar 

  14. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.

    Article  Google Scholar 

  15. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I et al. The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg. 2009;250(5):825–30.

    Article  PubMed  Google Scholar 

  16. Rahbari NN, Garden OJ, Padbury R, Brooke-Smith M, Crawford M, Adam R et al. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery. 2011;149(5):713–24.

    Article  PubMed  Google Scholar 

  17. Petrie JC, Grimshaw JM, Bryson A. The Scottish intercollegiate guidelines network initiative: getting validated guidelines into local practice. Health Bull (Edinb). 1995;53(6):345–8.

    CAS  PubMed  Google Scholar 

  18. DerSimonian R, Laird N. Meta-analysis in clinical trials. Controll Clin Trials. 1986;7(3):177–88.

    Article  CAS  PubMed  Google Scholar 

  19. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22(4):719–48.

    CAS  PubMed  Google Scholar 

  21. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36(3):1–48.

    Article  Google Scholar 

  22. Wallace BC, Dahabreh IJ, Trikalinos TA, Lau J, Trow P, Schmid CH. Closing the gap between methodologists and end-users: R as a computational back-end. J Stat Softw. 2012;49(5):1–15.

    Article  Google Scholar 

  23. Wan X, Wang W, Lui J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14:135.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lee KF, Chong CN, Wong J, Cheung YS, Wong J, Lai P. Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg. 2011;35(10):2268–74.

    Article  PubMed  Google Scholar 

  25. Xiao L, Xiang L-J, Li J-W, Chen J, Fan Y-D, Zheng S-G. Laparoscopic versus open liver resection for hepatocellular carcinoma in posterosuperior segments. Surg Endosc. 2015;29(10):2994–3001.

    Article  PubMed  Google Scholar 

  26. Hu B-S, Chen K, Tan HM, Ding X-M, Tan JW. Comparison of laparoscopic vs open liver lobectomy (segmentectomy) for hepatocellular carcinoma. World J Gastroenterol. 2011;17(42):4725–8.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ker CG, Chen JS, Kuo KK, Chuang SC, Wang SJ, Chang WC et al. Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol. 2011;2011:596792.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Aldrighetti L, Guzzetti E, Pulitanò C, Cipriani F, Catena M, Paganelli M et al. Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol. 2010;102(1):82–6.

    Article  PubMed  Google Scholar 

  29. Endo Y, Ohta M, Sasaki A, Kai S, Eguchi H, Iwaki K et al. A comparative study of the long-term outcomes after laparoscopy-assisted and open left lateral hepatectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech. 2009;19(5):e171–4.

    Article  PubMed  Google Scholar 

  30. Zhang Y, Huang J, Chen X-M, Sun D-L. A comparison of laparoscopic versus open left hemihepatectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech. 2016;26(2):146–9.

    Article  PubMed  Google Scholar 

  31. Ahn KS, Kang KJ, Kim YH, Kim T-S, Lim TJ. A propensity score-matched case-control comparative study of laparoscopic and open liver resection for hepatocellular carcinoma. J Laparoendosc Adv Surg Tech. 2014;24(12):872–7.

    Article  Google Scholar 

  32. Kim H, Suh K-S, Lee K-W, Yi N-J, Hong G, Suh S-W et al. Long-term outcome of laparoscopic versus open liver resection for hepatocellular carcinoma: a case-controlled study with propensity score matching. Surg Endosc. 2014;28(3):950–60.

    Article  PubMed  Google Scholar 

  33. Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S et al. (2011) Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc. 25(11):3668–77.

    Article  CAS  PubMed  Google Scholar 

  34. Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez PL. Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg. 2003;138(7):763–9. (discussion 769).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Luo L, Zou H, Yao Y, Huang X. Laparoscopic versus open hepatectomy for hepatocellular carcinoma: short- and long-term outcomes comparison. Int J Clin Exp Med. 2015;8(10):18772–8.

    PubMed  PubMed Central  Google Scholar 

  37. Beppu T, Hayashi H, Okabe H, Imai K, Nitta H, Masuda T et al. Hybrid-including endoscopic versus open hepatic resection for patients with hepatocellular carcinoma meeting the Milan criteria: a propensity case-matched analysis. Anticancer Res. 2015;35(3):1583–90.

    PubMed  Google Scholar 

  38. Cheung TT, Poon RTP, Dai WC, Chok KSH, Chan SC, Lo CM. Pure Laparoscopic versus open left lateral sectionectomy for hepatocellular carcinoma: a single-center experience. World J Surg. 2016;40(1):198–205.

    Article  PubMed  Google Scholar 

  39. Yamashita Y-I, Ikeda T, Kurihara T, Yoshida Y, Takeishi K, Itoh S et al. 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.

    Article  PubMed  Google Scholar 

  40. 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):2919–26.

    Article  PubMed  Google Scholar 

  41. Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamazoe S, Yamamoto S et al. Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc. 2013;27(7):2592–7.

    Article  PubMed  Google Scholar 

  42. Cheung TT, Poon RTP, Yuen WK, Chok KSH, Jenkins CR, Chan SC et al. 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.

    Article  PubMed  Google Scholar 

  43. Kobayashi S, Nagano H, Marubashi S, Kawamoto K, Wada H, Eguchi H et al. Hepatectomy based on the tumor hemodynamics for hepatocellular carcinoma: a comparison among the hybrid and pure laparoscopic procedures and open surgery. Surg Endosc. 2013;27(2):610–7.

    Article  PubMed  Google Scholar 

  44. Belli G, Fantini C, D’Agostino A, Cioffi L, Langella S, Russolillo N et al. Laparoscopic versus open liver resection for hepatocellular carcinoma in patients with histologically proven cirrhosis: short- and middle-term results. Surg Endosc. 2007;21(11):2004–11.

    Article  CAS  PubMed  Google Scholar 

  45. Kaneko H, Takagi S, Otsuka Y, Tsuchiya M, Tamura A, Katagiri T et al. Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg. 2005;189(2):190–4.

    Article  PubMed  Google Scholar 

  46. Shimada M, Hashizume M, Maehara S, Tsujita E, Rikimaru T, Yamashita Y et al. Laparoscopic hepatectomy for hepatocellular carcinoma. Surg Endosc. 2001;15(6):541–4.

    Article  CAS  PubMed  Google Scholar 

  47. 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.

    Article  PubMed  Google Scholar 

  48. Cho JY, Han H-S, Yoon Y-S, Choi Y, Lee W. Outcomes of laparoscopic right posterior sectionectomy in patients with hepatocellular carcinoma in the era of laparoscopic surgery. Surgery. 2015;158(1):135–41.

    Article  PubMed  Google Scholar 

  49. Kim S-J, Jung H-K, Lee DS, Yun SS, Kim HJ. The comparison of oncologic and clinical outcomes of laparoscopic liver resection for hepatocellular carcinoma. Ann Surg Treat Res. 2014;86(2):61–7.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Ai J-H, Li J-W, Chen J, Bie P, Wang S-G, Zheng S-G. Feasibility and safety of laparoscopic liver resection for hepatocellular carcinoma with a tumor size of 5–10 cm. PLoS ONE. 2013;8(8):e72328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kim HH, Park EK, Seoung JS, Hur YH, Koh YS, Kim JC et al. Liver resection for hepatocellular carcinoma: case-matched analysis of laparoscopic versus open resection. J Korean Surg Soc. 2011;80(6):412–9.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Nguyen KT, Marsh JW, Tsung A, Steel JJL, Gamblin TC, Geller DA. Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg. 2011;146(3):348–56.

    Article  PubMed  Google Scholar 

  53. Tranchart H, Di Giuro G, Lainas P, Roudie J, Agostini H, Franco D et al. Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc. 2010;24(5):1170–6.

    Article  PubMed  Google Scholar 

  54. Lai ECH, Tang CN, Ha JPY, Li MKW (2009) Laparoscopic liver resection for hepatocellular carcinoma: ten-year experience in a single center. Arch Surg. 144(2):143–7. (discussion 148).

    Article  PubMed  Google Scholar 

  55. Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N et al. 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. 2015;22(10):721–7.

    Article  PubMed  Google Scholar 

  56. Han H-S, Shehta A, Ahn S, Yoon Y-S, Cho JY, Choi Y. Laparoscopic versus open liver resection for hepatocellular carcinoma: case-matched study with propensity score matching. J Hepatol. 2015;63(3):643–50.

    Article  PubMed  Google Scholar 

  57. Lee JJ, Conneely JB, Smoot RL, Gallinger S, Greig PD, Moulton C-A et al. Laparoscopic versus open liver resection for hepatocellular carcinoma at a North-American Centre: a 2-to-1 matched pair analysis. HPB (Oxford). 2015;17(4):304–10.

    Article  PubMed  Google Scholar 

  58. Abu HM. Why do we need guidelines in laparoscopic liver surgery? HPB (Oxford). 2017;19(4):287–8.

    Article  Google Scholar 

  59. Katz SC, Shia J, Liau KH, Gonen M, Ruo L, Jarnagin WR et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg. 2009;249(4):617–23.

    Article  PubMed  Google Scholar 

  60. Kooby DA, Stockman J, Ben-Porat L, Gonen M, Jarnagin WR, DeMatteo RP et al. Influence of transfusions on perioperative and long-term outcome in patients following hepatic resection for colorectal metastases. Ann Surg. 2003;237(6):860–9. (discussion 869–70).

    PubMed  PubMed Central  Google Scholar 

  61. Twaij A, Pucher PH, Sodergren MH, Gall T, Darzi A, Jiao LR. Laparoscopic vs open approach to resection of hepatocellular carcinoma in patients with known cirrhosis: systematic review and meta-analysis. World J Gastroenterol. 2014;20(25):8274–81.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol. 2005;5:13.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ruben Ciria MD, PhD or Mohammed Abu Hilal MD, PhD.

Additional information

Manuscript and research performed in the context of the European Guidelines Meeting on Laparoscopic Liver Surgery held in Southampton, UK, from 9 to 11 February 2017.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Digital Content 1. PRISMA model flow chart of eligible studies (TIFF 22973 kb)

Supplementary Digital Content 2. Baseline descriptive results from all eligible studies. (DOCX 158 kb)

10434_2018_6926_MOESM3_ESM.docx

Supplementary Digital Content 3. Baseline descriptive results of post-hepatectomy liver failure (PHLF) including PHLF-A, -B or –C as defined by the ISGLS16 and mortality from all eligible studies. (DOCX 36 kb)

10434_2018_6926_MOESM4_ESM.tiff

Supplementary Digital Content 4. Meta-analysis of short-term outcomes (post-hepatectomy liver failure (PHLF) including PHLF-A, -B or –C as defined by the ISGLS16). (TIFF 5670 kb)

Supplementary Digital Content 5. Bias analysis (funnel plots) of short-term outcomes (I). (TIFF 22973 kb)

Supplementary Digital Content 6. Bias analysis (funnel plots) of short-term outcomes (II). (TIFF 22973 kb)

Supplementary Digital Content 7. Bias analysis (funnel plots) of long-term outcomes (I). (TIFF 22973 kb)

Supplementary Digital Content 8. Bias analysis (funnel plots) of long-term outcomes (II). (TIFF 22973 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ciria, R., Gomez-Luque, I., Ocaña, S. et al. A Systematic Review and Meta-Analysis Comparing the Short- and Long-Term Outcomes for Laparoscopic and Open Liver Resections for Hepatocellular Carcinoma: Updated Results from the European Guidelines Meeting on Laparoscopic Liver Surgery, Southampton, UK, 2017. Ann Surg Oncol 26, 252–263 (2019). https://doi.org/10.1245/s10434-018-6926-3

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-018-6926-3

Keywords

Navigation