Annals of Surgical Oncology

, Volume 20, Issue 4, pp 1203–1215 | Cite as

Short- and Long-term Outcomes after Laparoscopic and Open Hepatectomy for Hepatocellular Carcinoma: A Global Systematic Review and Meta-analysis

Hepatobiliary Tumors

Abstract

Background

Laparoscopic hepatectomy (LH) has been proposed as a safe and feasible treatment option for liver diseases. However, the short- and long-term outcomes of LH versus open hepatectomy (OH) for hepatocellular carcinoma (HCC) have not been adequately assessed. Thus, as another means of surgical therapy for hepatocellular carcinoma (HCC), we assessed the feasibility of performing LH as the standard procedure for disease in the left lateral lobe and peripheral right segments for HCC in selected patients.

Methods

Literature search included PubMed, Embase, Science Citation Index, SpringerLink, and secondary sources, from inception to March 2012, with no restrictions on languages or regions. The fixed-effects and random-effects models were used to measure the pooled estimates. The test of heterogeneity was performed by the Q statistic. Subgroup and sensitivity analyses were performed to explore heterogeneity between studies and to assess the effects of study quality.

Results

A total of 1238 patients (LH 485, OH 753) from 15 studies were included. The pooled odds ratios for postoperative morbidity and incidence of negative surgical margin in LH were found to be 0.37 (95 % confidence interval [CI] 0.27–0.52; P < 0.01) and 1.63 (95 % CI 0.82–3.22; P = 0.16), respectively, compared with OH. Blood loss was significantly decreased in the LH (weighted mean difference −224.63; 95 % CI −384.87 to −64.39; P = 0.006). No significant difference was observed between the both groups for long-term outcomes of overall survival and recurrence-free survival.

Conclusions

In patients with solitary left lateral lobe/right peripheral subcapsular tumors treated with minor resection, this meta-analysis demonstrated that compared to OH, LH may have short-term advantages in terms of blood loss and postoperative morbidity for HCC. Both procedures have similar long-term outcomes. It may be time to consider changing the standard procedures for treatment of HCC in the left lateral lobe and peripheral subcapsular right segments in selected patients.

Notes

Acknowledgment

This study was not supported by any pharmaceutical company or grants; the cost was borne by the authors’ institutions. The authors thank Prof. Yuantao Hao, Department of Medical Statistics, Sun Yat-sen University, Guangdong, China, for statistical advice; and Yan Jia, Medical Library of North Campus, Sun Yat-sen University, Guangdong, China, for the literature search. Neither of these persons received compensation for the work performed.

Supplementary material

10434_2012_2705_MOESM1_ESM.pdf (101 kb)
Supplementary material 1 (PDF 101 kb)

References

  1. 1.
    Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet. 2003;362:1907–17.PubMedCrossRefGoogle Scholar
  2. 2.
    Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection—2,804 patients. Ann Surg. 2009;250:831–41.PubMedCrossRefGoogle Scholar
  3. 3.
    Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg. 2009;250:825–30.PubMedCrossRefGoogle Scholar
  4. 4.
    Nguyen KT, Marsh JW, Tsung A, et al. Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg. 2011;146:348–56.PubMedCrossRefGoogle Scholar
  5. 5.
    Truant S, Bouras AF, Hebbar M, et al. Laparoscopic resection vs open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc. 2011;25:3668–77.PubMedCrossRefGoogle Scholar
  6. 6.
    Koffron AJ, Auffenberg G, Kung R, et al. Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg. 2007;246:385–92.PubMedCrossRefGoogle Scholar
  7. 7.
    Buell JF, Thomas MT, Rudich S, et al. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg. 2008;248:475–86.PubMedGoogle Scholar
  8. 8.
    Topal B, Fieuws S, Aerts R, et al. Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of short-term results. Surg Endosc. 2008;22:2208–13.PubMedCrossRefGoogle Scholar
  9. 9.
    Kazaryan AM, Pavlik Marangos I, Rosseland AR, et al. Laparoscopic liver resection for malignant and benign lesions: ten-year Norwegian single-center experience. Arch Surg. 2010;145:34–40.PubMedCrossRefGoogle Scholar
  10. 10.
    Lee KF, Chong CN, Wong J, et al. Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg. 2011;35:2268–74.PubMedCrossRefGoogle Scholar
  11. 11.
    Reddick EJ, Olsen DO. Laparoscopic laser cholecystectomy. A comparison with mini-lap cholecystectomy. Surg Endosc. 1989;3:131–3.PubMedCrossRefGoogle Scholar
  12. 12.
    Dubois F, Icard P, Berthelot G, et al. Coelioscopic cholecystectomy. Preliminary report of 36 cases. Ann Surg. 1990;211:60–2.PubMedCrossRefGoogle Scholar
  13. 13.
    Gigot JF, Glineur D, Santiago Azagra J, et al.; Hepatobiliary and Pancreatic Section of the Royal Belgian Society of Surgery and the Belgian Group for Endoscopic Surgery. Laparoscopic liver resection for malignant liver tumors: preliminary results of a multicenter European study. Ann Surg. 2002;236:90–7.PubMedCrossRefGoogle Scholar
  14. 14.
    Santambrogio R, Aldrighetti L, Barabino M, et al. Laparoscopic liver resections for hepatocellular carcinoma. Is it a feasible option for patients with liver cirrhosis? Langenbecks Arch Surg. 2009;394:255–64.PubMedCrossRefGoogle Scholar
  15. 15.
    Laurent A, Cherqui D, Lesurtel M, et al. Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg. 2003;138:763–9.PubMedCrossRefGoogle Scholar
  16. 16.
    Cherqui D, Laurent A, Tayar C, et al. Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: midterm results and perspectives. Ann Surg. 2006;243:499–506.PubMedCrossRefGoogle Scholar
  17. 17.
    Hu BS, Chen K, Tan HM, et al. Comparison of laparoscopic vs open liver lobectomy (segmentectomy) for hepatocellular carcinoma. World J Gastroenterol. 2011;17:4725–8.PubMedCrossRefGoogle Scholar
  18. 18.
    Kim HH, Park EK, Seoung JS, et al. Liver resection for hepatocellular carcinoma: case-matched analysis of laparoscopic versus open resection. J Korean Surg Soc. 2011;80:412–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Ker CG, Chen JS, Kuo KK, et al. Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol. 2011;2011:596792.PubMedGoogle Scholar
  20. 20.
    Belli G, Limongelli P, Fantini C, et al. Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg. 2009;96:1041–8.PubMedCrossRefGoogle Scholar
  21. 21.
    Lai EC, Tang CN, Ha JP, et al. Laparoscopic liver resection for hepatocellular carcinoma: ten-year experience in a single center. Arch Surg. 2009;144:143–7.PubMedCrossRefGoogle Scholar
  22. 22.
    Descottes B, Lachachi F, Sodji M, et al. Early experience with laparoscopic approach for solid liver tumors: initial 16 cases. Ann Surg. 2000;232:641–5.PubMedCrossRefGoogle Scholar
  23. 23.
    Dagher I, Di Giuro G, Dubrez J, et al. Laparoscopic versus open right hepatectomy: a comparative study. Am J Surg. 2009;198:173–7.PubMedCrossRefGoogle Scholar
  24. 24.
    Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA. 2000;283:2008–12.PubMedCrossRefGoogle Scholar
  25. 25.
    Wells GA, Shea B, O’Connell D, et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed February 29, 2012.
  26. 26.
    Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17:2815–34.PubMedCrossRefGoogle Scholar
  27. 27.
    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.PubMedCrossRefGoogle Scholar
  28. 28.
    Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions version 5.1.0. March 2011. Cochrane Collaboration, 2011. Available at: http://www.cochrane-handbook.org. Accessed March 29, 2012.
  29. 29.
    Sarpel U, Hefti MM, Wisnievsky JP, et al. Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: case-matched analysis. Ann Surg Oncol. 2009;16:1572–7.PubMedCrossRefGoogle Scholar
  30. 30.
    Tranchart H, Di Giuro G, Lainas P, et al. Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc. 2010;24:1170–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Hasegawa K, Kokudo N, Imamura H, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg. 2005;242:252–9.PubMedCrossRefGoogle Scholar
  32. 32.
    Kaneko H, Takagi S, Otsuka Y, et al. Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg. 2005;189:190–4.PubMedCrossRefGoogle Scholar
  33. 33.
    Endo Y, Ohta M, Sasaki A, 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:e171–4.PubMedCrossRefGoogle Scholar
  34. 34.
    Stephenson KR, Steinberg SM, Hughes KS, et al. Perioperative blood transfusions are associated with decreased time to recurrence and decreased survival after resection of colorectal liver metastases. Ann Surg. 1988;208:679–87.PubMedCrossRefGoogle Scholar
  35. 35.
    Jarnagin WR, Gonen M, Fong Y, et al. Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg. 2002;236:397–406.PubMedCrossRefGoogle Scholar
  36. 36.
    Kooby DA, Stockman J, Ben-Porat L, et al. Influence of transfusion on perioperative and long-term outcome in patients following hepatic resection for colorectal metastases. Ann Surg. 2003;237:860–9.PubMedGoogle Scholar
  37. 37.
    Figueras J, Llado L, Ruiz D, et al. Complete versus selective portal triad clamping for minor liver resections: a prospective randomized trial. Ann Surg. 2005;241:582–90.PubMedCrossRefGoogle Scholar
  38. 38.
    Scatton O, Massault PP, Dousset B, et al. Major liver resection without clamping: a prospective reappraisal in the era of modern surgical tools. J Am Coll Surg. 2004;199:702–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Sugiyama Y, Ishizaki Y, Imamura H, et al. Effects of intermittent Pringle’s manoeuvre on cirrhotic compared with normal liver. Br J Surg. 2010;97:1062–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Shi M, Guo RP, Lin XJ, et al. Partial hepatectomy with wide versus narrow resection margin for solitary hepatocellular carcinoma: a prospective randomized trial. Ann Surg. 2007;245:36–43.PubMedCrossRefGoogle Scholar
  41. 41.
    Clavien PA, Sanabria JR, Strasberg SM. Proposed classification of complications of surgery with examples of utility in cholecystectomy. Surgery. 1992;111:518–26.PubMedGoogle Scholar
  42. 42.
    Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6,336 patients and results of a survey. Ann Surg. 2004;240:205–13.PubMedCrossRefGoogle Scholar
  43. 43.
    Haga Y, Ikei S, Ogawa M. Estimation of physiologic ability and surgical stress (E-PASS) as a new prediction scoring system for postoperative morbidity and mortality following elective gastrointestinal surgery. Surg Today. 1999;29:219–25.PubMedCrossRefGoogle Scholar
  44. 44.
    Bruix J, Castells A, Bosch J, et al. Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology. 1996;111:1018–22.PubMedCrossRefGoogle Scholar
  45. 45.
    Powell-Jackson P, Greenway B, Williams R. Adverse effects of exploratory laparotomy in patients with unsuspected liver disease. Br J Surg. 1982;69:449–51.PubMedCrossRefGoogle Scholar
  46. 46.
    Schemmer P, Schoonhoven R, Swenberg JA, et al. Gentle in situ liver manipulation during organ harvest decreases survival after rat liver transplantation: role of Kupffer cells. Transplantation. 1998;65:1015–20.PubMedCrossRefGoogle Scholar
  47. 47.
    Schemmer P, Enomoto N, Bradford BU, et al. Activated Kupffer cells cause a hypermetabolic state after gentle in situ manipulation of liver in rats. Am J Physiol Gastrointest Liver Physiol. 2001;280:G1076–82.PubMedGoogle Scholar
  48. 48.
    Arroyo V, Ginès P, Planas R. Treatment of ascites in cirrhosis. Diuretics, peritoneovenous shunt, and large-volume paracentesis. Gastroenterol Clin North Am. 1992;21:237–56.PubMedGoogle Scholar
  49. 49.
    Kawamoto C, Ido K, Isoda N, et al. Long-term outcomes for patients with solitary hepatocellular carcinoma treated by laparoscopic microwave coagulation. Cancer. 2005;103:985–93.PubMedCrossRefGoogle Scholar
  50. 50.
    Aldrighetti L, Guzzetti E, Pulitanò C, et al. Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol. 2010;102:82–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Shimada M, Hashizume M, Maehara S, et al. Laparoscopic hepatectomy for hepatocellular carcinoma. Surg Endosc. 2001;15:541–4.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2012

Authors and Affiliations

  • Zi Yin
    • 1
  • Xinxiang Fan
    • 2
  • Hua Ye
    • 1
  • Dong Yin
    • 3
  • Jie Wang
    • 1
  1. 1.General Surgery Department, Cancer Research CenterSun Yat-sen Memorial Hospital of Sun Yat-sen UniversityGuangzhouChina
  2. 2.Urology DepartmentSun Yat-sen Memorial Hospital of Sun Yat-sen UniversityGuangzhouChina
  3. 3.Division of Hematology and OncologyCedars-Sinai Medical Center, University of California at Los Angeles School of MedicineLos AngelesUSA

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