Efficacy of laparoscopic <i>versus</i> open hepatectomy on the hepatocellular carcinoma patients with cirrhosis: a meta-analysis _Chinese Journal of Evidence-Based Medicine

Authors：

JIANG Song , WANG Zhaoying , OU Mingrui ,  CUI Peiyuan

The First Affiliated Hospital of Bengbu Medical College, Bengbu, 233000, P.R.China;

Corresponding author：

CUI Peiyuan, Email: Cpy666@126.com

Keywords：

Laparoscopic hepatectomy; Open hepatectomy; Hepatocellular carcinoma; Cirrhosis; Meta-analysis; Systematic review; Cohort study

DOI：

10.7507/1672-2531.201802054

Video：

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ObjectivesTo systematically review the efficacy of laparoscopic hepatectomy (LH) and open hepatectomy (OH) on the hepatocellular carcinoma patients with cirrhosis.MethodsPubMed, EMbase, Web of Science, The Cochrane Library, CBM, CNKI, WanFang Data and VIP databases were searched online to collect the cohort studies of LHvs.OH on hepatocellular carcinoma patients with cirrhosis from inception to November 31^st, 2017. Two reviewers independently screened literature, extracted data and assessed the risk of bias of included studies, then, meta-analysis was performed by using RevMan 5.3 software.ResultsA total of 15 cohort studies involving 1 720 patients were included. The results of meta-analysis showed that: compared with OH, LH had less blood loss (MD=–226.94, 95%CI –339.87 to –114.01, P<0.000 1), lower transfusion rate (OR=0.48, 95%CI 0.27 to 0.83,P=0.009), less occurrence of complications (OR=0.32, 95%CI 0.23 to 0.45, P<0.000 01), shorter postoperative hospital stay (MD=–3.66, 95%CI –5.19 to –2.14,P<0.000 01), lower mortality rate (OR=0.47, 95%CI 0.24 to 0.92,P=0.03), wider surgical margin (OR=0.78, 95%CI 0.20 to 1.36, P=0.009), higher 1, 3 and 5-year survival rate (OR=2.47, 95%CI 1.35 to 4.51, P=0.003; OR=1.62, 95%CI 1.11 to 2.36, P=0.01; OR=1.58, 95%CI 1.19 to 2.10, P=0.002, respectively) and 1-year disease free survival rate (OR=1.69, 95%CI=1.20 to 2.39, P=0.003). There were no significant differences in operation time (MD=28.64, 95%CI –7.53 to 64.82, P=0.12), tumor size (MD=–0.37, 95%CI –0.75 to 0.02, P=0.06), 3-year disease free survival rate (OR=1.14, 95%CI 0.86 to 1.51, P=0.36) and 5-year disease free survival rate (OR=0.99, 95%CI 0.77 to 1.28, P=0.97) between the two groups.ConclusionsThe perioperation and short-term postoperative outcomes of LH are significant in HCC patients with cirrhosis, and which have good long-term prognosis. Due to limited quality and quantity of the included studies, more high quality studies are required to verify above conclusions.

Citation： JIANG Song, WANG Zhaoying, OU Mingrui, CUI Peiyuan. Efficacy of laparoscopic versus open hepatectomy on the hepatocellular carcinoma patients with cirrhosis: a meta-analysis . Chinese Journal of Evidence-Based Medicine, 2018, 18(9): 931-940. doi: 10.7507/1672-2531.201802054 Copy

1.	Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet, 2003, 362(9399): 1907-1917.
2.	Hao K, Luk JM, Lee NP, et al. Predicting prognosis in hepatocellular carcinoma after curative surgery with common clinicopathologic parameters. BMC Cancer, 2009, 9: 389.
3.	Llovet JM, Bruix J. Novel advancements in the management of hepatocellular carcinoma in 2008. J Hepatol, 2008, 48(Suppl 1): S20-S37.
4.	Qi X, Zhao Y, Li H, et al. Management of hepatocellular carcinoma: an overview of major findings from meta-analyses. Oncotarget, 2016, 7(23): 34703-34751.
5.	Llovet JM, Fuster J, Bruix J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology, 1999, 30(6): 1434-1440.
6.	Gaillard M, Tranchart H, Dagher I. Laparoscopic liver resections for hepatocellular carcinoma: current role and limitations. World J Gastroenterol, 2014, 20(17): 4892-4899.
7.	Tanabe G, Sakamoto M, Akazawa K, et al. Intraoperative risk factors associated with hepatic resection. Br J Surg, 1995, 82(9): 1262-1265.
8.	Fan ST, Mau LC, Poon RT, et al. Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg, 2011, 253(4): 745-758.
9.	Kanazawa A, Tsukamoto T, Shimizu S, et al. Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc, 2013, 27(7): 2592-2597.
10.	Reynolds WJr. The first laparoscopic cholecystectomy. JSLS, 2001, 5(1): 89-94.
11.	Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg, 2009, 250(5): 825-830.
12.	许大彬. 中国大陆腹腔镜肝切除术发展历史及现状. 腹腔镜外科杂志, 2016, 21(9): 714-716.
13.	Kaneko H, Takagi S, Otsuka Y, et al. Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg, 2005, 189(2): 190-194.
14.	Twaij A, Pucher PH, Sodergren MH, et al. 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): 8274-8281.
15.	Chen J, Bai T, Zhang Y, et al. The safety and efficacy of laparoscopic and open hepatectomy in hepatocellular carcinoma patients with liver cirrhosis: a systematic review. Int J Clin Exp Med, 2015, 8(11): 20679-20689.
16.	马逸云, 蒋华, 张宏亨. 腹腔镜肝切除术与开腹肝切除术治疗肝硬化肝细胞癌患者的效果比较. 临床肝胆病杂志, 2016, 32(10): 1916-1919.
17.	Cheung TT, Dai WC, Tsang SH, et al. Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg, 2016, 264(4): 612-620.
18.	Tanaka S, Takemura S, Shinkawa H, et al. Outcomes of pure laparoscopic versus open hepatic resection for hepatocellular carcinoma in cirrhotic patients: a case-control study with propensity score matching. Eur Surg Res, 2015, 55(4): 291-301.
19.	Sposito C, Battiston C, Facciorusso A, et al. Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg, 2016, 103(7): 871-880.
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(9): 1041-1048.
21.	Yoon YI, Kim KH, Kang SH, et al. Pure laparoscopic versus open right hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score matched analysis. Ann Surg, 2017, 265(5): 856-863.
22.	徐军辉, 丁佑铭, 汪斌, 等. 腹腔镜肝切除术在肝癌合并肝硬化患者的应用. 临床肝胆病杂志, 2014, (6): 552-555.
23.	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(10): 2268-2274.
24.	Jiang X, Liu L, Zhang Q, et al. Laparoscopic versus open hepatectomy for hepatocellular carcinoma: long-term outcomes. J BUON, 2016, 21(1): 135-141.
25.	Memeo R, de'Angelis N, Compagnon P, et al. Laparoscopic vs. open liver resection for hepatocellular carcinoma of cirrhotic liver: a case-control study. World J Surg, 2014, 38(11): 2919-2926.
26.	Xu HW, Liu F, Li HY, et al. Outcomes following laparoscopic versus open major hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score-matched analysis. Surg Endosc, 2018, 32(2): 712-719.
27.	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(11): 3668-3677.
28.	Yamashita Y, Ikeda T, Kurihara T, 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): 1117-1123.
29.	王琦, 段键, 林杰, 等. 腹腔镜肝切除治疗肝癌合并肝硬化的短期疗效. 世界华人消化杂志, 2016, 24(12): 1910-1915.
30.	Worhunsky DJ, Dua MM, Tran TB, et al. Laparoscopic hepatectomy in cirrhotics: safe if you adjust technique. Surg Endosc, 2016, 30(10): 4307-4314.
31.	Cherian PT, Mishra AK, Kumar P, et al. Laparoscopic liver resection: wedge resections to living donor hepatectomy, are we heading in the right direction? World J Gastroenterol, 2014, 20(37): 13369-13381.
32.	Parks KR, Kuo YH, Davis JM, et al. Laparoscopic versus open liver resection: a meta-analysis of long-term outcome. HPB (Oxford), 2014, 16(2): 109-118.
33.	Chang SK, Tay CW, Shen L, et al. Long-term oncological safety of minimally invasive hepatectomy in patients with hepatocellular carcinoma: a case-control study. Ann Acad Med Singapore, 2016, 45(3): 91-97.
34.	Fancellu A, Rosman AS, Sanna V, et al. Meta-analysis of trials comparing minimally-invasive and open liver resections for hepatocellular carcinoma. J Surg Res, 2011, 171(1): e33-e45.
35.	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(1): 82-86.
36.	Mirnezami R, Mirnezami AH, Chandrakumaran K, et al. Short- and long-term outcomes after laparoscopic and open hepatic resection: systematic review and meta-analysis. HPB (Oxford), 2011, 13(5): 295-308.
37.	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(2): 143-147.
38.	Xiong JJ, Altaf K, Javed MA, et al. Meta-analysis of laparoscopic vs open liver resection for hepatocellular carcinoma. World J Gastroenterol, 2012, 18(45): 6657-6668.
39.	Lesurtel M, Cherqui D, Laurent A, et al. Laparoscopic versus open left lateral hepatic lobectomy: a case-control study. J Am Coll Surg, 2003, 196(2): 236-242.
40.	Laurent A, Cherqui D, Lesurtel M, et al. Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg, 2003, 138(7): 763-769.
41.	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(6): 412-419.
42.	Guro H, Cho JY, Han HS, et al. Current status of laparoscopic liver resection for hepatocellular carcinoma. Clin Mol Hepatol, 2016, 22(2): 212-218.
43.	Katz SC, Shia J, Liau KH, et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg, 2009, 249(4): 617-623.
44.	Novitsky YW, Litwin DE, Callery MP. The net immunologic advantage of laparoscopic surgery. Surg Endosc, 2004, 18(10): 1411-1419.
45.	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(1): 36-43.

1. Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet, 2003, 362(9399): 1907-1917.
2. Hao K, Luk JM, Lee NP, et al. Predicting prognosis in hepatocellular carcinoma after curative surgery with common clinicopathologic parameters. BMC Cancer, 2009, 9: 389.
3. Llovet JM, Bruix J. Novel advancements in the management of hepatocellular carcinoma in 2008. J Hepatol, 2008, 48(Suppl 1): S20-S37.
4. Qi X, Zhao Y, Li H, et al. Management of hepatocellular carcinoma: an overview of major findings from meta-analyses. Oncotarget, 2016, 7(23): 34703-34751.
5. Llovet JM, Fuster J, Bruix J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology, 1999, 30(6): 1434-1440.
6. Gaillard M, Tranchart H, Dagher I. Laparoscopic liver resections for hepatocellular carcinoma: current role and limitations. World J Gastroenterol, 2014, 20(17): 4892-4899.
7. Tanabe G, Sakamoto M, Akazawa K, et al. Intraoperative risk factors associated with hepatic resection. Br J Surg, 1995, 82(9): 1262-1265.
8. Fan ST, Mau LC, Poon RT, et al. Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg, 2011, 253(4): 745-758.
9. Kanazawa A, Tsukamoto T, Shimizu S, et al. Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc, 2013, 27(7): 2592-2597.
10. Reynolds WJr. The first laparoscopic cholecystectomy. JSLS, 2001, 5(1): 89-94.
11. Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg, 2009, 250(5): 825-830.
12. 许大彬. 中国大陆腹腔镜肝切除术发展历史及现状. 腹腔镜外科杂志, 2016, 21(9): 714-716.
13. Kaneko H, Takagi S, Otsuka Y, et al. Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg, 2005, 189(2): 190-194.
14. Twaij A, Pucher PH, Sodergren MH, et al. 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): 8274-8281.
15. Chen J, Bai T, Zhang Y, et al. The safety and efficacy of laparoscopic and open hepatectomy in hepatocellular carcinoma patients with liver cirrhosis: a systematic review. Int J Clin Exp Med, 2015, 8(11): 20679-20689.
16. 马逸云, 蒋华, 张宏亨. 腹腔镜肝切除术与开腹肝切除术治疗肝硬化肝细胞癌患者的效果比较. 临床肝胆病杂志, 2016, 32(10): 1916-1919.
17. Cheung TT, Dai WC, Tsang SH, et al. Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg, 2016, 264(4): 612-620.
18. Tanaka S, Takemura S, Shinkawa H, et al. Outcomes of pure laparoscopic versus open hepatic resection for hepatocellular carcinoma in cirrhotic patients: a case-control study with propensity score matching. Eur Surg Res, 2015, 55(4): 291-301.
19. Sposito C, Battiston C, Facciorusso A, et al. Propensity score analysis of outcomes following laparoscopic or open liver resection for hepatocellular carcinoma. Br J Surg, 2016, 103(7): 871-880.
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(9): 1041-1048.
21. Yoon YI, Kim KH, Kang SH, et al. Pure laparoscopic versus open right hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score matched analysis. Ann Surg, 2017, 265(5): 856-863.
22. 徐军辉, 丁佑铭, 汪斌, 等. 腹腔镜肝切除术在肝癌合并肝硬化患者的应用. 临床肝胆病杂志, 2014, (6): 552-555.
23. 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(10): 2268-2274.
24. Jiang X, Liu L, Zhang Q, et al. Laparoscopic versus open hepatectomy for hepatocellular carcinoma: long-term outcomes. J BUON, 2016, 21(1): 135-141.
25. Memeo R, de'Angelis N, Compagnon P, et al. Laparoscopic vs. open liver resection for hepatocellular carcinoma of cirrhotic liver: a case-control study. World J Surg, 2014, 38(11): 2919-2926.
26. Xu HW, Liu F, Li HY, et al. Outcomes following laparoscopic versus open major hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score-matched analysis. Surg Endosc, 2018, 32(2): 712-719.
27. 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(11): 3668-3677.
28. Yamashita Y, Ikeda T, Kurihara T, 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): 1117-1123.
29. 王琦, 段键, 林杰, 等. 腹腔镜肝切除治疗肝癌合并肝硬化的短期疗效. 世界华人消化杂志, 2016, 24(12): 1910-1915.
30. Worhunsky DJ, Dua MM, Tran TB, et al. Laparoscopic hepatectomy in cirrhotics: safe if you adjust technique. Surg Endosc, 2016, 30(10): 4307-4314.
31. Cherian PT, Mishra AK, Kumar P, et al. Laparoscopic liver resection: wedge resections to living donor hepatectomy, are we heading in the right direction? World J Gastroenterol, 2014, 20(37): 13369-13381.
32. Parks KR, Kuo YH, Davis JM, et al. Laparoscopic versus open liver resection: a meta-analysis of long-term outcome. HPB (Oxford), 2014, 16(2): 109-118.
33. Chang SK, Tay CW, Shen L, et al. Long-term oncological safety of minimally invasive hepatectomy in patients with hepatocellular carcinoma: a case-control study. Ann Acad Med Singapore, 2016, 45(3): 91-97.
34. Fancellu A, Rosman AS, Sanna V, et al. Meta-analysis of trials comparing minimally-invasive and open liver resections for hepatocellular carcinoma. J Surg Res, 2011, 171(1): e33-e45.
35. 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(1): 82-86.
36. Mirnezami R, Mirnezami AH, Chandrakumaran K, et al. Short- and long-term outcomes after laparoscopic and open hepatic resection: systematic review and meta-analysis. HPB (Oxford), 2011, 13(5): 295-308.
37. 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(2): 143-147.
38. Xiong JJ, Altaf K, Javed MA, et al. Meta-analysis of laparoscopic vs open liver resection for hepatocellular carcinoma. World J Gastroenterol, 2012, 18(45): 6657-6668.
39. Lesurtel M, Cherqui D, Laurent A, et al. Laparoscopic versus open left lateral hepatic lobectomy: a case-control study. J Am Coll Surg, 2003, 196(2): 236-242.
40. Laurent A, Cherqui D, Lesurtel M, et al. Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg, 2003, 138(7): 763-769.
41. 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(6): 412-419.
42. Guro H, Cho JY, Han HS, et al. Current status of laparoscopic liver resection for hepatocellular carcinoma. Clin Mol Hepatol, 2016, 22(2): 212-218.
43. Katz SC, Shia J, Liau KH, et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg, 2009, 249(4): 617-623.
44. Novitsky YW, Litwin DE, Callery MP. The net immunologic advantage of laparoscopic surgery. Surg Endosc, 2004, 18(10): 1411-1419.
45. 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(1): 36-43.

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Efficacy of laparoscopic versus open hepatectomy on the hepatocellular carcinoma patients with cirrhosis: a meta-analysis

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