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Published in: Annals of Surgical Oncology 4/2013

01-04-2013 | Hepatobiliary Tumors

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

Authors: Zi Yin, MD, Xinxiang Fan, MD, Hua Ye, MD, Dong Yin, PhD, Jie Wang, MD, PhD

Published in: Annals of Surgical Oncology | Issue 4/2013

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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.
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Literature
2.
go back to reference Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection—2,804 patients. Ann Surg. 2009;250:831–41.PubMedCrossRef Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection—2,804 patients. Ann Surg. 2009;250:831–41.PubMedCrossRef
3.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
4.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
5.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
6.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
7.
go back to reference Buell JF, Thomas MT, Rudich S, et al. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg. 2008;248:475–86.PubMed Buell JF, Thomas MT, Rudich S, et al. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg. 2008;248:475–86.PubMed
8.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
9.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
10.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
11.
go back to reference Reddick EJ, Olsen DO. Laparoscopic laser cholecystectomy. A comparison with mini-lap cholecystectomy. Surg Endosc. 1989;3:131–3.PubMedCrossRef Reddick EJ, Olsen DO. Laparoscopic laser cholecystectomy. A comparison with mini-lap cholecystectomy. Surg Endosc. 1989;3:131–3.PubMedCrossRef
12.
go back to reference Dubois F, Icard P, Berthelot G, et al. Coelioscopic cholecystectomy. Preliminary report of 36 cases. Ann Surg. 1990;211:60–2.PubMedCrossRef Dubois F, Icard P, Berthelot G, et al. Coelioscopic cholecystectomy. Preliminary report of 36 cases. Ann Surg. 1990;211:60–2.PubMedCrossRef
13.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
14.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
15.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
16.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
17.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference Ker CG, Chen JS, Kuo KK, et al. Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol. 2011;2011:596792.PubMed Ker CG, Chen JS, Kuo KK, et al. Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol. 2011;2011:596792.PubMed
20.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
23.
go back to reference Dagher I, Di Giuro G, Dubrez J, et al. Laparoscopic versus open right hepatectomy: a comparative study. Am J Surg. 2009;198:173–7.PubMedCrossRef Dagher I, Di Giuro G, Dubrez J, et al. Laparoscopic versus open right hepatectomy: a comparative study. Am J Surg. 2009;198:173–7.PubMedCrossRef
24.
go back to reference Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA. 2000;283:2008–12.PubMedCrossRef Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA. 2000;283:2008–12.PubMedCrossRef
26.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
31.
go back to reference Hasegawa K, Kokudo N, Imamura H, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg. 2005;242:252–9.PubMedCrossRef Hasegawa K, Kokudo N, Imamura H, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg. 2005;242:252–9.PubMedCrossRef
32.
go back to reference Kaneko H, Takagi S, Otsuka Y, et al. Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg. 2005;189:190–4.PubMedCrossRef Kaneko H, Takagi S, Otsuka Y, et al. Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg. 2005;189:190–4.PubMedCrossRef
33.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
34.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
35.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
36.
go back to reference 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.PubMed 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.PubMed
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
40.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
41.
go back to reference Clavien PA, Sanabria JR, Strasberg SM. Proposed classification of complications of surgery with examples of utility in cholecystectomy. Surgery. 1992;111:518–26.PubMed Clavien PA, Sanabria JR, Strasberg SM. Proposed classification of complications of surgery with examples of utility in cholecystectomy. Surgery. 1992;111:518–26.PubMed
42.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
43.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
44.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
45.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
46.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
47.
go back to reference 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.PubMed 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.PubMed
48.
go back to reference 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.PubMed 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.PubMed
49.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
50.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
51.
go back to reference Shimada M, Hashizume M, Maehara S, et al. Laparoscopic hepatectomy for hepatocellular carcinoma. Surg Endosc. 2001;15:541–4.PubMedCrossRef Shimada M, Hashizume M, Maehara S, et al. Laparoscopic hepatectomy for hepatocellular carcinoma. Surg Endosc. 2001;15:541–4.PubMedCrossRef
Metadata
Title
Short- and Long-term Outcomes after Laparoscopic and Open Hepatectomy for Hepatocellular Carcinoma: A Global Systematic Review and Meta-analysis
Authors
Zi Yin, MD
Xinxiang Fan, MD
Hua Ye, MD
Dong Yin, PhD
Jie Wang, MD, PhD
Publication date
01-04-2013
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 4/2013
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-012-2705-8

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