Liver resection can improve long-term survival for liver metastases from colorectal cancer. Laparoscopic hepatectomy is gaining increasing applications in colorectal liver metastases. We conducted a meta-analysis to investigate the safety, feasibility, and efficacy of laparoscopic liver resection compared with open hepatectomy for patients with colorectal liver metastases.
Materials and Methods:
We performed both database and manual searching for comparative studies published before June 2013 without language or region restriction. Outcomes of interest consisted of perioperative outcomes and oncologic outcomes.
Results:
Seven observational studies including 624 patients (241 in the laparoscopic group, 383 in the open group) were included. No randomized controlled trials were available. Pooled long-term oncologic outcomes of overall survival (hazard ratio=0.844; 95% confidence interval [CI] 0.412, 1.730; P=.644; I2=80.6%) and disease-free survival (hazard ratio=1.234; 95% CI 0.652, 2.333; P=.518; I2=79.6%) were similar in both groups. Subgroup analyses of studies with high quality and homogeneity confirmed the above outcomes. However, a lower incidence of R1 resection was observed in the laparoscopic group (relative risk [RR]=0.357; 95% CI 0.180, 0.708; P=.003; I2=0.0%) than in the open group. As for perioperative outcomes, laparoscopic hepatectomy presented a lower occurrence of postoperative complications (RR=0.647; 95% CI 0.477, 0.877; P=.005; I2=0.0%) and similar mortality (RR=0.625; 95% CI 0.12, 3.25; P=.576; I2=0.0%); less blood loss and less need for transfusion were also found in laparoscopic patients, whereas comparable operative time and length of hospital stay were required in the two groups.
Conclusions:
Laparoscopic hepatectomy is a safe procedure for colorectal liver metastases with long-term survival comparable to that of open hepatectomy. More prospective studies with adequate subgroup analyses are awaited to construct defined criteria for patient selection. Future randomized controlled trials are needed to eliminate potential selection bias and to confirm this conclusion.
Get full access to this article
View all access options for this article.
References
1.
GagnerM, RheaultM, DubucJ. Laparoscopic partial hepatectomy for liver tumor [abstract]. In: Abstracts of the 1992 Scientific Session of the Society of American Gastrointestinal Surgeons (SAGES), Washington, D.C., USA, April 11–12, 1992. Surg Endosc, 1992;6:99.
2.
CherquiD, HussonE, HammoudR, MalassagneB, StephanF, BensaidS, RotmanN, FagniezPL. Laparoscopic liver resections: A feasibility study in 30 patients. Ann Surg, 2000; 232:753–761.
SzecelD, DerooverA, DelwaideJ, PolusM, KabaA, HonoreP, DetryO. Laparoscopic liver resection: A single center experience [abstract #O155]. Surg Endosc, 2013; 27:S36.
8.
MorinoM, MorraI, RossoE, MigliettaC, GarroneC. Laparoscopic vs open hepatic resection: A comparative study. Surg Endosc, 2003; 17:1914–1918.
9.
KoffronAJ, AuffenbergG, KungR, AbecassisM. Evaluation of 300 minimally invasive liver resections at a single institution. Ann Surg, 2007; 246:385–394.
10.
TsinbergM, TelliogluG, SimpfendorferCH, WalshMR, VogtD, FungJ, BerberE. Comparison of laparoscopic versus open liver tumor resection: A case-controlled study. Surg Endosc, 2008; 23:847–853.
11.
ChangSKY, LimEKW, ShenL, YuRRQ, GanpathiIS, LomantoD, MadhavanK. Comparative study of 45 laparoscopic liver resections [abstract #629]. Hepatology, 2009; 50:602A.
12.
ItoK, ItoH, AreC, AllenPJ, FongY, DeMatteoRP, JarnaginWR, D'AngelicaMI. Laparoscopic versus open liver resection: A matched-pair case control study. J Gastrointest Surg, 2009; 13:2276–2283.
13.
GardenOJ. Guidelines for resection of colorectal cancer liver metastases. Gut, 2006; 55(Suppl 3):iii1–iii8.
14.
SiegelR, NaishadhamD, JemalA. Cancer statistics, 2013. CA Cancer J Clin, 2013; 63:11–30.
15.
Altendorf-HofmannA, ScheeleJ. A critical review of the major indicators of prognosis after resection of hepatic metastases from colorectal carcinoma. Surg Oncol Clin North Am, 2003; 12:165–192, xi.
16.
LeporrierJ, MaurelJ, ChicheL, BaraS, SegolP, LaunoyG. A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg, 2006; 93:465–474.
FongY, FortnerJ, SunRL, BrennanMF, BlumgartLH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: Analysis of 1001 consecutive cases. Ann Surg., 1999; 230:309–318; discussion 318–321.
19.
ChotiMA, SitzmannJV, TiburiMF, SumetchotimethaW, RangsinR, SchulickRD, LillemoeKD, YeoCJ, CameronJL. Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg, 2002; 235:759–766.
20.
TomlinsonJS, JarnaginWR, DeMatteoRP, FongY, KornpratP, GonenM, KemenyN, BrennanMF, BlumgartLH, D'AngelicaM. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol, 2007; 25:4575–4580.
21.
MalaT, EdwinB, GladhaugI, FosseE, SoreideO, BerganA, MathisenO. A comparative study of the short-term outcome following open and laparoscopic liver resection of colorectal metastases. Surg Endosc, 2002; 16:1059–1063.
22.
CastaingD, VibertE, RiccaL, AzoulayD, AdamR, GayetB. Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg, 2009; 250:849–855.
23.
Abu HilalM, UnderwoodT, ZuccaroM, PrimroseJ, PearceN. Short- and medium-term results of totally laparoscopic resection for colorectal liver metastases. Br J Surg, 2010; 97:927–933.
24.
EnestvedtCK, DiggsBS, SheppardBC, OrloffS, BillingsleyKG. Laparoscopic hepatic resection: Favorable short-term outcomes for colorectal cancer metastases of the left hemiliver [abstract #347]. J Clin Oncol Conf, 2011; 29(4 Suppl 1).
25.
CannonRM, ScogginsCR, CallenderGG, McMastersKM, Martin RC 2nd. Laparoscopic versus open resection of hepatic colorectal metastases. Surgery, 2012; 152:567–573; discussion 573–564.
26.
MontaltiR, Den BosscheBV, CavanigliaD, CastagnolaG, LaurentS, GeboesK, De HemptinneB, TroisiRI. Laparoscopic resection of colorectal liver metastases: A single center case-control matched-pairs analysis [abstract #663]. HPB (Oxford), 2012; 14:412.
27.
TopalH, TiekJ, AertsR, TopalB. Outcome of laparoscopic major liver resection for colorectal metastases. Surg Endosc, 2012; 26:2451–2455.
28.
GuerronAD, AliyevS, AgcaogluO, AksoyE, TaskinHE, AucejoF, MillerC, FungJ, BerberE. Laparoscopic versus open resection of colorectal liver metastasis. Surg Endosc, 2013; 27:1138–1143.
29.
InoueY, HayashiM, TanakaR, KomedaK, HirokawaF, UchiyamaK. Short-term results of laparoscopic versus open liver resection for liver metastasis from colorectal cancer: A comparative study. Am Surg, 2013; 79:495–501.
30.
IwahashiS, ShimadaM, UtsunomiyaT, ImuraS, MorineY, IkemotoT, ArakawaY, MoriH, KanamotoM, YamadaS, MiyakeH. Laparoscopic hepatic resection for metastatic liver tumor of colorectal cancer: Comparative analysis of short and long term results [abstract #S006]. Surg Endosc, 2013; 27:S252.
31.
StroupDF, BerlinJA, MortonSC, OlkinI, WilliamsonGD, RennieD, MoherD, BeckerBJ, SipeTA, ThackerSB. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA, 2000; 283:2008–2012.
32.
WellsG, SheaB, O'ConnellD, PetersonJ, WelchV, LososM. The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. www.ohri.ca/programs/clinical_epidemiology/oxford.htm (accessed June16, 2013).
33.
HozoSP, DjulbegovicB, HozoI. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol, 2005; 5:13.
34.
HigginsJPT, GreenS. Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0 [updated March 2011]. The Cochrane Collaboration. 2011. www.cochrane-handbook.org (accessed June26, 2013).
35.
TierneyJF, StewartLA, GhersiD, BurdettS, SydesMR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 2007; 8:16.
36.
BeggCB, MazumdarM. Operating characteristics of a rank correlation test for publication bias. Biometrics, 1994; 50:1088–1101.
37.
RahusenFD, CuestaMA, BorgsteinPJ, BleichrodtRP, BarkhofF, DoesburgT, MeijerS. Selection of patients for resection of colorectal metastases to the liver using diagnostic laparoscopy and laparoscopic ultrasonography. Ann Surg, 1999; 230:31–37.
38.
GholghesaeiM, Van MuiswinkelJM, KuiperJW, KazemierG, TilanusHW, IjzermansJNM. Value of laparoscopy and laparoscopic ultrasonography in determining resectability of colorectal hepatic metastases. HPB (Oxford), 2003; 5:100–104.
39.
KarunaST, ThirlbyR, BiehlT, VeenstraD. Cost-effectiveness of laparoscopy versus laparotomy for initial surgical evaluation and treatment of potentially resectable hepatic colorectal metastases: A decision analysis. J Surg Oncol, 2008; 97:396–403.
40.
HaoCY, JiJF. Surgical treatment of liver metastases of colorectal cancer: Strategies and controversies in 2006. Eur J Surg Oncol, 2006; 32:473–483.
41.
NguyenKT, GellerDA. Outcomes of laparoscopic hepatic resection for colorectal cancer metastases. J Surg Oncol, 2010; 102:975–977.
42.
LewinJ, BryantR, MartinI, NathansonL, FieldingG, O'RourkeN. Long term survival after laparoscopic resection of colorectal liver metastases [abstract #877]. HPB (Oxford), 2013; 15:55.
43.
PulitanoC, CastilloF, AldrighettiL, BodingbauerM, ParksRW, FerlaG, WigmoreSJ, GardenOJ. What defines ‘cure’ after liver resection for colorectal metastases? Results after 10 years of follow-up. HPB (Oxford), 2010; 12:244–249.
44.
ViganòL, FerreroA, Lo TesoriereR, CapussottiL. Liver surgery for colorectal metastases: Results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann Surg Oncol, 2008; 15:2458–2464.
45.
SettmacherU, DittmarY, KnoselT, SchoneU, HeiseM, JandtK, Altendorf-HofmannAK. Predictors of long-term survival in patients with colorectal liver metastases: A single center study and review of the literature. Int J Colorectal Dis, 2011; 26:967–981.
46.
AndreouA, AloiaTA, BrouquetA, DicksonPV, ZimmittiG, MaruDM, KopetzS, LoyerEM, CurleySA, AbdallaEK, VautheyJN. Margin status remains an important determinant of survival after surgical resection of colorectal liver metastases in the era of modern chemotherapy. Ann Surg, 2013; 257:1079–1088.
47.
PoultsidesGA, SchulickRD, PawlikTM. Hepatic resection for colorectal metastases: The impact of surgical margin status on outcome. HPB (Oxford), 2010; 12:43–49.
48.
MuratoreA, RiberoD, ZimmittiG, MellanoA, LangellaS, CapussottiL. Resection margin and recurrence-free survival after liver resection of colorectal metastases. Ann Surg Oncol, 2010; 17:1324–1329.
49.
WelshFK, TekkisPP, O'RourkeT, JohnTG, ReesM. Quantification of risk of a positive (R1) resection margin following hepatic resection for metastatic colorectal cancer: An aid to clinical decision-making. Surg Oncol, 2008; 17:3–13.
50.
ReesM, TekkisPP, WelshFKS, O'RourkeT, JohnTG. Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer—A multifactorial model of 929 patients. Ann Surg, 2008; 247:125–135.
51.
FinchRJB, MalikHZ, HamadyZZR, Al-MukhtarA, AdairR, PrasadKR, LodgeJPA, ToogoodGJ. Effect of type of resection on outcome of hepatic resection for colorectal metastases. Br J Surg, 2007; 94:1242–1248.
52.
PawlikTM, ScogginsCR, ZorziD, AbdallaEK, AndresA, EngC, CurleySA, LoyerEM, MuratoreA, MenthaG, CapussottiL, VautheyJ-N. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg, 2005; 241:715–724.
53.
NuzzoG, GiulianteF, ArditoF, VelloneM, GiovanniniI, FedericoB, VecchioFM. Influence of surgical margin on type of recurrence after liver resection for colorectal metastases: A single-center experience. Surgery, 2008; 143:384–393.
54.
InoueY, HayashiM, KomedaK, MasubuchiS, YamamotoM, YamanaH, KayanoH, ShimizuT, AsakumaM, HirokawaF, MiyamotoY, TakeshitaA, ShibayamaY, UchiyamaK. Resection margin with anatomic or nonanatomic hepatectomy for liver metastasis from colorectal cancer. J Gastrointest Surg, 2012; 16:1171–1180.
55.
ReissfelderC, RahbariNN, KochM, UlrichA, PfeilschifterI, WaltertA, MullerSA, SchemmerP, BuchlerMW, WeitzJ. Validation of prognostic scoring systems for patients undergoing resection of colorectal cancer liver metastases. Ann Surg Oncol, 2009; 16:3279–3288.
56.
de HaasRJ, WichertsDA, FloresE, AzoulayD, CastaingD, AdamR. R1 resection by necessity for colorectal liver metastases: Is it still a contraindication to surgery?. Ann Surg, 2008; 248:626–637.
57.
HamadyZZ, CameronIC, WyattJ, PrasadRK, ToogoodGJ, LodgeJP. Resection margin in patients undergoing hepatectomy for colorectal liver metastasis: A critical appraisal of the 1cm rule. Eur J Surg Oncol, 2006; 32:557–563.
58.
KanasGP, TaylorA, PrimroseJN, LangebergWJ, KelshMA, MowatFS, AlexanderDD, ChotiMA, PostonG. Survival after liver resection in metastatic colorectal cancer: Review and meta-analysis of prognostic factors. Clin Epidemiol, 2012; 4:283–301.
59.
AreC, GonenM, ZazzaliK, DematteoRP, JarnaginWR, FongY, BlumgartLH, D'AngelicaM. The impact of margins on outcome after hepatic resection for colorectal metastasis. Ann Surg, 2007; 246:295–300.
60.
GagnerM, RogulaT, SelzerD. Laparoscopic liver resection: Benefits and controversies. Surg Clin North Am, 2004; 84:451–462.
61.
GigotJF, GlineurD, Santiago AzagraJ, GoergenM, CeuterickM, MorinoM, EtienneJ, MarescauxJ, MutterD, van KrunckelsvenL, DescottesB, ValleixD, LachachiF, BertrandC, MansveltB, HubensG, SaeyJP, SchockmelR. Laparoscopic liver resection for malignant liver tumors: Preliminary results of a multicenter European study. Ann Surg, 2002; 236:90–97.
62.
MalaT, EdwinB. Role and limitations of laparoscopic liver resection of colorectal metastases. Dig Dis, 2005; 23:142–150.
63.
DeMatteoR, PaleseC, JanmginW, SimR, BlumgartL, FongY. Anatomic segmental hepatic resection is superior to wedge resection as an oncologic operation for colorectal liver metastases. J Gastrointest Surg, 2000; 4:178–184.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
