Is minimally invasive esophagectomy effective for preventing anastomotic leakages after esophagectomy for cancer? A systematic review and meta-analysis

Can Zhou, Gang Ma, Xiao Li, Juan Li, Yu Yan, Peijun Liu, Jianjun He, Yu Ren, Can Zhou, Gang Ma, Xiao Li, Juan Li, Yu Yan, Peijun Liu, Jianjun He, Yu Ren

Abstract

Background: Compared with open esophagectomy (OE), minimally invasive esophagectomy (MIE) proves to have clear benefits in reducing the risk of pulmonary complications for patients with resectable esophageal cancer. The objectives of our study were to explore the superiority of MIE in reducing the occurrence of anastomotic leakages (ALs) when compared to OE.

Methods: A systematic review and meta-analysis was performed to assess the superiority of MIE on the occurrence of ALs over OE, by searching many sources (through December, 2014) such as Medline, Embase, Wiley Online Library, and Cochrane Library. Fixed-effects model was used to calculate summary odds ratios (ORs) to quantify associations between OE and MIE groups. Cochran's Q and I(2) statistics were used to evaluate heterogeneity among studies.

Results: Among a total of 43 studies involving 5537 patients included in the meta-analysis, 2527 (45.6%) cases underwent MIE and 3010 (54.4%) cases underwent OE. Compared to patients undergoing OE, patients undergoing MIE did not have statistical significance in reduced occurrence of ALs (OR = 0.97, 95% CI = 0.80-1.17). Insignificant reduced occurrence of ALs was not associated with anastomotic location (OR = 0.90, 95% CI = 0.71-1.13) or anastomotic procedure (OR = 1.02, 95% CI = 0.79-1.30).

Conclusions: More proofs are needed to clarify the strengths or weaknesses of MIE in preventing anastomotic leakages after esophagectomy for cancer. A largely randomized, controlled trial should be undertaken to resolve this contentious issue urgently.

Figures

Fig. 1
Fig. 1
Flow diagram of the search and selection method
Fig. 2
Fig. 2
MIE and risk of anastomotic leakages (ALs)
Fig. 3
Fig. 3
Anastomotic location of MIE and risk of anastomotic leakages (ALs)
Fig. 4
Fig. 4
Anastomotic procedure of MIE and risk of anastomotic leakages (ALs)
Fig. 5
Fig. 5
Begg plot of included studies

References

    1. Beitler AL, Urschel JD. Comparison of stapled and hand-sewn esophagogastric anastomoses. Am J Surg. 1998;175:337–40. doi: 10.1016/S0002-9610(98)00002-6.
    1. Schweigert M, Dubecz A, Stadlhuber RJ, Muschweck H, Stein HJ. Treatment of intrathoracic esophageal anastomotic leaks by means of endoscopic stent implantation. Interact Cardiovasc Thorac Surg. 2011;12:147–151. doi: 10.1510/icvts.2010.247866.
    1. Morita M, Nakanoko T, Fujinaka Y, Kubo N, Yamashita N, Yoshinaga K, Saeki H, Emi Y, Kakeji Y, Shirabe K, Maehara Y. In-hospital mortality after a surgical resection for esophageal cancer: analyses of the associated factors and historical changes. Ann Surg Oncol. 2011;18:1757–1765. doi: 10.1245/s10434-010-1502-5.
    1. Korst RJ, Port JL, Lee PC, Altorki NK. Intrathoracic manifestations of cervical anastomotic leaks after transthoracic esophagectomy for carcinoma. Ann Thorac Surg. 2005;80:1185–1190. doi: 10.1016/j.athoracsur.2005.04.020.
    1. Weidenhagen R, Hartl WH, Gruetzner KU, Eichhorn ME, Spelsberg F, Jauch KW. Anastomotic leakage after esophageal resection: new treatment options by endoluminal vacuum therapy. Ann Thorac Surg. 2010;90:1674–1681. doi: 10.1016/j.athoracsur.2010.07.007.
    1. Lorentz T, Fok M, Wong J. Anastomotic leakage after resection and bypass for esophageal cancer: lessons learned from the past. World J Surg. 1989;13:472–477. doi: 10.1007/BF01660760.
    1. Hopkins RA, Alexander JC, Postlethwait RW. Stapled esophagogastric anastomosis. Am J Surg. 1984;147:283–287. doi: 10.1016/0002-9610(84)90108-9.
    1. Law S, Fok M, Chu KM, Wong J. Comparison of hand-sewn and stapled esophagogastric anastomosis after esophageal resection for cancer: a prospective randomized controlled trial. Ann Surg. 1997;226:169–173. doi: 10.1097/00000658-199708000-00008.
    1. Cuschieri A, Shimi S, Banting S. Endoscopic oesophagectomy through a right thoracoscopic approach. J R Coll Surg Edinb. 1992;37:7–11.
    1. Depaula AL, Hashiba K, Ferreira EA, de Paula RA, Grecco E. Laparoscopic transhiatal esophagectomy with esophagogastroplasty. Surg Laparosc Endosc Percut Tec. 1995;5:1–5.
    1. Willer BL, Worrell SG, Fitzgibbons RJ, Jr, Mittal SK. Incidence of diaphragmatic hernias following minimally invasive versus open transthoracic Ivor Lewis McKeown esophagectomy. Hernia. 2012;16:185–90. doi: 10.1007/s10029-011-0884-z.
    1. Kipfmüller K, Naruhn M, Melzer A, Kessler S, Buess G. Endoscopic microsurgical dissection of the esophagus. Results in an animal model. Surg Endosc. 1989;3:63–69. doi: 10.1007/BF00590902.
    1. Law S. Minimally invasive techniques for oesophageal cancer surgery. Best Pract Res Clin Gastroenterol. 2006;20:925–940. doi: 10.1016/j.bpg.2006.03.011.
    1. Pham TH, Perry KA, Dolan JP, Schipper P, Sukumar M, Sheppard BC, Hunter JG. Comparison of perioperative outcomes after combined thoracoscopic-laparoscopic esophagectomy and open Ivor-Lewis esophagectomy. Am J Surg. 2010;199:594–598. doi: 10.1016/j.amjsurg.2010.01.005.
    1. Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR, Gisbertz SS, Klinkenbijl JH, Hollmann MW, de Lange ES, Bonjer HJ, van der Peet DL, Cuesta MA. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet. 2012;379:1887–1892. doi: 10.1016/S0140-6736(12)60516-9.
    1. Lee L, Sudarshan M, Li C, Latimer E, Fried GM, Mulder DS, Feldman LS, Ferri LE. Cost-effectiveness of minimally invasive versus open esophagectomy for esophageal cancer. Ann Surg Oncol. 2013;20:3732–3739. doi: 10.1245/s10434-013-3103-6.
    1. Yamamoto M, Weber JM, Karl RC, Meredith KL. Minimally invasive surgery for esophageal cancer: review of the literature and institutional experience. Cancer Control. 2013;20:130–137.
    1. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6 doi: 10.1371/journal.pmed.1000100.
    1. Slim K, Nini E, Forestier D, Kwiatkowski F, Panis Y, Chipponi J. Methodological index for non-randomized studies (MINORS): development and validation of a new instrument. ANZ J Surg. 2003;73:712–716. doi: 10.1046/j.1445-2197.2003.02748.x.
    1. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634. doi: 10.1136/bmj.315.7109.629.
    1. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560. doi: 10.1136/bmj.327.7414.557.
    1. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–1558. doi: 10.1002/sim.1186.
    1. Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560. doi: 10.1136/bmj.327.7414.557.
    1. Nguyen NT, Follette DM, Wolfe BM, Schneider PD, Roberts P, Goodnight JE., Jr Comparison of minimally invasive esophagectomy with transthoracic and transhiatal esophagectomy. Arch Surg. 2000;135:920–925. doi: 10.1001/archsurg.135.8.920.
    1. Kubo N, Ohira M, Yamashita Y, et al. The impact of combined thoracoscopic and laparoscopic surgery on pulmonary complications after radical esophagectomy in patients with resectable esophageal cancer. Anticancer Res. 2014;34:2399–404.
    1. Braghetto I, Csendes A, Cardemil G, Burdiles P, Korn O, Valladares H. Open transthoracic or transhiatal esophagectomy versus minimally invasive esophagectomy in terms of morbidity, mortality and survival. Surg Endosc. 2006;20:1681–1686. doi: 10.1007/s00464-006-0009-4.
    1. Fabian T, Martin JT, McKelvey AA, Federico JA. Minimally invasive esophagectomy: a teaching hospital’s first year experience. Dis Esophagus. 2008;21:220–225. doi: 10.1111/j.1442-2050.2007.00783.x.
    1. Shiraishi T, Kawahara K, Shirakusa T, Yamamoto S, Maekawa T. Risk analysis in resection of thoracic esophageal cancer in the era of endoscopic surgery. Ann Thorac Surg. 2006;81:1083–1089. doi: 10.1016/j.athoracsur.2005.08.057.
    1. Tsujimoto H, Ono S, Sugasawa H, Ichikura T, Yamamoto J, Hase K. Gastric tube reconstruction by laparoscopy-assisted surgery attenuates postoperative systemic inflammatory response after esophagectomy for esophageal cancer. World J Surg. 2010;34:2830–2836. doi: 10.1007/s00268-010-0757-0.
    1. Schröder W, Hölscher AH, Bludau M, Vallböhmer D, Bollschweiler E, Gutschow C. Ivor-Lewis esophagectomy with and without laparoscopic conditioning of the gastric conduit. World J Surg. 2010;34:738–743. doi: 10.1007/s00268-010-0403-x.
    1. Gao Y, Wang Y, Chen L, Zhao Y. Comparison of open three-field and minimally-invasive esophagectomy for esophageal cancer. Interact Cardiovasc Thorac Surg. 2011;12:366–369. doi: 10.1510/icvts.2010.258632.
    1. Nafteux P, Moons J, Coosemans W, Decaluwé H, Decker G, De Leyn P, Van Raemdonck D, Lerut T. Minimally invasive oesophagectomy: a valuable alternative to open oesophagectomy for the treatment of early oesophageal and gastro-oesophageal junction carcinoma. Eur J Cardiothorac Surg. 2011;40:1455–1463.
    1. Sundaram A, Geronimo JC, Willer BL, Hoshino M, Torgersen Z, Juhasz A, Lee TH, Mittal SK. Survival and quality of life after minimally invasive esophagectomy: a single-surgeon experience. Surg Endosc. 2012;26:168–176. doi: 10.1007/s00464-011-1850-7.
    1. Maas KW, Biere SS, Scheepers JJ, Gisbertz SS, van-der-Peet DL, Cuesta MA. Laparoscopic versus open transhiatal esophagectomy for distal and junction cancer. Rev Esp Enferm Dig. 2012;104:197–202. doi: 10.4321/S1130-01082012000400005.
    1. Tsujimoto H, Takahata R, Nomura S, Yaguchi Y, Kumano I, Matsumoto Y, Yoshida K, Horiguchi H, Hiraki S, Ono S, Yamamoto J, Hase K. Video-assisted thoracoscopic surgery for esophageal cancer attenuates postoperative systemic responses and pulmonary complications. Surgery. 2012;151:667–673. doi: 10.1016/j.surg.2011.12.006.
    1. Mu J, Yuan Z, Zhang B, Li N, Lyu F, Mao Y, Xue Q, Gao S, Zhao J, Wang D, Li Z, Gao Y, Zhang L, Huang J, Shao K, Feng F, Zhao L, Li J, Cheng G, Sun K, He J. Comparative study of minimally invasive versus open esophagectomy for esophageal cancer in a single cancer center. Chin Med J (Engl) 2014;127:747–752.
    1. Kauppi J, Räsänen J, Sihvo E, Huuhtanen R, Nelskylä K, Salo J. Open versus minimally invasive esophagectomy: clinical outcomes for locally advanced esophageal adenocarcinoma. Surg Endosc. 2014,[Epub ahead of print].
    1. Meng F, Li Y, Ma H, Yan M, Zhang R. Comparison of outcomes of open and minimally invasive esophagectomy in 183 patients with cancer. J Thorac Dis. 2014;6:1218–1224.
    1. Zhang J, Xu M, Guo M, Mei X, Liu C. Analysis of postoperative quality of life in patients with middle thoracic esophageal carcinoma undergoing minimally invasive Ivor-Lewis esophagectomy. Zhonghua Wei Chang Wai Ke Za Zhi. 2014;17:915–919.
    1. Li J, Shen Y, Tan L, Feng M, Wang H, Xi Y, Wang Q. Is minimally invasive esophagectomy beneficial to elderly patients with esophageal cancer. Surg Endosc. 2015;29:925–930.
    1. Javidfar J, Bacchetta M, Yang JA, Miller J, D’Ovidio F, Ginsburg ME, Gorenstein LA, Bessler M, Sonett JR. The use of a tailored surgical technique for minimally invasive esophagectomy. J Thorac Cardiovasc Surg. 2012;143:1125–1129. doi: 10.1016/j.jtcvs.2012.01.071.
    1. Smithers BM, Gotley DC, Martin I, Thomas JM. Comparison of the outcomes between open and minimally invasive esophagectomy. Ann Surg. 2007;245:232–240. doi: 10.1097/01.sla.0000225093.58071.c6.
    1. Kunisaki C, Hatori S, Imada T, Akiyama H, Ono H, Otsuka Y, Matsuda G, Nomura M, Shimada H. Video-assisted thoracoscopic esophagectomy with a voice-controlled robot: the AESOP System. Langenbecks Arch Surg. 2009;394:617–21. doi: 10.1007/s00423-008-0354-y.
    1. Osugi H, Takemura M, Higashino M, Sakurai K, Toyokawa T, Tanaka H, Muguruma K, Shibutani M, Yamazoe S, Kimura K, Nagahara H, Amano R, Ohtani H, Yashiro M, Maeda K, Hirakawa K. A comparison of video-assisted thoracoscopic oesophagectomy and radical lymph node dissection for squamous cell cancer of the oesophagus with open operation. Br J Surg. 2003;90:108–113. doi: 10.1002/bjs.4022.
    1. Benzoni E, Terrosu G, Bresadola V, Uzzau A, Intini S, Noce L, Cedolini C, Bresadola F, De Anna D. A comparative study of the transhiatal laparoscopic approach versus laparoscopic gastric mobilisation and right open transthoracic esophagectomy for esophageal cancer management. J Gastrointestin Liver Dis. 2007;16:395–401.
    1. Perry KA, Enestvedt CK, Pham T, Welker M, Jobe BA, Hunter JG, Sheppard BC. Comparison of laparoscopic inversion esophagectomy and open transhiatal esophagectomy for high-grade dysplasia and stage I esophageal adenocarcinoma. Arch Surg. 2009;144:679–684. doi: 10.1001/archsurg.2009.113.
    1. Hamouda AH, Forshaw MJ, Tsigritis K, Jones GE, Noorani AS, Rohatgi A, Botha AJ. Perioperative outcomes after transition from conventional to minimally invasive Ivor-Lewis esophagectomy in a specialized center. Surg Endosc. 2010;24:865–869. doi: 10.1007/s00464-009-0679-9.
    1. Schoppmann SF, Prager G, Langer FB, Riegler FM, Kabon B, Fleischmann E, Zacherl J. Open versus minimally invasive esophagectomy: a single-center case controlled study. Surg Endosc. 2010;24:3044–3053. doi: 10.1007/s00464-010-1083-1.
    1. Safranek PM, Cubitt J, Booth MI, Dehn TC. Review of open and minimal access approaches to oesophagectomy for cancer. Br J Surg. 2010;97:1845–1853. doi: 10.1002/bjs.7231.
    1. Lee JM, Cheng JW, Lin MT, Huang PM, Chen JS, Lee YC. Is there any benefit to incorporating a laparoscopic procedure into minimally invasive esophagectomy? The impact on perioperative results in patients with esophageal cancer. World J Surg. 2011;35:790–797. doi: 10.1007/s00268-011-0955-4.
    1. Sihag S, Wright CD, Wain JC, Gaissert HA, Lanuti M, Allan JS, Mathisen DJ, Morse CR. Comparison of perioperative outcomes following open versus minimally invasive Ivor Lewis oesophagectomy at a single, high-volume centre. Eur J Cardiothorac Surg. 2012;42:430–437. doi: 10.1093/ejcts/ezs031.
    1. Kinjo Y, Kurita N, Nakamura F, Okabe H, Tanaka E, Kataoka Y, Itami A, Sakai Y, Fukuhara S. Effectiveness of combined thoracoscopic-laparoscopic esophagectomy: comparison of postoperative complications and midterm oncological outcomes in patients with esophageal cancer. Surg Endosc. 2012;26:381–390. doi: 10.1007/s00464-011-1883-y.
    1. Noble F, Kelly JJ, Bailey IS, Yaguchi Y, Kumano I, Matsumoto Y, Yoshida K, Horiguchi H, Hiraki S, Ono S, Yamamoto J, Hase K. A prospective comparison of totally minimally invasive versus open Ivor Lewis esophagectomy. Dis Esophagus. 2013;26:263–271. doi: 10.1111/j.1442-2050.2012.01356.x.
    1. Kitagawa H, Akimori T, Okabayashi T, Namikawa T, Sugimoto T, Kobayashi M, Hanazaki K. Total laparoscopic gastric mobilization for esophagectomy. Langenbecks Arch Surg. 2009;394:617–621. doi: 10.1007/s00423-008-0354-y.
    1. Ichikawa H, Miyata G, Miyazaki S, Onodera K, Kamei T, Hoshida T, Kikuchi H, Kanba R, Nakano T, Akaishi T, Satomi S. Esophagectomy using a thoracoscopic approach with an open laparotomic or hand-assisted laparoscopic abdominal stage for esophageal cancer: analysis of survival and prognostic factors in 315 patients. Ann Surg. 2013;257:873–885. doi: 10.1097/SLA.0b013e31826c87cd.
    1. Berger AC, Bloomenthal A, Weksler B, Evans N, Chojnacki KA, Yeo CJ, Rosato EL. Oncologic efficacy is not compromised, and may be improved with minimally invasive esophagectomy. J Am Coll Surg. 2011;212:560–566. doi: 10.1016/j.jamcollsurg.2010.12.042.
    1. Yamasaki M, Miyata H, Fujiwara Y, Takiguchi S, Nakajima K, Kurokawa Y, Mori M, Doki Y. Minimally invasive esophagectomy for esophageal cancer: comparative analysis of open and hand-assisted laparoscopic abdominal lymphadenectomy with gastric conduit reconstruction. J Surg Oncol. 2011;104:623–628. doi: 10.1002/jso.21991.
    1. Law S, Fok M, Chu KM, Wong J. Thoracoscopic esophagectomy for esophageal cancer. Surgery. 1997;122:8–14. doi: 10.1016/S0039-6060(97)90257-9.
    1. Wang H, Feng M, Tan L, Wang Q. Comparison of the short-term quality of life in patients with esophageal cancer after subtotal esophagectomy via video-assisted thoracoscopic or open surgery. Dis Esophagus. 2010;23:408–414. doi: 10.1111/j.1442-2050.2009.01035.x.
    1. Parameswaran R, Veeramootoo D, Krishnadas R, Cooper M, Berrisford R, Wajed S. Comparative experience of open and minimally invasive esophagogastric resection. World J Surg. 2009;33:1868–1875. doi: 10.1007/s00268-009-0116-1.
    1. Saha AK, Sutton CD, Sue-Ling H, Dexter SP, Sarela AI. Comparison of oncological outcomes after laparoscopic transhiatal and open esophagectomy for T1 esophageal adenocarcinoma. Surg Endosc. 2009;23:119–124. doi: 10.1007/s00464-008-0065-z.
    1. Van den Broek WT, Makay O, Berends FJ, Yuan JZ, Houdijk AP, Meijer S, Cuesta MA. Laparoscopically assisted transhiatal resection for malignancies of the distal esophagus. Surg Endosc. 2004;18:812–817. doi: 10.1007/s00464-003-9173-y.
    1. Zingg U, McQuinn A, DiValentino D, Esterman AJ, Bessell JR, Thompson SK, Jamieson GG, Watson DI. Minimally invasive versus open esophagectomy for patients with esophageal cancer. Ann Thorac Surg. 2009;87:911–919. doi: 10.1016/j.athoracsur.2008.11.060.
    1. Bresadola V, Terrosu G, Cojutti A, Benzoni E, Baracchini E, Bresadola F. Laparoscopic versus open gastroplasty in esophagectomy for esophageal cancer: a comparative study. Surg Laparosc Endosc Percutan Tech. 2006;16:63–67. doi: 10.1097/00129689-200604000-00001.
    1. Luketich JD, Pennathur A, Awais O, Levy RM, Keeley S, Shende M, Christie NA, Weksler B, Landreneau RJ, Abbas G, Schuchert MJ, Nason KS. Outcomes after minimally invasive esophagectomy: review of over 1000 patients. Ann Surg. 2012;256:95–103. doi: 10.1097/SLA.0b013e3182590603.
    1. Markar SR, Arya S, Karthikesalingam A, Hanna GB. Technical factors that affect anastomotic integrity following esophagectomy: systematic review and meta-analysis. Ann Surg Oncol. 2013;20:4274–4281. doi: 10.1245/s10434-013-3189-x.
    1. Bardini R, Asolati M, Ruol A, Bonavina L, Baseggio S, Peracchia A. Anastomosis. World J Surg. 1994;18:373–8. doi: 10.1007/BF00316817.
    1. Walther B, Johansson J, Johnsson F, Von Holstein CS, Zilling T. Cervical or thoracic anastomosis after esophageal resection and gastric tube reconstruction: a prospective randomized trial comparing sutured neck anastomosis with stapled intrathoracic anastomosis. Ann Surg. 2003;238:803–814. doi: 10.1097/01.sla.0000098624.04100.b1.
    1. Patil PK, Patel SG, Mistry RC, Deshpande RK, Desai PB. Cancer of the esophagus: esophagogastric anastomotic leak—a retrospective study of predisposing factors. J Surg Oncol. 1992;49:163–167. doi: 10.1002/jso.2930490307.
    1. Ravitch MM, Steichen FM. A stapling instrument for end-to-end inverting anastomoses in the gastrointestinal tract. Ann Surg. 1979;189:791–797. doi: 10.1097/00000658-197906000-00017.
    1. Santos RS, Raftopoulos Y, Singh D, DeHoyos A, Fernando HC, Keenan RJ, Luketich JD, Landreneau RJ. Utility of total mechanical stapled cervical esophagogastric anastomosis after esophagectomy: a comparison to conventional anastomotic techniques. Surgery. 2004;136:917–925. doi: 10.1016/j.surg.2004.06.032.
    1. Valverde A, Hay JM, Fingerhut A, Elhadad A. Manual versus mechanical esophagogastric anastomosis after resection for carcinoma: a controlled trial. French Associations for Surgical Research. Surgery. 1996;120:476–483. doi: 10.1016/S0039-6060(96)80066-3.
    1. Ercan S, Rice TW, Murthy SC, Rybicki LA, Blackstone EH. Does esophagogastric anastomotic technique influence the outcome of patients with esophageal cancer? J Thorac Cardiovasc Surg. 2005;129:623–631. doi: 10.1016/j.jtcvs.2004.08.024.

Source: PubMed

3
订阅