Annals of Surgical Oncology

, Volume 20, Issue 13, pp 4274–4281 | Cite as

Technical Factors that Affect Anastomotic Integrity Following Esophagectomy: Systematic Review and Meta-analysis

  • Sheraz R. MarkarEmail author
  • Shobhit Arya
  • Alan Karthikesalingam
  • George B. Hanna
Thoracic Oncology



Due to the significant contribution of anastomotic leak, with its disastrous consequences to patient morbidity and mortality, multiple parameters have been proposed and individually meta-analyzed for the formation of the ideal esophagogastric anastomosis following cancer resection. The purpose of this pooled analysis was to examine the main technical parameters that impact on anastomotic integrity.


Medline, Embase, trial registries, and conference proceedings were searched. Technical factors evaluated included hand-sewn versus stapled esophagogastric anastomosis (EGA), cervical versus thoracic EGA, minimally invasive versus open esophagectomy, anterior versus posterior route of reconstruction and ischemic conditioning of the gastric conduit. The outcome of interest was the incidence of anastomotic leak, for which pooled odds ratios were calculated for each technical factor.


No significant difference in the incidence of anastomotic leak was demonstrated for the following technical factors: hand-sewn versus stapled EGA, minimally invasive versus open esophagectomy, anterior versus posterior route of reconstruction and ischemic conditioning of the gastric conduit. Four randomized, controlled trials comprising 298 patients were included that compared cervical and thoracic EGA. Anastomotic leak was seen more commonly in the cervical group (13.64 %) than in the thoracic group (2.96 %). Pooled analysis demonstrated a significantly increased incidence of anastomotic leak in the cervical group (pooled odds ratio = 4.73; 95 % CI 1.61–13.9; P = 0.005).


A tailored surgical approach to the patient’s physiology and esophageal cancer stage is the most important factor that influences anastomotic integrity after esophagectomy.


Anastomotic Leak Minimally Invasive Esophagectomy Pool Odds Ratio Gastric Conduit Esophagogastric Anastomosis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Conflict of interest



  1. 1.
    Biere SS, van Berge Henegouwen MI, Maas KW, et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet. 2012;379:1887–92.PubMedCrossRefGoogle Scholar
  2. 2.
    Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRefGoogle Scholar
  3. 3.
    Siegel R, Naishadham D, Jemal A. Cancer statistics. CA Cancer J Clin. 2012;62(1):10–29.PubMedCrossRefGoogle Scholar
  4. 4.
    Coupland VH, Lagergren J, Luchtenborg M, et al. Hospital volume, proportion resected and mortality from oesophageal and gastric cancer: a population-based study in England, 2004–2009. Gut. 2013;62(7):961–6. PubMedCrossRefGoogle Scholar
  5. 5.
    Hanna GB, Boshier PR, Knaggs A, et al. Improving outcomes after gastroesophageal cancer resection: can Japanese results be reproduced in Western centers? Arch Surg. 2012;147(8):738–45.PubMedGoogle Scholar
  6. 6.
    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.PubMedCrossRefGoogle Scholar
  7. 7.
    Law S, Fok M, Chu KM, et al. Comparison of hand-sewn and stapled esophagogastric anastomosis after esophageal resection for cancer: a prospective randomized controlled trial. Ann Surg. 1997;226(2):169–73.PubMedCrossRefGoogle Scholar
  8. 8.
    Hsu HH, Chen JS, Huang PM, et al. Comparison of manual and mechanical cervical esophagogastric anastomosis after esophageal resection for squamous cell carcinoma: a prospective randomized controlled trial. Eur J Cardiothorac Surg. 2004;25(6):1097–101.PubMedCrossRefGoogle Scholar
  9. 9.
    Laterza E, de’Manzoni G, Veraldi GF, et al. Manual compared with mechanical cervical oesophagogastric anastomosis: a randomised trial. Eur J Surg. 1999;165(11):1051–4.PubMedCrossRefGoogle Scholar
  10. 10.
    Valverde A, Hay JM, Fingerhut A, et al. Manual versus mechanical esophagogastric anastomosis after resection for carcinoma: a controlled trial. French Associations for Surgical Research. Surgery. 1996;120(3):476–83.PubMedCrossRefGoogle Scholar
  11. 11.
    Luechakiettisak P, Kasetsunthom S. Comparison of hand-sewn and stapled in esophagogastric anastomosis after esophageal cancer resection: a prospective randomized study. J Med Assoc Thai. 2008;91(5):681–5.PubMedGoogle Scholar
  12. 12.
    Walther B, Johansson J, Johansson F, et al. 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(6):803–12.PubMedCrossRefGoogle Scholar
  13. 13.
    Okuyama M, Motoyama S, Suzuki H, et al. Hand-sewn cervical anastomosis versus stapled intra-thoracic anastomosis after esophagectomy for middle or lower thoracic esophageal cancer: a prospective randomized controlled study. Surg Today. 2007;37(11):947–52.PubMedCrossRefGoogle Scholar
  14. 14.
    Craig SR, Walker WS, Cameron EW, et al. A prospective randomized study comparing stapled with handsewn oesophagogastric anastomoses. J R Coll Surg Edinb. 1996;41(1):17–9.PubMedGoogle Scholar
  15. 15.
    George WD, West of Scotland and Highland Anastomosis Study Group. Suturing or stapling in gastrointestinal surgery: a prospective randomized study. Br J Surg. 1991;78:337–41.CrossRefGoogle Scholar
  16. 16.
    Saluja SS, Ray S, Pal S, et al. Randomized trial comparing side-to-side stapled and hand-sewn esophagogastric anastomosis in neck. J Gastrointest Surg. 2012;16(7):1287–95.PubMedCrossRefGoogle Scholar
  17. 17.
    Chasseray VM, Kiroff GK, Buard JL, et al. Cervical or thoracic anastomosis for esophagectomy for carcinoma. Surg Gynecol Obstet. 1989;169(1):55–62.PubMedGoogle Scholar
  18. 18.
    Ribet M, Debrueres B, Lecomte-Houcke M. Resection for advanced cancer of the thoracic esophagus: cervical or thoracic anastomosis? Late results of a prospective randomized study. J Thorac Cardiovasc Surg. 1992;103(4):784–9.PubMedGoogle Scholar
  19. 19.
    Lam TC, Fok M, Cheng SW, et al. Anastomotic complications after esophagectomy for cancer. A comparison of neck and chest anastomoses. J Thorac Cardiovasc Surg. 1992;104:395–400.PubMedGoogle Scholar
  20. 20.
    Nurnberger HR, Lohlein D. Experiences with reliability and rate of complications in collar or thoracic anastomosis after subtotal esophagectomy. Zentralbl Chir. 1994;119:233–9.PubMedGoogle Scholar
  21. 21.
    Blewett CJ, Miller JD, Young JE, et al. Anastomotic leaks after esophagectomy for esophageal cancer: a comparison of thoracic and cervical anastomoses. Ann Thorac Cardiovasc Surg. 2001;7:75–8.PubMedGoogle Scholar
  22. 22.
    Egberts JH, Schniewind B, Bestmann B, et al. Impact of the site of anastomosis after oncologic esophagectomy on quality of life–a prospective, longitudinal outcome study. Ann Surg Oncol. 2008;15:566–75.PubMedCrossRefGoogle Scholar
  23. 23.
    Klink CD, Binnebosel M, Otto J, et al. Intrathoracic versus cervical anastomosis after resection of esophageal cancer: a matched pair analysis of 72 patients in a single center study. World J Surg Oncol. 2012;10:1477–9.CrossRefGoogle Scholar
  24. 24.
    Ben-David K, Sarosi GA, Cendan JC, et al. Decreasing morbidity and mortality in 100 consecutive minimally invasive esophagectomies. Surg Endosc. 2012;26:162–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Berger AC, Bloomenthal A, Weksler B, et al. Oncologic efficacy is not compromised, and may be improved with minimally invasive esophagectomy. J Am Coll Surg. 2011;212(4):560–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Gao Y, Wang Y, Chen L, et al. Comparison of open three-field and minimally invasive esophagectomy for esophageal cancer. Interact Cardiovasc Thorac Surg. 2011;12:366–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Hamouda AH, Forshaw MJ, Tsigritis K, et al. Perioperative outcomes after transition from conventional to minimally invasive Ivor-Lewis esophagectomy in a specialized center. Surg Endosc. 2010;24:865–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Lee JM, Cheng JW, Lin MT, et al. 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;35:790–7.PubMedCrossRefGoogle Scholar
  29. 29.
    Nafteux P, Moons J, Coosemans W, et al. 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;40:1455–63.PubMedGoogle Scholar
  30. 30.
    Safranek PM, Cubitt J, Booth MI, et al. Review of open and minimal access approaches to oesophagectomy for cancer. Br J Surg. 2010;97:1845–53.PubMedCrossRefGoogle Scholar
  31. 31.
    Schroder W, Holscher AH, Bludau M, et al. Ivor-Lewis esophagectomy with and without laparoscopic conditioning of the gastric conduit. World J Surg. 2010;34:738–43. PubMedCrossRefGoogle Scholar
  32. 32.
    Smithers BM, Gotley DC, Martin I, et al. Comparison of the outcomes between open and minimally invasive esophagectomy. Ann Surg. 2007;245:232–40.PubMedCrossRefGoogle Scholar
  33. 33.
    Yamasaki M, Miyata H, Fujiwara Y, et al. Minimally invasive esophagectomy for esophageal cancer: comparative analysis of open and hand-assisted laparoscopic abdominal lymphadenectomy with gastric conduit reconstruction. J Surg Oncol. 2011;104:623–8.PubMedCrossRefGoogle Scholar
  34. 34.
    Zingg U, McQuinn A, DiValentino D, et al. Minimally invasive versus open esophagectomy for patients with esophageal cancer. Ann Thorac Surg. 2009;87:911–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Biere SS, Maas KW, Cuesta MA, et al. Cervical or thoracic anastomosis after esophagectomy for cancer: a systematic review and meta-analysis. Dig Surg. 2011;28:29–35.PubMedCrossRefGoogle Scholar
  36. 36.
    Bartels H, Thorban S, Siewert JR. Anterior versus posterior reconstruction after transhiatal oesophagectomy: a randomized controlled trial. Br J Surg 1993;80:1141–4.PubMedCrossRefGoogle Scholar
  37. 37.
    Gawad KA, Hosch SB, Bumann D, et al. How important is the route of reconstruction after esophagectomy: a prospective randomized study. Am J Gastroenterol. 1999;94:1490–6.PubMedCrossRefGoogle Scholar
  38. 38.
    van Lanschot JJ, van Blankenstein M, Oei HY, et al. Randomized comparison of prevertebral and retrosternal gastric tube reconstruction after resection of oesophageal carcinoma. Br J Surg. 1999;86:102–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Zieren HU, Muller JM, Pichlmaier H. Prospective randomized study of one- or two-layer anastomosis following oesophageal resection and cervical oesophagogastrostomy. Br J Surg. 1993;80:608–11.PubMedCrossRefGoogle Scholar
  40. 40.
    Motoyama S, Kitamura M, Saito R, et al. Surgical outcome of colon interposition by the posterior mediastinal route for thoracic esophageal cancer. Ann Thorac Surg. 2007;83:1273–8.PubMedCrossRefGoogle Scholar
  41. 41.
    Khiria LS, Pal S, Peush S, et al. Impact on outcome of the route of conduit transposition after transhiatal oesophagectomy: a randomized controlled trial. Dig Liver Dis. 2009;41:711–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Chan ML, Hsieh CC, Wang CW, et al. Reconstruction after esophagectomy for esophageal cancer: retrosternal or posterior mediastinal route? J Chin Med Assoc. 2011;74:505–10.PubMedCrossRefGoogle Scholar
  43. 43.
    Akiyama S, Ito S, Sekiguchi H, et al. Preoperative embolization of gastric arteries for esophageal cancer. Surgery. 1996;120:542–6.PubMedCrossRefGoogle Scholar
  44. 44.
    Akiyama S, Kodera Y, Sekiguchi H, et al. Preoperative embolization therapy for esophageal operation. J Surg Oncol. 1998;69:219–23.PubMedCrossRefGoogle Scholar
  45. 45.
    Isomura T, Itoh S, Akiyama S, et al. Efficacy of gastric blood supply redistribution by transarterial embolization: preoperative procedure to prevent postoperative anastomotic leaks following esophagoplasty for esophageal carcinoma. Cardiovasc Intervent Radiol. 1999;22:119–23.PubMedCrossRefGoogle Scholar
  46. 46.
    Diana M, Hubner M, Vuilleumier H, et al. Redistribution of gastric blood flow by embolization of gastric arteries before esophagectomy. Ann Thorac Surg. 2011;91:1546–51.PubMedCrossRefGoogle Scholar
  47. 47.
    Farran L, Miro M, Alba E, et al. Preoperative gastric conditioning in cervical gastroplasty. Dis Esophagus. 2011;24:205–10.PubMedCrossRefGoogle Scholar
  48. 48.
    Nguyen NT, Nguyen XT, Reavis KM, et al. Minimally invasive esophagectomy with and without gastric ischemic conditioning. Surg Endosc. 2012;26:1637–41.PubMedCrossRefGoogle Scholar
  49. 49.
    Perry KA, Enestvedt CK, Pham TH, et al. Esophageal replacement following gastric devascularization is safe, feasible, and may decrease anastomotic complications. J Gastrointest Surg. 2010;14:1069–73.PubMedCrossRefGoogle Scholar
  50. 50.
    Berrisford RG, Veeramootoo D, Parameswaran R, et al. Laparoscopic ischaemic conditioning of the stomach may reduce gastric-conduit morbidity following total minimally invasive oesophagectomy. Eur J Cardiothorac Surg. 2009;36:888–93.PubMedCrossRefGoogle Scholar
  51. 51.
    Veeramootoo D, Shore AC, Shields B, et al. Ischemic conditioning shows a time-dependent influence on the fate of the gastric conduit after minimally invasive esophagectomy. Surg Endosc. 2010;24:1126–31.PubMedCrossRefGoogle Scholar
  52. 52.
    Wajed SA, Veeramootoo D, Shore AC. Surgical optimisation of the gastric conduit for minimally invasive oesophagectomy. Surg Endosc. 2012;26:271–6.PubMedCrossRefGoogle Scholar
  53. 53.
    Zahedi M, Ganai S, Yetasook AK, et al. Laparoscopic ischemic conditioning as a modality to reduce gastric conduit morbidity following esophagectomy. Digestive Disease Week 2012; Poster presentation.Google Scholar
  54. 54.
    Law S, Wong KH, Kwok KF, et al. Predictive factors for postoperative pulmonary complications and mortality after esophagectomy for cancer. Ann Surg. 2004;240:791–800.PubMedCrossRefGoogle Scholar
  55. 55.
    Marietter C, Taillier G, Van Seuningen I, et al. Factors affecting postoperative course and survival after en bloc resection for esophageal carcinoma. Ann Thorac Surg. 2004;78:1177–83.CrossRefGoogle Scholar
  56. 56.
    Noble F, Curtis N, Harris S, South Coast Cancer Collaboration-Oesophago-Gastric (SC-OG), et al. Risk assessment using a novel score to predict anastomotic leak and major complications after oesophageal resection. J Gastrointest Surg. 2012;16:1083–95.PubMedCrossRefGoogle Scholar
  57. 57.
    Alanezi K, Urschel JD. Mortality secondary to esophageal anastomotic leak. Ann Thorac Cardiovasc Surg. 2004;10:71–5.PubMedGoogle Scholar
  58. 58.
    Hulscher JB, Tijssen JG, Obertop H, et al. Transthoracic versus transhiatal resection for carcinoma of the esophagus: a meta-analysis. Ann Thorac Surg. 2001;72:306–13.PubMedCrossRefGoogle Scholar
  59. 59.
    Verhoef C, van der Weyer R, Schaapveld M, et al. Better survival in patients with esophageal cancer after surgical treatment in university hospitals: a plea for performance by surgical oncologists. Ann Surg Oncol. 2007;14:1678–87.PubMedCrossRefGoogle Scholar
  60. 60.
    Markar SR, Karthikesalingam A, Vyas S, et al. Hand-sewn versus stapled oesophago-gastric anastomosis: systematic review and meta-analysis. J Gastrointest Surg. 2011;15(5):876–84.PubMedCrossRefGoogle Scholar
  61. 61.
    Blencowe NS, Strong S, McNair AG, et al. Reporting of short-term clinical outcomes after esophagectomy: a systematic review. Ann Surg. 2012;255:658–66.PubMedCrossRefGoogle Scholar
  62. 62.
    Carrott PW, Markar SR, Kuppusamy MK, et al. Accordian severity grading system: assessment of relationship between costs, length of hospital stay, and survival in patients with complications after esophagectomy for cancer. J Am Coll Surg. 2012;215(3):331–6.PubMedCrossRefGoogle Scholar
  63. 63.
    Markar SR, Karthikesalingam A, Low DE. Outcomes assessment of the surgical management of esophageal cancer in younger and older patients. Ann Thorac Surg. 2012;94(5):1652–8.PubMedCrossRefGoogle Scholar
  64. 64.
    Schroder W, Beckurts KT, Stahler D, et al. Microcirculatory changes associated with gastric tube formation in the pig. Eur Surg Res. 2002;34:411–7.PubMedCrossRefGoogle Scholar
  65. 65.
    National Oesophago-Gastric Cancer Audit—The Royal College of Surgeons of England 2010.Google Scholar
  66. 66.
    Luketich JD, Pennathur A, Awais O, et al. Outcomes after minimally invasive esophagectomy: review of over 1000 patients. Ann Surg. 2012;256(1):95–103.PubMedCrossRefGoogle Scholar
  67. 67.
    Reavis KM, Chang EY, Hunter JG, Jobe BA. Utilization of the delay phenomenon improves blood flow and reduces collage deposition in esophagogastric anastomoses. Ann Surg. 2005;241:736–47.PubMedCrossRefGoogle Scholar
  68. 68.
    Urschel JD, Antkowiak JG, Delacure MD, Takita H. Ischemic conditioning (delay phenomenon) improves esophagogastric anastomotic wound healing in the rat. J Surg Oncol. 1997;66:254–6.PubMedCrossRefGoogle Scholar
  69. 69.
    Stiles BM, Mirza F, Coppolino A, et al. Clinical T2-T3N0MO esophageal cancer: the risk of node positive disease. Ann Thorac Surg. 2011;92(2):491–6.PubMedCrossRefGoogle Scholar
  70. 70.
    Hamai Y, Hihara J, Emi M, et al. Esophageal reconstruction using the terminal ileum and right colon in esophageal cancer surgery. Surg Today. 2012;42(4):342–50. PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2013

Authors and Affiliations

  • Sheraz R. Markar
    • 1
    Email author
  • Shobhit Arya
    • 1
  • Alan Karthikesalingam
    • 2
  • George B. Hanna
    • 1
  1. 1.Division of Surgery, Department of Surgery and Cancer, St Mary’s HospitalImperial College LondonLondonUK
  2. 2.Department of Outcome Research, St George’s Vascular InstituteSt George’s HospitalLondonUK

Personalised recommendations