Journal of Gastrointestinal Surgery

, Volume 23, Issue 1, pp 43–50 | Cite as

Multivisceral Resection for Locally Advanced Gastric and Gastroesophageal Junction Cancers—11-Year Experience at a High-Volume North American Center

  • J. C. MolinaEmail author
  • A. Al-Hinai
  • A. Gosseling-Tardif
  • P. Bouchard
  • J. Spicer
  • D. Mulder
  • C. L. Mueller
  • L. E. Ferri
2017 SSAT Plenary Presentation



The oncologic benefit of multivisceral en bloc resections for T4 gastroesophageal tumors has been questioned, given the increased morbidity associated. We thus sought to investigate the surgical and oncologic outcomes of curative-intent en bloc multivisceral resections for T4 gastroesophageal carcinomas.


Between 2005 and 2016, 35 of the 525 patients who had gastric or EGJ carcinomas underwent curative-intent multivisceral resections for direct invasion or adhesion to adjacent organs.


Postoperative complications occurred in 16(46%), 10 of which were Clavien-Dindo ≥ 3 (29%). Ninety-day mortality was 3%. The R0 resection rate was 94% (33). Direct organ invasion (pT4b) was confirmed on pathological analysis in 14 (40%) and did not affect survival. The majority (28, 80%) had lymph node involvement with a high nodal disease burden and was associated with decreased survival. Overall 5-year survival rate was 34%, and the vast majority of recurrences were distant/peritoneal (81%). On multivariate analysis, positive lymph nodes (H.R. 21.2; 95%CI 2.34–192) and R1 resection (H.R. 5.6; 95%CI 1.02–30.9) were predictors of survival.


Multivisceral resections for T4 gastric and GEJ adenocarcinomas, in combination with effective systemic therapy, result in prolonged long-term survival with acceptable morbidity. Complete resection to negative margins should remain a mainstay of curative-intent treatment in carefully selected patients.


Gastric cancer Locally advanced T4 Surgery 


Compliance with Ethical Standards

This study was approved by the McGill University Health Center’s (MUHC) institutional review board.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. International Journal of Cancer. 2015;136(5).
  2. 2.
    Cools-Lartigue J, Spicer J, Ferri LE. Current Status of Management of Malignant Disease: Current Management of Esophageal Cancer. Journal of Gastrointestinal Surgery. 2015;19(5):964–72. Scholar
  3. 3.
    Napier KJ. Esophageal cancer: A Review of epidemiology, pathogenesis, staging workup and treatment modalities. World Journal of Gastrointestinal Oncology. 2014;6(5):112. Scholar
  4. 4.
    Li Z, Rice TW. Diagnosis and Staging of Cancer of the Esophagus and Esophagogastric Junction. Surgical Clinics of North America. 2012;92(5):11051126. Scholar
  5. 5.
    Tran TB, Worhunsky DJ, Norton JA, Squires M, Jin LX, Spolverato G et al. Multivisceral Resection for Gastric Cancer: Results from the US Gastric Cancer Collaborative. Annals of Surgical Oncology. 2015;22(S3):840–7. Scholar
  6. 6.
    Pacelli F, Cusumano G, Rosa F, Marrelli D, Dicosmo M, Cipollari C et al. Multivisceral resection for locally advanced gastric cancer: an Italian multicenter observational study. JAMA Surgery. 2013;148(4):353–60. Scholar
  7. 7.
    Brar SS, Seevaratnam R, Cardoso R, Yohanathan L, Law C, Helyer L et al. Multivisceral resection for gastric cancer: a systematic review. Gastric Cancer. 2012;15(S1):100–7. Scholar
  8. 8.
    Martin RC, Jaques DP, Brennan MF, Karpeh M. Extended local resection for advanced gastric cancer: increased survival versus increased morbidity. Annals of surgery. 2002;236(2):159–65. CrossRefGoogle Scholar
  9. 9.
    Carboni F, Lepiane P, Santoro R, Lorusso R, Mancini P, Sperduti I et al. Extended multiorgan resection for T4 gastric carcinoma: 25-year experience. Journal of Surgical Oncology. 2005;90(2):95–100. Scholar
  10. 10.
    Ozer I, Bostanci BE, Orug T, Ozogul YB, Ulas M, Ercan M et al. Surgical outcomes and survival after multiorgan resection for locally advanced gastric cancer. The American Journal of Surgery. 2009;198(1):25–30. Scholar
  11. 11.
    Tran TB, Hatzaras I, Worhunsky DJ, Vitiello GA, Squires M, Jin LX et al. Gastric remnant cancer: A distinct entity or simply another proximal gastric cancer? Journal of Surgical Oncology. 2015;112(8):877–82. Scholar
  12. 12.
    Kim J-H, Jang Y-J, Park S-S, Park S-H, Kim S-J, Mok Y-J et al. Surgical Outcomes and Prognostic Factors for T4 Gastric Cancers. Asian Journal of Surgery. 2009;32(4):198–204. Scholar
  13. 13.
    Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of oncology : official journal of the European Society for Medical Oncology. 2016;27(suppl 5):v38-v49. CrossRefGoogle Scholar
  14. 14.
    Kuwano H, Nishimura Y, Oyama T, Kato H, Kitagawa Y, Kusano M et al. Guidelines for Diagnosis and Treatment of Carcinoma of the Esophagus April 2012 edited by the Japan Esophageal Society. Esophagus. 2015;12:1–30. Scholar
  15. 15.
    Kasakura Y, Fujii M, Mochizuki F, Kochi M, Kaiga T. Is there a benefit of pancreaticosplenectomy with gastrectomy for advanced gastric cancer? The American Journal of Surgery. 2000;179(3):237–42. Scholar
  16. 16.
    Otsuji E, Yamaguchi T, Sawai K, Okamoto K, Takahashi T. Total gastrectomy with simultaneous pancreaticosplenectomy or splenectomy in patients with advanced gastric carcinoma. British Journal of Cancer. 1999;79(11):1789–93. Scholar
  17. 17.
    Kitamura K, Nishida S, Ichikawa D, Taniguchi H, Hagiwara A, Yamaguchi T et al. No survival benefit from combined pancreaticosplenectomy and total gastrectomy for gastric cancer. British Journal of Surgery. 1999;86(1):119–22. Scholar
  18. 18.
    Kim DY, Joo JK, Seo KW, Park YK, Ryu SY, Kim HR et al. T4 GASTRIC CARCINOMA: THE BENEFIT OF NON-CURATIVE RESECTION. ANZ journal of surgery. 2006;76(6):453–7. Scholar
  19. 19.
    Oñate-Ocaña LF, Becker M, Carrillo JF, Aiello-Crocifoglio V, Gallardo-Rincón D, Brom-Valladares R et al. Selection of best candidates for multiorgan resection among patients with T4 gastric carcinoma. Journal of Surgical Oncology. 2008;98(5):336–42. Scholar
  20. 20.
    Colen KL, Marcus SG, Newman E, Berman RS, Yee H, Hiotis SP. Multiorgan resection for gastric cancer: intraoperative and computed tomography assessment of locally advanced disease is inaccurate. Journal of Gastrointestinal Surgery. 2004;8(7):897–900. Scholar
  21. 21.
    Zhang M, Zhang H, Ma Y, Zhu G, Xue Y. Prognosis and surgical treatment of gastric cancer invading adjacent organs. ANZ journal of surgery. 2010;80(7–8):510–4. Scholar
  22. 22.
    Saito H, Tsujitani S, Maeda Y, Fukuda K, Yamaguchi K, Ikeguchi M et al. Combined resection of invaded organs in patients with T4 gastric carcinoma. Gastric Cancer. 2001;4(4):206–11. Scholar
  23. 23.
    Siewert JR, Bottcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg. 1998;228(4):449–61.CrossRefGoogle Scholar
  24. 24.
    Allgayer H, Heiss MM, Schildberg FW. Prognostic factors in gastric cancer. The British journal of surgery. 1997;84(12):1651–64.CrossRefGoogle Scholar
  25. 25.
    Cuschieri A, Fayers P, Fielding J, Craven J, Bancewicz J, Joypaul V et al. Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomised controlled surgical trial. The Surgical Cooperative Group. Lancet (London, England). 1996;347(9007):995–9.CrossRefGoogle Scholar
  26. 26.
    Al-Batran S-E, Homann N, Pauligk C, Illerhaus G, Martens UM, Stoehlmacher J et al. Effect of Neoadjuvant Chemotherapy Followed by Surgical Resection on Survival in Patients With Limited Metastatic Gastric or Gastroesophageal Junction Cancer: The AIO-FLOT3 Trial. JAMA Oncology. 2017.
  27. 27.
    Serrano OK, Huang K, Ng N, Yang J, Friedmann P, Libutti SK et al. Correlation between preoperative endoscopic ultrasound and surgical pathology staging of gastric adenocarcinoma: A single institution retrospective review. Journal of Surgical Oncology. 2016;113(1):42–5. Scholar
  28. 28.
    Spolverato G, Ejaz A, Kim Y, Squires MH, Poultsides GA, Fields RC et al. Use of endoscopic ultrasound in the preoperative staging of gastric cancer: a multi-institutional study of the US gastric cancer collaborative. Journal of the American College of Surgeons. 2015;220(1):48–56. Scholar
  29. 29.
    Jeong O, Choi W, Park Y. Appropriate selection of patients for combined organ resection in cases of gastric carcinoma invading adjacent organs. Journal of Surgical Oncology. 2009;100(2):115–20. Scholar
  30. 30.
    Min J-S, Jin S-H, Park S, Kim S-B, Bang H-Y, Lee J-I. Prognosis of Curatively Resected pT4b Gastric Cancer with Respect to Invaded Organ Type. Annals of Surgical Oncology. 2011;19(2):494–501. Scholar
  31. 31.
    Sudarshan M, Alcindor T, Ades S, Aloraini A, van Huyse M, Asselah J et al. Survival and recurrence patterns after neoadjuvant docetaxel, cisplatin, and 5-fluorouracil (DCF) for locally advanced esophagogastric adenocarcinoma. Ann Surg Oncol. 2015;22(1):324–30. Scholar
  32. 32.
    Kidane B, Coughlin S, Vogt K, Malthaner R. Preoperative chemotherapy for resectable thoracic esophageal cancer. The Cochrane database of systematic reviews. 2015;(5):Cd001556.
  33. 33.
    Ferri LE, Ades S, Alcindor T, Chasen M, Marcus V, Hickeson M et al. Perioperative docetaxel, cisplatin, and 5-fluorouracil (DCF) for locally advanced esophageal and gastric adenocarcinoma: a multicenter phase II trial. Annals of oncology : official journal of the European Society for Medical Oncology. 2012;23(6):1512–7. CrossRefGoogle Scholar
  34. 34.
    Ychou M, Boige V, Pignon JP, Conroy T, Bouche O, Lebreton G et al. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2011;29(13):1715–21. CrossRefGoogle Scholar
  35. 35.
    Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. The New England journal of medicine. 2006;355(1):11–20. CrossRefGoogle Scholar
  36. 36.
    Group. MRCOCW. Surgical resection with or without preoperative chemotherapy in oesophageal cancer: a randomised controlled trial. Lancet (London, England). 2002;359(9319):1727–33. CrossRefGoogle Scholar
  37. 37.
    Al-Batran S-E, Homann N, Schmalenberg H, Kopp H-G, Haag GM, Luley KB et al. Perioperative chemotherapy with docetaxel, oxaliplatin, and fluorouracil/leucovorin (FLOT) versus epirubicin, cisplatin, and fluorouracil or capecitabine (ECF/ECX) for resectable gastric or gastroesophageal junction (GEJ) adenocarcinoma (FLOT4-AIO): A multicenter, randomized phase 3 trial. Journal of Clinical Oncology. 2017;35(15_suppl):4004. Scholar
  38. 38.
    Desiderio J, Chao J, Melstrom L, Warner S, Tozzi F, Fong Y et al. The 30-year experience-A meta-analysis of randomised and high-quality non-randomised studies of hyperthermic intraperitoneal chemotherapy in the treatment of gastric cancer. European journal of cancer (Oxford, England: 1990). 2017;79:1–14. CrossRefGoogle Scholar
  39. 39.
    Seshadri RA, Glehen O. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in gastric cancer. World Journal of Gastroenterology. 2016;22(3):1114–30. Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  1. 1.Division of Thoracic and Upper Gastrointestinal SurgeryMcGill University Health CentreMontrealCanada

Personalised recommendations