Journal of Gastrointestinal Surgery

, Volume 23, Issue 2, pp 357–366 | Cite as

The Impact of a Multivisceral Resection and Adjuvant Therapy in Locally Advanced Colon Cancer

  • Lieve G. J. Leijssen
  • Anne M. Dinaux
  • R. Amri
  • Hiroko Kunitake
  • Liliana G. Bordeianou
  • David L. BergerEmail author
Original Article



Multivisceral resection for locally advanced colon cancer is mandatory to achieve complete tumor resection. We aimed to determine if local multivisceral resections (LMR) for pT4 and pT3 tumors impact perioperative and long-term oncological outcomes.


All stage II or III colon cancer patients who had surgery between 2004 and 2014 were identified. We analyzed patients with non-multivisceral resections (NMR) for pT4 tumors vs. pT4-LMR. In addition, outcomes were compared to both NMR and LMR pT3 patients.


LMR was performed in 55 (29.7%) of all patients with pT4 tumors and in 48 (8.9%) of all patients with pT3 tumors. The most commonly involved areas of extension were the abdominal wall and the small intestine. Transverse colon cancer was correlated with LMR. Morbidity rates were comparable between NMR and LMR, with the exception of higher rates of blood transfusion and postoperative ileus. Over one third of all pT4-NMR patients developed recurrent disease, which was higher compared to all other groups. Subsequently, overall and disease-specific survival, as well as disease-free survival (DFS), was worse for pT4-NMR, even after adjustment for pTN-staging, adjuvant therapy, and R0 resection. Furthermore, when analyzing only curative resections, radial margin < 1 cm along with nodal disease was independent predictor for worse DFS. Long-term outcomes were comparable between pT4-LMR and pT3 patients.


Multivisceral resection for locally advanced colon cancer preserves long-term oncological outcomes without increased postoperative morbidity. Moreover, LMR in pT3 tumors does not contribute to postoperative morbidity. Our study underlines the feasibility and importance of performing LMR when locally advanced cancer is suspected.


Colon cancer Surgery Tumor invasion Multivisceral resection Morbidity Survival 


Authors’ Contribution

All authors have contributed to this manuscript in the following way: substantial contributions to the conception or design of the work, or the acquisition, analysis, or interpretation of the data. Furthermore, all authors drafted or revised the manuscript critically for important intellectual content. All authors approved the final version and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Grant Support

LL received a grant from the Prins Bernhard Cultuurfonds and Hendrik Muller’s Fonds.

Compliance with Ethical Standards

This study was approved by the Institutional Review Board.

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Howlader N, Noone AM, Krapcho M, Miller D, Bishop K, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds). SEER Cancer Statistics Review, 1975–2013, National Cancer Institute. Bethesda, MD,, based on November 2015 SEER data submission, posted to the SEER web site, April 2016
  2. 2.
    Gebhardt C, Meyer W, Ruckriegel S, Meier U. Multivisceral resection of advanced colorectal carcinoma. Langenbecks Arch Surg 1999;384:194–199CrossRefGoogle Scholar
  3. 3.
    Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010; 17:1471–1474CrossRefGoogle Scholar
  4. 4.
    Zoucas E, Frederiksen S, Lydrup ML, Månsson W, Gustafson P, Alberius P. Pelvis exenteration for advanced and recurrent malignancy. World J Surg 2010;34:2177–2184CrossRefGoogle Scholar
  5. 5.
    Mohan HM, Evans MD, Larkin JO, Beynon J, Winter DC. Multivisceral resection in colorectal cancer: a systematic review. Ann Surg Oncol 2013;20:2929–2936CrossRefGoogle Scholar
  6. 6.
    Chang GJ, Kaiser AM, Mills S, Rafferty JF, Buie WD; Standards Practice Task Force of the American Society of Colon and Rectal Surgeons. Practice Parameters for the Management of Colon Cancer. Dis Colon Rectum 2012;55:831–843CrossRefGoogle Scholar
  7. 7.
    Govindarajan A, Coburn NG, Kiss A, Rabeneck L, Smith AJ, Law CH. Population based assessment of the surgical management of locally advanced colorectal cancer. J Natl Cancer Inst 2006;98:1474–1481CrossRefGoogle Scholar
  8. 8.
    Courtney D, McDermott F, Heeney A, Winter DC. Clinical review: surgical management of locally advanced and recurrent colorectal cancer. Langenbecks Arch Surg 2014;399:33–40CrossRefGoogle Scholar
  9. 9.
    Croner RS, Merkel S, Papadopoulos T, Schellerer V, Hohenberger W, Goehl J. Multivisceral resection for colon carcinoma. Dis Colon Rectum 2009;52:1381–1386CrossRefGoogle Scholar
  10. 10.
    Moertel CG, Fleming TR, Macdonald JS, et al. Fluorouracil plus levamisole as effective adjuvant therapy after resection of stage III colon carcinoma: a final report. Ann Intern Med 1995;122:321–326CrossRefGoogle Scholar
  11. 11.
    Efficacy of adjuvant fluorouracil and folinic acid in colon cancer. International Multicentre Pooled Analysis of Colon Cancer Trials (IMPACT) investigators. Lancet 1995;345:939–944CrossRefGoogle Scholar
  12. 12.
    National Comprehensive Cancer Network. Colon Cancer (Version 2.2016).Google Scholar
  13. 13.
    Bowne WB, Lee B, Wong WD, Ben-Porat L, Shia J, Cohen AM, Enker WE, Guillem JG, Paty PB, Weiser MR. Operative salvage for locoregional recurrent colon cancer after curative resection: an analysis of 100 cases. Dis Colon Rectum 2005;48:897–909CrossRefGoogle Scholar
  14. 14.
    Galandiuk S, Wieand HS, Moertel CG, Cha SS, Fitzgibbons RJ Jr, Pemberton JH, Wolff BG. Patterns of recurrence after curative resection of carcinoma of the colon and rectum. Surg Gynecol Obstet 1992;174:27–32Google Scholar
  15. 15.
    Nelson H, Petrelli N, Carlin A, Couture J, Fleshman J, Guillem J, Miedema B, Ota D, Sargent D; National Cancer Institute Expert Panel. Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst 2001;93:583–596CrossRefGoogle Scholar
  16. 16.
    Khan MA, Hakeem AR, Scott N, Saunders RN. Significance of R1 resection margin in colon cancer resections in the modern era. Colorectal Dis 2015;17:943–953CrossRefGoogle Scholar
  17. 17.
    Nakafusa Y, Tanaka T, Tanaka M, Kitajima Y, Sato S, Miyazaki K: Comparison of multivisceral resection and standard operation for locally advanced colorectal cancer: analysis of prognostic factors for short-term and long-term outcome. Dis Colon Rectum 2004;47:2055–2063CrossRefGoogle Scholar
  18. 18.
    Hashiguchi Y, Hase K, Ueno H, Mochizuki H, Shinto E, Yamamoto J. Optimal margins and lymphadenectomy in colonic cancer surgery. Br J Surg. 2011;98:1171–1178CrossRefGoogle Scholar
  19. 19.
    Rørvig S, Schlesinger N, Mårtensson NL, Engel S, Engel U, Holck S. Is the longitudinal margin of carcinoma-bearing colon resections a neglected parameter? Clin Colorectal Cancer. 2014;13:68–72CrossRefGoogle Scholar
  20. 20.
    Amri R, Bordeianou LG, Sylla P, Berger DL. Association of radial margin positivity with colon cancer. JAMA Surg 2015;150:890–898CrossRefGoogle Scholar
  21. 21.
    Radespiel-Troger M, Hohenberger W, Reingruber B. Improved prediction of recurrence after curative resection of colon carcinoma using tree-based risk stratification. Cancer 2004;100:958–967CrossRefGoogle Scholar
  22. 22.
    Longo WE, Virgo KS, Johnson FE, Oprian CA, Vernava AM, Wade TP, Phelan MA, Henderson WG, Daley J, Khuri SF. Risk factors for morbidity and mortality after colectomy for colon cancer. Dis Colon Rectum 2000;43:83–91CrossRefGoogle Scholar
  23. 23.
    Artinyan A, Nunoo-Mensah JW, Balasubramaniam S, Gauderman J, Essani R, Gonzalez-Ruiz C, Kaiser AM, Beart RW Jr. Prolonged postoperative ileus-definition, risk factors, and predictors after surgery. World J Surg. 2008;32:1495–1500CrossRefGoogle Scholar
  24. 24.
    Kiran RP, Delaney CP, Senagore AJ, Millward BL, Fazio VW. Operative blood loss and use of blood products after laparoscopic and conventional open colorectal operations. Arch Surg. 2004;139:39–42CrossRefGoogle Scholar
  25. 25.
    Halabi WJ, Jafari MD, Nguyen VQ, Carmichael JC, Mills S, Pigazzi A, Stamos MJ. Blood transfusions in colorectal cancer surgery: incidence, outcomes, and predictive factors: an American College of Surgeons National Surgical Quality Improvement Program analysis. Am J Surg 2013;206:1024–1032CrossRefGoogle Scholar
  26. 26.
    Colorectal Cancer Collaborative Group. Surgery for colorectal cancer in elderly patients: a systematic review. Lancet 2000;356:968–974CrossRefGoogle Scholar
  27. 27.
    Chen YG, Liu YL, Jiang SX, Wang XS. Adhesion pattern and prognosis studies of T4N0M0 colorectal cancer following en bloc multivisceral resection: evaluation of T4 subclassification. Cell Biochem Biophys 2011;59:1–6CrossRefGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  • Lieve G. J. Leijssen
    • 1
  • Anne M. Dinaux
    • 1
  • R. Amri
    • 1
  • Hiroko Kunitake
    • 1
  • Liliana G. Bordeianou
    • 1
  • David L. Berger
    • 1
    Email author
  1. 1.Department of General and Gastrointestinal Surgery, Massachusetts General HospitalHarvard Medical SchoolBostonUSA

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