Surgery
Volume 147, Issue 1 , Pages 120-126 , January 2010

Postoperative intra-abdominal infection increases angiogenesis and tumor recurrence after surgical excision of colon cancer in mice

  • Bernhard Bohle, MD

      Affiliations

    • Colorectal Surgery Unit, Department of Surgery, Hospital del Mar, Barcelona, Spain
    • Colorectal Cancer Research Group, Cancer Research Program, Municipal Institute for Medical Research (IMIM-Hospital del Mar), Barcelona, Spain
    • ,
  • Miguel Pera, MD

      Affiliations

    • Colorectal Surgery Unit, Department of Surgery, Hospital del Mar, Barcelona, Spain
    • Colorectal Cancer Research Group, Cancer Research Program, Municipal Institute for Medical Research (IMIM-Hospital del Mar), Barcelona, Spain
    • Corresponding Author InformationReprint requests: Miguel Pera, MD, Colorectal Surgery Unit, Department of Surgery, Hospital del Mar, Passeig Marítim 25-29, 08003 Barcelona, Spain.
    • ,
  • Marta Pascual, MD

      Affiliations

    • Colorectal Surgery Unit, Department of Surgery, Hospital del Mar, Barcelona, Spain
    • Colorectal Cancer Research Group, Cancer Research Program, Municipal Institute for Medical Research (IMIM-Hospital del Mar), Barcelona, Spain
    • ,
  • Sandra Alonso, MD

      Affiliations

    • Colorectal Surgery Unit, Department of Surgery, Hospital del Mar, Barcelona, Spain
    • Colorectal Cancer Research Group, Cancer Research Program, Municipal Institute for Medical Research (IMIM-Hospital del Mar), Barcelona, Spain
    • ,
  • Xavier Mayol, PhD

      Affiliations

    • Colorectal Cancer Research Group, Cancer Research Program, Municipal Institute for Medical Research (IMIM-Hospital del Mar), Barcelona, Spain
    • ,
  • Margarita Salvado, MD

      Affiliations

    • Department of Microbiology, Laboratori de Referència de Catalunya, Barcelona, Spain
    • ,
  • Jan Schmidt, MD

      Affiliations

    • Department of General Surgery, University of Heidelberg, Heidelberg, Germany
    • ,
  • Luis Grande, MD

      Affiliations

    • Colorectal Surgery Unit, Department of Surgery, Hospital del Mar, Barcelona, Spain

,Accepted 30 June 2009.

References 

  1. Karanjia N, Corder A, Bearn P, Heald RJ. Leakage from stapled low anastomosis after total mesorectal excision for carcinoma of the rectum. Br J Surg. 1994;81:1224–1226
  2. Bruce J, Krukowski ZH, Al-Khairy G, Russell EM, Park KG. Systematic review of the definition and measurement of anastomotic leak after gastrointestinal surgery. Br J Surg. 2001;88:1157–1168
  3. Chambers WM, Mortensen NJ. Postoperative leakage and abscess formation after colorectal surgery. Best Pract Res Clin Gastroenterol. 2004;18:865–880
  4. Rullier E, Laurent C, Garrelon JL, Michel P, Saric J, Parneix M. Risk factors for anastomotic leakage after resection of rectal cancer. Br J Surg. 1998;85:355–358
  5. Akyol A, McGregor J, Galloway D, Murray GD, George WD. Anastomotic leaks in colorectal cancer surgery: a risk factor for recurrence?. Int J Colorectal Dis. 1991;6:179–183
  6. Fujita S, Teramoto T, Watanabe M, Kodaira S, Kitajima M. Anastomotic leakage after colorectal cancer surgery: a risk factor for recurrence and poor prognosis. Jpn J Clin Oncol. 1993;23:299–302
  7. Petersen S, Freitag M, Hellmich G, Ludwig K. Anastomotic leakage: impact on local recurrence and survival in surgery of colorectal cancer. Int J Colorectal Dis. 1998;13:160–163
  8. Merkel S, Wang WY, Schmidt O, Dworak O, Wittekind C, Hohenberger W, et al. Locoregional recurrence in patients with anastomotic leakage after anterior resection for rectal carcinoma. Colorectal Dis. 2001;3:154–160
  9. Bell SW, Walker KG, Rickard MJ, Sinclair G, Dent OF, Chapuis PH, et al. Anastomotic leakage after curative anterior resection results in a higher prevalence of local recurrence. Br J Surg. 2003;90:1261–1266
  10. Walker K, Bell S, Rickard MJ, Mehanna D, Dent OF, Chapuis PH, et al. Anastomotic leakage is predictive of diminished survival after potentially curative resection for colorectal cancer. Ann Surg. 2004;240:255–259
  11. Branagan G, Finnis D. Prognosis after anastomotic leakage in colorectal surgery. Dis Colon Rectum. 2005;48:1021–1026
  12. McArdle CS, McMillan DC, Hole D. Impact of anastomotic leakage on long-term survival of patients undergoing curative resection for colorectal cancer. Br J Surg. 2005;92:1150–1154
  13. Law WI, Choi H, Lee Y, Ho JW, Seto CL. Anastomotic leakage is associated with poor long-term outcome in patients after curative colorectal resection for malignancy. J Gastrointest Surg. 2007;11:8–15
  14. Ptok H, Marusch F, Meyer F, Schubert D, Gastinger I, Lippert H Study Group Colon/Rectum Carcinoma (Primary Tumour). Impact of anastomotic leakage on oncological outcome after rectal cancer resection. Br J Surg. 2007;94:1548–1554
  15. Phillips R, Hittinger R, Blesovsky L, Fry JS, Fielding LP. Local recurrence following ‘curative’ surgery for large bowel cancer: I. The overall picture. Br J Surg. 1984;71:12–16
  16. Varty P, Linehan I, Boulos P. Intra-abdominal sepsis and survival after surgery for colorectal cancer. Br J Surg. 1994;81:915–918
  17. Kressner U, Graf W, Mahteme H, Påhlman L, Glimelius B. Septic complications and prognosis after surgery for rectal cancer. Dis Colon Rectum. 2002;45:316–321
  18. Eriksen MT, Wibe A, Norstein J, Haffner J, Wiig JN Norwegian Rectal Cancer Group. Anastomotic leakage following routine mesorectal excision for rectal cancer in a national cohort of patients. Colorectal Dis. 2005;7:51–57
  19. Martin C, Boisson C, Haccoun M, Thomachot L, Mege JL. Patterns of cytokine evolution (tumor necrosis factor-alpha and interleukin-6) after septic shock, hemorrhagic shock, and severe trauma. Crit Care Med. 1997;25:1813–1819
  20. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86:353–364
  21. Kut C, Mac Gabhann F, Popel A. Where is the VEGF in the body? A meta-analysis of VEGF distribution in cancer. Br J Cancer. 2007;97:978–985
  22. Cascinu S, Staccioli M, Gasparini G, Giordani P, Catalano V, Ghiselli R, et al. Expression of vascular endothelial growth factor can predict event-free survival in stage II colon cancer. Clin Cancer Res. 2000;6:2803–2807
  23. Vermeulen P, Van den Eynden G, Huget P, Goovaerts G, Weyler J, Lardon F, et al. Prospective study of intratumoral microvessel density, p53 expression and survival in colorectal cancer. Br J Cancer. 1999;79:316–322
  24. Pera M, Nelson H, Rajkumar SV, Young-Fadok TM, Burgart LJ. Influence of postoperative acute-phase response on angiogenesis and tumor growth: open vs. laparoscopic-assisted surgery in mice. J Gastrointest Surg. 2003;76:783–790
  25. Bresalier R, Hujanen E, Raper S, Roll FJ, Itzkowitz SH, Martin GR, et al. An animal model for colon cancer metastasis: establishment and characterization of murine cell lines with enhanced liver-metastasizing ability. Cancer Res. 1987;47:1398–1406
  26. Gollapudi SV, Gupta A, Thadepalli H, Perez A. Use of lymphokines in treatment of experimental intra-abdominal abscess caused by Bacteroides fragilis. Infect Immun. 1988;56:2369–2372
  27. Shapiro ME, Onderdonk AB, Kasper DL, Finberg RW. Cellular immunity to Bacteroides fragilis capsular polysaccharide. J Exp Med. 1982;155:1188–1197
  28. Bouvy N, Marquet R, Jeekel J, Bonjer HJ. Laparoscopic surgery is associated with less tumor growth stimulation than conventional surgery: an experimental study. Br J Surg. 1997;84:358–361
  29. Pidgeon G, Harmey J, Kay E, Da Costa M, Redmond HP, Bouchier-Hayes DJ. The role of endotoxin/lipopolysaccharide in surgically induced tumour growth in a murine model of metastatic disease. Br J Cancer. 1999;81:1311–1317
  30. Peeters K, Marijnen C, Nagtegaal I, Kranenbarg EK, Putter H, Wiggers T, et al. The TME trial after a median follow-up of 6 years: increased local control but no survival benefit in irradiated patients with resectable carcinoma. Ann Surg. 2007;247:693–701
  31. Cohen T, Nahari D, Cerem L, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem. 1996;271:736–741
  32. Akagi Y, Liu W, Xie K, Shaheen RM, Ellis LM. Regulation of vascular endothelial growth factor expression in human colon cancer by interleukin-1β. Br J Cancer. 1999;80:1506–1511
  33. Salgado R, Vermeulen P, Benoy I, Weytjens R, Huget P, Van Marck E, et al. Platelet number and interleukin-6 correlate with VEGF but not with bFGF serum levels of advanced cancer patients. Br J Cancer. 1999;80:892–897
  34. Belluco C, Nitti D, Frantz M, Toppan P, Basso D, Plebani M, et al. Interleukin-6 blood level is associated with circulating carcinoembryonic antigen and prognosis in patients with colorectal cancer. Ann Surg Oncol. 2000;7:133–138
  35. Buyne O, Bleichrodt R, Verweij P, Groenewoud HM, van Goor H, Hendriks T. A peritonitis model with low mortality and persisting intra-abdominal abscesses. Int J Exp Pathol. 2006;87:361–368
  36. Rittirsch D, Hoesel L, Ward P. The disconnect between animal models of sepsis and human sepsis. J Leukoc Biol. 2007;81:137–143
  37. Woods DR, Heffley S, Peyton JC, Cheadle WG. Antibiotic modulation in a clinically relevant model of chronic intraabdominal infection. Am Surg. 2006;72:655–660

 Supported by a research grant from the Asociación Española Contra el Cáncer (No. 449).

PII: S0039-6060(09)00420-6

doi: 10.1016/j.surg.2009.06.035

Surgery
Volume 147, Issue 1 , Pages 120-126 , January 2010

Article Tools

* Image Usage & Resolution