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Perioperative host-tumor inflammatory interactions: A potential trigger for disease recurrence following a curative resection for colorectal cancer

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Abstract

The aim of the present review was to investigate whether host-tumor interactions are causal or consecutive clinical factors associated with surgical stress that influence the long-term survival after a curative resection of colorectal cancer. A Medline/PubMed search was conducted to identify the relevant articles investigating the factors related to surgical stress and their effects on the long-term survival after a curative resection of colorectal cancer. The intraoperative state is defined as a cytokine storm in which ongoing local cytokine production occurs at the site of the tumor, thus further enhancing the autocrine cytokine loop for angiogenic factor production. The postoperative state is defined as tissue regeneration in which surgery-related clinical events enhance the systemic induction of inflammatory cytokines, which in turn synergistically exaggerate the local activation of tumor growth factors. Host-tumor interactions under surgical stress may act synergistically as potent tumor growth factors, and may thus influence long-term survival. Controlling surgical insults and/or regulating perioperative inflammatory responses may therefore lead to new therapeutic approaches for controlling disease recurrence.

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References

  1. Mitry E, Douillard JY, van Cutsem E, Cunningham D, Magherini E, Mery-Mignard D, et al. Predicitive factors of survival in patients with advanced colorectal cancer: an individual data analysis of 602 patients included in irinotecan phase III trials. Ann Oncol 2004;15:1013–1017.

    Article  PubMed  CAS  Google Scholar 

  2. Kondo E, Koda K, Takiguchi N, Oda K, Seike K, Ishizuka M, et al. Preoperative natural killer cell activity as a prognostic factor for distant metastasis following surgery for colon cancer. Dig Surg 2003;20:445–451.

    Article  PubMed  Google Scholar 

  3. Heys SD, Walker LG, Deehan DJ, Eremin OE. Serum albumin: a prognostic indicator in patients with colorectal cancer. J R Coll Surg Edinb 1998;43:163–168.

    PubMed  CAS  Google Scholar 

  4. McMillan DC, Wotherspoon HA, Fearon KC, Sturgeon C, Cooke TG, McArdle CS. A prospective study of tumor recurrence and the acute-phase response after apparently curative colorectal cancer surgery. Am J Surg 1995;170;319–322.

    Article  PubMed  CAS  Google Scholar 

  5. ten Kate M, Hofland LJ, van Grevenstein WMU, van Koetsveld PV, Jeekel J, van Eijck CH. Influence of proinflammatory cytokines on the adhesion of human colon carcinoma cells to lung microvascular endothelim. Int J Cancer 2004;112:943–950.

    Article  PubMed  CAS  Google Scholar 

  6. Higashiyama A, Watanabe H, Okuyama K, Yagita H. Involvement of tumor necrosis factor alpha and very late activation antigen 4/vascular cell adhesion molecule-1 interaction in surgical-stress-enhanced experimental metastasis. Cancer Immunol Immunother 1996;42:231–236.

    Article  PubMed  CAS  Google Scholar 

  7. Ben-Eliyahu S. The promotion of tumor metastasis by surgery and stress: Immunological basis and implications for psychoneuroimmunology. Brain Behav Immun 2003;17:S27–S36.

    Article  PubMed  CAS  Google Scholar 

  8. Ben-Eliyahu S, Shakhar G, Rosenne E, Levinson Y, Beilin B. Hypothermia in barbiturate-anesthetized rats suppresses natural killer cell activity and compromises resistance to tumor metastasis: a role for adrenergic mechanisms. Anesthesiology 1999;91:732–740.

    Article  PubMed  CAS  Google Scholar 

  9. Riche F, Dosquet C, Panis Y, Valleur P, Laisné MJ, Briard C, et al. Levels of portal and systemic blood cytokines after colectomy in patients with carcinoma or Crohn’s disease. J Am Coll Surg 1995;180(6):718–724.

    PubMed  CAS  Google Scholar 

  10. Syk I, Hedges SR, Zederfeldt B, Risberg B. Enhanced cytokine response to surgical trauma in patients with colorectal cancer. Int J Surg Invest 1999;1(3):167–176.

    CAS  Google Scholar 

  11. Ito H, Miki C. Profile of circulating levels of interleukin-1 receptor antagonist and interleukin-6 in colorectal cancer patients. Scand J Gastroenterol 1999;34:1139–1143.

    Article  PubMed  CAS  Google Scholar 

  12. Syk I, Mangell P, Bjartell A, Jeppsson B. Systemic interleukin-6 response to colorectal surgery originates from the bowel. Dig Surg 2002;19:210–215.

    Article  PubMed  CAS  Google Scholar 

  13. Kinoshita T, Ito H, Miki C. Serum interleukin-6 level reflects tumor proliferative activity in colorectal cancer patients. Cancer 1999;85(12):2526–2531.

    Article  PubMed  CAS  Google Scholar 

  14. Miki C, Tonouchi H, Wakuda R, Hatada T, Inoue Y, Minato E, et al. Intra-tumoral interleukin-6 down-regulation system and genetic mutations of tumor suppressor genes in colorectal carcinoma. Cancer 2002;94(5):1584–1592.

    Article  PubMed  CAS  Google Scholar 

  15. Miki C, Konishi N, Ojima E, Hatada T, Inoue Y, Kusunoki M. C-reactive protein as a prognostic variable that reflects uncontrolled up-regulation of the IL-1-IL-6 network system in colorectal carcinoma. Dig Dis Sci 2004;49:970–976.

    Article  PubMed  CAS  Google Scholar 

  16. McArdle CS, McMillan DC, Hole DJ. The impact of blood loss, obstruction and perforation on survival in patients undergoing curative resection for colon cancer. Br J Surg 2006;93:483–488.

    Article  PubMed  CAS  Google Scholar 

  17. Ishijima N, Suzuki H. Blood transfusion and postoperative serum interleukin-6 levels in colorectal cancer patients. Hepatogastroenterology 1998;45:1011–1013.

    PubMed  CAS  Google Scholar 

  18. Hensler T, Heinemann B, Sauerland S, Lefering R, Bouillon B, Andermahr J, et al. Immunologic alterations associated with high blood transfusion volume after multiple injury: effects on plasmatic cytokine and cytokine receptor concentrations. Shock 2003;20:497–502.

    Article  PubMed  Google Scholar 

  19. Mynster T, Christensen IJ, Moesgaard F, Nielsen HJ. Effects of the combination of blood transfusion and postoperative infectious complications on prognosis after surgery for colorectal cancer. Br J Surg 2000;87:1553–1562.

    Article  PubMed  CAS  Google Scholar 

  20. Jensen LS, Hokland M, Nielsen HJ. A randomized controlled study of the effect of whole blood transfusion in patients undergoing elective colorectal surgery. Br J Surg 1996;83:973–977.

    Article  PubMed  CAS  Google Scholar 

  21. Mathiesen O, Lund L, Brodthagen U, Gandrup P, Gunnet N, Balslev I, et al. The effect of previous blood transfuion on lymphocyte subsets and natural killer cell function in patients with colorectal cancer. Vox Sang 1994;67:36–41.

    Article  PubMed  CAS  Google Scholar 

  22. Liewald F, Wirsching RP, Zulke C, Demmel N, Mempel W. Influence of blood transfusions on tumor recurrence and survival rate in colorectal carcinoma. Eur J Cancer 1990;26:327–335.

    PubMed  CAS  Google Scholar 

  23. Marquet RL, Busch OR, Jeekel J, Heiss MM, Amato AC. Are allogeneic blood transfusions acceptable in elective surgery in colorectal carcinoma? Eur J Cancer 1999;35:352–360.

    Article  PubMed  CAS  Google Scholar 

  24. Busch ORC, Hop WCJ, Marquet RL, Jeekel J. Blood transfusions and local tumor recurrence in colorectal cancer: evidence of a noncausal relationship. Ann Surg 1994;220:791–797.

    Article  PubMed  CAS  Google Scholar 

  25. Heiss MM, Mempel W, Delanoff C, Jauch KW, Gabka C, Mempel M, et al. Blood transfusion-modulated tumor recurrence: first results of a randomized study of autologous versus allogeneic blood transfusion in colorectal cancer surgery. J Clin Oncol 1994;12:1859–1867.

    PubMed  CAS  Google Scholar 

  26. Edna TH, Bjerkeset T. Perioperative blood transfusions reduce long-term survival following surgery for colorectal cancer. Dis Colon Rectum 1998;41:451–459.

    Article  PubMed  CAS  Google Scholar 

  27. Chung M, Steinmetz OK, Gordon PH. Perioperative blood transfusion and outcome after resection for colorectal carcinoma. Br J Surg 1993;80:427–432.

    Article  PubMed  CAS  Google Scholar 

  28. Tartter PI. The association of perioperative blood transfusion with colorectal cancer recurrence. Ann Surg 1992;216:633–638.

    Article  PubMed  CAS  Google Scholar 

  29. Younes RN, Rogatko A, Brennan MF. The influence of intraoperative hypotension and perioperative blood transfusion on disease-free survival in patients with complete resection of colorectal liver metastasis. Ann Surg 1991;214:107–113.

    Article  PubMed  CAS  Google Scholar 

  30. Beynon J, Davies PW, Billings PJ, Channer JL, Protheroe D, Umpleby HC, et al. Perioperative blood transfusion increases the risk of recurrence in colorectal cancer. Dis Colon Rectum 1989;32:975–979.

    Article  PubMed  CAS  Google Scholar 

  31. Blumberg N, Heal J, Chuang C, Murphy P, Agarwal M. Further evidence supporting a cause and effect relationship between blood transfusion and earlier cancer recurrence. Ann Surg 1988;207:410–415.

    Article  PubMed  CAS  Google Scholar 

  32. Parrott NR, Lennard TW, Taylor RM, Proud G, Shenton BK, Johnson ID. Effect of perioperative blood transfusion on recurrence of colorectal cancer. Br J Surg 1986;73:970–973.

    Article  PubMed  CAS  Google Scholar 

  33. Wobbes T, Joosen KH, Kuypers HH, Beerthuizen GI, Theeuwes GM. The effect of packed cells and whole blood transfusions on survival after curative resection for colorectal carcinoma. Dis Colon Rectum 1989;32:743–748.

    Article  PubMed  CAS  Google Scholar 

  34. Shao W, Edelman L, Sullivan DJ, Nelson EW, Shelby J. Long-term cytokine alterations following allogeneic blood transfusion. J Invest Med 1998;46:161–167.

    CAS  Google Scholar 

  35. Amato A, Pescatori M. Perioperative blood transfusions for the recurrence of colorectal cancer. Cochrane Database Syst Rev 2006;25:CD005033.

    Google Scholar 

  36. Busch OR, Hop WC, Hoynck van Papendrect MAW, Marquet RL, Jeekel J. Blood transfusions and prognosis in colorectal cancer. N Engl J Med 1993;328:1372–1376.

    Article  PubMed  CAS  Google Scholar 

  37. Cheslyn-Curtis S, Fielding LP, Hittinger R, Hittinger R, Fry JS, Phillips RK. Large bowel cancer: the effect of perioperative blood transfusion on outcome. Ann R Coll Surg Engl 1990;72:53–59.

    PubMed  CAS  Google Scholar 

  38. Miki C, Hiro J, Ojima E, Inoue Y, Mohri Y, Kusunoki M. Perioperative allogeneic blood transfusion, the related cytokine response and long-term survival following potentially curative resection of colorectal cancer. Clin Oncol 2006;18:60–66.

    Article  CAS  Google Scholar 

  39. Nozoe T, Matsumata T, Sugimachi K. Preoperative elevation of serum C-reactive protein is related to impaired immunity in patients with colorectal cancer. Am J Clin Oncol 2000;23:263–266.

    PubMed  CAS  Google Scholar 

  40. Ikuta S, Miki C, Tanaka K, Konishi N, Mohri Y, Tonouchi H, et al. Serum immunosuppressive acidic protein as an interleukin-6 related index of deteriorating condition in gastric cancer patients. Dig Surg 2003;20:532–538.

    Article  PubMed  CAS  Google Scholar 

  41. Hatada T, Miki C. Nutritional status and postoperative cytokine response in colorectal cancer patients. Cytokine 2000;12:1331–1336.

    Article  PubMed  CAS  Google Scholar 

  42. Yamashita J, Kurusu Y, Fujino N, Saisyoji T, Ogawa M. Detection of circulating cancer cells in patients with non-small cell lung cancer undergoing lobectomy by video-assisted thoracic surgery: a potential hazard for intraoperative hematogenous tumor cell dissemination. J Thorac Cardiovasc Surg 2000;119:899–905.

    Article  PubMed  CAS  Google Scholar 

  43. Jensen LS, Andersen AJ, Christiansen PM, Hokland P, Juhl CO, Madsen G, et al. Postoperative infection and natural killer cell function following blood transfusion in patients undergoing elective colorectal surgery. Br J Surg 1992;79:513–516.

    Article  PubMed  CAS  Google Scholar 

  44. Cristaldi M, Rovatti M, Elli M, Gerlinzani S, Lesma A, Balzarotti L, et al. Lymphocyte subpopulation changes after open and laparoscopic cholecystectomy: a prospective and comparative study on 38 patients. Surg Laparosc Endosc 1997;7:255–261.

    Article  PubMed  CAS  Google Scholar 

  45. Ben-Eliyahu S. The promotion of tumor metastasis by surgery and stress: immunological basis and implications for psychoneuroimmunology. Brain Behav Immun 2003;17:S27–S36.

    Article  PubMed  CAS  Google Scholar 

  46. McArdle CS, McMillan DC, Hole DJ. Impact of anastomotic leakage on long-term survival of patients undergoing curative resection for colorectal cancer. Br J Surg 2005;92:1150–1154.

    Article  PubMed  CAS  Google Scholar 

  47. Nowacki MP, Szymendera JJ. The strongest prognostic factors in colorectal carcinoma. Surgicopathologic stage of disease and postoperative fever. Dis Colon Rectum 1983;26:263–268.

    Article  PubMed  CAS  Google Scholar 

  48. Nespoli A, Gianotti L, Bovo G, Bovo G, Nespoli L, Chiodini P, et al. Correlation between postoperative infections and long-term survival after colorectal resection for cancer. Tumori 2004;90:485–490.

    PubMed  Google Scholar 

  49. Laurent C, Sa Cunha A, Couderc E, Rullier E, Saric J. Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg 2003;90:1131–1136.

    Article  PubMed  CAS  Google Scholar 

  50. Fermor B, Umpleby HC, Lever JV, Symes MO, Williamson RC. Proliferative and metastatic potential of exfoliated colorectal cancer cells. J Natl Cancer Inst 1986;76:347–349.

    PubMed  CAS  Google Scholar 

  51. van den Tol PM, van Rossen EE, van Eijck CH, Bonthuis F, Marquet RL, Jeekel H. Reduction of peritoneal trauma by using nonsurgical gauze leads to less implantation metastasis of spilled tumor cells. Ann Surg 1998;227:242–248.

    Article  PubMed  Google Scholar 

  52. Akyol AM, McGregor JR, Galloway DJ, Murray GD, George WD. Anastomotic leaks in colorectal cancer surgery: a risk factor for recurrence? Int J Colorectal Dis 1991;6:179–183.

    Article  PubMed  CAS  Google Scholar 

  53. Akyol AM, McGregor JR, Galloway DJ, Murray G, George WD. Recurrence of colorectal cancer after sutured and stapled large bowel anastomoses. Br J Surg 1991;78:1297–1300.

    Article  PubMed  CAS  Google Scholar 

  54. Chang SC, Lin JK, Yang JK, Jiang JK, Chen WC, Lin TC. Longterm outcome of anastomosis leakage after curative resection for mid and low rectal cancer. Hepatogastroenterology 2003;50:1898–1902.

    PubMed  Google Scholar 

  55. Peterson 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.

    Article  Google Scholar 

  56. Branagan G, Finnis D. Prognosis after anastomotic leakage in colorectal surgery. Dis Colon Rectum 2005;48:1021–106.

    Article  PubMed  Google Scholar 

  57. Walker KG, Bell SW, Rickard MJFX, Mehanna D, Dent OF, Chapuis PH, et al. Anastomotic leakage is predictive of diminished survival after potentially curative resection of colorectal cancer. Ann Surg 2004;240:255–259.

    Article  PubMed  Google Scholar 

  58. Bell SW, Walker KG, Rickard MJFX, 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.

    Article  PubMed  CAS  Google Scholar 

  59. Kressner U, Graf W, Mahteme H, Påhlman L, Glimelius B. Septic complications and prognosis after surgery for rectal cancers. Dis Colon Rectum 2002;45:316–321.

    Article  PubMed  Google Scholar 

  60. Sietses C, Beelen RHJ, Meijer S, Cuesta MA. Immunological consequences of laparoscopic surgery, speculations on the cause and clinical implications. Langenbeck’s Arch Surg 1999;384:250–258.

    Article  CAS  Google Scholar 

  61. Eriksen MT, Wibe A, Norstein J, Haffner J, Wiig JN. Anastomotic leakage following routine mesorectal excision for rectal cancer in a national cohort of patients. Colorectal Dis 2005;7:51–57.

    Article  PubMed  CAS  Google Scholar 

  62. Ito R, Yasui W, Kuniyasu H, Yokozaki H, Tahara E. Expression of interleukin-6 and its effect on the cell growth of gastric carcinoma cell lines. Jpn J Cancer Res 1997;88:953–958.

    PubMed  CAS  Google Scholar 

  63. Vittimberga FJ, Foley DP, Meyers WC, Callery MP. Laparoscopic surgery and the systemic immune response. Ann Surg 1998;227:326–334.

    Article  PubMed  Google Scholar 

  64. Allendorf JD, Bessler M, Horvath KD, Marvin MR, Laird DA, Whelan RL. Increased tumor establishment and growth after open vs laparoscopic surgery in mice may be related to differences in postoperative T-cell function. Surg Endosc 1999;13:233–235.

    Article  PubMed  CAS  Google Scholar 

  65. Da Costa M, Redmond P, Bouchier-Hyaes DJ. The effect of laparotomy and laparoscopy on the establishment of spontaneous tumor metastases. Surgery 1998;124:516–525.

    Article  PubMed  Google Scholar 

  66. Brivio F, Lissoni P, Perego MS, Lissoni A, Fumagalli L. Abrogation of surgery-induced IL-6 hypersecretion by presurgical immunotherapy with IL-2 and its importance in the prevention of postoperative complications. J Biol Regul Homeost Agents 2001;15:370–374.

    PubMed  CAS  Google Scholar 

  67. Yamashita Y, Shimada M, Hamatsu T, Rikimaru T, Tanaka S, Shirabe K, et al. Effects of preoperative steroid administration on surgical stress in hepatic resection: prospective randomized trial. Arch Surg 2001;136:328–333.

    Article  PubMed  CAS  Google Scholar 

  68. Kilger E, Weis F, Briegel J, Frey L, Goetz AE, Reuter D, et al. Stress doses of hydrocortisone reduce severe systemic inflammatory response syndrome and improve early outcome in a risk group of patients after cardiac surgery. Crit Care Med 2003;31:1068–1074.

    Article  PubMed  CAS  Google Scholar 

  69. Nakamura E, Kitagawa Y, Ozawa S, Suda K, Ando N, Ueda M, et al. Role of steroid administration to reduce inflammation after thoracotomy in a rat surgical stress model. J Surg Res 2006;135:364–369.

    Article  PubMed  CAS  Google Scholar 

  70. Aldrighetti L, Pulitano C, Arru M, Finazzi R, Catena M, Soldini L, et al. Impact of preoperative steroids administration on ischemia-reperfusion injury and systemic responses in liver surgery: a prospective randomized study. Liver Transpl 2006;12:941–949.

    Article  PubMed  Google Scholar 

  71. Swails WS, Kenler AS, Driscoll DF, DeMichele SJ, Babineau TJ, Utsunamiya T, et al. Effect of a fish oil structured lipid-based diet on prostaglandin release from mononuclear cells in cancer patients after surgery. J Parenteral Enteral Nutr 1997;21:266–274.

    Article  CAS  Google Scholar 

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Miki, C., Tanaka, K., Inoue, Y. et al. Perioperative host-tumor inflammatory interactions: A potential trigger for disease recurrence following a curative resection for colorectal cancer. Surg Today 38, 579–584 (2008). https://doi.org/10.1007/s00595-007-3674-6

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