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Laparoscopic surgery induced interleukin-6 levels in serum and gut mucosa: implications of peritoneum integrity and gas factors

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Abstract

Background

The peritoneum serves as an integral part of host immunity, and the homeostasis of intraperitoneal environment is held to be beneficial for patient recovery after abdominal surgery. How minimal invasive access to the abdomen by laparoscopy and incisions would alter the intraperitoneal immune response is not fully defined. This study examined the levels of IL-6 in serum and gut mucosa following laparoscopic surgery with reference to the peritoneum integrity and gas factors.

Methods

BALB/c mice were divided into three groups (ten animals in each group) that underwent different abdominal surgical treatments: laparotomy (open group), laparoscopy with atmospheric air (air group) or carbon dioxide pneumoperitoneum (CO2 group). A 3-cm incision of the skin and muscle was made in all animals except the peritoneum was left intact in the latter two animal groups in order to cancel out the incisional tissue injury present in laparotomy. Four hours after surgery, serum, and jejunal mucosa were extracted for IL-6 measurement by enzyme-linked immunosorbent assay (ELISA).

Results

Open laparotomy resulted in significant elevation of serum IL-6 level when compared to the laparoscopic procedures in the descending order of open > air > CO2 groups. For the mucosal IL-6 level, both the open and air groups were significantly higher than the CO2 group. Data from multivariate analysis revealed that breaching or incision of the peritoneum was an important factor for the elevated levels of IL-6 in serum (p < 0.001) and jejunal mucosa (p = 0.032).

Conclusion

The present study suggests that laparoscopic techniques to minimize the size of the peritoneal incision as well as exposure to atmospheric air can potentially reduce postoperative stress responses associated with abdominal surgery and prompt early recovery.

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References

  1. Meyer TA, Wang J, Tiao GM, Ogle CK, Fischer JE, Hasselgren PO (1995) Sepsis and endotoxemia stimulate intestinal interleukin-6 production. Surgery 118:336–342

    Article  PubMed  CAS  Google Scholar 

  2. Pritts T, Hungness E, Wang Q, Robb B, Hershko D, Hasselgren PO (2002) Mucosal and enterocyte IL-6 production during sepsis and endotoxemia–role of transcription factors and regulation by the stress response. Am J Surg 183:372–383

    Article  PubMed  CAS  Google Scholar 

  3. Tung PH, Wang Q, Ogle CK, Smith CD (1998) Minimal increase in gut-mucosal interleukin-6 during laparoscopy. Surg Endosc 12:409–411

    Article  PubMed  CAS  Google Scholar 

  4. Tung PH, Smith CD (1999) Laparoscopic insufflation with room air causes exaggerated interleukin-6 response. Surg Endosc 13:473–475

    Article  PubMed  CAS  Google Scholar 

  5. Broche F, Tellado JM (2001) Defense mechanisms of the peritoneal cavity. Curr Opin Crit Care 7:105–116

    Article  PubMed  CAS  Google Scholar 

  6. Kuhry E, Jeekel J, Bonjer HJ (2004) Effect of laparoscopy on the immune system. Semin Laparosc Surg 11:37–44

    PubMed  CAS  Google Scholar 

  7. Novitsky YW, Litwin DE, Callery MP (2004) The net immunologic advantage of laparoscopic surgery. Surg Endosc 18:1411–1419

    Article  PubMed  CAS  Google Scholar 

  8. Luk JM, Zhang QS, Lee NP, Wo JY, Leung PP, Liu LX, Hu MY, Cheung KF, Hui CK, Lau GK, Fan ST (2007) Hepatic stellate cell-targeted delivery of M6P-HSA-glycyrrhetinic acid attenuates hepatic fibrogenesis in a bile duct ligation rat model. Liver Int 27:548–557

    Article  PubMed  CAS  Google Scholar 

  9. Wong KF, Luk JM, Cheng RH, Klickstein LB, Fan ST (2007) Characterization of two novel LPS-binding sites in leukocyte integrin betaA domain. FASEB J 21:3231–3239

    Article  PubMed  CAS  Google Scholar 

  10. Ni Choileain N, Redmond HP (2006) Cell response to surgery. Arch Surg 141:1132–1140

    Article  PubMed  Google Scholar 

  11. West MA, Baker J, Bellingham J (1996) Kinetics of decreased LPS-stimulated cytokine release by macrophages exposed to CO2. J Surg Res 63:269–274

    Article  PubMed  CAS  Google Scholar 

  12. Ohzato H, Yoshizaki K, Nishimoto N, Ogata A, Tagoh H, Monden M, Gotoh M, Kishimoto T, Mori T (1992) Interleukin-6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and C-reactive protein after surgery. Surgery 111:201–209

    PubMed  CAS  Google Scholar 

  13. Evrard S, Falkenrodt A, Park A, Tassetti V, Mutter D, Marescaux J (1997) Influence of CO2 pneumoperitoneum on systemic and peritoneal cell-mediated immunity. World J Surg 21:353–356; discussion 357

    Article  PubMed  CAS  Google Scholar 

  14. Ueo H, Honda M, Adachi M, Inoue H, Nakashima H, Arinaga S, Akiyoshi T (1994) Minimal increase in serum interleukin-6 levels during laparoscopic cholecystectomy. Am J Surg 168:358–360

    Article  PubMed  CAS  Google Scholar 

  15. Shenkin A, Fraser WD, Series J, Winstanley FP, McCartney AC, Burns HJ, Van Damme J (1989) The serum interleukin 6 response to elective surgery. Lymphokine Res 8:123–127

    PubMed  CAS  Google Scholar 

  16. Maruszynski M, Pojda Z (1995) Interleukin 6 (IL-6) levels in the monitoring of surgical trauma. A comparison of serum IL-6 concentrations in patients treated by cholecystectomy via laparotomy or laparoscopy. Surg Endosc 9:882–885

    PubMed  CAS  Google Scholar 

  17. Cho JM, LaPorta AJ, Clark JR, Schofield MJ, Hammond SL, Mallory PL 2nd (1994) Response of serum cytokines in patients undergoing laparoscopic cholecystectomy. Surg Endosc 8:1380–1383; discussion 1383–1384

    Article  PubMed  CAS  Google Scholar 

  18. Glaser F, Sannwald GA, Buhr HJ, Kuntz C, Mayer H, Klee F, Herfarth C (1995) General stress response to conventional and laparoscopic cholecystectomy. Ann Surg 221:372–380

    Article  PubMed  CAS  Google Scholar 

  19. Chang CK, Zdon MJ (2005) Inflammatory response of interleukin-1beta and interleukin-6 in septic rats undergoing laparotomy and laparoscopy. Surg Laparosc Endosc Percutan Tech 15:124–128

    Article  PubMed  Google Scholar 

  20. Bessler M, Whelan RL, Halverson A, Treat MR, Nowygrod R (1994) Is immune function better preserved after laparoscopic versus open colon resection? Surg Endosc 8:881–883

    Article  PubMed  CAS  Google Scholar 

  21. Harmon GD, Senagore AJ, Kilbride MJ, Warzynski MJ (1994) Interleukin-6 response to laparoscopic and open colectomy. Dis Colon Rectum 37:754–759

    Article  PubMed  CAS  Google Scholar 

  22. Kuntz C, Wunsch A, Bay F, Windeler J, Glaser F, Herfarth C (1998) Prospective randomized study of stress and immune response after laparoscopic vs conventional colonic resection. Surg Endosc 12:963–967

    Article  PubMed  CAS  Google Scholar 

  23. Wortel CH, van Deventer SJ, Aarden LA, Lygidakis NJ, Buller HR, Hoek FJ, Horikx J, ten Cate JW (1993) Interleukin-6 mediates host defense responses induced by abdominal surgery. Surgery 114:564–570

    PubMed  CAS  Google Scholar 

  24. Mester M, Carter EA, Tompkins RG, Gelfand JA, Dinarello CA, Burke JF, Clark BD (1994) Thermal injury induces very early production of interleukin-1 alpha in the rat by mechanisms other than endotoxemia. Surgery 115:588–596

    PubMed  CAS  Google Scholar 

  25. Jeschke MG, Herndon DN, Finnerty CC, Bolder U, Thompson JC, Mueller U, Wolf SE, Przkora R (2005) The effect of growth hormone on gut mucosal homeostasis and cellular mediators after severe trauma. J Surg Res 127:183–189

    Article  PubMed  CAS  Google Scholar 

  26. Jeschke MG, Bolder U, Finnerty CC, Przkora R, Muller U, Maihofer R, Thompson JC, Wolf SE, Herndon DN (2005) The effect of hepatocyte growth factor on gut mucosal apoptosis and proliferation, and cellular mediators after severe trauma. Surgery 138:482–489

    Article  PubMed  Google Scholar 

  27. Badia JM, Whawell SA, Scott-Coombes DM, Abel PD, Williamson RC, Thompson JN (1996) Peritoneal and systemic cytokine response to laparotomy. Br J Surg 83:347–348

    Article  PubMed  CAS  Google Scholar 

  28. Allendorf JD, Bessler M, Whelan RL, Trokel M, Laird DA, Terry MB, Treat MR (1997) Postoperative immune function varies inversely with the degree of surgical trauma in a murine model. Surg Endosc 11:427–430

    Article  PubMed  CAS  Google Scholar 

  29. Jacobi CA, Ordemann J, Bohm B, Zieren HU, Liebenthal C, Volk HD, Muller JM (1997) The influence of laparotomy and laparoscopy on tumor growth in a rat model. Surg Endosc 11:618–621

    Article  PubMed  CAS  Google Scholar 

  30. Jacobi CA, Ordemann J, Zieren HU, Volk HD, Bauhofer A, Halle E, Muller JM (1998) Increased systemic inflammation after laparotomy vs laparoscopy in an animal model of peritonitis. Arch Surg 133:258–262

    Article  PubMed  CAS  Google Scholar 

  31. Targarona EM, Martinez J, Nadal A, Balague C, Cardesa A, Pascual S, Trias M (1998) Cancer dissemination during laparoscopic surgery: tubes, gas, and cells. World J Surg 22:55–60; discussion 60–51

    Article  PubMed  CAS  Google Scholar 

  32. Carter JJ, Whelan RL (2001) The immunologic consequences of laparoscopy in oncology. Surg Oncol Clin North Am 10:655–677

    CAS  Google Scholar 

  33. Watson RWG, Redmond HP, McCarthy J, Burke PE, Bouchier-Hayes D (1995) Exposure of the peritoneal cavity to air regulates early inflammatory responses ti surgery in murine model. Br J Surg 82:1060–1065

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The work was supported by grants from the Research Grants Council of Hong Kong (HKU732002M) and the research seed fund from the CRCG committee of the University of Hong Kong. The authors would like to thank the superb assistance of Dr. Jana Wo and Mr. Jensen To on animal surgery.

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Correspondence to Simon Law.

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Luk, J.M., Tung, P.H., Wong, KF. et al. Laparoscopic surgery induced interleukin-6 levels in serum and gut mucosa: implications of peritoneum integrity and gas factors. Surg Endosc 23, 370–376 (2009). https://doi.org/10.1007/s00464-008-9948-2

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  • DOI: https://doi.org/10.1007/s00464-008-9948-2

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