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CO2 pneumoperitoneum increases secretory IgA levels in the gut compared with laparotomy in an experimental animal model

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Abstract

Background

Secretory immunoglobulin A (s-IgA) plays an important role in both gut and systemic immunity. This study aimed to investigate the production of s-IgA resulting from a CO2 pneumoperitoneum compared with a laparotomy.

Methods

Using enzyme-linked immunosorbent assays, s-IgA in stool, malondialdehyde (MDA), and Toll-like receptor 4 (TLR4) in the ileal tissue were evaluated as markers for gut and systemic immune responses in an animal model. The rats were randomly divided into (i) anesthesia-only as the control group; (ii) laparotomy-only as the open group; and (iii) CO2 pneumoperitoneum-only as the pneumoperitoneum group. To evaluate the gut immune system in a time-dependent manner, each group was further divided into short- and long-time subgroups.

Results

s-IgA levels did not increase in the open group but significantly increased in the pneumoperitoneum group compared with the control group (p < 0.05). In addition, s-IgA levels in the long-time subgroup significantly increased compared with the short-time subgroup of the pneumoperitoneum group (p < 0.05). TLR4 levels steeply and gradually increased in the open and pneumoperitoneum groups, respectively. MDA levels in the pneumoperitoneum group increased during the early phase and were significantly higher than those in the open group at 24 h (p < 0.05).

Conclusions

This study demonstrated that s-IgA levels in stool increased in the pneumoperitoneum group compared with the open group, suggesting that CO2 pneumoperitoneum may cause transitory damage to the intestinal mucosa.

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References

  1. Leduc LJ, Mitchell A (2006) Intestinal ischemia after laparoscopic cholecystectomy. JSLS 10:236–238

    PubMed Central  PubMed  Google Scholar 

  2. Bandyopadhyay D, Kapadia CR (2003) Large bowel ischemia following laparoscopic inguinal hernioplasty. Surg Endosc 17:520–521

    Article  CAS  PubMed  Google Scholar 

  3. Etoh T, Shiraishi N, Tajima M, Shiromizu A, Yasuda K, Inomata M et al (2007) Transient liver dysfunction after laparoscopic gastrectomy for gastric cancer patients. World J Surg 31:1115–1120

    Article  PubMed  Google Scholar 

  4. Windberger UB, Auer R, Keplinger F, Längle F, Heinze G, Schindl M et al (1999) The role of intra-abdominal pressure on splanchnic and pulmonary hemodynamic and metabolic changes during carbon dioxide pneumoperitoneum. Gastrointest Endosc 49:84–91

    Article  CAS  PubMed  Google Scholar 

  5. Glantzounis GK, Tselepis AD, Tambaki AP, Trikalinos TA, Manataki AD, Galaris DA et al (2001) Laparoscopic surgery-induced changes in oxidative stress markers in human plasma. Surg Endosc 15:1315–1319

    Article  CAS  PubMed  Google Scholar 

  6. Windsor MA, Bonham MJ, Rumball M (1997) Splanchnic mucosal ischemia: an unrecognized consequence of routine pneumoperitoneum. Surg Laparosc Endosc 7:480–482

    Article  CAS  PubMed  Google Scholar 

  7. Nickkholgh A, Barro-Bejarano M, Liang R, Zorn M, Mehrabi A, Gebhard MM et al (2008) Signs of reperfusion injury following CO2 pneumoperitoneum: an in vivo microscopy study. Surg Endosc 22:122–128

    Article  PubMed  Google Scholar 

  8. Kaya Y, Coskun T, Demir MA, Var A, Ozsoy Y, Aydemir EO (2002) Abdominal insufflation-deflation injury in small intestine in rabbits. Eur J Surg 168:410–417

    Article  PubMed  Google Scholar 

  9. Eleftheriadis E, Kotzampassi K, Papanotas K, Heliadis N, Sarris K (1996) Gut ischemia, oxidative stress, and bacterial translocation in elevated abdominal pressure in rats. World J Surg 20:11–16

    Article  CAS  PubMed  Google Scholar 

  10. Tsuboi S, Kitano S, Yoshida T, Bandoh T, Ninomiya K, Baatar D (2002) Effects of carbon dioxide pneumoperitoneum on hemodynamics in cirrhotic rats. Surg Endosc 16:1220–1225

    Article  CAS  PubMed  Google Scholar 

  11. Ke B, Shen XD, Kamo N, Ji H, Yue S, Gao F et al (2013) β-catenin regulates innate and adaptive immunity in mouse liver ischemia-reperfusion injury. Hepatology 57:1203–1214

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Eltzschig HK, Eckle T (2011) Ischemia and reperfusion: from mechanism to translation. Nat Med 17:1391–1401

    Article  CAS  PubMed  Google Scholar 

  13. Hase K, Kawano K, Nochi T, Pontes GS, Fukuda S, Ebisawa M et al (2009) Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 462:226–230

    Article  CAS  PubMed  Google Scholar 

  14. Medzhitov R, Preston-Hurlburt P, Janeway CA (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394–397

    Article  CAS  PubMed  Google Scholar 

  15. Shang L, Fukata M, Thirunarayanan N, Martin AP, Arnaboldi P, Maussang D et al (2008) Toll-like receptor signaling in small intestinal epithelium promotes B-cell recruitment and IgA production in lamina propria. Gastroenterology 135:529–538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15:316–328

    Article  PubMed  Google Scholar 

  17. Russell MW, Sibley DA, Nikolova EB, Tomana M, Mestecky J (1997) IgA antibody as a non-inflammatory regulator of immunity. Biochem Soc Trans 25:466–470

    CAS  PubMed  Google Scholar 

  18. Flohé L, Brigelius-Flohé R, Saliou C, Traber MG, Packer L (1997) Redox regulation of NF-kappa B activation. Free Radic Biol Med 22:1115–1126

    Article  PubMed  Google Scholar 

  19. Janssen-Heininger YM, Poynter ME, Baeuerle PA (2000) Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic Biol Med 28:1317–1327

    Article  CAS  PubMed  Google Scholar 

  20. Kato T, Owen RL (2005) Structure and function of intestinal mucosal eptihelium. In: Mestecky J, Lamm ME, McGhee JR, Bienenstock J, Mayer L, Strober W (eds) Mucosal immunology. Elsevier Inc., San Diego, pp 131–151

    Chapter  Google Scholar 

  21. Neutra MR, Kraehenbuhl J-P (2005) Cellular and molecular basis for antigen transport across epithelial barriers. In: Mestecky J, Lamm ME, McGhee JR, Bienenstock J, Mayer L, Strober W (eds) Mucosal immunology. Elsevier Inc., San Diego, pp 111–130

    Chapter  Google Scholar 

  22. Vijay-Kumar M, Gewirtz AT (2005) Role of epithelium in mucosal immunity. In: Mestecky J, Lamm ME, McGhee JR, Bienenstock J, Mayer L, Strober W (eds) Mucosal immunology. Elsevier Inc., San Diego, pp 423–434

    Chapter  Google Scholar 

  23. Unsal MA, Guven S, Imamoglu M, Aydin S, Alver A (2009) The effect of CO2 insufflation-desufflation attacks on tissue oxidative stress markers during laparoscopy: a rat model. Fertil Steril 92:363–368

    Article  CAS  PubMed  Google Scholar 

  24. Dai S, Sodhi C, Cetin S, Richardson W, Branca M, Neal MD et al (2010) Extracellular high mobility group box-1 (HMGB1) inhibits enterocyte migration via activation of Toll-like receptor-4 and increased cell-matrix adhesiveness. J Biol Chem 285:4995–5002

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Yao L, Kan EM, Lu J, Hao A, Dheen ST, Kaur C et al (2013) Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia. J Neuroinflammation 10:23

    Article  PubMed Central  PubMed  Google Scholar 

  26. Zhang Y, Peng T, Zhu H, Zheng X, Zhang X, Jiang N et al (2010) Prevention of hyperglycemia-induced myocardial apoptosis by gene silencing of Toll-like receptor-4. J Transl Med 8:133

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Akira S, Sato S (2003) Toll-like receptors and their signaling mechanisms. Scand J Infect Dis 35:555–562

    Article  CAS  PubMed  Google Scholar 

  28. Kimoto M, Nagasawa K, Miyake K (2003) Role of TLR4/MD-2 and RP105/MD-1 in innate recognition of lipopolysaccharide. Scand J Infect Dis 35:568–572

    Article  CAS  PubMed  Google Scholar 

  29. Miyake K (2004) Innate recognition of lipopolysaccharide by Toll-like receptor 4-MD-2. Trends Microbiol 12:186–192

    Article  CAS  PubMed  Google Scholar 

  30. Kontoulis TM, Pissas DG, Pavlidis TE, Pissas GG, Lalountas MA, Koliakos G et al (2012) The oxidative effect of prolonged CO(2) pneumoperitoneum a comparative study in rats. J Surg Res 175:259–264

    Article  CAS  PubMed  Google Scholar 

  31. Sammour T, Mittal A, Loveday BP, Kahokehr A, Phillips AR, Windsor JA et al (2009) Systematic review of oxidative stress associated with pneumoperitoneum. Br J Surg 96:836–850

    Article  CAS  PubMed  Google Scholar 

  32. Jakimowicz J, Stultiëns G, Smulders F (1998) Laparoscopic insufflation of the abdomen reduces portal venous flow. Surg Endosc 12:129–132

    Article  CAS  PubMed  Google Scholar 

  33. Takagi S (1998) Hepatic and portal vein blood flow during carbon dioxide pneumoperitoneum for laparoscopic hepatectomy. Surg Endosc 12:427–431

    Article  CAS  PubMed  Google Scholar 

  34. Evasovich MR, Clark TC, Horattas MC, Holda S, Treen L (1996) Does pneumoperitoneum during laparoscopy increase bacterial translocation? Surg Endosc 10:1176–1179

    Article  CAS  PubMed  Google Scholar 

  35. Hiki N, Shimizu N, Yamaguchi H, Imamura K, Kami K, Kubota K et al (2006) Manipulation of the small intestine as a cause of the increased inflammatory response after open compared with laparoscopic surgery. Br J Surg 93:195–204

    Article  CAS  PubMed  Google Scholar 

  36. Galdeano CM, Perdigón G (2006) The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 13:219–226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Kawamoto S, Tran TH, Maruya M, Suzuki K, Tsutsui Y et al (2012) The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science 336:485–489

    Article  CAS  PubMed  Google Scholar 

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Disclosures

Drs. Toru Kusano, Tsuyoshi Etoh, Masafumi Inomata, Norio Shiraishi, and Seigo Kitano have no conflicts of interest or financial ties to disclose.

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Correspondence to Masafumi Inomata.

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Kusano, T., Etoh, T., Inomata, M. et al. CO2 pneumoperitoneum increases secretory IgA levels in the gut compared with laparotomy in an experimental animal model. Surg Endosc 28, 1879–1885 (2014). https://doi.org/10.1007/s00464-013-3408-3

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  • DOI: https://doi.org/10.1007/s00464-013-3408-3

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