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Lactobacillus plantarum Prevents Bacterial Translocation in Rats Following Ischemia and Reperfusion Injury

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Abstract

Background

Bacterial translocation is considered a major cause of initiation and development of systemic sepsis and multiple organ dysfunction in clinic. The aim of this study was to determine the ability of a defined Lactobacillus plantarum to prevent ischemia/reperfusion (I/R) induced intestinal infection.

Methods

Female Sprague-Dawley rats were randomly allocated into three groups: (1) controls (sham-operated, no treatment), (2) ischemia/reperfusion and (3) ischemia/reperfusion and Lactobacillus plantarum treatment. Lactobacillus plantarum L2 was administered daily intragastrically 14 days prior to induction of I/R. Rats were then sacrificed, and tissue and blood samples were cultured to determine bacterial translocation. Cytokines in plasma were detected by ELISA. Ileal segments were removed for morphological examination.

Results

Intestinal I/R induced excess pro-inflammatory cytokine secretion and barrier dysfunction (increased epithelial cell apoptosis, cecal flora dysbiosis, disruption of mucosa and multiple erosions) in the intestine, associated with increased bacterial translocation to extraintestinal sites. Approximately 87.5% of rats exposed to I/R had bacterial translocation while there was no bacterial translocation in controls. However, pretreatment of animals with Lactobacillus plantarum completely prevented I/R induced bacterial translocation, reduced pro-inflammatory cytokine release, and intestinal epithelial cell apoptosis, resulting in recovered microflora and mucosal integrity.

Conclusions

These findings indicate that Lactobacillus plantarum L2 can prevent I/R-induced bacterial translocation and intestinal barrier dysfunction and, thereby, exert beneficial effects in the intestinal tract.

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References

  1. Berg RD. The indigenous gastrointestinal microflora. Trends Microbiol. 1996;4:430–435.

    Article  PubMed  CAS  Google Scholar 

  2. Simon GL, Gorbach SL. The human intestinal microflora. Dig Dis Sci. 1986;31:147S–162S.

    Article  PubMed  CAS  Google Scholar 

  3. Hopkins MJ, Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J Med Microbiol. 2002;51:448–454.

    PubMed  CAS  Google Scholar 

  4. MacFie J, O’Boyle C, Mitchell C, Buckley P, Johnstone D, Sudworth P. Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. Gut. 1999;45:223–228.

    Article  PubMed  CAS  Google Scholar 

  5. Berg RD. Bacterial translocation from the gastrointestinal tract. Trends Microbiol. 1995;3:149–154.

    Article  PubMed  CAS  Google Scholar 

  6. Wells CL, VandeWesterlo EM, Jechorek RP, Erlandsen SL. Effect of hypoxia on enterocyte endocytosis of enteric bacteria. Crit Care Med. 1996;24:985–991.

    Article  PubMed  CAS  Google Scholar 

  7. Kong SE, Blennerhassett LR, Heel KA, McCauley RD, Hall JC. Ischemia-reperfusion injury to the intestine. Aust N Z J Surg. 1998;68:554–561.

    Article  PubMed  CAS  Google Scholar 

  8. Kuzu MA, Kale IT, Cöl C, Tekeli A, Tanik A, Köksoy C. Obstructive jaundice promotes bacterial translocation in humans. Hepatogastroenterology. 1999;46:2159–2164.

    PubMed  CAS  Google Scholar 

  9. Cicalese L, Sileri P, Green M, Abu-Elmagd K, Kocoshis S, Reyes J. Bacterial translocation in clinical intestinal transplantation. Transplantation. 2001;71:1414–1417.

    Article  PubMed  CAS  Google Scholar 

  10. Cirera I, Bauer TM, Navasa M, et al. Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol. 2001;34:32–37.

    Article  PubMed  CAS  Google Scholar 

  11. Peitzman AB, Udekwu AO, Ochoa J, Smith S. Bacterial translocation in trauma patients. J Trauma. 1991;31:1083–1086.

    PubMed  CAS  Google Scholar 

  12. Riddington DW, Venkatesh B, Boivin CM, et al. Intestinal permeability, gastric intramucosal pH, and systemic endotoxemia in patients undergoing cardiopulmonary bypass. JAMA. 1996;275:1007–1012.

    Article  PubMed  CAS  Google Scholar 

  13. Hebra A, Hong J, McGowan KL, Smith C, Mckernan ML, Ross AJ 3rd. Bacterial translocation in mesenteric ischemia-reperfusion injury: is dysfunctional motility the link. J Pediatr Surg. 1994;29:280–285.

    Article  PubMed  CAS  Google Scholar 

  14. Leaphart CL, Tepas JJ 3rd. The gut is a motor of organ system dysfunction. Surgery. 2007;141:563–569.

    Article  PubMed  Google Scholar 

  15. Mattila-Sandholm T, Mättö J, Saarela M. Lactic acid bacteria with health claims—interactions and interference with gastrointestinal flora. Int Dairy J. 1999;9:25–35.

    Article  Google Scholar 

  16. Merk K, Borelli C, Korting HC. Lactobacilli-bacteria-host interactions with special regard to the urogenital tract. Int J Med Microbiol. 2005;295:9–18.

    Article  PubMed  CAS  Google Scholar 

  17. Foligne B, Nutten S, Grangette C, et al. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. W J Gastroenterol. 2007;13:236–243.

    Google Scholar 

  18. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics and prebiotics. Gastroenterology. 2004;126:1620–1633.

    Article  PubMed  Google Scholar 

  19. Biller JA, Katz AJ, Flores AF, Buie TM, Gorbach SL. Treatment of recurrent Clostridium difficile colitis with Lactobacillus GG. J Pediatr Gastroenterol Nutr. 1995;21:224–226.

    Article  PubMed  CAS  Google Scholar 

  20. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology. 1999;116:1107–1114.

    Article  PubMed  CAS  Google Scholar 

  21. Mangell P, Nejdfors P, Wang M, et al. Lactobacillus plantarum 299V inhibits Escherichia coli-induced intestinal permeability. Dig Dis Sci. 2002;47:511–516.

    Article  PubMed  Google Scholar 

  22. Zareie M, Johnson-Henry K, Jury J, et al. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut. 2006;55:1553–1560.

    Article  PubMed  CAS  Google Scholar 

  23. Wang B, Li J, Zhang H, Li Q, Li N. Isolation of adhesive strains and evaluation of the colonization and immune response by Lactobacillus plantarum L2 in the rat gastrointestinal tract. Int J Food Microbiol. 2009;132:59–66.

    Article  PubMed  CAS  Google Scholar 

  24. Yamamoto S, Tanabe M, Wakabayashi G, Shimazu M, Matsumoto K, Kitajima M. The role of tumor necrosis factor-α and interleukin-1β in ischemia-reperfusion injury of the rat small intestine. J Surg Res. 2001;99:134–141.

    Article  PubMed  CAS  Google Scholar 

  25. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg. 1970;101:478–483.

    PubMed  CAS  Google Scholar 

  26. van Minnen LP, Timmerman HM, Lutgendorff F, et al. Modification of intestinal flora with multispecies probiotics reduces bacterial translocation and improves clinical course in a rat model of acute pancreatitis. Surgery. 2007;141:470–480.

    Article  PubMed  Google Scholar 

  27. Roller M, Rechkemmer G, Watzl B. Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr. 2004;134:153–156.

    PubMed  CAS  Google Scholar 

  28. Dalwai F, Spratt DA, Pratten J. Modeling shifts in microbial populations associated with health or disease. Appl Environ Microbiol. 2006;72:3678–3684.

    Article  PubMed  CAS  Google Scholar 

  29. Stecher B, Hardt WD. The role of microbiota in infectious disease. Trends Microbiol. 2008;16:107–114.

    Article  PubMed  CAS  Google Scholar 

  30. Grotz MR, Deitch EA, Ding J, Xu D, Huang Q, Regel G. Intestinal cytokine response after gut ischemia: role of gut barrier failure. Ann Surg. 1999;229:478–486.

    Article  PubMed  CAS  Google Scholar 

  31. Kurtel H, Fujimoto K, Zimmerman BJ, Granger DN, Tso P. Ischemia-reperfusion-induced mucosal dysfunction: role of neutrophils. Am J Physiol. 1991;261:G490–G496.

    PubMed  CAS  Google Scholar 

  32. Grotz MR, Ding J, Guo W, Huang Q, Deitch EA. Comparison of plasma cytokine levels in rats subjected to superior mesenteric artery occlusion or hemorrhagic shock. Shock. 1995;3:362–368.

    Article  PubMed  CAS  Google Scholar 

  33. Souza DG, Teixeira MM. The balance between the production of tumor necrosis factor-alpha and interleukin-10 determines tissue injury and lethality during intestinal ischemia and reperfusion. Mem Inst Oswaldo Cruz. 2005;100:59–66.

    Article  PubMed  CAS  Google Scholar 

  34. Zeng H, Wu H, Sloane V, et al. Flagellin/TLR5 responses in epithelia reveal intertwined activation of inflammatory and apoptotic pathways. Am J Physiol Gastrointest Liver Physiol. 2006;290:G96–G108.

    Article  PubMed  CAS  Google Scholar 

  35. Wu B, Qiu W, Wang P, et al. p53 independent induction of PUMA mediates intestinal apoptosis in response to ischaemia-reperfusion. Gut. 2007;56:645–654.

    Article  PubMed  CAS  Google Scholar 

  36. Yan F, Polk DB. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem. 2002;277:50959–50965.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The present work was financially supported by the National Natural Science Foundation of China (Grants 30801090 and 30830098).

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Correspondence to Jieshou Li.

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Wang, B., Huang, Q., Zhang, W. et al. Lactobacillus plantarum Prevents Bacterial Translocation in Rats Following Ischemia and Reperfusion Injury. Dig Dis Sci 56, 3187–3194 (2011). https://doi.org/10.1007/s10620-011-1747-2

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  • DOI: https://doi.org/10.1007/s10620-011-1747-2

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