Skip to main content

Advertisement

Log in

Protection against increased intestinal permeability and bacterial translocation induced by intestinal obstruction in mice treated with viable and heat-killed Saccharomyces boulardii

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Background

There are substantial evidences suggesting that probiotics can protect the gastrointestinal tract against inflammatory or infectious episodes. The effects of oral treatment with viable or heat-killed cells of Saccharomyces boulardii (Sb) on bacterial translocation, intestinal permeability, histological aspect of the ileum, and some immunological parameters were evaluated in a murine intestinal obstruction (IO) model.

Results

Bacterial translocation and intestinal permeability in the IO group were significantly higher when compared to a Sham group (p < 0.05). Pretreatment with both viable and heat-killed S. boulardii prevented these increases, and the data obtained for IO + Sb and IO + heat-killed Sb groups were similar to those observed in the Sham group (p > 0.05). Histological analysis showed preservation of the ileum mucosa in mice that received both forms of the yeast when compared to the lesions observed in the IO group. The levels of serum interleukin (IL)-10 and intestinal secretory immunoglobulin A (sIgA) were higher in the animals that received both yeast treatments when compared to those from IO and Sham groups.

Conclusion

Oral treatment with viable or heat-killed cells of S. boulardii maintained intestinal integrity and modulated the immune system in a murine IO model, preventing bacterial translocation and intestinal lesions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Soeters PB (2008) Probiotics: did we go wrong, and if so, where? Clin Nutr 27:173–178

    Article  Google Scholar 

  2. Correia MITD, Nicoli JR (2006) The role of probiotics in gastrointestinal surgery. Curr Opin Clin Nutr Metab Care 9:618–621

    Article  Google Scholar 

  3. Watkinson PJ, Barber VS, Dark P, Young JD (2007) The use of pre-pro and synbiotics in adult intensive care unit patients: systematic review. Clin Nutr 26:182–192

    Article  Google Scholar 

  4. Sun Z, Wang X, Roland A (1998) Role of intestinal permeability in monitoring mucosal barrier function. Dig Surg 15:386–397

    Article  CAS  Google Scholar 

  5. Gatt M, Reddy BS, MacFie J (2007) Review article: bacterial translocation in the critically ill- evidence and methods of prevention. Aliment Pharmacol Ther 25:741–757

    Article  CAS  Google Scholar 

  6. Timmerman HM, Niers LE, Ridwan BU, Koning CJ, Mulder L, Akkermans LM, Rombouts FM, Rijkers GT (2007) Design of a multispecies probiotics mixture to prevent infectious complications in critically ill patients. Clin Nutr 26:450–459

    Article  Google Scholar 

  7. Lichtman SM (2001) Bacterial translocation in humans. J Pediatr Gastroenterol Nutr 33:1–10

    Article  CAS  Google Scholar 

  8. Wiest R, Rath HC (2003) Bacterial translocation in the gut. Best Pract Res Clin Gastroenterol 17:397–425

    Article  Google Scholar 

  9. Seehofer D, Rayes N, Schiller R, Stockmann M, Müller AR, Schirmeier A, Schaeper F, Tullius SG, Bengmark S, Neuhaus P (2004) Probiotics partly reverse increased bacterial translocation after simultaneous liver resection and colonic anastomosis in rats. J Surg Res 117:262–271

    Article  Google Scholar 

  10. Demirer S, Aydintug S, Aslim B, Kepenekci I, Sengül N, Evirgen O, Gerceker D, Andrieu MN, Ulusoy C, Karahüseyinoglu S (2005) Effects of probiotics on radiation-induced intestinal injury in rats. Nutrition 22:179–186

    Article  Google Scholar 

  11. Geyik MF, Aldemir M, Hosoglu S, Ayaz C, Satilmis S, Buyukbayram H, Kokoglu OF (2006) The effects of Saccharomyces boulardii on bacterial translocation in rats with obstructive jaundice. Ann R Coll Surg Engl 88:176–180

    Article  Google Scholar 

  12. Mogilner JG, Srugo I, Lurie M, Shaoul R, Coran AG, Shiloni E, Sukhotnik I (2007) Effect of probiotics on intestinal regrowth and bacterial translocation after massive small bowel resection in a rat. J Pediatr Surg 42:1365–1371

    Article  Google Scholar 

  13. Quirino IEP, Correia MITD, Cardoso VN (2007) The impact of arginine on bacterial translocation in an intestinal obstruction model in rats. Clin Nutr 26:335–340

    Article  CAS  Google Scholar 

  14. MacFie J, Reddy BS, Gatt M, Jain PK, Sowdi R, Mitchell CJ (2006) Bacterial translocation studied in 927 patients over 13 years. Br J Surg 93:87–93

    Article  CAS  Google Scholar 

  15. Zareie M, Johnson-Henry K, Jury J, Yang PC, Ngan BY, McKay DM, Soderholm JD, Perdue MH, Sherman PM (2006) Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 55:1553–1560

    Article  CAS  Google Scholar 

  16. Food and Agriculture Organization of the United Nations & World Health Organization. Guidelines for the evaluation of probiotics in food, food and agriculture organization of the united nations & world health organization working group report, London, Ontario, Canada, 30 April–1 May 2002

  17. Kataria J, Li N, Wynn JL, Neu J (2009) Probiotic microbes: do they need to be alive to be beneficial? Nutr Rev 67:546–550

    Article  Google Scholar 

  18. Li N, Russell WM, Douglas-Escobar M, Hauser N, Lopez M, Neu J (2009) Live and heat-killed Lactobacillus rhamnosus GG: effects on pro-inflammatory and anti-inflammatory cytokines/chemokines in gastrostomy-fed infants rats. Pediatr Res 66:203–207

    Article  CAS  Google Scholar 

  19. Liong MT (2008) Safety of probiotics: translocation and infection. Nutr Rev 66:192–202

    Article  Google Scholar 

  20. Beaugerie L, Flahaut A, Barbut F, Atlan P, Lalande V, Cousin P (2001) Antibiotic associated diarrhea and Clostridium difficile in the community. Aliment Pharmacol Ther 17:905–912

    Article  Google Scholar 

  21. Elmer GW, McFarland LV (2001) Biotherapeutic agents in the treatment of infectious diarrhea. Gastroenterol Clin North Am 30:837–854

    Article  CAS  Google Scholar 

  22. Czerucka D, Rampal P (2002) Experimental effects of Saccharomyces boulardii on diarrheal pathogens. Microbes Infect 4:733–739

    Article  Google Scholar 

  23. D′Souza AL, Rajkumar C, Cooke J, Bulpitt CJ (2002) Probiotics in prevention of antibiotic associated diarrhoea: meta analysis. BMJ 324:1–6

    Google Scholar 

  24. MacFarland LV (2006) Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am J Gastroenterol 101:812–822

    Article  Google Scholar 

  25. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC (2009) Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 15(2):300–310

    Article  CAS  Google Scholar 

  26. Oliveira MA, Lemos DL, Diniz ASOF, Coelho J, Cardoso VN (2006) Prevention of bacterial translocation using glutamine: a new strategy of investigation. Nutrition 22:419–424

    Article  Google Scholar 

  27. Diniz ASOF, Resende BM, Nunan EA, Simal CJR, Cardoso VN (1999) 99mTechnetium labelled Escherichia coli. Appl Radiat Isot 51:33–36

    Article  CAS  Google Scholar 

  28. Viana ML, Santos RG, Generoso SV, Arantes RM, Correia MI, Cardoso VN (2010) Pretreatment with arginine preserves intestinal barrier integrity and reduces bacterial translocation in mice. Nutrition 26:218–223

    Article  CAS  Google Scholar 

  29. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN (1970) Intestinal mucosal lesion in low flow states. Arch Surg 101:478–483

    CAS  Google Scholar 

  30. Rodrigues ACP, Cara DC, Fretez SHG, Cunha FQ, Vieira EC, Nicoli JR (2000) Saccharomyces boulardii stimulates sIgA production and the phagocytic system of gnotobiotic mice. J Appl Microbiol 89:404–414

    Article  CAS  Google Scholar 

  31. Kelly D, King T, Aminov R (2007) Importance of microbial colonization of the gut in early life to the development of immunity. Mutat Res 622:58–69

    CAS  Google Scholar 

  32. Deich EA (2002) Bacterial translocation or lymphatic drainage of toxic products from the gut: what is important in human beings? Surgery 131:241–245

    Article  Google Scholar 

  33. Mcnaught CE, Woodcock NP, Anderson ADG, Macfie J (2005) A prospective randomized trial of probiotics in critically ill patients. Clin Nutr 24:211–219

    Article  Google Scholar 

  34. Salzedas-Netto AA, Silva RM, Martins JL, Menchaca-Diaz JL, Bugni GM, Watanabe AY, Silva FJP, Fagundes-Neto U, Koh IHJ (2006) Can bacterial translocation be a beneficial event? Transplant Proc 38:1836–1837

    Article  CAS  Google Scholar 

  35. Herek O, Kara IG, Kaleli I (2004) Effects of antibiotics and Saccharomyces boulardii on bacterial translocation in burn injury. Surg Today 34:256–260

    Article  CAS  Google Scholar 

  36. Martins FS, Rodrigues ACP, Tiago FCP, Penna FJ, Rosa CA, Arantes RME, Nardi RMD, Neves MJ, Nicoli JR (2007) Saccharomyces cerevisiae strain 905 reduces the translocation of Salmonella enterica serotype Typhimurium and stimulates the immune system in gnotobiotic and conventional mice. J Med Microbiol 56:352–359

    Article  CAS  Google Scholar 

  37. White JS, Hoper M, Parkers RW, Clements WDB, Diamond T (2006) Patterns of bacterial translocation in experimental biliary obstruction. J Surg Res 132:80–84

    Article  CAS  Google Scholar 

  38. Aldemir M, Kökoglu OF, Geyik MF, Büyükbayram H (2002) Effects of octreotide acetate and Saccharomyces boulardii on bacterial translocation in an experimental intestinal loop obstruction model of rats. Tohoku J Exp Med 198:1–9

    Article  CAS  Google Scholar 

  39. Chang T, Lu R, Tsai L (2001) Glutamine ameliorates mechanical obstruction-induced intestinal injury. J Surg Res 95:133–140

    Article  CAS  Google Scholar 

  40. Katouzian F, Sblattero D, Not T, Tommasini A, Giusto E, Meiacco D, Stebel M, Marzari R, Fasano A, Ventura A (2005) Dual sugar gut-permeability testing on blood drop in animal models. Clin Chim Acta 352:191–197

    Article  CAS  Google Scholar 

  41. Arrieta MC, Bistritz L, Meddings JB (2006) Alterations in intestinal permeability. Gut 55:1512–1520

    Article  CAS  Google Scholar 

  42. Czerucka D, Dahan S, Mograbi B, Rossi B, Rampal P (2000) Saccharomyces boulardii preserves the barrier function and modulates the signal transduction pathway induced in enteropathogenic Escherichia coli infected T84 cells. Infect Immun 68:5998–6004

    Article  CAS  Google Scholar 

  43. Dahan S, Dalmasso G, Imbert V, Peyron JF, Rampal P, Czerucka D (2003) Saccharomyces boulardii interferes with enterohemorrhagic Escherichia coli-induced signaling pathways in T84 cells. Infect Immun 71:766–773

    Article  CAS  Google Scholar 

  44. Martins FS, Dalmasso G, Arantes RM, Doye A, Lemichez E, Lagadec P, Imbert V, Peyron JF, Rampal P, Nicoli JR, Czerucka D (2010) Interaction of Saccharomyces boulardii with Salmonella enterica serovar Typhimurium protects mice and modifies T84 cell response to the infection. PLoS One 5:e8925

    Article  Google Scholar 

  45. Vilela EG, de Abreu Ferrari ML, de Gama Torres HO, Martins FP, Goulart EM, Lima AS, Cunha AS (2008) Influence of Saccharomyces boulardii on the intestinal permeability of patients with Crohn′s disease in remission. Scand J Gastroenterol 43:842–848

    Article  CAS  Google Scholar 

  46. Marchiando AM, Granham WV, Turner JR (2010) Epithelial barriers in homeostasis and disease. Annu Rev Pathol 5:119–144

    Article  CAS  Google Scholar 

  47. Yan F, Polk DB (2010) Probiotics: progress toward novel therapies for intestinal diseases. Curr Opin Gastroenterol 26:95–101

    Article  Google Scholar 

Download references

Acknowledgments

The study was supported by grants from Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simone V. Generoso.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Generoso, S.V., Viana, M.L., Santos, R.G. et al. Protection against increased intestinal permeability and bacterial translocation induced by intestinal obstruction in mice treated with viable and heat-killed Saccharomyces boulardii . Eur J Nutr 50, 261–269 (2011). https://doi.org/10.1007/s00394-010-0134-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-010-0134-7

Keywords

Navigation