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Digestive Diseases and Sciences

, Volume 49, Issue 2, pp 320–327 | Cite as

Modulation of the Effect of Dextran Sulfate Sodium-Induced Acute Colitis by the Administration of Different Probiotic Strains of Lactobacillus and Bifidobacterium

  • Nadia Osman
  • Diya Adawi
  • Siv Ahrne
  • Bengt Jeppsson
  • Göran Molin
Article

Abstract

The pathogenic mechanism of inflammatory bowel diseases is not fully understood but colonic microflora including Lactobacillus and Bifidobacterium species may affect the induction of colonic inflammation. In this study the relative efficacy of different probiotic organisms in the prevention of colitis was compared in an induced rat colitis model. Three Lactobacillus strains and two Bifidobacterium strains were fed to Sprague–Dawley rats for 7 days prior to offering the rats 5% dextran sulfate sodium (DSS) in their drinking water to induce colitis and the administration of the probiotics continued for 7 days with the DSS. Colitis severity was assessed daily using a disease activity index (DAI). Samples were collected 7 days after colitis induction for intestinal bacterial flora and bacterial translocation. The DAI decreased significantly on days 4, 5, 6, and 7 in the Lactobacillusplantarum DSM 9843, Bifidobacterium sp. 3B1, and Bifidobacterium infantis DSM 15158 groups compared to the colitis control. It decreased significantly on days 5, 6, and 7 in the Bifidobacterium infantis DSM 15158 group compared to the Lactobacillus paracaesi DSM 13434 and Lactobacillus gasseri 5B3 groups. It also decreased significantly on day 7 in the L. plantarum DSM 9843 group compared to the L. gasseri 5B3 group. Bacterial translocation to the mesenteric lymph nodes decreased significantly in all treatment groups compared to the colitis control. Enterobacteriaceae bacterial translocation to the liver decreased in all treatment groups compared to the colitis control. Administration of certain strains of Lactobacillusand Bifidobacterium significantly improves the DAI and reduces bacterial translocation, and L. plantarum DSM 9843, Bifidobacterium sp. 3B1, and Bifidobacterium infantis DSM 15158 seem to have the best effect.

bacterial translocation colitis intestinal bacteria probiotics 

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REFERENCES

  1. 1.
    Gardiner KR, Anderson NH, Rowlands BJ, Barbul A: Colitis and colonic mucosal barrier dysfunction. Gut 37(4): 530-355, 1995Google Scholar
  2. 2.
    Gardiner KR, Erwin PJ, Anderson NH, Barr JG, Halliday MI, Rowlands BJ: Colonic bacteria and bacterial translocation in experimental colitis. Br J Surg 80(4): 512-516, 1993Google Scholar
  3. 3.
    Gorbach SL, Chang TW, Goldin B: Successful treatment of relapsing Clostridium difficile colitis with Lactobacillus GG [letter]. Lancet 2(8574):1519, 1987Google Scholar
  4. 4.
    Andrejak M, Schmit JL, Tondriaux A: The clinical significance of antibiotic-associated pseudomembranous colitis in the 1990s. Drug Saf 6(5): 339-349, 1991Google Scholar
  5. 5.
    Butzner JD, Parmar R, Bell CJ, Dalal V: Butyrate enema therapy stimulates mucosal repair in experimental colitis in the rat. Gut 38(4): 568-573, 1996Google Scholar
  6. 6.
    Fabia R, Ar'Rajab A, Johansson ML, Willen R, Andersson R, Molin G, Bengmark S: The effect of exogenous administration of Lactobacillus reuteri R2LC and oat iber on acetic acid-induced colitis in the rat. Scand J Gastroenterol 28(2): 155-162, 1993Google Scholar
  7. 7.
    Herias MV, Hessle C, Telemo E, Midtvedt T, Hanson LA, Wold AE: Immunomodulatory effects of Lactobacillus plantarum colonizing the intestine of gnotobiotic rats. Clin Exp Immunol 116(2): 283-290, 1999Google Scholar
  8. 8.
    Schultz M, Veltkamp C, Dieleman LA, Grenther WB, Wyrick PB, Tonkonogy SL, Sartor RB: Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis 8(2): 71-80, 2002Google Scholar
  9. 9.
    Elson CO, Sartor RB, Tennyson GS, Riddell RH: Experimental models of inflammatory bowel disease. Gastroenterology 118: 23-29, 1995Google Scholar
  10. 10.
    Molin G, Jeppsson B, Ahrné S, Johansson M-L, Nobaek S, Ståhl M, Bengmark S: Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines. J Appl Bacterio 74: 314-323, 1993Google Scholar
  11. 11.
    Johansson M-L, Quednau M, Ahrné S, Molin G: Classification of Lactobacillus plantarum by restriction endonuclease analysis of total chromosomal DNA using conventional agarose gel electrophoresis. Int J Syst Bacteriol 45: 670-675, 1995Google Scholar
  12. 12.
    Ahrné S, Nobaek S, Jeppsson B, Adlerberth I, Wold A, Molin G: The normal Lactobacillus flora of healthy human rectal and oral mucosa. J Appl Microbiol 85: 88-94, 1998Google Scholar
  13. 13.
    Antonsson, M: Lactobacillus in Semi-hard Cheese and Their Use as Adjunct Cultures. PhD thesis. Division of Food Technology, Lund Institute of Technology, Lund University, Lund, Sweden, 2001Google Scholar
  14. 14.
    Vásquez A, Jakobsson T, Ahrné S, Forsum U, Molin G: Vaginal Lactobacillus flora of healthy Swedish women. J Clin Microbiol 40(8): 2746-2749, 2002Google Scholar
  15. 15.
    Johansson ML, Molin G, Jeppsson B, Nobaek S, Ahrne S, Bengmark S: Administration of different Lactobacillus strains in fermented oatmeal soup: in vivo colonization of human intestinal mucosa and effect on the indigenous flora. Appl Environ Microbiol 59(1): 15-20, 1993Google Scholar
  16. 16.
    Murthy SN, Cooper HS, Shim H, Shah RS, Ibrahim SA, Sedergran DI: Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig Dis Sci 38(9): 1722-1734, 1993Google Scholar
  17. 17.
    Cooper HS, Murthy SN, Shah RS, Sedergran DI: Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 69(2): 238-249, 1993Google Scholar
  18. 18.
    Murthy S, Murthy NS, Coppola D, Wood DL: The efficacy of BAY y 1015 in dextran sulfate model of mouse colitis. Inflamm Res 46: 224-233, 1997Google Scholar
  19. 19.
    Quednau M, Ahrné S, Peterson AC, Molin G: Identification of clinically important species of Enterococcus within 1 day with randomly amplified poymorphic DNA (RAPD). Curr Microbiol 36: 332-336, 1998Google Scholar
  20. 20.
    Romersberg HC: Cluster Analysis for Research. Belmont, California, USA: Lifetime Learning, 1984Google Scholar
  21. 21.
    Johansson ML, Quednau M, Molin G, Ahrne S: Randomly amplified polymorphic DNA (RAPD) for rapid typing of Lactobacillus plantarum strains. Lett Appl Microbiol 21: 155-159, 1995Google Scholar
  22. 22.
    Linskens RK, Huijsdens XW, Savelkoul PH, Vandenbroucke-Grauls CM, Meuwissen SG: The bacterial flora in inflammatory bowel disease: current insights in pathogenesis and the influence of antibiotics and probiotics. Scand J Gastroenterol Suppl 234: 29-40, 2001Google Scholar
  23. 23.
    Gorbach SL: Probiotics and gastrointestinal health. Am J Gastroenterol 95(Suppl):S1-S4, 2000Google Scholar
  24. 24.
    Madsen KL: The use of probiotics in gastrointestinal disease. Can J Gastroenterol 15: 817-822, 2001Google Scholar
  25. 25.
    Schultz M, Sartor RB: Probiotics and inflammatory bowel diseases. Am J Gastroenterol 95(Suppl):S19-S21, 2000Google Scholar
  26. 26.
    Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN: Lactobacillus sp prevents development of enterocolitis in interleukin-10 gene deficient mice. Gastroenterology 116: 1107-1114, 1999Google Scholar
  27. 27.
    Shanahan F: Therapeutic manipulation of gut flora. Science 289: 1311-1312, 2000Google Scholar
  28. 28.
    Adlerberth I, Ahrne S, Johansson ML, Molin G, Hanson Lå, Wold AE: A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line HT-29. Appl Environ Microbiol 62: 2244-2251, 1996Google Scholar
  29. 29.
    Mao Y, Nobaek S, Adawi D, Molin G, Jeppsson B: Comparison of the effects of different strains of Lactobacillus in reducing bacterial translocation on methotrexate induced-enterocolitis in rats. Dig Surg 14: 284-291, 1997Google Scholar
  30. 30.
    Mao Y, Nobaek S, Kasravi B, Adawi D, Stenram U, Molin G, Jeppsson B: The effects of Lactobacillus strains and oat fiber on methotrexate-induced enterocolitis in rats. Gastroenterology 111(2): 334-344, 1996Google Scholar
  31. 31.
    Mao Y, Yu J-L, Ljungh å, Molin G, Jeppsson B: Intestinal immune response to oral administration of Lactobacillus reuteri R2LC, Lactobacillus DSM 9843, pectin and oatbase on methotrexate-induced enterocolitis in rats. Microbial Ecol Health Dis 9: 261-270, 1996Google Scholar
  32. 32.
    Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T: Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J Am Coll Nutr 22(1): 56-63, 2003Google Scholar
  33. 33.
    Adawi D, Ahrne S, Molin G: Effects of different probiotic strains of Lactobacillus and Bifidobacterium on bacterial translocation and liver injury in an acute liver injury model. Int J Food Microbiol 70: 213-220, 2001Google Scholar
  34. 34.
    Caradonna L, Amati L, Magrone T, Pellegrino NM, Jirillo E, Caccavo D: Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 6(3): 205-214, 2000Google Scholar
  35. 35.
    Fooks LJ, Gibson GR: Probiotics as modulators of the gut flora. Br J Nutr 88(Suppl 1):S39-S49, 2002Google Scholar
  36. 36.
    D'Argenio G, Mazzacca G: Short-chain fatty acid in the human colon. Relation to inflammatory bowel diseases and colon cancer. Adv Exp Med Biol 472: 149-158, 1999Google Scholar
  37. 37.
    Herias MV, Hessle C, Telemo E, Midtvedt T, Hanson LA, Wold AE: Immunomodulatory effects of Lactobacillus plantarum colonizing the intestine of gnotobiotic rats. Clin Exp Immunol 116(2): 283-290, 1999Google Scholar
  38. 38.
    Olah A, Belagyi T, Issekutz A, Gamal ME, Bengmark S: Randomized clinical trial of specific lactobacillus and fibre supplement to early enteral nutrition in patients with acute pancreatitis. Br J Surg 89(9): 1103-1107, 2002Google Scholar
  39. 39.
    Rayes N, Seehofer D, Hansen S, Boucsein K, Muller AR, Serke S, Bengmark S, Neuhaus P: Early enteral supply of lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation 74(1): 123-127, 2002Google Scholar
  40. 40.
    Rayes N, Hansen S, Seehofer D, Muller AR, Serke S, Bengmark S, Neuhaus P: Early enteral supply of fiber and Lactobacilli versus conventional nutrition: A controlled trial in patients with major abdominal surgery. Nutrition 18(7–8):609-615, 2002Google Scholar
  41. 41.
    McNaught CE, Woodcock NP, MacFie J, Mitchell CJ: A prospective randomised study of the probiotic Lactobacillus plantarum 299V on indices of gut barrier function in elective surgical patients. Gut 51(6): 827-831, 2002Google Scholar
  42. 42.
    Araki Y, Andoh A, Tsujikawa T, Fujiyama Y, Bamba T: Alterations in intestinal microflora, faecal bile acids and short chain fatty acids in dextran sulphate sodium-induced experimental acute colitis in rats. Eur J Gastroenterol Hepatol 13(2): 107-112, 2001Google Scholar
  43. 43.
    O'Mahony L, Feeney M, O'Halloran S, Murphy L, Kiely B, Fitzgibbon J, Lee G, O'Sullivan G, Shanahan F, Collins JK: Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment Pharmacol Ther 15(8): 1219-1225, 2001Google Scholar
  44. 44.
    Favier C, Neut C, Mizon C: Fecal beta-D-galactosidase production and bifidobacteria are decreased in Crohn's disease. Dig Dis Sci 42: 817-822, 1997Google Scholar
  45. 45.
    Brigidi P, Vitali B, Swennen E, Bazzocchi G, Matteuzzi D: Effects of probiotic administration upon the composition and enzymatic activity of human fecal microbiota in patients with irritable bowel syndrome or functional diarrhea. Res Microbiol 152(8): 735-741, 2001Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Nadia Osman
    • 1
  • Diya Adawi
    • 2
  • Siv Ahrne
    • 1
  • Bengt Jeppsson
    • 1
  • Göran Molin
  1. 1.Department of Food TechnologyEngineering and NutritionMalmöSweden
  2. 2.Department of Surgery, University Hospital MalmöLund UniversityMalmöSweden

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