Table of Contents 
Ulcers
Volume 2011 (2011), Article ID 841651, 13 pages
http://dx.doi.org/10.1155/2011/841651
Review Article

Potential Application of Probiotics in the Prevention and Treatment of Inflammatory Bowel Diseases

Silvina del Carmen,1 Alejandra de Moreno de LeBlanc,1 Anderson Miyoshi,2 Clarissa Santos Rocha,2 Vasco Azevedo,2 and Jean Guy LeBlanc1

1Centro de Referencia para Lactobacilos (CERELA-CONICET), Chacabuco 145, San Miguel de Tucumán T4000ILC, Argentina
2Institute of Biological Sciences, Federal University of Minas Gerais (UFMG-ICB), Belo Horizonte, MG, CEP 31270-901, Brazil

Received 13 August 2010; Accepted 25 November 2010

Academic Editor: Gyula Mozsik

Copyright © 2011 Silvina del Carmen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. A. Head and J. S. Jurenka, “Inflammatory bowel disease part I: ulcerative colitis—pathophysiology and conventional and alternative treatment options,” Alternative Medicine Review, vol. 8, no. 3, pp. 247–283, 2003. View at Google Scholar · View at Scopus
  2. D. C. Baumgart and W. J. Sandborn, “Inflammatory bowel disease: clinical aspects and established and evolving therapies,” The Lancet, vol. 369, no. 9573, pp. 1641–1657, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. A. B. Price, “Inflammatory bowel disease,” in Oxford Textbook of Pathology, J. O. D. McGee, P. G. Isaacson, and N. A. Wright, Eds., Oxford University Press, Oxford, UK, 1992. View at Google Scholar
  4. C. O. Elson and C. T. Weaver, “Experimental mouse models of inflammatory bowel disease: new insights into pathogenic mechanisms,” in Inflammatory Bowel Disease. From Bench to Bedside, S. R. Targan, F. Shanahan, and L. C. Karp, Eds., pp. 1–4, Springer Science+Business Media, New York, NY, USA, 2003. View at Google Scholar
  5. A. R. Jurjus, N. N. Khoury, and J. M. Reimund, “Animal models of inflammatory bowel disease,” Journal of Pharmacological and Toxicological Methods, vol. 50, no. 2, pp. 81–92, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Furrie, S. Macfarlane, A. Kennedy et al., “Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial,” Gut, vol. 54, no. 2, pp. 242–249, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. H. H. Cui, C. L. Chen, J. D. Wang et al., “Effects of probiotic on intestinal mucosa of patients with ulcerative colitis,” World Journal of Gastroenterology, vol. 10, no. 10, pp. 1521–1525, 2004. View at Google Scholar · View at Scopus
  8. I. M. Carroll, J. M. Andrus, J. M. Bruno-Bárcena, T. R. Klaenhammer, H. M. Hassan, and D. S. Threadgill, “Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis,” American Journal of Physiology, vol. 293, no. 4, pp. G729–G738, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Peran, S. Sierra, M. Comalada et al., “A comparative study of the preventative effects exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis,” British Journal of Nutrition, vol. 97, no. 1, pp. 96–103, 2007. View at Publisher · View at Google Scholar
  10. S. Matsumoto, T. Hara, T. Hori et al., “Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells,” Clinical and Experimental Immunology, vol. 140, no. 3, pp. 417–426, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Carol, N. Borruel, M. Antolin et al., “Modulation of apoptosis in intestinal lymphocytes by a probiotic bacteria in Crohn's disease,” Journal of Leukocyte Biology, vol. 79, no. 5, pp. 917–922, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Schultz, C. Veltkamp, L. A. Dieleman et al., “Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice,” Inflammatory Bowel Diseases, vol. 8, no. 2, pp. 71–80, 2002. View at Google Scholar · View at Scopus
  13. J. A. Peña and J. Versalovic, “Lactobacillus rhamnosus GG decreases TNF-α production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism,” Cellular Microbiology, vol. 5, no. 4, pp. 277–285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Majamaa and E. Isolauri, “Probiotics: a novel approach in the management of food allergy,” Journal of Allergy and Clinical Immunology, vol. 99, no. 2, pp. 179–185, 1997. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Sheil, J. McCarthy, L. O'Mahony et al., “Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis,” Gut, vol. 53, no. 5, pp. 694–700, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. L. O'Mahony, M. Feeney, S. O'Halloran et al., “Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice,” Alimentary Pharmacology and Therapeutics, vol. 15, no. 8, pp. 1219–1225, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Flynn, D. van Sinderen, G. M. Thornton, H. Holo, I. F. Nes, and J. K. Collins, “Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118,” Microbiology, vol. 148, no. 4, pp. 973–984, 2002. View at Google Scholar · View at Scopus
  18. K. L. Madsen, J. S. Doyle, L. D. Jewell, M. M. Tavernini, and R. N. Fedorak, “Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice,” Gastroenterology, vol. 116, no. 5, pp. 1107–1114, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Gionchetti, F. Rizzello, U. Helwig et al., “Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial,” Gastroenterology, vol. 124, no. 5, pp. 1202–1209, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Venturi, P. Gionchetti, F. Rizzello et al., “Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis,” Alimentary Pharmacology and Therapeutics, vol. 13, no. 8, pp. 1103–1108, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. J. G. H. R. van Embden, W. R. Schouten, and L. M. C. Van Lieshout, “Pouchitis: result of microbial imbalance?” Gut, vol. 35, no. 5, pp. 658–664, 1994. View at Google Scholar · View at Scopus
  22. P. Gionchetti, C. Amadini, F. Rizzello, A. Venturi, G. Poggioli, and M. Campieri, “Probiotics for the treatment of postoperativecomplications following intestinal surgery,” Best Practice & Research in Clinical Gastroenterology, vol. 17, no. 5, pp. 821–831, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Kajander and R. Korpela, “Clinical studies on alleviating the symptoms of irritable bowel syndrome with a probiotic combination,” Asia Pacific Journal of Clinical Nutrition, vol. 15, no. 4, pp. 576–580, 2006. View at Google Scholar · View at Scopus
  24. N. Osman, D. Adawi, S. Ahrne, B. Jeppsson, and G. Molin, “Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium,” Digestive Diseases and Sciences, vol. 49, no. 2, pp. 320–327, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Gupta, H. Andrew, B. S. Kirschner, and S. Guandalini, “Is Lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study,” Journal of Pediatric Gastroenterology and Nutrition, vol. 31, no. 4, pp. 453–457, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. M. V. Herías, J. F. J. G. Koninkx, J. G. Vos, J. H. J. Huis in't Veld, and J. E. van Dijk, “Probiotic effects of Lactobacillus casei on DSS-induced ulcerative colitis in mice,” International Journal of Food Microbiology, vol. 103, no. 2, pp. 143–155, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. H. C. Rath, K. H. Wilson, and R. B. Sartor, “Differential induction of colitis and gastritis in HLA-B27 transgenic rats selectively colonized with Bacteroides vulgatus or Escherichia coli,” Infection and Immunity, vol. 67, no. 6, pp. 2969–2974, 1999. View at Google Scholar · View at Scopus
  28. E. F. Verdù, P. Bercik, B. Cukrowska et al., “Oral administration of antigens from intestinal flora anaerobic bacteria reduces the severity of experimental acute colitis in BALB/c mice,” Clinical and Experimental Immunology, vol. 120, no. 1, pp. 46–50, 2000. View at Google Scholar · View at Scopus
  29. P. Chandran, S. Satthaporn, A. Robins, and O. Eremin, “Inflammatory bowel disease: dysfunction of GALT and gut bacterial flora (I),” Surgeon, vol. 1, no. 2, pp. 63–75, 2003. View at Google Scholar · View at Scopus
  30. S. Videla, J. Vilaseca, F. Guarner et al., “Role of intestinal microflora in chronic inflammation and ulceration of the rat colon,” Gut, vol. 35, no. 8, pp. 1090–1097, 1994. View at Google Scholar · View at Scopus
  31. C. Favier, C. Neut, C. Mizon, A. Cortot, J. F. Colombel, and J. Mizon, “Fecal β-D-galactosidase production and Bifidobacteria are decreased in Crohn's disease,” Digestive Diseases and Sciences, vol. 42, no. 4, pp. 817–822, 1997. View at Google Scholar · View at Scopus
  32. P. Seksik, L. Rigottier-Gois, G. Gramet et al., “Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon,” Gut, vol. 52, no. 2, pp. 237–242, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Swidsinski, A. Ladhoff, A. Pernthaler et al., “Mucosal flora in inflammatory bowel disease,” Gastroenterology, vol. 122, no. 1, pp. 44–54, 2002. View at Google Scholar · View at Scopus
  34. C. Schultsz, F. M. van den Berg, F. Ten Kate, G. N. J. Tytgat, and J. Dankert, “The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls,” Gastroenterology, vol. 117, no. 5, pp. 1089–1097, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. S. J. Ott, M. Musfeldt, D. F. Wenderoth et al., “Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease,” Gut, vol. 53, no. 5, pp. 685–693, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. M. P. Conte, S. Schippa, I. Zamboni et al., “Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease,” Gut, vol. 55, no. 12, pp. 1760–1767, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Mylonaki, N. B. Rayment, D. S. Rampton, B. N. Hudspith, and J. Brostoff, “Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 11, no. 5, pp. 481–487, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Vanderpool, F. Yan, and D. B. Polk, “Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases,” Inflammatory Bowel Diseases, vol. 14, no. 11, pp. 1585–1596, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Garrido, A. Suau, P. Pochart, S. Cruchet, and M. Gotteland, “Modulation of the fecal microbiota by the intake of a Lactobacillus johnsonii La1-containing product in human volunteers,” FEMS Microbiology Letters, vol. 248, no. 2, pp. 249–256, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. J. G. LeBlanc, A. de Moreno de Leblanc, G. Perdigón et al., “Anti-inflammatory properties of lactic acid bacteria: current knowledge, applications and prospects,” Anti-Infective Agents in Medicinal Chemistry, vol. 7, no. 3, pp. 148–154, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. FAO/WHO, “Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria,” 2001. View at Google Scholar
  42. P. Marteau, P. Lepage, I. Mangin et al., “Gut flora and inflammatory bowel disease,” Alimentary Pharmacology and Therapeutics, vol. 20, no. 4, pp. 18–23, 2004. View at Google Scholar · View at Scopus
  43. C. P. Tamboli, C. Caucheteux, A. Cortot, J. F. Colombel, and P. Desreumaux, “Probiotics in inflammatory bowel disease: a critical review,” Best Practice & Research in Clinical Gastroenterology, vol. 17, no. 5, pp. 805–820, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Guslandi, G. Mezzi, M. Sorghi, and P. A. Testoni, “Saccharomyces boulardii in maintenance treatment of Crohn's disease,” Digestive Diseases and Sciences, vol. 45, no. 7, pp. 1462–1464, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Malin, H. Suomalainen, M. Saxelin, and E. Isolauri, “Promotion of IgA immune response in patients with Crohn's disease by oral bacteriotherapy with Lactobacillus GG,” Annals of Nutrition and Metabolism, vol. 40, no. 3, pp. 137–145, 1996. View at Google Scholar · View at Scopus
  46. L. O'Mahony, J. Mccarthy, P. Kelly et al., “Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles,” Gastroenterology, vol. 128, no. 3, pp. 541–551, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. A. C. Bittner, R. M. Croffut, M. C. Stranahan, and T. N. Yokelson, “Prescript-assist probiotic-prebiotic treatment for irritable bowel syndrome: an open-label, partially controlled, 1-year extension of a previously published controlled clinical trial,” Clinical Therapeutics, vol. 29, no. 6, pp. 1153–1160, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. A. C. Bittner, R. M. Croffut, and M. C. Stranahan, “Prescript-assist probiotic-prebiotic treatment for irritable bowel syndrome: a methodologically oriented, 2-week, randomized, placebo-controlled, double-blind clinical study,” Clinical Therapeutics, vol. 27, no. 6, pp. 755–761, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Mimura, F. Rizzello, U. Helwig et al., “Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis,” Gut, vol. 53, no. 1, pp. 108–114, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. W. Kruis, P. Frič, J. Pokrotnieks et al., “Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine,” Gut, vol. 53, no. 11, pp. 1617–1623, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Tursi, G. Brandimarte, G. M. Giorgetti, G. Forti, M. E. Modeo, and A. Gigliobianco, “Low-dose balsalazide plus a high-potency probiotic preparation is more effective than balsalazide alone or mesalazine in the treatment of acute mild-to-moderate ulcerative colitis,” Medical Science Monitor, vol. 10, no. 11, pp. PI126–PI131, 2004. View at Google Scholar · View at Scopus
  52. O. Karimi, A. S. Peña, and A. A. van Bodegraven, “Probiotics (VSL#3) in arthralgia in patients with ulcerative colitis and Crohn's disease: a pilot study,” Drugs of Today, vol. 41, no. 7, pp. 453–459, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Isolauri, S. Salminen, and A. C. Ouwehand, “Microbial-gut interactions in health and disease. Probiotics,” Best Practice & Research Clinical Gastroenterology, vol. 18, pp. 299–313, 2004. View at Google Scholar
  54. T. R. Klaenhammer, “Bacteriocins of lactic acid bacteria,” Biochimie, vol. 70, no. 3, pp. 337–349, 1988. View at Google Scholar · View at Scopus
  55. M. C. Rea, E. Clayton, P. M. O'Connor et al., “Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains,” Journal of Medical Microbiology, vol. 56, no. 7, pp. 940–946, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Schultz, K. Munro, G. W. Tannock et al., “Effects of feeding a probiotic preparation (SIM) containing inulin on the severity of colitis and on the composition of the intestinal microflora in HLA-B27 transgenic rats,” Clinical and Diagnostic Laboratory Immunology, vol. 11, no. 3, pp. 581–587, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Campieri, F. Rizzello, A. Venturi et al., “Combination of antibiotic and probiotic treatment is efficacious in prophylaxis of post-operative recurrence of Crohn’s disease: a randomised controlled study v. mesalazine,” Gastroenterology, vol. 118, p. A4179, 2000. View at Google Scholar
  58. P. Gionchetti, F. Rizzello, A. Venturi et al., “Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial,” Gastroenterology, vol. 119, no. 2, pp. 305–309, 2000. View at Google Scholar · View at Scopus
  59. M. J. Ruddy, G. C. Wong, X. K. Liu et al., “Functional cooperation between interleukin-17 and tumor necrosis factor-α is mediated by CCAAT/enhancer-binding protein family members,” Journal of Biological Chemistry, vol. 279, no. 4, pp. 2559–2567, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. F. Leon, L. E. Smythies, P. D. Smith, and B. L. Kelsall, “Involvement of dendritic cells in the pathogenesis of inflammatory bowel disease,” Advances in Experimental Medicine and Biology, vol. 579, pp. 117–132, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. D. K. Podolsky, “Inflammatory bowel disease,” The New England Journal of Medicine, vol. 347, no. 6, pp. 417–429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Brand, “Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease,” Gut, vol. 58, no. 8, pp. 1152–1167, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. M. F. Neurath, I. Fuss, B. L. Kelsall, D. H. Presky, W. Waegell, and W. Strober, “Experimental granulomatous colitis in mice is abrogated by induction of TGF-β-mediated oral tolerance,” Journal of Experimental Medicine, vol. 183, no. 6, pp. 2605–2616, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Jonuleit, E. Schmitt, M. Stassen, A. Tuettenberg, J. Knop, and A. H. Enk, “Identification and functional characterization of human CD4+CD25+ T cells with regulatory properties isolated from peripheral blood,” Journal of Experimental Medicine, vol. 193, no. 11, pp. 1285–1294, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Cong, C. T. Weaver, A. Lazenby, and C. O. Elson, “Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora,” Journal of Immunology, vol. 169, no. 11, pp. 6112–6119, 2002. View at Google Scholar · View at Scopus
  66. A. Kappeler and C. Mueller, “The role of activated cytotoxic T cells in inflammatory bowel disease,” Histology and Histopathology, vol. 15, no. 1, pp. 167–172, 2000. View at Google Scholar · View at Scopus
  67. G. Perdigón, E. Vintiñi, S. Alvarez, M. Medina, and M. Medici, “Study of the possible mechanisms involved in the mucosal immune system activation by lactic acid bacteria,” Journal of Dairy Science, vol. 82, no. 6, pp. 1108–1114, 1999. View at Google Scholar · View at Scopus
  68. G. Perdigon, M. Medina, E. Vintini, and J. C. Valdez, “Intestinal pathway of internalisation of lactic acid bacteria and gut mucosal immunostimulation,” International Journal of Immunopathology and Pharmacology, vol. 13, no. 3, pp. 141–150, 2000. View at Google Scholar · View at Scopus
  69. T. Pessi, Y. Sütas, M. Hurme, and E. Isolauri, “Interleukin-10 generation in atopic children following oral lactobacillus rhamnosus GG,” Clinical and Experimental Allergy, vol. 30, no. 12, pp. 1804–1808, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. A. de Moreno de Leblanc, S. Chaves, and G. Perdigón, “Effect of yoghurt on the cytokine profile using a murine model of intestinal inflammation,” European Journal of Inflammation, vol. 7, no. 2, pp. 97–109, 2009. View at Google Scholar · View at Scopus
  71. A. P. Bai, Q. Ouyang, X. R. Xiao, and S. F. Li, “Probiotics modulate inflammatory cytokine secretion from inflamed mucosa in active ulcerative colitis,” International Journal of Clinical Practice, vol. 60, no. 3, pp. 284–288, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. C. O. Elson, “From cheese to pharma: a designer probiotic for IBD,” Clinical Gastroenterology and Hepatology, vol. 4, no. 7, pp. 836–837, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Ina, J. Itoh, K. Fukushima et al., “Resistance of Crohn's disease T cells to multiple apoptotic signals is associated with a Bcl-2/Bax mucosal imbalance,” Journal of Immunology, vol. 163, no. 2, pp. 1081–1090, 1999. View at Google Scholar · View at Scopus
  74. J. Itoh, C. de la Motte, S. A. Strong, A. D. Levine, and C. Fiocchi, “Decreased Bax expression by mucosal T cells favours resistance to apoptosis in Crohn's disease,” Gut, vol. 49, no. 1, pp. 35–41, 2001. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Atreya, J. Mudter, S. Finotto et al., “Erratum: Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo,” Nature Medicine, vol. 16, no. 11, p. 1341, 2010. View at Publisher · View at Google Scholar
  76. G. Friedman and J. T. George, “Treatment of refractory ‘pouchitis’ with prebiotic and probiotic therapy,” Gastroenterology, vol. 118, p. A4167, 2000. View at Google Scholar
  77. W. Kruis, E. Schütz, P. Fric, B. Fixa, G. Judmaier, and M. Stolte, “Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis,” Alimentary Pharmacology and Therapeutics, vol. 11, no. 5, pp. 853–858, 1997. View at Google Scholar · View at Scopus
  78. B. J. Rembacken, A. M. Snelling, P. M. Hawkey, D. M. Chalmers, and A. T. R. Axon, “Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial,” The Lancet, vol. 354, no. 9179, pp. 635–639, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Kuhn, J. Lohler, D. Rennick, K. Rajewsky, and W. Muller, “Interleukin-10-deficient mice develop chronic enterocolitis,” Cell, vol. 75, no. 2, pp. 263–274, 1993. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Tilg, C. Van Montfrans, A. Van den Ende et al., “Treatment of Crohn's disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon γ,” Gut, vol. 50, no. 2, pp. 191–195, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. H. H. Uhlig, J. Coombes, C. Mottet et al., “Characterization of Foxp3+CD4+CD25+ and IL-10-secreting CD4+CD25+ T cells during cure of colitis,” Journal of Immunology, vol. 177, no. 9, pp. 5852–5860, 2006. View at Google Scholar · View at Scopus
  82. M. Roselli, A. Finamore, S. Nuccitelli et al., “Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of γδT and regulatory T cells of intestinal intraepithelial lymphocytes,” Inflammatory Bowel Diseases, vol. 15, no. 10, pp. 1526–1536, 2009. View at Publisher · View at Google Scholar
  83. E. Mengheri, “Health, probiotics, and inflammation,” Journal of clinical gastroenterology, vol. 42, pp. S177–S178, 2008. View at Google Scholar · View at Scopus
  84. S. Ishihara, M. A. K. Rumi, C. F. Ortega-Cava et al., “Therapeutic targeting of toll-like receptors in gastrointestinal inflammation,” Current Pharmaceutical Design, vol. 12, no. 32, pp. 4215–4228, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. P. Pimentel-Nunes, J. B. Soares, R. Roncon-Albuquerque, M. Dinis-Ribeiro, and A. F. Leite-Moreira, “Toll-like receptors as therapeutic targets in gastrointestinal diseases,” Expert Opinion on Therapeutic Targets, vol. 14, no. 4, pp. 347–368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. C. M. Galdeano, A. de Moreno de Leblanc, G. Vinderola, M. E. Bonet, and G. Perdigón, “Proposed model: mechanisms of immunomodulation induced by probiotic bacteria,” Clinical and Vaccine Immunology, vol. 14, no. 5, pp. 485–492, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. C. M. Galdeano, A. de Moreno de Leblanc, E. Carmuega, R. Weill, and G. Perdigón, “Mechanisms involved in the immunostimulation by probiotic fermented milk,” Journal of Dairy Research, vol. 76, no. 4, pp. 446–454, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. M. G. Vizoso Pinto, M. Rodriguez Gómez, S. Seifert, B. Watzl, W. H. Holzapfel, and C. M. A. P. Franz, “Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro,” International Journal of Food Microbiology, vol. 133, no. 1-2, pp. 86–93, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Schultz and A. L. Lindström, “Rationale for probiotic treatment strategies in inflammatory bowel disease,” Expert Review of Gastroenterology and Hepatology, vol. 2, no. 3, pp. 337–355, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Fukata and M. T. Abreu, “TLR4 signalling in the intestine in health and disease,” Biochemical Society Transactions, vol. 35, no. 6, pp. 1473–1478, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. C. A. Dogi, C. M. Galdeano, and G. Perdigón, “Gut immune stimulation by non pathogenic Gram+ and Gram− bacteria. Comparison with a probiotic strain,” Cytokine, vol. 41, no. 3, pp. 223–231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. Y. W. Chung, J. H. Choi, T. Y. Oh, C. S. Eun, and D. S. Han, “Lactobacillus casei prevents the development of dextran sulphate sodium-induced colitis in Toll-like receptor 4 mutant mice,” Clinical and Experimental Immunology, vol. 151, no. 1, pp. 182–189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Rachmilewitz, F. Karmeli, K. Takabayashi et al., “Immunostimulatory DNA ameliorates experimental and spontaneous murine colitis,” Gastroenterology, vol. 122, no. 5, pp. 1428–1441, 2002. View at Google Scholar · View at Scopus
  94. F. Obermeier, N. Dunger, U. G. Strauch et al., “CpG motifs of bacterial DNA essentially contribute to the perpetuation of chronic intestinal inflammation,” Gastroenterology, vol. 129, no. 3, pp. 913–927, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Akhtar, J. L. Watson, A. Nazli, and D. M. McKay, “Bacterial DNA evokes epithelial IL-8 production by a MAPK-dependent, NF-kappaB-independent pathway,” The FASEB Journal, vol. 17, no. 10, pp. 1319–1321, 2003. View at Google Scholar · View at Scopus
  96. J. Lee, D. Rachmilewitz, and E. Raz, “Homeostatic effects of TLR9 signaling in experimental colitis,” Annals of the New York Academy of Sciences, vol. 1072, pp. 351–355, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. D. Rachmilewitz, K. Katakura, F. Karmeli et al., “Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis,” Gastroenterology, vol. 126, no. 2, pp. 520–528, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. D. Rachmilewitz, F. Karmeli, S. Shteingart, J. Lee, K. Takabayashi, and E. Raz, “Immunostimulatory oligonucleotides inhibit colonic proinflammatory cytokine production in ulcerative colitis,” Inflammatory Bowel Diseases, vol. 12, no. 5, pp. 339–345, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. N. Kamada, N. Inoue, T. Hisamatsu et al., “Nonpathogenic Escherichia coli strain Nissle 1917 prevents murine acute and chronic colitis,” Inflammatory Bowel Diseases, vol. 11, no. 5, pp. 455–463, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. A. Miyoshi, L. Bermudez-Humaran, M. Pacheco de Azevedo, P. Langella, and V. Azevedo, “Lactic acid bacteria as live vectors: heterologous protein production and delivery systems,” in Biotechnology of Lactic Acid Bacteria Novel Applications, F. Mozzi, R. Raya, and G. Vignolo, Eds., pp. 1–9, Blackwell Publishing, Ames, Iowa, USA, 2010. View at Google Scholar
  101. L. Steidler, W. Hans, L. Schotte et al., “Treatment of murine colitis by Lactococcus lactis secreting interleukin-10,” Science, vol. 289, no. 5483, pp. 1352–1355, 2000. View at Publisher · View at Google Scholar · View at Scopus
  102. H. Braat, P. Rottiers, D. W. Hommes et al., “A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease,” Clinical Gastroenterology and Hepatology, vol. 4, no. 6, pp. 754–759, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. F. A. V. Marinho, L. G. G. Pacífico, A. Miyoshi et al., “An intranasal administration of Lactococcus lactis strains expressing recombinant interleukin-10 modulates acute allergic airway inflammation in a murine model,” Clinical and Experimental Allergy, vol. 40, no. 10, pp. 1541–1551, 2010. View at Publisher · View at Google Scholar
  104. A. Keshavarzian, A. Banan, A. Farhadi et al., “Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease,” Gut, vol. 52, no. 5, pp. 720–728, 2003. View at Publisher · View at Google Scholar · View at Scopus
  105. L. Lih-Brody, S. R. Powell, K. P. Collier et al., “Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease,” Digestive Diseases and Sciences, vol. 41, no. 10, pp. 2078–2086, 1996. View at Publisher · View at Google Scholar · View at Scopus
  106. S. Sedghi, J. Z. Fields, M. Klamut et al., “Increased production of luminol enhanced chemiluminescence by the inflamed colonic mucosa in patients with ulcerative colitis,” Gut, vol. 34, no. 9, pp. 1191–1197, 1993. View at Google Scholar · View at Scopus
  107. N. J. Simmonds, R. E. Allen, T. R. J. Stevens, R. N. M. Van Someren, D. R. Blake, and D. S. Rampton, “Chemiluminescence assay of mucosal reactive oxygen metabolites in inflammatory bowel disease,” Gastroenterology, vol. 103, no. 1, pp. 186–196, 1992. View at Google Scholar · View at Scopus
  108. S. Condon, “Responses of lactic acid bacteria to oxygen,” FEMS Microbiology Letters, vol. 46, no. 3, pp. 269–280, 1987. View at Google Scholar · View at Scopus
  109. D. Roos, “The involvement of oxygen radicals in microbicidal mechanisms of leukocytes and macrophages,” Klinische Wochenschrift, vol. 69, no. 21-23, pp. 975–980, 1991. View at Google Scholar · View at Scopus
  110. B. S. Berlett and E. R. Stadtman, “Protein oxidation in aging, disease, and oxidative stress,” Journal of Biological Chemistry, vol. 272, no. 33, pp. 20313–20316, 1997. View at Publisher · View at Google Scholar · View at Scopus
  111. S. B. Farr and T. Kogoma, “Oxidative stress responses in Escherichia coli and Salmonella typhimurium,” Microbiological Reviews, vol. 55, no. 4, pp. 561–585, 1991. View at Google Scholar · View at Scopus
  112. T. P. Szatrowski and C. F. Nathan, “Production of large amounts of hydrogen peroxide by human tumor cells,” Cancer Research, vol. 51, no. 3, pp. 794–798, 1991. View at Google Scholar · View at Scopus
  113. L. Kruidenier and H. W. Verspaget, “Oxidative stress as a pathogenic factor in inflammatory bowel disease—radicals or ridiculous?” Alimentary Pharmacology and Therapeutics, vol. 16, no. 12, pp. 1997–2015, 2002. View at Publisher · View at Google Scholar · View at Scopus
  114. L. Kruidenier, M. E. van Meeteren, I. Kuiper et al., “Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice,” Free Radical Biology and Medicine, vol. 34, no. 6, pp. 753–765, 2003. View at Publisher · View at Google Scholar · View at Scopus
  115. B. G. Spyropoulos, E. P. Misiakos, C. Fotiadis, and C. N. Stoidis, “Antioxidant properties of probiotics and their protective effects in the pathogenesis of radiation-induced enteritis and colitis,” Digestive Diseases and Sciences. In press. View at Publisher · View at Google Scholar · View at Scopus
  116. C. Grangette, S. Nutten, E. Palumbo et al., “Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 29, pp. 10321–10326, 2005. View at Publisher · View at Google Scholar · View at Scopus
  117. T. Rochat, L. Bermúdez-Humarán, J. J. Gratadoux et al., “Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice,” Microbial Cell Factories, vol. 6, article no. 22, 2007. View at Publisher · View at Google Scholar · View at Scopus
  118. A. de Moreno de Leblanc, J. G. LeBlanc, G. Perdigón et al., “Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice,” Journal of Medical Microbiology, vol. 57, no. 1, pp. 100–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. W. Han, A. Mercenier, A. Ait-Belgnaoui et al., “Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase,” Inflammatory Bowel Diseases, vol. 12, no. 11, pp. 1044–1052, 2006. View at Publisher · View at Google Scholar · View at Scopus
  120. L. Watterlot, T. Rochat, H. Sokol et al., “Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice,” International Journal of Food Microbiology, vol. 144, no. 1, pp. 35–41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. J. G. LeBlanc, S. del Carmen, A. Miyoshi et al., “Use of superoxide dismutase and catalase expressing lactic acid bacteria to attenuate TNBS induced Crohn’s disease in mice,” Journal of Biotechnology. In press. View at Publisher · View at Google Scholar
  122. L. Watterlot, T. Rochat, H. Sokol et al., “Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice,” International Journal of Food Microbiology, vol. 144, pp. 35–41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. T. Rochat, A. Miyoshi, J. J. Gratadoux et al., “High-level resistance to oxidative stress in Lactococcus lactis conferred by Bacillus subtilis catalase KatE,” Microbiology, vol. 151, no. 9, pp. 3011–3018, 2005. View at Publisher · View at Google Scholar · View at Scopus
  124. T. Rochat, J. J. Gratadoux, A. Gruss et al., “Production of a heterologous nonheme catalase by Lactobacillus casei: an efficient tool for removal of H2O2 and protection of Lactobacillus bulgaricus from oxidative stress in milk,” Applied and Environmental Microbiology, vol. 72, no. 8, pp. 5143–5149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  125. P. Mallon, D. McKay, S. Kirk, and K. Gardiner, “Probiotics for induction of remission in ulcerative colitis,” Cochrane Database of Systematic Reviews, no. 4, Article ID CD005573, 2007. View at Google Scholar · View at Scopus
  126. A. Tursi, G. Brandimarte, A. Papa et al., “Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study,” American Journal of Gastroenterology, vol. 105, no. 10, pp. 2218–2227, 2010. View at Publisher · View at Google Scholar