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BioMed Research International
Volume 2013 (2013), Article ID 435268, 9 pages
http://dx.doi.org/10.1155/2013/435268
Review Article

Gut Microbial Flora, Prebiotics, and Probiotics in IBD: Their Current Usage and Utility

1Department of Internal Medicine, Gastroenterology Division, Catholic University of Sacred Hearth, Policlinico “A. Gemelli” Hospital, lgo Gemelli 8, 00168 Roma, Italy
2Institute of Pathology, Catholic University of Sacred Hearth, lgo Gemelli 8, 00168 Rome, Italy

Received 19 April 2013; Revised 29 June 2013; Accepted 8 July 2013

Academic Editor: Michael Mahler

Copyright © 2013 Franco Scaldaferri 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. R. B. Sartor, “Microbial influences in inflammatory bowel diseases,” Gastroenterology, vol. 134, no. 2, pp. 577–594, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Schmidt and A. Stallmach, “Etiology and pathogenesis of inflammatory bowel disease,” Minerva Gastroenterologica e Dietologica, vol. 51, no. 2, pp. 127–145, 2005. View at Scopus
  3. P. B. Eckburg, P. W. Lepp, and D. A. Relman, “Archaea and their potential role in human disease,” Infection and Immunity, vol. 71, no. 2, pp. 591–596, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Breitbart, I. Hewson, B. Felts et al., “Metagenomic analyses of an uncultured viral community from human feces,” Journal of Bacteriology, vol. 185, no. 20, pp. 6220–6223, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Hayashi, M. Sakamoto, and Y. Benno, “Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods,” Microbiology and Immunology, vol. 46, no. 8, pp. 535–548, 2002. View at Scopus
  6. A. Suau, R. Bonnet, M. Sutren et al., “Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut,” Applied and Environmental Microbiology, vol. 65, no. 11, pp. 4799–4807, 1999. View at Scopus
  7. J. L. Sonnenburg, L. T. Angenent, and J. I. Gordon, “Getting a grip on things: how do communities of bacterial symbionts become established in our intestine?” Nature Immunology, vol. 5, no. 6, pp. 569–573, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. G. De Hertogh, J. Aerssens, R. De Hoogt et al., “Validation of 16S rDNA sequencing in microdissected bowel/biopsies from Crohn's disease patients to assess bacterial flora diversity,” Journal of Pathology, vol. 209, no. 4, pp. 532–539, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Scaldaferri, M. Pizzoferrato, V. Gerardi, L. Lopetuso, and A. Gasbarrini, “The gut barrier: new acquisitions and therapeutic approaches,” Journal of Clinical Gastroenterology, vol. 46, Supplement, pp. S12–S17, 2012.
  10. J. L. Round, R. M. O'Connell, and S. K. Mazmanian, “Coordination of tolerogenic immune responses by the commensal microbiota,” Journal of Autoimmunity, vol. 34, no. 3, pp. J220–J225, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Nell, S. Suerbaum, and C. Josenhans, “The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models,” Nature Reviews Microbiology, vol. 8, no. 8, pp. 564–577, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. N. S. Hotte, S. Y. Salim, R. H. Tso, et al., “Patients with inflammatory bowel disease exhibit dysregulated responses to microbial DNA,” PloS ONE, vol. 7, no. 5, Article ID e37932, 2012.
  13. S. Rakoff-Nahoum, J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov, “Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis,” Cell, vol. 118, no. 2, pp. 229–241, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. J. M. Natividad and E. F. Verdu, “Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications,” Pharmacological Research, vol. 69, no. 1, pp. 42–51, 2013. View at Publisher · View at Google Scholar
  15. H. J. De Silva, P. R. Millard, N. Soper, M. Kettlewell, N. Mortensen, and D. P. Jewell, “Effects of the faecal stream and stasis on the ileal pouch mucosa,” Gut, vol. 32, no. 10, pp. 1166–1169, 1991. View at Scopus
  16. P. B. Eckburg, E. M. Bik, C. N. Bernstein et al., “Microbiology: diversity of the human intestinal microbial flora,” Science, vol. 308, no. 5728, pp. 1635–1638, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. R. B. Sartor, “Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis,” Nature Clinical Practice Gastroenterology and Hepatology, vol. 3, no. 7, pp. 390–407, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. G. R. Veerappan, J. Betteridge, and P. E. Young, “Probiotics for the treatment of inflammatory bowel disease,” Current Gastroenterology Reports, vol. 14, no. 4, pp. 324–333, 2012.
  19. M. De Vrese and J. Schrezenmeir, “Probiotics, prebiotics, and synbiotics,” Advances in Biochemical Engineering/Biotechnology, vol. 111, pp. 1–66, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. A. C. Looijer-van Langen and L. A. Dieleman, “Prebiotics in chronic intestinal inflammation,” Inflammatory Bowel Diseases, vol. 15, no. 3, pp. 454–462, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. A. L. Servin, “Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens,” FEMS Microbiology Reviews, vol. 28, no. 4, pp. 405–440, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. M. C. Collado, J. Meriluoto, and S. Salminen, “Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus,” Letters in Applied Microbiology, vol. 45, no. 4, pp. 454–460, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Bouhnik, L. Raskine, G. Simoneau et al., “The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study,” American Journal of Clinical Nutrition, vol. 80, no. 6, pp. 1658–1664, 2004. View at Scopus
  24. R. J. Chiodini, H. J. Van Kruiningen, and R. Thayer, “Possible role of mycobacteria in inflammatory bowel disease. I. An unclassified Mycobacterium species isolated from patients with Crohn's disease,” Digestive Diseases and Sciences, vol. 29, no. 12, pp. 1073–1079, 1984. View at Scopus
  25. K. Hultén, A. Almashhrawi, F. A. K. El-Zaatari, and D. Y. Graham, “Antibacterial therapy for Crohn's disease: a review emphasizing therapy directed against mycobacteria,” Digestive Diseases and Sciences, vol. 45, no. 3, pp. 445–456, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Selby, P. Pavli, B. Crotty et al., “Two-year combination antibiotic therapy with clarithromycin, rifabutin, and clofazimine for crohn's disease,” Gastroenterology, vol. 132, no. 7, pp. 2313–2319, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Chassaing and A. Darfeuillemichaud, “The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases,” Gastroenterology, vol. 140, no. 6, pp. 1720–1728, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. N. A. Nagalingam and S. V. Lynch, “Role of the microbiota in inflammatory bowel diseases,” Inflammatory Bowel Diseases, vol. 18, no. 5, pp. 968–980, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. G. De Hertogh and K. Geboes, “Crohn's disease and infections: a complex relationship,” MedGenMed Medscape General Medicine, vol. 6, no. 3, 2004. View at Scopus
  30. D. Comito and C. Romano, “Dysbiosis in the pathogenesis of pediatric inflammatory bowel diseases,” International Journal of Inflammation, vol. 2012, Article ID 687143, 7 pages, 2012. View at Publisher · View at Google Scholar
  31. B. P. Willing, J. Dicksved, J. Halfvarson et al., “A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes,” Gastroenterology, vol. 139, no. 6, pp. 1844.e1–1854.e1, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Ohkusa, N. Sato, T. Ogihara, K. Morita, M. Ogawa, and I. Okayasu, “Fusobacterium varium localized in the colonic mucosa of patients with ulcerative colitis stimulates species-specific antibody,” Journal of Gastroenterology and Hepatology, vol. 17, no. 8, pp. 849–853, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Ohkusa, I. Okayasu, T. Ogihara, K. Morita, M. Ogawa, and N. Sato, “Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis,” Gut, vol. 52, no. 1, pp. 79–83, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Sokol, P. Lepage, P. Seksik, J. Doré, and P. Marteau, “Temperature gradient gel electrophoresis of fecal 16S rRNA reveals active Escherichia coli in the microbiota of patients with ulcerative colitis,” Journal of Clinical Microbiology, vol. 44, no. 9, pp. 3172–3177, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. R. K. Sellon, S. Tonkonogy, M. Schultz et al., “Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice,” Infection and Immunity, vol. 66, no. 11, pp. 5224–5231, 1998. View at Scopus
  36. G. R. D'Haens, K. Geboes, M. Peeters, F. Baert, F. Penninckx, and P. Rutgeerts, “Early lesions of recurrent Crohn's disease caused by infusion of intestinal contents in excluded ileum,” Gastroenterology, vol. 114, no. 2, pp. 262–267, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Sokol, B. Pigneur, L. Watterlot et al., “Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 43, pp. 16731–16736, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Fava and S. Danese, “Intestinal microbiota in inflammatory bowel disease: friend of foe?” World Journal of Gastroenterology, vol. 17, no. 5, pp. 557–566, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Manichanh, N. Borruel, F. Casellas, and F. Guarner, “The gut microbiota in IBD,” Nature Reviews, vol. 9, no. 10, pp. 599–608, 2012.
  40. M. Joossens, G. Huys, M. Cnockaert et al., “Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives,” Gut, vol. 60, no. 5, pp. 631–637, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Shen, “Acute and chronic pouchitis-pathogenesis, diagnosis and treatment,” Nature Reviews Gastroenterology and Hepatology, vol. 9, pp. 323–333, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. S. D. McLaughlin, A. W. Walker, C. Churcher et al., “The bacteriology of pouchitis: a molecular phylogenetic analysis using 16s rRNA gene cloning and sequencing,” Annals of Surgery, vol. 252, no. 1, pp. 90–98, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. W. E. W. Roediger, A. Duncan, O. Kapaniris, and S. Millard, “Reducing sulfur compounds of the colon impair colonocyte nutrition: implications for ulcerative colitis,” Gastroenterology, vol. 104, no. 3, pp. 802–809, 1993. View at Scopus
  44. T. Ohkusa, M. Yamada, T. Takenaga et al., “Protective effect of metronidazole in experimental ulcerative colitis induced by dextran sulfate sodium,” Japanese Journal of Gastroenterology, vol. 84, no. 10, pp. 2337–2346, 1987. View at Scopus
  45. F. Rowan, N. G. Docherty, M. Murphy, B. Murphy, J. C. Coffey, and P. R. O'Connell, “Desulfovibrio bacterial species are increased in ulcerative colitis,” Diseases of the Colon and Rectum, vol. 53, no. 11, pp. 1530–1536, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. C. L. Pitcher, E. R. Beatty, and J. H. Cummings, “The contribution of sulphate reducing bacteria and 5-aminosalicylic acid to faecal sulphide in patients with ulcerative colitis,” Gut, vol. 46, no. 1, pp. 64–72, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. C. J. Damman, S. I. Miller, C. M. Surawicz, and T. L. Zisman, “The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation?” The American Journal of Gastroenterology, vol. 107, no. 10, pp. 1452–1459, 2012.
  48. S. A. Kahn, R. Gorawara-Bhat, and D. T. Rubin, “Fecal bacteriotherapy for ulcerative colitis: patients are ready, are we?” Inflammatory Bowel Diseases, vol. 18, no. 4, pp. 676–684, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. S. J. Ott, T. Kühbacher, M. Musfeldt et al., “Fungi and inflammatory bowel diseases: alterations of composition and diversity,” Scandinavian Journal of Gastroenterology, vol. 43, no. 7, pp. 831–841, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. Q. Wang, G. M. Garrity, J. M. Tiedje, and J. R. Cole, “Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy,” Applied and Environmental Microbiology, vol. 73, no. 16, pp. 5261–5267, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Laurin, M. L. Everett, and W. Parker, “The cecal appendix: one more immune component with a function disturbed by post-industrial culture,” Anatomical Record, vol. 294, no. 4, pp. 567–579, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. R. J. Berry, “The true caecal apex, or the vermiform appendix: its minute and comparative anatomy,” Journal of Anatomy and Physiology, vol. 35, pp. 83–100, 1900.
  53. R. Randal Bollinger, A. S. Barbas, E. L. Bush, S. S. Lin, and W. Parker, “Biofilms in the large bowel suggest an apparent function of the human vermiform appendix,” Journal of Theoretical Biology, vol. 249, no. 4, pp. 826–831, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. J. W. Costerton, “Overview of microbial biofilms,” Journal of Industrial Microbiology, vol. 15, no. 3, pp. 137–140, 1995. View at Publisher · View at Google Scholar · View at Scopus
  55. J. W. Costerton, “Introduction to biofilm,” International Journal of Antimicrobial Agents, vol. 11, no. 3-4, pp. 217–221, 1999. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Schoof, M. R. John, B. Arndt et al., “Solid phase competitive luminescence immunoassay for immunoglobulin A in faeces: development and clinical validation,” Clinica Chimica Acta, vol. 261, no. 1, pp. 1–17, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. G. L. Radford-Smith, J. E. Edwards, D. M. Purdie et al., “Protective role of appendicectomy on onset and severity of ulcerative colitis and Crohn's disease,” Gut, vol. 51, no. 6, pp. 808–813, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Cosnes, F. Carbonnel, L. Beaugerie, A. Blain, D. Reijasse, and J.-P. Gendre, “Effects of appendicectomy on the course of ulcerative colitis,” Gut, vol. 51, no. 6, pp. 803–807, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Naganuma, B.-E. Iizuka, A. Torii et al., “Appendectomy protects against the development of ulcerative colitis and reduces its recurrence: results of a multicenter case-controlled study in japan,” American Journal of Gastroenterology, vol. 96, no. 4, pp. 1123–1126, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. W. S. Selby, S. Griffin, N. Abraham, and M. J. Solomon, “Appendectomy protects against the development of ulcerative colitis but does not affect its course,” American Journal of Gastroenterology, vol. 97, no. 11, pp. 2834–2838, 2002. View at Scopus
  61. G. L. Radford-Smith, “What is the importance of appendectomy in the natural history of IBD?” Inflammatory Bowel Diseases, vol. 14, pp. S72–S74, 2008. View at Scopus
  62. 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
  63. 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 Scopus
  64. C. F. M. Welters, E. Heineman, F. B. J. M. Thunnissen, A. E. J. M. Van den Bogaard, P. B. Soeters, and C. G. M. I. Baeten, “Effect of dietary inulin supplementation on inflammation of pouch mucosa in patients with an ileal pouch-anal anastomosis,” Diseases of the Colon and Rectum, vol. 45, no. 5, pp. 621–627, 2002. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Schultz, A. Timmer, H. H. Herfarth, R. B. Sartor, J. A. Vanderhoof, and H. C. Rath, “Lactobacillus GG in inducing and maintaining remission of Crohn's disease,” BMC Gastroenterology, vol. 4, article 5, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Bousvaros, S. Guandalini, R. N. Baldassano et al., “A randomized, double-blind trial of lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn's disease,” Inflammatory Bowel Diseases, vol. 11, no. 9, pp. 833–839, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. V. E. Rolfe, P. J. Fortun, C. J. Hawkey, and F. Bath-Hextall, “Probiotics for maintenance of remission in Crohn's disease,” Cochrane Database of Systematic Reviews, no. 4, Article ID CD004826, 2006. View at Scopus
  68. R. Rahimi, S. Nikfar, F. Rahimi et al., “A meta-analysis on the efficacy of probiotics for maintenance of remission and prevention of clinical and endoscopic relapse in Crohn's disease,” Digestive Diseases and Sciences, vol. 53, no. 9, pp. 2524–2531, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Doherty, G. Bennett, S. Patil, A. Cheifetz, and A. C. Moss, “Interventions for prevention of post-operative recurrence of Crohn's disease,” Cochrane Database of Systematic Reviews, no. 4, Article ID CD006873, 2009. View at Scopus
  70. M. A. Zocco, L. Z. Dal Verme, F. Cremonini et al., “Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis,” Alimentary Pharmacology and Therapeutics, vol. 23, no. 11, pp. 1567–1574, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Bibiloni, R. N. Fedorak, G. W. Tannock et al., “VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis,” American Journal of Gastroenterology, vol. 100, no. 7, pp. 1539–1546, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Miele, F. Pascarella, E. Giannetti, L. Quaglietta, R. N. Baldassano, and A. Staiano, “Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis,” American Journal of Gastroenterology, vol. 104, no. 2, pp. 437–443, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. 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
  74. M. H. Floch, W. A. Walker, K. Madsen et al., “Recommendations for probiotic use—2011 update,” Journal of Clinical Gastroenterology, vol. 45, no. 3, pp. S168–S171, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. 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
  76. 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
  77. 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
  78. E. Garcia Vilela, M. De Lourdes De Abreu Ferrari, H. Oswaldo Da Gama Torres et al., “Influence of Saccharomyces boulardii on the intestinal permeability of patients with Crohn's disease in remission,” Scandinavian Journal of Gastroenterology, vol. 43, no. 7, pp. 842–848, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. 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 Scopus
  80. B. J. Meijer and L. A. Dieleman, “Probiotics in the treatment of human inflammatory bowel diseases: update 2011,” Journal of Clinical Gastroenterology, vol. 45, no. 3, pp. S139–S144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. J. O. Lindsay, K. Whelan, A. J. Stagg et al., “Clinical, microbiological, and immunological effects of fructo-oligosaccharide in patients with Crohn's disease,” Gut, vol. 55, no. 3, pp. 348–355, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. J. L. Benjamin, C. R. H. Hedin, A. Koutsoumpas et al., “Randomised, double-blind, placebo-controlled trial of fructo- oligosaccharides in active Crohn's disease,” Gut, vol. 60, no. 7, pp. 923–929, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. T. Bamba, O. Kanauchi, A. Andoh, and Y. Fujiyama, “A new prebiotic from germinated barley for nutraceutical treatment of ulcerative colitis,” Journal of Gastroenterology and Hepatology, vol. 17, no. 8, pp. 818–824, 2002. View at Publisher · View at Google Scholar · View at Scopus
  84. O. Kanauchi, T. Suga, M. Tochihara et al., “Treatment of ulcerative colitis by feeding with germinated barley foodstuff: first report of a multicenter open control trial,” Journal of Gastroenterology, vol. 37, no. 14, pp. 67–72, 2002. View at Scopus
  85. C. Hallert, M. Kaldma, and B.-G. Petersson, “Ispaghula husk may relieve gastrointestinal symptoms in ulcerative colitis in remission,” Scandinavian Journal of Gastroenterology, vol. 26, no. 7, pp. 747–750, 1991. View at Scopus
  86. F. Casellas, N. Borruel, A. Torrejón et al., “Oral oligofructose-enriched inulin supplementation in acute ulcerative colitis is well tolerated and associated with lowered faecal calprotectin,” Alimentary Pharmacology and Therapeutics, vol. 25, no. 9, pp. 1061–1067, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. S. J. Langlands, M. J. Hopkins, N. Coleman, and J. H. Cummings, “Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel,” Gut, vol. 53, no. 11, pp. 1610–1616, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Videla, J. Vilaseca, M. Antolín et al., “Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat,” American Journal of Gastroenterology, vol. 96, no. 5, pp. 1486–1493, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Winkler, R. Butler, and E. Symonds, “Fructo-oligosaccharide reduces inflammation in a dextran sodium sulphate mouse model of colitis,” Digestive Diseases and Sciences, vol. 52, no. 1, pp. 52–58, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Cherbut, C. Michel, and G. Lecannu, “The prebiotic characteristics of fructooligosaccharides are necessary for reduction of TNBS-induced colitis in rats,” Journal of Nutrition, vol. 133, no. 1, pp. 21–27, 2003. View at Scopus
  91. D. Camuesco, L. Peran, M. Comalada et al., “Preventative effects of lactulose in the trinitrobenzenesulphonic acid model of rat colitis,” Inflammatory Bowel Diseases, vol. 11, no. 3, pp. 265–271, 2005. View at Publisher · View at Google Scholar · View at Scopus