Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 505878, 15 pages
http://dx.doi.org/10.1155/2015/505878
Review Article

The Role of Probiotic Lactic Acid Bacteria and Bifidobacteria in the Prevention and Treatment of Inflammatory Bowel Disease and Other Related Diseases: A Systematic Review of Randomized Human Clinical Trials

1Department of Biochemistry & Molecular Biology I, School of Sciences, University of Granada, 18071 Granada, Spain
2Institute of Nutrition & Food Technology “José Mataix”, Biomedical Research Center, University of Granada, 18100 Armilla, Spain
3Department of Biochemistry & Molecular Biology II, School of Pharmacy, University of Granada, 18071 Granada, Spain

Received 5 July 2014; Revised 4 September 2014; Accepted 12 September 2014

Academic Editor: Clara G. de los Reyes-Gavilán

Copyright © 2015 Maria Jose Saez-Lara 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. D. J. Mulder, A. J. Noble, C. J. Justinich, and J. M. Duffin, “A tale of two diseases: The history of inflammatory bowel disease,” Journal of Crohn's and Colitis, vol. 8, no. 5, pp. 341–348, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Wijmenga, “Expressing the differences between Crohn disease and ulcerative colitis,” PLoS Medicine, vol. 2, no. 8, article e230, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. D. L. Topping and P. M. Clifton, “Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides,” Physiological Reviews, vol. 81, no. 3, pp. 1031–1064, 2001. View at Google Scholar · View at Scopus
  4. A. L. Kau, P. P. Ahern, N. W. Griffin, A. L. Goodman, and J. I. Gordon, “Human nutrition, the gut microbiome and the immune system,” Nature, vol. 474, no. 7351, pp. 327–336, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Bermudez-Brito, J. Plaza-Díaz, S. Muñoz-Quezada, C. Gómez-Llorente, and A. Gil, “Probiotic mechanisms of action,” Annals of Nutrition and Metabolism, vol. 61, no. 2, pp. 160–174, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Fontana, M. Bermudez-Brito, J. Plaza-Diaz, S. Muñoz-Quezada, and A. Gil, “Sources, isolation, characterisation and evaluation of probiotics,” The British Journal of Nutrition, vol. 109, no. supplement 2, pp. S35–S50, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Mattu and A. Chauhan, “Lactic acid bacteria and its use in probiotics,” Journal of Bioremediation & Biodegradation, vol. 4, article e140, p. 8, 2013. View at Publisher · View at Google Scholar
  8. P. Tian, B. Xu, and G. An, “A new therapies for intestinal flora imbalance used ampicillin resistant probiotics,” Journal of Microbiology and Biotechnology, vol. 24, no. 9, pp. 1300–1312, 2014. View at Google Scholar
  9. E. Mani-López, E. Palou, and A. López-Malo, “Probiotic viability and storage stability of yogurts and fermented milks prepared with several mixtures of lactic acid bacteria,” Journal of Dairy Science, vol. 97, no. 5, pp. 2578–2590, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. O. C. Thompson-Chagoyán, J. Maldonado, and A. Gil, “Colonization and impact of disease and other factors on intestinal microbiota,” Digestive Diseases and Sciences, vol. 52, no. 9, pp. 2069–2077, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. O. C. Thompson-Chagoyán, J. Maldonado, and A. Gil, “Aetiology of inflammatory bowel disease (IBD): role of intestinal microbiota and gut-associated lymphoid tissue immune response,” Clinical Nutrition, vol. 24, no. 3, pp. 339–352, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. FAO/WHO, Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria, 2001, ftp://ftp.fao.org/docrep/fao/009/a0512e/a0512e00.pdf.
  13. D. Moher, A. Liberati, J. Tetzlaff, D. G. Altman, and PRISMA Group, “Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement,” PLoS Medicine, vol. 6, no. 6, Article ID e1000097, 2009. View at Google Scholar
  14. P. Jantchou, S. Morois, F. Clavel-Chapelon, M.-C. Boutron-Ruault, and F. Carbonnel, “Animal protein intake and risk of inflammatory bowel disease: the E3N prospective study,” The American Journal of Gastroenterology, vol. 105, no. 10, pp. 2195–2201, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Tragnone, D. Valpiani, F. Miglio et al., “Dietary habits as risk factors for inflammatory bowel disease,” European Journal of Gastroenterology and Hepatology, vol. 7, no. 1, pp. 47–51, 1995. View at Google Scholar · View at Scopus
  16. J. K. Hou, B. Abraham, and H. El-Serag, “Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature,” The American Journal of Gastroenterology, vol. 106, no. 4, pp. 563–573, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Kanai, K. Matsuoka, M. Naganuma, A. Hayashi, and T. Hisamatsu, “Diet, microbiota, and inflammatory bowel disease: lessons from Japonese foods,” The Korean Journal of Internal Medicine, vol. 29, no. 4, pp. 409–415, 2014. View at Google Scholar
  18. C. Zallot, D. Quilliot, J.-B. Chevaux et al., “Dietary beliefs and behavior among inflammatory bowel disease patients,” Inflammatory Bowel Diseases, vol. 19, no. 1, pp. 66–72, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Hwang, V. Ross, and U. Mahadevan, “Popular exclusionary diets for inflammatory bowel disease: the search for a dietary culprit,” Inflammatory Bowel Diseases, vol. 20, no. 4, pp. 732–741, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. M. B. Lopes, R. Rocha, A. C. Lyra et al., “Restriction of dairy products; a reality in inflammatory bowel disease patients,” Nutricion Hospitalaria, vol. 29, no. 3, pp. 575–581, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. C. E. G. M. Spooren, M. J. Pierik, M. P. Zeegers, E. J. M. Feskens, A. A. M. Masclee, and D. M. A. E. Jonkers, “The association of diet with onset and relapse in patients with inflammatory bowel disease,” Alimentary Pharmacology and Therapeutics, vol. 38, no. 10, pp. 1172–1187, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. C. R. H. Hedin, M. Mullard, E. Sharratt et al., “Probiotic and prebiotic use in patients with inflammatory bowel disease: a case-control study,” Inflammatory Bowel Diseases, vol. 16, no. 12, pp. 2099–2108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. 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,” The American Journal of Gastroenterology, vol. 104, no. 2, pp. 437–443, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. K. O. Laake, A. Bjørneklett, G. Aamodt et al., “Outcome of four weeks' intervention with probiotics on symptoms and endoscopic appearance after surgical reconstruction with a J-configurated ileal-pouch-anal-anastomosis in ulcerative colitis,” Scandinavian Journal of Gastroenterology, vol. 40, no. 1, pp. 43–51, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. M. E. Sanders and J. Huis In't Veld, “Bringing a probiotic-containing functional food to the market: microbiological, product, regulatory and labeling issues,” Antonie van Leeuwenhoek, vol. 76, no. 1–4, pp. 293–315, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Saggioro, “Probiotics in the treatment of irritable bowel syndrome,” Journal of Clinical Gastroenterology, vol. 38, no. 6, pp. S104–S106, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Mercer, M. A. Brinich, G. Geller et al., “How patients view probiotics: findings from a multicenter study of patients with inflammatory bowel disease and irritable bowel syndrome,” Journal of Clinical Gastroenterology, vol. 46, no. 2, pp. 138–144, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Rauch and S. V. Lynch, “The potential for probiotic manipulation of the gastrointestinal microbiome,” Current Opinion in Biotechnology, vol. 23, no. 2, pp. 192–201, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. J. A. Hawrelak and S. P. Myers, “The causes of intestinal dysbiosis: a review,” Alternative Medicine Review, vol. 9, no. 2, pp. 180–197, 2004. View at Google Scholar · View at Scopus
  30. R. E. Click, “Successful treatment of asymptomatic or clinically terminal bovine Mycobacterium avium subspecies paratuberculosis infection (Johne's disease) with the bacterium Dietzia used as a probiotic alone or in combination with dexamethasone: adaption to chronic human diarrheal diseases,” Virulence, vol. 2, no. 2, pp. 131–143, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Patricio Retamal, M. Caroll Beltrán, P. Pedro Abalos, P. Rodrigo Quera, and R. Marcela Hermoso, “Possible association between Mycobacterium avium subsp paratuberculosis infection and crohn's disease,” Revista Medica de Chile, vol. 139, no. 6, pp. 794–801, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. 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
  33. A. A. Nanji and F. G. Denardi, “Primary adult lactose intolerance protects against development of inflammatory bowel disease,” Medical Hypotheses, vol. 19, no. 1, pp. 1–6, 1986. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Saadatzadeh, F. Atyabi, M. R. Fazeli et al., “Biochemical and pathological evidences on the benefit of a new biodegradable nanoparticles of probiotic extract in murine colitis,” Fundamental and Clinical Pharmacology, vol. 26, no. 5, pp. 589–598, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Cario, “Toll-like receptors in inflammatory bowel diseases: a decade later,” Inflammatory Bowel Diseases, vol. 16, no. 9, pp. 1583–1597, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. S. de Kivit, M. C. Tobin, C. B. Forsyth, A. Keshavarzian, and A. L. Landay, “Regulation of intestinal immune responses through TLR activation: implications for pro- and prebiotics,” Frontiers in Immunology, vol. 5, p. 60, 2014. View at Google Scholar
  37. L. H. Zeuthen, L. N. Fink, and H. Frøkiær, “Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells,” Immunology, vol. 124, no. 4, pp. 489–502, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. E. R. Mann and X. Li, “Intestinal antigen-presenting cells in mucosal immune homeostasis: crosstalk between dendritic cells, macrophages and B-cells,” World Journal of Gastroenterology, vol. 20, no. 29, pp. 9653–9664, 2014. View at Google Scholar
  39. M. Bermudez-Brito, S. Muñoz-Quezada, C. Gomez-Llorente et al., “Human intestinal dendritic cells decrease cytokine release against Salmonella infection in the presence of Lactobacillus paracasei upon TLR activation,” PLoS ONE, vol. 7, no. 8, Article ID e43197, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Bermudez-Brito, S. Muñoz-Quezada, C. Gomez-Llorente et al., “Cell-free culture supernatant of Bifidobacterium breve CNCM I-4035 decreases pro-inflammatory cytokines in human dendritic cells challenged with Salmonella typhi through TLR activation,” PLoS ONE, vol. 8, no. 3, Article ID e59370, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Lorea Baroja, P. V. Kirjavainen, S. Hekmat, and G. Reid, “Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients,” Clinical and Experimental Immunology, vol. 149, no. 3, pp. 470–479, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Di Giacinto, M. Marinaro, M. Sanchez, W. Strober, and M. Boirivant, “Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-β-bearing regulatory cells,” The Journal of Immunology, vol. 174, no. 6, pp. 3237–3246, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. M. S. Longhi, A. Moss, A. Bai et al., “Characterization of human CD39+ Th17 cells with suppressor activity and modulation in inflammatory bowel disease,” PLoS ONE, vol. 9, no. 2, Article ID e87956, 2014. View at Publisher · View at Google Scholar
  44. 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
  45. J. A. Katz, “Treatment of inflammatory bowel disease with corticosteroids,” Gastroenterology Clinics of North America, vol. 33, no. 2, pp. 171–189, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Friedman, “General principles of medical therapy of inflammatory bowel disease,” Gastroenterology Clinics of North America, vol. 33, no. 2, pp. 191–208, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. R. De Franchis, P. Omodei, T. Ranzi et al., “Controlled trial of oral 5-aminosalicylic acid for the prevention of early relapse in Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 11, no. 5, pp. 845–852, 1997. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Prantera, F. Pallone, G. Brunetti, M. Cottone, and M. Miglioli, “Oral 5-aminosalicylic acid (asacol) in the maintenance treatment of Crohn's disease,” Gastroenterology, vol. 103, no. 2, pp. 363–368, 1992. View at Google Scholar · View at Scopus
  49. C. Prantera and M. L. Scribano, “Probiotics and Crohn’s disease,” Digestive and Liver Disease, vol. 34, no. 2, pp. S66–S67, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Prantera, M. L. Scribano, G. Falasco, A. Andreoli, and C. Luzi, “Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn's disease: a randomised controlled trial with Lactobacillus GG,” Gut, vol. 51, no. 3, pp. 405–409, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. 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
  52. 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
  53. P. Marteau, M. Lémann, P. Seksik et al., “Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn's disease: a randomised, double blind, placebo controlled GETAID trial,” Gut, vol. 55, no. 6, pp. 842–847, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. A. van Gossum, O. Dewit, E. Louis et al., “Multicenter randomized-controlled clinical trial of probiotics (Lactobacillus johnsonii. LA1) on early endoscopic recurrence of Crohn’s disease after ileo-caecal resection,” Inflammatory Bowel Diseases, vol. 13, no. 2, pp. 135–142, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Fujimori, A. Tatsuguchi, K. Gudis et al., “High dose probiotic and prebiotic cotherapy for remission induction of active Crohn's disease,” Journal of Gastroenterology and Hepatology, vol. 22, no. 8, pp. 1199–1204, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. I. Chermesh, A. Tamir, R. Reshef et al., “Failure of synbiotic 2000 to prevent postoperative recurrence of Crohn's disease,” Digestive Diseases and Sciences, vol. 52, no. 2, pp. 385–389, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Steed, G. T. MacFarlane, K. L. Blackett et al., “Clinical trial: the microbiological and immunological effects of synbiotic consumption—a randomized double-blind placebo-controlled study in active Crohn’s disease,” Alimentary Pharmacology and Therapeutics, vol. 32, no. 7, pp. 872–883, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. 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
  59. C. Ramirez-Farias, K. Slezak, Z. Fuller, A. Duncan, G. Holtrop, and P. Louis, “Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii,” The British Journal of Nutrition, vol. 101, no. 4, pp. 541–550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Ishikawa, I. Akedo, Y. Umesaki, R. Tanaka, A. Imaoka, and T. Otani, “Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis,” Journal of the American College of Nutrition, vol. 22, no. 1, pp. 56–63, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. 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,” The American Journal of Gastroenterology, vol. 105, no. 10, pp. 2218–2227, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Kato, S. Mizuno, Y. Umesaki et al., “Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis,” Alimentary Pharmacology and Therapeutics, vol. 20, no. 10, pp. 1133–1141, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. 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
  64. S. Wildt, I. Nordgaard, U. Hansen, E. Brockmann, and J. J. Rumessen, “A randomised double-blind placebo-controlled trial with Lactobacillus acidophilus La-5 and Bifidobacterium animalis subsp. lactis BB-12 for maintenance of remission in ulcerative colitis,” Journal of Crohn's and Colitis, vol. 5, no. 2, pp. 115–121, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. 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
  66. D. Groeger, L. O'Mahony, E. F. Murphy et al., “Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut,” Gut Microbes, vol. 4, no. 4, pp. 325–339, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. 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
  68. S. K. Hegazy and M. M. El-Bedewy, “Effect of probiotics on pro-inflammatory cytokines and NF-κb activation in ulcerative colitis,” World Journal of Gastroenterology, vol. 16, no. 33, pp. 4145–4151, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Oliva, G. di Nardo, F. Ferrari et al., “Randomised clinical trial: the effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis,” Alimentary Pharmacology and Therapeutics, vol. 35, no. 3, pp. 327–334, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. R. D'Incà, M. Barollo, M. Scarpa et al., “Rectal administration of Lactobacillus casei DG modifies flora composition and toll-like receptor expression in colonic mucosa of patients with mild ulcerative colitis,” Digestive Diseases and Sciences, vol. 56, no. 4, pp. 1178–1187, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. 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
  72. S. Fujimori, K. Gudis, K. Mitsui et al., “A randomized controlled trial on the efficacy of synbiotic versus probiotic or prebiotic treatment to improve the quality of life in patients with ulcerative colitis,” Nutrition, vol. 25, no. 5, pp. 520–525, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. H. Ishikawa, S. Matsumoto, Y. Ohashi et al., “Beneficial effects of probiotic Bifidobacterium and galacto-oligosaccharide in patients with ulcerative colitis: a randomized controlled study,” Digestion, vol. 84, no. 2, pp. 128–133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. 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
  75. 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
  76. 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
  77. P. Gionchetti, F. Rizzello, C. Morselli et al., “High-dose probiotics for the treatment of active pouchitis,” Diseases of the Colon and Rectum, vol. 50, no. 12, pp. 2075–2082, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. T. Kühbacher, S. J. Ott, U. Helwig et al., “Bacterial and fungal microbiota in relation to probiotic therapy (VSL#3) in pouchitis,” Gut, vol. 55, no. 6, pp. 833–841, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Pronio, C. Montesani, C. Butteroni et al., “Probiotic administration in patients with ileal pouch-anal anastomosis for ulcerative colitis is associated with expansion of mucosal regulatory cells,” Inflammatory Bowel Diseases, vol. 14, no. 5, pp. 662–668, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. N. Waugh, E. Cummins, P. Royle et al., “Faecal calprotectin testing for differentiating amongst inflammatory and non-inflammatory bowel diseases: systematic review and economic evaluation,” Health Technology Assessment, vol. 17, no. 55, pp. 1–211, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Whelan and E. M. M. Quigley, “Probiotics in the management of irritable bowel syndrome and inflammatory bowel disease,” Current Opinion in Gastroenterology, vol. 29, no. 2, pp. 184–189, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. J.-R. Malagelada, “A symptom-based approach to making a positive diagnosis of irritable bowel syndrome with constipation,” International Journal of Clinical Practice, vol. 60, no. 1, pp. 57–63, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. R. Spiller and K. Garsed, “Postinfectious irritable bowel syndrome,” Gastroenterology, vol. 136, no. 6, pp. 1979–1988, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. Y.-S. Hong, K. S. Hong, M.-H. Park et al., “Metabonomic understanding of probiotic effects in humans with irritable bowel syndrome,” Journal of Clinical Gastroenterology, vol. 45, no. 5, pp. 415–425, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Dughera, C. Elia, M. Navino et al., “Effects of symbiotic preparations on constipated irritable bowel syndrome symptoms,” Acta Biomedica de l'Ateneo Parmense, vol. 78, no. 2, pp. 111–116, 2007. View at Google Scholar · View at Scopus
  86. T. P. Kinney, “Management of ascending cholangitis,” Gastrointestinal Endoscopy Clinics of North America, vol. 17, no. 2, pp. 289–306, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. F. P. Vleggaar, J. F. Monkelbaan, and K. J. van Erpecum, “Probiotics in primary sclerosing cholangitis: a randomized placebo-controlled crossover pilot study,” European Journal of Gastroenterology and Hepatology, vol. 20, no. 7, pp. 688–692, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Shimizu, H. Iwasaki, S. Mase, and A. Yachie, “Successful treatment of primary sclerosing cholangitis with a steroid and a probiotic,” Case Reports in Gastroenterology, vol. 6, no. 2, pp. 249–253, 2012. View at Publisher · View at Google Scholar · View at Scopus