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Evidence-Based Complementary and Alternative Medicine
Volume 2016, Article ID 9048574, 16 pages
http://dx.doi.org/10.1155/2016/9048574
Research Article

Probiotics and the Microbiome in Celiac Disease: A Randomised Controlled Trial

1Faculty of Pharmacy, University of Sydney, Sydney, NSW 2006, Australia
2NatMed-Research, Division of Research, Southern Cross University, Military Road, Lismore, NSW 2480, Australia
3University Centre for Rural Health, School of Public Health, University of Sydney, 61 Uralba Street, Lismore, NSW 2480, Australia

Received 2 April 2016; Accepted 22 June 2016

Academic Editor: Toku Takahashi

Copyright © 2016 Joanna Harnett 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. J. M. Laparra and Y. Sanz, “Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion,” Journal of Cellular Biochemistry, vol. 109, no. 4, pp. 801–807, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. J. M. Laparra, M. Olivares, O. Gallina, and Y. Sanz, “Bifidobacterium longum CECT 7347 modulates immune responses in a gliadin-induced enteropathy animal model,” PLoS ONE, vol. 7, no. 2, Article ID e30744, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. I. Nadal, E. Donant, C. Ribes-Koninckx, M. Calabuig, and Y. Sanz, “Imbalance in the composition of the duodenal microbiota of children with coeliac disease,” Journal of Medical Microbiology, vol. 56, no. 12, pp. 1669–1674, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. M. C. Collado, E. Donat, C. Ribes-Koninckx, M. Calabuig, and Y. Sanz, “Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease,” Journal of Clinical Pathology, vol. 62, no. 3, pp. 264–269, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. C. Collado, M. Calabuig, and Y. Sanz, “Differences between the fecal microbiota of coeliac infants and healthy controls,” Current Issues in Intestinal Microbiology, vol. 8, no. 1, pp. 9–14, 2007. View at Google Scholar · View at Scopus
  6. E. Sánchez, I. Nadal, E. Donat, C. Ribes-Koninckx, M. Calabuig, and Y. Sanz, “Reduced diversity and increased virulence-gene carriage in intestinal enterobacteria of coeliac children,” BMC Gastroenterology, vol. 8, article 50, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. G. De Palma, I. Nadal, M. Medina et al., “Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children,” BMC Microbiology, vol. 10, no. 1, article 63, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Sánchez, E. Donat, C. Ribes-Koninckx, M. Calabuig, and Y. Sanz, “Intestinal Bacteroides species associated with coeliac disease,” Journal of Clinical Pathology, vol. 63, no. 12, pp. 1105–1111, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Cheng, M. Kalliomäki, H. G. H. J. Heilig et al., “Duodenal microbiota composition and mucosal homeostasis in pediatric celiac disease,” BMC Gastroenterology, vol. 13, no. 1, article 113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Wacklin, P. Laurikka, K. Lindfors et al., “Altered Duodenal microbiota composition in celiac disease patients suffering from persistent symptoms on a long-term gluten-free diet,” American Journal of Gastroenterology, vol. 109, no. 12, pp. 1933–1941, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Nistal, A. Caminero, A. R. Herrán et al., “Differences of small intestinal bacteria populations in adults and children with/without celiac disease: effect of age, gluten diet, and disease,” Inflammatory Bowel Diseases, vol. 18, no. 4, pp. 649–656, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Lionetti and C. Catassi, “New clues in celiac disease epidemiology, pathogenesis, clinical manifestations, and treatment,” International Reviews of Immunology, vol. 30, no. 4, pp. 219–231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. G. De Palma, J. Cinova, R. Stepankova, L. Tuckova, and Y. Sanz, “Pivotal advance: bifidobacteria and gram-negative bacteria differentially influence immune responses in the proinflammatory milieu of celiac disease,” Journal of Leukocyte Biology, vol. 87, no. 5, pp. 765–778, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Lindfors, T. Blomqvist, K. Juuti-Uusitalo et al., “Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture,” Clinical and Experimental Immunology, vol. 152, no. 3, pp. 552–558, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Smecuol, H. J. Hwang, E. Sugai et al., “Exploratory, randomized, double-blind, placebo-controlled study on the effects of bifidobacterium infantis natren life start strain super strain in active celiac disease,” Journal of Clinical Gastroenterology, vol. 47, no. 2, pp. 139–147, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. D. Angelis, C. G. Rizzello, A. Fasano et al., “VSL#3 probiotic preparation has the capacity to hydrolyze gliadin polypeptides responsible for Celiac Sprue,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1762, no. 1, pp. 80–93, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. H. E. Mardini and A. Y. Grigorian, “Probiotic mix VSL#3 is effective adjunctive therapy for mild to moderately active ulcerative colitis: a meta-analysis,” Inflammatory Bowel Diseases, vol. 20, no. 9, pp. 1562–1567, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Shen, Z.-X. Zuo, and A.-P. Mao, “Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn's disease, and pouchitis: meta-analysis of randomized controlled trials,” Inflammatory Bowel Diseases, vol. 20, no. 1, pp. 21–35, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Stewart, B. Crumley, and K. Walton, “Effects of probiotic VSL#3 on cytokine and tight junction protein expression in intestinal epithelial cells,” The FASEB Journal, vol. 29, no. 1, supplement, Article ID 1010.4, 2015. View at Google Scholar
  20. D. L. Scott, J. A. Bralley, and J. M. George, “Process and method for monitoring gastrointestinal microbiota,” Google Patents, 2012.
  21. H. L. MacGillivray, “Skewness and asymmetry: measures and orderings,” The Annals of Statistics, vol. 14, no. 3, pp. 994–1011, 1986. View at Publisher · View at Google Scholar · View at MathSciNet
  22. W. Häuser, J. Gold, A. Stallmach, W. F. Caspary, and J. Stein, “Development and validation of the Celiac Disease Questionnaire (CDQ), a disease-specific health-related quality of life measure for adult patients with celiac disease,” Journal of Clinical Gastroenterology, vol. 41, no. 2, pp. 157–166, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Bibiloni, R. N. Fedorak, G. W. Tannock et al., “VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis,” The American Journal of Gastroenterology, vol. 100, no. 7, pp. 1539–1546, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. 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
  25. P. H. R. Green and C. Cellier, “Celiac disease,” The New England Journal of Medicine, vol. 357, no. 17, pp. 1731–1743, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Sainsbury, D. S. Sanders, and A. C. Ford, “Prevalence of irritable bowel syndrome-type symptoms in patients with celiac disease: a meta-analysis,” Clinical Gastroenterology and Hepatology, vol. 11, no. 4, pp. 359–365, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Marasco, A. Colecchia, and D. Festi, “Dysbiosis in celiac disease patients with persistent symptoms on gluten-free diet: a condition similar to that present in irritable bowel syndrome patients?” The American Journal of Gastroenterology, vol. 110, no. 4, p. 598, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Tursi, G. Brandimarte, and G. Giorgetti, “High prevalence of small intestinal bacterial overgrowth in celiac patients with persistence of gastrointestinal symptoms after gluten withdrawal,” American Journal of Gastroenterology, vol. 98, no. 4, pp. 839–843, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. S. J. Shepherd, F. C. Parker, J. G. Muir, and P. R. Gibson, “Dietary triggers of abdominal symptoms in patients with irritable bowel syndrome: randomized placebo-controlled evidence,” Clinical Gastroenterology and Hepatology, vol. 6, no. 7, pp. 765–771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Stasi, I. Marafini, R. Caruso et al., “Frequency and cause of persistent symptoms in celiac disease patients on a long-term gluten-free diet,” Journal of Clinical Gastroenterology, vol. 50, no. 3, pp. 239–243, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. W. C. Chen and E. M. M. Quigley, “Probiotics, prebiotics & synbiotics in small intestinal bacterial overgrowth: opening up a new therapeutic horizon!,” The Indian Journal of Medical Research, vol. 140, no. 5, pp. 582–584, 2014. View at Google Scholar · View at Scopus
  32. C. C. Almeida, S. L. S. Lorena, C. R. Pavan, H. M. I. Akasaka, and M. A. Mesquita, “Beneficial effects of long-term consumption of a probiotic combination of Lactobacillus casei Shirota and Bifidobacterium breve Yakult may persist after suspension of therapy in lactose-intolerant patients,” Nutrition in Clinical Practice, vol. 27, no. 2, pp. 247–251, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. R. del Campo, M. Garriga, A. Pérez-Aragón et al., “Improvement of digestive health and reduction in proteobacterial populations in the gut microbiota of cystic fibrosis patients using a Lactobacillus reuteri probiotic preparation: a double blind prospective study,” Journal of Cystic Fibrosis, vol. 13, no. 6, pp. 716–722, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Pedersen, N. N. Andersen, Z. Végh et al., “Ehealth: low FODMAP diet vs Lactobacillus rhamnosus GG in irritable bowel syndrome,” World Journal of Gastroenterology, vol. 20, no. 43, pp. 16215–16226, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Corridoni, L. Pastorelli, B. Mattioli et al., “Probiotic bacteria regulate intestinal epithelial permeability in experimental ileitis by a TNF-dependent mechanism,” PLoS ONE, vol. 7, no. 7, Article ID e42067, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. M. H. Floch, “Recommendations for probiotic use in humans—a 2014 update,” Pharmaceuticals, vol. 7, no. 10, pp. 999–1007, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Sanz, E. Sánchez, M. Marzotto, M. Calabuig, S. Torriani, and F. Dellaglio, “Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis,” FEMS Immunology and Medical Microbiology, vol. 51, no. 3, pp. 562–568, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. C. J. Smith and A. M. Osborn, “Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology,” FEMS Microbiology Ecology, vol. 67, no. 1, pp. 6–20, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. 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
  40. 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
  41. A. Sood, V. Midha, G. K. Makharia et al., “The probiotic preparation, VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis,” Clinical Gastroenterology and Hepatology, vol. 7, no. 11, pp. 1202–1209, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. J.-F. Turcotte and H. Q. Huynh, “Treatment with the probiotic VSL#3 as an adjunctive therapy in relapsing mild-to-moderate ulcerative colitis significantly reduces ulcerative colitis disease activity,” Evidence-Based Medicine, vol. 16, no. 4, pp. 108–109, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. M. L. Ritchie and T. N. Romanuk, “A meta-analysis of probiotic efficacy for gastrointestinal diseases,” PLoS ONE, vol. 7, no. 4, Article ID e34938, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Bezkorovainy, “Probiotics: determinants of survival and growth in the gut,” The American Journal of Clinical Nutrition, vol. 73, no. 2, pp. 399s–405s, 2001. View at Google Scholar · View at Scopus
  45. S. Stummer, S. Salar-Behzadi, F. M. Unger, S. Oelzant, M. Penning, and H. Viernstein, “Application of shellac for the development of probiotic formulations,” Food Research International, vol. 43, no. 5, pp. 1312–1320, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. T. A. Tompkins, I. Mainville, and Y. Arcand, “The impact of meals on a probiotic during transit through a model of the human upper gastrointestinal tract,” Beneficial Microbes, vol. 2, no. 4, pp. 295–303, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. R. L. Mones, A. Yankah, D. Duelfer, R. Bustami, and G. Mercer, “Disaccharidase deficiency in pediatric patients with celiac disease and intact villi,” Scandinavian Journal of Gastroenterology, vol. 46, no. 12, pp. 1429–1434, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. 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
  49. 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
  50. A. Rehman, F.-A. Heinsen, M. E. Koenen et al., “Effects of probiotics and antibiotics on the intestinal homeostasis in a computer controlled model of the large intestine,” BMC Microbiology, vol. 12, article 47, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Malfertheiner, F. Megraud, C. A. O'Morain et al., “Management of Helicobacter pylori infection—the Maastricht IV/Florence consensus report,” Gut, vol. 61, no. 5, pp. 646–664, 2012. View at Publisher · View at Google Scholar
  52. M. R. Amieva and E. M. El-Omar, “Host-bacterial interactions in Helicobacter pylori infection,” Gastroenterology, vol. 134, no. 1, pp. 306–323, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. G. R. Norman, J. A. Sloan, and K. W. Wyrwich, “Interpretation of changes in health-related quality of life the remarkable universality of half a standard deviation,” Medical Care, vol. 41, no. 5, pp. 582–592, 2003. View at Google Scholar · View at Scopus