Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases

Nutrients

Volumn 9, Issue 6, 2017, Pages

  Plaza Díaz, Julio ^a,b   Ruiz Ojeda, Francisco Javier ^a,b   Vilchez Padial, Laura Maria ^a   Gil, Angel ^a,b,c  

^a UNIVERSITY OF GRANADA   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

^c Instituto de Salud Carlos III   (Spain)

Author keywords

Anti inflammatory effects; Inflammatory bowel diseases; Intestinal diseases; Probiotics

Indexed keywords

ANTIINFLAMMATORY AGENT; CYTOKINE; DEXTRAN SULFATE; MYELOPEROXIDASE; PROBIOTIC AGENT; SYNBIOTIC AGENT; TOLL LIKE RECEPTOR; TRINITROBENZENESULFONIC ACID;

APOPTOSIS; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM LONGUM; CHRONIC DISEASE; CROHN DISEASE; DOWN REGULATION; ENTEROPATHY; HISTOLOGY; HUMAN; INFLAMMATION; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS PLANTARUM; MUCUS; NONHUMAN; REVIEW; ULCERATIVE COLITIS; ANIMAL; BIFIDOBACTERIUM BREVE; DISEASE MODEL; INTESTINE; INTESTINE FLORA; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS RHAMNOSUS; MICROBIOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC);

ANIMALS; BIFIDOBACTERIUM BREVE; DISEASE MODELS, ANIMAL; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINAL DISEASES; INTESTINES; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SYNBIOTICS;

EID: 85020046878     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9060555     Document Type: Review

References (77)

1. Metchnikoff, E. The Prolongation of Life: Optimistic Studies, 1st ed., Mitchell, P.C., Ed., G.P. Putnam’s Sons: New York, NY, USA, 1908.
2. DeMorenode LeBlanc, A., LeBlanc, J.G. Effect of probiotic administration on the intestinal microbiota, current knowledge and potential applications. World J. Gastroenterol. 2014, 20, 16518-16528.
3. Fontana, L., Bermudez-Brito, M., Plaza-Diaz, J., Muñoz-Quezada, S., Gil, A. Sources, isolation, characterisation and evaluation of probiotics. Br. J. Nutr. 2013, 109, 35-50.
4. Gibson, G.R., Roberfroid, M.B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995, 125, 1401-1412.
5. Ouwehand, A.C., Salminen, S., Isolauri, E. Probiotics: An overview of beneficial effects. Antonie Van Leeuwenhoek 2002, 82, 279-289.
6. Hamilton-Miller, J.M., Gibson, G.R., Bruck, W. Some insights into the derivation and early uses of the word ‘probiotic’. Br. J. Nutr. 2003, 90, 845.
7. Food and Agriculture Organization/World Health Organization. Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria, American Cordoba Park Hotel: Cordoba, Argentina, 2001, pp. 1-2.
8. Roberfroid, M.B. Prebiotics and probiotics: are they functional foods? Am. J. Clin. Nutr. 2000, 71, 1682-1687.
9. Giahi, L., Aumueller, E., Elmadfa, I., Haslberger, A.G. Regulation of TLR4, p38 MAPkinase, IκB and miRNAs by inactivated strains of lactobacilli in human dendritic cells. Benef. Microbes 2012, 3, 91-98.
10. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., Morelli, L., Canani, R.B., Flint, H.J., Salminen, S., et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506-514.
11. Collado, M.C., Isolauri, E., Salminen, S., Sanz, Y. The impact of probiotic on gut health. Curr. Drug. Metab. 2009, 10, 68-78.
12. Plaza-Díaz, J., Robles-Sánchez, C., Abadía-Molina, F., Morón-Calvente, V., Sáez-Lara, M.J., Ruiz-Bravo, A., Jiménez-Valera, M., Gil, A., Gómez-Llorente, C., Fontana, L. Adamdec1, Ednrb and Ptgs1/Cox1, inflammation genes upregulated in the intestinalmucosa of obese rats, are downregulated by three probiotic strains. Sci. Rep. 2017, 7, 1939.
13. Bermudez-Brito, M., Plaza-Díaz, J., Muñoz-Quezada, S., Gómez-Llorente, C., Gil, A. Probiotic mechanisms of action. Ann. Nutr. Metab. 2012, 61, 160-174.
14. Plaza-Díaz, J., Fernandez-Caballero, J.Á., Chueca, N., Garcia, F., Gómez-Llorente, C., Sáez-Lara, M.J., Fontana, L., Gil, A. Pyrosequencing analysis reveals changes in intestinal microbiota of healthy adults who received a daily dose of immunomodulatory probiotic strains. Nutrients 2015, 7, 3999-4015.
15. Plaza-Diaz, J., Gomez-Llorente, C., Abadia-Molina, F., Saez-Lara, M.J., Campaña-Martin, L., Muñoz-Quezada, S., Romero, F., Gil, A., Fontana, L. Effects of Lactobacillus paracasei CNCM I-4034, Bifidobacterium breve CNCM I-4035 and Lactobacillus rhamnosus CNCM I-4036 on hepatic steatosis in Zucker rats. PLoS ONE 2014, 9, e98401.
16. Plaza-Diaz, J., Gomez-Llorente, C., Campaña-Martin, L., Matencio, E., Ortuño, I., Martínez-Silla, R., Gomez-Gallego, C., Periago, M.J., Ros, G., Chenoll, E., et al. Safety and immunomodulatory effects of three probiotic strains isolated from the feces of breast-fed infants in healthy adults: SETOPROB study. PLoS ONE 2013, 8, e78111.
17. Pineiro, M., Asp, N.G., Reid, G., Macfarlane, S., Morelli, L., Brunser, O., Tuohy, K. FAO Technical meeting on prebiotics. J. Clin. Gastroenterol. 2008, 42, S156-S159.
18. Sáez-Lara, M.J., Robles-Sanchez, C., Ruiz-Ojeda, F.J., Plaza-Diaz, J., Gil, A. Effects of Probiotics and Synbiotics on Obesity, Insulin Resistance Syndrome, Type 2 Diabetes and Non-Alcoholic Fatty Liver Disease: A Review of Human Clinical Trials. Int. J. Mol. Sci. 2016, 17, 928.
19. Tojo, R., Suárez, A., Clemente, M.G., Delos Reyes-Gavilán, C.G., Margolles, A., Gueimonde, M., Ruas-Madiedo, P. Intestinal microbiota in health and disease: Role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 2014, 20, 15163-15176.
20. Upadhyay, N., Moudgal, V. Probiotics: A Review. J. Clin. Outcomes Manag. 2012, 19, 76-84.
21. Molodecky, N.A., Soon, I.S., Rabi, D.M., Ghali, W.A., Ferris, M., Chernoff, G., Benchimol, E.I., Panaccione, R., Ghosh, S., Barkema, H.W., et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012, 142, 46-54.
22. Wedlake, L., Slack, N., Andreyev, H.J., Whelan, K. Fiber in the treatment and maintenance of inflammatory bowel disease: A systematic review of randomized controlled trials. Inflamm. Bowel Dis. 2014, 20, 576-586.
23. Podolsky, D.K. Inflammatory bowel disease. N. Engl. J. Med. 2002, 347, 417-429.
24. Münch, A., Aust, D., Bohr, J., Bonderup, O., Fernández Bañares, F., Hjortswang, H., Madisch, A., Munck, L.K., Ström, M., Tysk, C., et al. Microscopic colitis: Current status, present and future challenges: Statements of the European Microscopic Colitis Group. J. Crohns Colitis. 2012, 6, 932-945.
25. Kaser, A., Zeissig, S., Blumberg, R.S. Inflammatory bowel disease. Annu. Rev. Immunol. 2010, 28, 573-621.
26. Abraham, C., Cho, J.H. Inflammatory bowel disease. N. Engl. J. Med. 2009, 361, 2066-2078.
27. Derikx, L.A., Dieleman, L.A., Hoentjen, F. Probiotics and prebiotics in ulcerative colitis. Best Pract. Res. Clin. Gastroenterol. 2016, 30, 55-71.
28. Magro, F., Gionchetti, P., Eliakim, R., Ardizzone, S., Armuzzi, A., Barreiro-de Acosta, M., Burisch, J., Gecse, K.B., Hart, A.L., Hindryckx, P., et al. Third European Evidence-Based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders. J. Crohns Colitis. 2017, 11, 1-39.
29. Ringel, Y., Carroll, I.M. Alterations in the intestinal microbiota and functional bowel symptoms. Gastrointest. Endosc. Clin. N. Am. 2009, 19, 141-150.
30. O’Toole, P.W., Cooney, J.C. Probiotic bacteria influence the composition and function of the intestinal microbiota. Interdiscip. Perspect. Infect. Dis. 2008, 2008.
31. Butler, M., Ng, C.Y., Van Heel, D.A., Lombardi, G., Lechler, R., Playford, R.J., Ghosh, S. Modulation of dendritic cell phenotype and function in an in vitro model of the intestinal epithelium. Eur. J. Immunol. 2006, 36, 864-874.
32. Mann, E.R., Bernardo, D., Ng, S.C., Rigby, R.J., Al-Hassi, H.O., Landy, J., Peake, S.T.C., Spranger, H., English, N.R., Thomas, L.V., et al. Human gut dendritic cells drive aberrant gut-specific T-cell responses in ulcerative colitis, characterized by increased IL-4 production and loss of IL-22 and IFN-. Inflamm. Bowel Dis. 2014, 20, 2299-2307.
33. Mann, E.R., You, J., Horneffer-vander Sluis, V., Bernardo, D., Omar Al-Hassi, H., Landy, J., Peake, S.T., Thomas, L.V., Tee, C.T., Lee, G.H., et al. Dysregulated circulating dendritic cell function in ulcerative colitis is partially restored by probiotic strain Lactobacillus casei Shirota. Mediators Inflamm. 2013, 2013, 573-576.
34. Gómez-Llorente, C., Muñoz, S., Gil, A. Role of toll-like receptors in the development of immunotolerance mediated by probiotics. Proc. Nutr. Soc. 2010, 69, 381-389.
35. Wu, Y., Zhu, C., Chen, Z., Chen, Z., Zhang, W., Ma, X., Wang, L., Yang, X., Jiang, Z. Protective effects of Lactobacillus plantarum on epithelial barrier disruption caused by enterotoxigenic Escherichia coli in intestinal porcine epithelial cells. Vet. Immunol. Immunopathol. 2016, 172, 55-63.
36. Wachi, S., Kanmani, P., Tomosada, Y., Kobayashi, H., Yuri, T., Egusa, S., Shimazu, T., Suda, Y., Aso, H., Sugawara, M., et al. Lactobacillus delbrueckii TUA4408L and its extracellular polysaccharides attenuate enterotoxigenic Escherichia coli-induced inflammatory response in porcine intestinal epitheliocytes via Toll-like receptor-2 and 4. Mol. Nutr. Food Res. 2014, 58, 2080-2093.
37. Prisciandaro, L.D., Geier, M.S., Chua, A.E., Butler, R.N., Cummins, A.G., Sander, G.R., Howarth, G.S. Probiotic factors partially prevent changes to caspases 3 and 7 activation and transepithelial electrical resistance in a model of 5-fluorouracil-induced epithelial cell damage. Support Care Cancer 2012, 20, 3205-3210.
38. Bermudez-Brito, M., Muñoz-Quezada, S., Gomez-Llorente, C., Romero, F., Gil, A. Lactobacillus rhamnosus and its cell-free culture supernatant differentially modulate inflammatory biomarkers in Escherichia coli-challenged human dendritic cells. Br. J. Nutr. 2014, 111, 1727-1737.
39. Bermudez-Brito, M., Muñoz-Quezada, S., Gomez-Llorente, C., Matencio, E., Bernal, M.J., Romero, F., Gil, A. 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 2013, 8, e59370.
40. Bermudez-Brito, M., Muñoz-Quezada, S., Gomez-Llorente, C., Matencio, E., Bernal, M.J., Romero, F., Gil, A. Human intestinal dendritic cells decrease cytokine release against Salmonella infection in the presence of Lactobacillus paracasei upon TLR activation. PLoS ONE 2012, 7, e43197.
41. Abdelouhab, K., Rafa, H., Toumi, R., Bouaziz, S., Medjeber, O., Touil-Boukoffa, C. Mucosal intestinal alteration in experimental colitis correlates with nitric oxide production by peritoneal macrophages: Effect of probiotics and prebiotics. Immunopharmacol. Immunotoxicol. 2012, 34, 590-597.
42. Toumi, R., Abdelouhab, K., Rafa, H., Soufli, I., Raissi-Kerboua, D., Djeraba, Z., Touil-Boukoffa, C. Beneficial role of the probiotic mixture Ultrabiotique on maintaining the integrity of intestinal mucosal barrier in DSS-induced experimental colitis. Immunopharmacol. Immunotoxicol. 2013, 35, 403-409.
43. Atkins, H.L., Geier, M.S., Prisciandaro, L.D., Pattanaik, A.K., Forder, R.E., Turner, M.S., Howarth, G.S. Effects of a Lactobacillus reuteri BR11 mutant deficient in the cystine-transport system in a rat model of inflammatory bowel disease. Dig. Dis. Sci. 2012, 57, 713-719.
44. Cui, Y., Wei, H., Lu, F., Liu, X., Liu, D., Gu, L., Ouyang, C. Different effects of three selected Lactobacillus strains in dextran sulfate sodium-induced colitis in BALB/c mice. PLoS ONE 2016, 11, e0148241.
45. Wong, C.C., Zhang, L., Li, Z.J., Wu, W.K., Ren, S.X., Chen, Y.C., Ng, T.B., Cho, C.H. Protective effects of cathelicidin-encoding Lactococcus lactis in murine ulcerative colitis. J. Gastroenterol. Hepatol. 2012, 27, 1205-1212.
46. Hong, Y.S., Ahn, Y.T., Park, J.C., Lee, J.H., Lee, H., Huh, C.S., Kim, D.H., Ryu, D.H., Hwang, G.S. 1H NMR-based metabonomic assessment of probiotic effects in a colitis mouse model. Arch. Pharm. Res. 2010, 33, 1091-1101.
47. Garrido-Mesa, N., Utrilla, P., Comalada, M., Zorrilla, P., Garrido-Mesa, J., Zarzuelo, A., Rodríguez-Cabezas, M.E., Gálvez, J. The association of minocycline and the probiotic Escherichia coli Nissle 1917 results in an additive beneficial effect in a DSS model of reactivated colitis in mice. Biochem. Pharmacol. 2011, 82, 1891-1900.
48. Zheng, B., van Bergenhenegouwen, J., van de Kant, H.J., Folkerts, G., Garssen, J., Vos, A.P., Morgan, M.E., Kraneveld, A.D. Specific probiotic dietary supplementation leads to different effects during remission and relapse in murine chronic colitis. Benef. Microbes 2016, 7, 205-213.
49. Talero, E., Bolivar, S., Ávila-Román, J., Alcaide, A., Fiorucci, S., Motilva, V. Inhibition of chronic ulcerative colitis-associated adenocarcinoma development in mice by VSL#3. Inflamm. Bowel. Dis. 2015, 21, 1027-1037.
50. Dai, C., Zheng, C.Q., Meng, F.J., Zhou, Z., Sang, L.X., Jiang, M. VSL#3 probiotics exerts the anti-inflammatory activity via PI3k/Akt and NF-κB pathway in rat model of DSS-induced colitis. Mol. Cell Biochem. 2013, 374, 1-11.
51. Salim, S.Y., Young, P.Y., Lukowski, C.M., Madsen, K.L., Sis, B., Churchill, T.A., Khadaroo, R.G. VSL#3 probiotics provide protection against acute intestinal ischaemia/reperfusion injury. Benef. Microbes 2013, 4, 357-365.
52. Zhang, H.L., Li, W.S., Xu, D.N., Zheng, W.W., Liu, Y., Chen, J., Qiu, Z.B., Dorfman, R.G., Zhang, J., Liu, J. Mucosa-reparing and microbiota-balancing therapeutic effect of Bacillus subtilis alleviates dextrate sulfate sodium-induced ulcerative colitis in mice. Exp. Ther. Med. 2016, 12, 2554-2562.
53. Satish Kumar, C., Kondal Reddy, K., Reddy, A.G., Vinoth, A., Ch, S.R., Boobalan, G., Rao, G.S. Protective effect of Lactobacillus plantarum 21, a probiotic on trinitrobenzenesulfonic acid-induced ulcerative colitis in rats. Int. Immunopharmacol. 2015, 25, 504-510.
54. Yang, X., Fu, Y., Liu, J., Ren, H.Y. Impact of probiotics on toll-like receptor 4 expression in an experimental model of ulcerative colitis. J. Huazhong Univ. Sci. Technol. Med. Sci. 2013, 33, 661-665.
55. Eeckhaut, V., Machiels, K., Perrier, C., Romero, C., Maes, S., Flahou, B., Steppe, M., Haesebrouck, F., Sas, B., Ducatelle, R., et al. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 2013, 62, 1745-1752.
56. Schmitz, S., Werling, D., Allenspach, K. Effects of ex-vivo and in-vivo treatment with probiotics on the inflammasome in dogs with chronic enteropathy. PLoS ONE 2015, 10, e0120779.
57. Schmitz, S., Glanemann, B., Garden, O.A., Brooks, H., Chang, Y.M., Werling, D., Allenspach, K. A prospective, randomized, blinded, placebo-controlled pilot study on the effect of Enterococcus faecium on clinical activity and intestinal gene expression in canine food-responsive chronic enteropathy. J. Vet. Intern. Med. 2015, 29, 533-543.
58. Sun, Q., Shi, Y., Wang, F., Han, D., Lei, H., Zhao, Y., Sun, Q. Study on the effects of microencapsulated Lactobacillus delbrueckii on the mouse intestinal flora. J. Microencapsul. 2015, 32, 669-676.
59. Štofilová, J., Szabadosová, V., Hrˇcková, G., Salaj, R., Bertková, I., Hijová, E., Strojný, L., Bomba, A. Co-administration of a probiotic strain Lactobacillus plantarum LS/07 CCM7766 with prebiotic inulin alleviates the intestinal inflammation in rats exposed to N,N-dimethylhydrazine. Int. Immunopharmacol. 2015, 24, 361-368.
60. Ogita, T., Bergamo, P., Maurano, F., D’Arienzo, R., Mazzarella, G., Bozzella, G., Luongo, D., Sashihara, T., Suzuki, T., Tanabe, S., et al. Modulatory activity of Lactobacillus rhamnosus OLL2838 in a mouse model of intestinal immunopathology. Immunobiology 2015, 220, 701-710.
61. Wu, S., Yoon, S., Zhang, Y.G., Lu, R., Xia, Y., Wan, J., Petrof, E.O., Claud, E.C., Chen, D., Sun, J. Vitamin D receptor pathway is required for probiotic protection in colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 309, 341-349.
62. Tamaki, H., Nakase, H., Inoue, S., Kawanami, C., Itani, T., Ohana, M., Kusaka, T., Uose, S., Hisatsune, H., Tojo, M., et al. Efficacy of probiotic treatment with Bifidobacterium longum 536 for induction of remission in active ulcerative colitis: A randomized, double-blinded, placebo-controlled multicenter trial. Dig. Endosc. 2016, 28, 67-74.
63. Yoshimatsu, Y., Yamada, A., Furukawa, R., Sono, K., Osamura, A., Nakamura, K., Aoki, H., Tsuda, Y., Hosoe, N., Takada, N., et al. Effectiveness of probiotic therapy for the prevention of relapse in patients with inactive ulcerative colitis. World J. Gastroenterol. 2015, 21, 5985-5994.
64. Krag, A., Munkholm, P., Israelsen, H., von Ryberg, B., Andersen, K.K., Bendtsen, F. Profermin is efficacious in patients with active ulcerative colitis-a randomized controlled trial. Inflamm. Bowel Dis. 2013, 19, 2584-2592.
65. Meini, S., Laureano, R., Fani, L., Tascini, C., Galano, A., Antonelli, A., Rossolini, G.M. Breakthrough Lactobacillus rhamnosus GG bacteremia associated with probiotic use in an adult patient with severe active ulcerative colitis: case report and review of the literature. Infection 2015, 43, 777-781.
66. Suskind, D.L., Namita Singh, N., Nielson, H., Wahbeh, G. Fecal microbial transplant via nasogastric tube for active pediatric ulcerative colitis. J. Pediatr. Gastroenterol. Nutr. 2015, 60, 27-29.
67. Paramsothy, S., Kamm, M.A., Kaakoush, N.O., Walsh, A.J., van den Bogaerde, J., Samuel, D., Leong, R.W., Connor, S., Ng, W., Paramsothy, R., et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: A randomised placebo-controlled trial. Lancet 2017, 389, 1218-1228.
68. Brace, C., Gloor, G.B., Ropeleski, M., Allen-Verco, E., Petrof, E.O. Microbial composition analysis of Clostridium difficile infections in an ulcerative colitis patient treated with multiple fecal microbiota transplantations. J. Crohns Colitis 2014, 8, 1133-1137.
69. Vahabnezhad, E., Mochon, A.B., Wozniak, L.Y., Ziring, D.A. Lactobacillus bacteremia associated with probiotic use in a pediatric patient with ulcerative colitis. Clin. Gastroenterol. 2013, 47, 437-439.
70. Gouriet, F., Million, M., Henri, M., Fournier, P.E., Raoult, D. Lactobacillus rhamnosus bacteremia: An emerging clinical entity. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31, 2469-2480.
71. Petersen, A.M., Mirsepasi, H., Halkjær, S.I., Mortensen, E.M., Nordgaard-Lassen, I., Krogfelt, K.A. Ciprofloxacin and probiotic Escherichia coli Nissle add-on treatment in active ulcerative colitis: A double-blind randomized placebo controlled clinical trial. J. Crohns Colitis 2014, 8, 1498-1505.
72. Fedorak, R.N., Feagan, B.G., Hotte, N., Leddin, D., Dieleman, L.A., Petrunia, D.M., Enns, R., Bitton, A., Chiba, N., Paré, P. The probiotic VSL#3 has anti-inflammatory effects and could reduce endoscopic recurrence after surgery for crohn’s disease. Clin. Gastroenterol. Hepatol. 2015, 13, 928-935.
73. Hevia, A., López, P., Suárez, A., Jacquot, C., Urdaci, M.C., Margolles, A., Sánchez, B. Association of levels of antibodies from patients with inflammatory bowel disease with extracellular proteins of food and probiotic bacteria. Biomed. Res. Int. 2014, 2014, 351204.
74. Ahmed, J., Reddy, B.S., Mølbak, L., Leser, T.D., MacFie, J. Impact of probiotics on colonic microflora in patients with colitis: A prospective double blind randomised crossover study. Int. J. Surg. 2013, 11, 1131-1136.
75. Persborn, M., Gerritsen, J., Wallon, C., Carlsson, A., Akkermans, L.M.A., Söderholm, J.D. The effects of probiotics on barrier function and mucosal pouch microbiota during maintenance treatment for severe pouchitis in patients with ulcerative colitis. Aliment Pharmacol. Ther. 2013, 38, 772-783.
76. Groeger, D., O’Mahony, L., Murphy, E.F., Bourke, J.F., Dinan, T.G., Kiely, B., Shanahan, F., Quigley, E.M.M. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes 2013, 4, 325-339.
77. Bourreille, A., Cadiot, G., Le Dreau, G., Laharie, D., Beaugerie, L., Dupas, J.L., Marteau, P., Rampal, P., Moyse, D., Saleh, A. Saccharomyces boulardii does not prevent relapse of Crohn0s disease. Clin. Gastroenterol. Hepatol. 2013, 11, 982-987.