Probiotics in Inflammatory Bowel Disease

Gastroenterology Clinics of North America

Volumn 46, Issue 4, 2017, Pages 769-782

  Abraham, Bincy P ^a   Quigley, Eamonn M M ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

Crohn disease; Inflammation; Inflammatory bowel disease; Microbiome; Microbiota; Pouchitis; Probiotic; Ulcerative colitis

Indexed keywords

PROBIOTIC AGENT;

ANTIINFLAMMATORY ACTIVITY; BACTERIAL STRAIN; BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE; COMMENSAL; CROHN DISEASE; DISEASE CONTROL; DISEASE COURSE; DISEASE SEVERITY; DRUG QUALITY; DRUG SAFETY; ESCHERICHIA COLI; EVIDENCE BASED MEDICINE; FAECALIBACTERIUM PRAUSNITZII; HOST PATHOGEN INTERACTION; HUMAN; ILEITIS; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; MICROBIAL ACTIVITY; NONHUMAN; PATHOGENESIS; QUALITY CONTROL; REMISSION; REVIEW; TREATMENT RESPONSE; ULCERATIVE COLITIS; ANIMAL; INTESTINE FLORA;

ANIMALS; COLITIS, ULCERATIVE; CROHN DISEASE; GASTROINTESTINAL MICROBIOME; HUMANS; POUCHITIS; PROBIOTICS; REMISSION INDUCTION;

EID: 85030481903     PISSN: 08898553     EISSN: 15581942     Source Type: Journal    
DOI: 10.1016/j.gtc.2017.08.003     Document Type: Review

References (112)

1. Cheifetz, A.S., Gianotti, R., Luber, R., et al. Complementary and alternative medicines used by patients with inflammatory bowel diseases. Gastroenterology 152 (2017), 415–429.
2. Kostic, A.D., Xavier, R.J., Gevers, D., The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146 (2014), 1489–1499.
3. Babickova, J., Gardlik, R., Pathological and therapeutic interactions between bacteriophages, microbes and the host in inflammatory bowel disease. World J Gastroenterol 21 (2015), 11321–11330.
4. Sartor, R.B., Wu, G.D., Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology 152 (2017), 327–339.
5. Leone, V., Chang, E.B., Devkota, S., Diet, microbes, and host genetics: the perfect storm in inflammatory bowel diseases. J Gastroenterol 48 (2013), 315–321.
6. Shanahan, F., Quigley, E.M., Manipulation of the microbiota for treatment of IBS and IBD–challenges and controversies. Gastroenterology 146 (2014), 1554–1563.
7. Bejaoui, M., Sokol, H., Marteau, P., Targeting the microbiome in inflammatory bowel disease: critical evaluation of current concepts and moving to new horizons. Dig Dis 33:Suppl 1 (2015), 105–112.
8. Hansen, J.J., Sartor, R.B., Therapeutic manipulation of the microbiome in IBD: current results and future approaches. Curr Treat Options Gastroenterol 13 (2015), 105–120.
9. Anderson, J.L., Edney, R.J., Whelan, K., Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther 36 (2012), 503–516.
10. Scaldaferri, F., Pecere, S., Petito, V., et al. Efficacy and mechanisms of action of fecal microbiota transplantation in ulcerative colitis: pitfalls and promises from a first meta-analysis. Transplant Proc 48 (2016), 402–407.
11. Moayyedi, P., Surette, M.G., Kim, P.T., et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149 (2015), 102–109.
12. Howarth, G.S., Wang, H., Role of endogenous microbiota, probiotics and their biological products in human health. Nutrients 5 (2013), 58–81.
13. FAO/WHO, Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. 2002, World Health Organization, London.
14. Hill, C., Guarner, F., Reid, G., 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 11 (2014), 506–514.
15. Grimoud, J., Durand, H., de Souza, S., et al. In vitro screening of probiotics and synbiotics according to anti-inflammatory and anti-proliferative effects. Int J Food Microbiol 144 (2010), 42–50.
16. Laurell, A., Sjöberg, K., Prebiotics and synbiotics in ulcerative colitis. Scand J Gastroenterol 52 (2017), 477–485.
17. Kaila, M., Isolauri, E., Soppi, E., et al. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res 32 (1992), 141–144.
18. Ogawa, T., Asai, Y., Tamai, R., et al. Natural killer cell activities of synbiotic Lactobacillus casei ssp. casei in conjunction with dextran. Clin Exp Immunol 143 (2006), 103–109.
19. Petrof, E.O., Kojima, K., Ropeleski, M.J., et al. Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 127 (2004), 1474–1487.
20. Di Marzio, L., Russo, F.P., D'Alo, S., et al. Apoptotic effects of selected strains of lactic acid bacteria on a human T leukemia cell line are associated with bacterial arginine deiminase and/or sphingomyelinase activities. Nutr Cancer 40 (2001), 185–196.
21. Maassen, C.B., van Holten-Neelen, C., Balk, F., et al. Strain-dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 18 (2000), 2613–2623.
22. Morita, H., He, F., Fuse, T., et al. Adhesion of lactic acid bacteria to caco-2 cells and their effect on cytokine secretion. Microbiol Immunol 46 (2002), 293–297.
23. Ma, D., Forsythe, P., Bienenstock, J., Live lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun 72 (2004), 5308–5314.
24. West, C.E., Jenmalm, M.C., Prescott, S.L., The gut microbiota and its role in the development of allergic disease: a wider perspective. Clin Exp Allergy 45 (2015), 43–53.
25. Konieczna, P., Akdis, C.A., Quigley, E.M., et al. Portrait of an immunoregulatory Bifidobacterium. Gut Microbes 3 (2012), 261–266.
26. McCarthy, J., O'Mahony, L., O'Callaghan, L., et al. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 2 (2003), 975–980.
27. O'Hara, A.M., O'Regan, P., Fanning, A., et al. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118 (2006), 202–215.
28. O'Mahony, L., O'Callaghan, L., McCarthy, J., et al. Differential cytokine response from dendritic cells to commensal and pathogenic bacteria in different lymphoid compartments in humans. Am J Physiol Gastrointest Liver Physiol 290 (2006), G839–G845.
29. Gad, M., Ravn, P., Søborg, D.A., et al. Regulation of the IL-10/IL-12 axis in human dendritic cells with probiotic bacteria. FEMS Immunol Med Microbiol 63 (2011), 93–107.
30. Konieczna, P., Groeger, D., Ziegler, M., et al. Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: potential role for myeloid and plasmacytoid dendritic cells. Gut 61 (2012), 354–366.
31. Groeger, D., O'Mahony, L., Murphy, E.F., et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes 4 (2013), 325–339.
32. O'Mahony, C., Scully, P., O'Mahony, D., et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog, 4, 2008, e1000112.
33. Konieczna, P., Ferstl, R., Ziegler, M., et al. Immunomodulation by Bifidobacterium infantis 35624 in the murine lamina propria requires retinoic acid-dependent and independent mechanisms. PLoS One, 8, 2013, e62617.
34. Scully, P., Macsharry, J., O'Mahony, D., et al. Bifidobacterium infantis suppression of Peyer's patch MIP-1α and MIP-1β secretion during Salmonella infection correlates with increased local CD4+CD25+ T cell numbers. Cell Immunol 281 (2013), 134–140.
35. Altmann, F., Kosma, P., O'Callaghan, A., et al. Genome analysis and characterisation of the exopolysaccharide produced by Bifidobacterium longum subsp. longum 35624™. PLoS One, 11, 2016, e0162983.
36. Schiavi, E., Gleinser, M., Molloy, E., et al. The surface-associated exopolysaccharide of Bifidobacterium longum 35624 plays an essential role in dampening host proinflammatory responses and repressing local TH17 responses. Appl Environ Microbiol 82 (2016), 7185–7196.
37. Cao, Y., Shen, J., Ran, Z.H., Association between Faecalibacterium prausnitzii reduction and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Gastroenterol Res Pract, 2014, 2014, 872725.
38. Rossi, O., van Berkel, L.A., Chain, F., et al. Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci Rep, 6, 2016, 18507.
39. Martín, R., Miquel, S., Chain, F., et al. Faecalibacterium prausnitzii prevents physiological damages in a chronic low-grade inflammation murine model. BMC Microbiol, 15, 2015, 67.
40. Vindigni, S.M., Zisman, T.L., Suskind, D.L., et al. The intestinal microbiome, barrier function, and immune system in inflammatory bowel disease: a tripartite pathophysiological circuit with implications for new therapeutic directions. Therap Adv Gastroenterol 9 (2016), 606–625.
41. Lomasney, K.W., Cryan, J.F., Hyland, N.P., Converging effects of a Bifidobacterium and Lactobacillus probiotic strain on mouse intestinal physiology. Am J Physiol Gastrointest Liver Physiol 307 (2014), G241–G247.
42. Srutkova, D., Schwarzer, M., Hudcovic, T., et al. Bifidobacterium longum CCM 7952 promotes epithelial barrier function and prevents acute DSS-induced colitis in strictly strain-specific manner. PLoS One, 10, 2015, e0134050.
43. Yan, F., Polk, D.B., Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 277 (2002), 50959–50965.
44. Ahrne, S., Hagslatt, M.L., Effect of lactobacilli on paracellular permeability in the gut. Nutrients 3 (2011), 104–117.
45. Lomasney, K.W., Houston, A., Shanahan, F., et al. Selective influence of host microbiota on cAMP-mediated ion transport in mouse colon. Neurogastroenterol Motil 26 (2014), 887–890.
46. Souza, É.L., Elian, S.D., Paula, L.M., et al. Escherichia coli strain Nissle 1917 ameliorates experimental colitis by modulating intestinal permeability, the inflammatory response and clinical signs in a faecal transplantation model. J Med Microbiol 65 (2016), 201–210.
47. Mack, D.R., Ahrne, S., Hyde, L., et al. Extra-cellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52 (2003), 827–833.
48. Shiba, T., Aiba, Y., Ishikawa, H., et al. The suppressive effect of bifidobacteria on Bacteroides vulgatus, a putative pathogenic microbe in inflammatory bowel disease. Microbiol Immunol 47 (2003), 371–378.
49. Servin, A.L., Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28 (2004), 405–440.
50. Sartor, R.B., Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126 (2004), 1620–1633.
51. Constante, M., Fragoso, G., Lupien-Meilleur, J., et al. Iron supplements modulate colon microbiota composition and potentiate the protective effects of probiotics in dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 23 (2017), 753–766.
52. Kuhbacher, T., Ott, S.J., Helwig, U., et al. Bacterial and fungal microbiota in relation to probiotic therapy (VSL#3) in pouchitis. Gut 55 (2006), 833–841.
53. Ewaschuk, J.B., Walker, J.W., Diaz, H., et al. Bioproduction of conjugated linoleic acid by probiotic bacteria occurs in vitro and in vivo in mice. J Nutr 136 (2006), 1483–1487.
54. Collado, M.C., Surono, I.S., Meriluoto, J., et al. Potential probiotic characteristics of Lactobacillus and Enterococcus strains isolated from traditional dadih fermented milk against pathogen intestinal colonization. J Food Prot 70 (2007), 700–705.
55. McKernan, D.P., Fitzgerald, P., Dinan, T.G., et al. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil 22 (2010), 1029–1035.
56. Johnson, A.C., Greenwood-Van Meerveld, B., McRorie, J., Effects of Bifidobacterium infantis 35624 on post-inflammatory visceral hypersensitivity in the rat. Dig Dis Sci 56 (2011), 3179–3186.
57. Emge, J.R., Huynh, K., Miller, E.N., et al. Modulation of the microbiota-gut-brain axis by probiotics in a murine model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 310 (2016), G989–G998.
58. Desbonnet, L., Garrett, L., Clarke, G., et al. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170 (2010), 1179–1188.
59. Naidoo, K., Gordon, M., Fagbemi, A.O., et al. Probiotics for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev(12), 2011 CD007443.
60. Rolfe, V.E., Fortun, P.J., Hawkey, C.J., et al. Probiotics for maintenance of remission in Crohn's disease. Cochrane Database Syst Rev(4), 2006 CD004826.
61. Mallon, P., McKay, D., Kirk, S., et al. Probiotics for induction of remission in ulcerative colitis. Cochrane Database Syst Rev(4), 2007 CD005573.
62. Zigra, P.I., Maipa, V.E., Alamanos, Y.P., Probiotics and remission of ulcerative colitis: a systematic review. Neth J Med 65 (2007), 411–418.
63. Rahimi, R., Nikfar, S., Rahimi, F., 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. Dig Dis Sci 53 (2008), 2524–2531.
64. Veerappan, G.R., Betteridge, J., Young, P.E., Probiotics for the treatment of inflammatory bowel disease. Curr Gastroenterol Rep 14 (2012), 324–333.
65. Ghouri, Y.A., Richards, D.M., Rahimi, E.F., et al. Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol 7 (2014), 473–487.
66. Fujiya, M., Ueno, N., Kohgo, Y., Probiotic treatments for induction and maintenance of remission in inflammatory bowel diseases: a meta-analysis of randomized controlled trials. Clin J Gastroenterol 7 (2014), 1–13.
67. Shen, J., Zuo, Z.X., Mao, A.P., Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn's disease, and pouchitis: meta-analysis of randomized controlled trials. Inflamm Bowel Dis 20 (2014), 21–35.
68. Dong, J., Teng, G., Wei, T., et al. Methodological quality assessment of meta-analyses and systematic reviews of probiotics in inflammatory bowel disease and pouchitis. PLoS One, 11, 2016, e0168785.
69. Gupta, P., Andrew, H., Kirschner, B.S., et al. Is Lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study. J Pediatr Gastroenterol Nutr 31 (2000), 453–457.
70. Fujimori, S., Tatsuguchi, A., Gudis, K., et al. High dose probiotic and prebiotic cotherapy for remission induction of active Crohn's disease. J Gastroenterol Hepatol 22 (2007), 1199–1204.
71. Schultz, M., Timmer, A., Herfarth, H.H., et al. Lactobacillus GG in inducing and maintaining remission of Crohn's disease. BMC Gastroenterol, 4, 2004, 5.
72. Bousvaros, A., Guandalini, S., Baldassano, R.N., et al. A randomized, double-blind trial of Lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn's disease. Inflamm Bowel Dis 11 (2005), 833–839.
73. Fedorak, R.N., Feagan, B.G., Hotte, N., et al. The probiotic VSL#3 has anti-inflammatory effects and could reduce endoscopic recurrence after surgery for Crohn's disease. Clin Gastroenterol Hepatol 13 (2015), 928–935.
74. Bourreille, A., Cadiot, G., Le Dreau, G., et al., FLORABEST Study Group. Saccharomyces boulardii does not prevent relapse of Crohn's disease. Clin Gastroenterol Hepatol 11 (2013), 982–987.
75. Plein, K., Hotz, J., Therapeutic effects of Saccharomyces boulardii on mild residual symptoms in a stable phase of Crohn's disease with special respect to chronic diarrhea – a pilot study. Z Gastroenterol 31 (1993), 129–134.
76. Guslandi, M., Mezzi, G., Sorghi, M., et al. Saccharomyces boulardii in maintenance treatment of Crohn's disease. Dig Dis Sci 45 (2000), 1462–1464.
77. Garcia Vilela, E., De Lourdes De Abreu Ferrari, M., Oswaldo Da Gama Torres, H., et al. Influence of Saccharomyces boulardii on the intestinal permeability of patients with Crohn's disease in remission. Scand J Gastroenterol 43 (2008), 842–848.
78. Marteau, P., Lemann, M., Seksik, P., 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 55 (2006), 842–847.
79. Van Gossum, A., Dewit, O., Louis, E., et al. Multicenter randomized-controlled clinical trial of probiotics (Lactobacillus johnsonii, LA1) on early endoscopic recurrence of Crohn's disease after ileo-caecal resection. Inflamm Bowel Dis 13 (2007), 135–142.
80. Malchow, H.A., Crohn's disease and Escherichia coli: a new approach to therapy to maintain remission of colonic Crohn's disease. J Clin Gastroenterol 25 (1997), 653–658.
81. Sood, A., Midha, V., Makharia, G.K., et al. The probiotic preparation, VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis. Clin Gastroenterol Hepatol 7 (2009), 1202–1209.
82. Tursi, A., Brandimarte, G., Papa, A., 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. Am J Gastroenterol 105 (2010), 2218–2227.
83. Miele, E., Pascarella, F., Giannetti, E., et al. Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol 104 (2009), 437–443.
84. Kato, K., Mizuno, S., Umesaki, Y., et al. Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Aliment Pharmacol Ther 20 (2004), 1133–1141.
85. Petersen, A., Mirsepasi, H., Halkjaer, S., et al. Ciprofloxacin and probiotic Escherichia coli Nissle add-on treatment in active ulcerative colitis: a double blind randomized placebo controlled clinical trial. J Crohns Colitis 8 (2014), 1498–1505.
86. Matthes, H., Krummenerl, T., Giensch, M., et al. Clinical trial: probiotic treatment of acute distal ulcerative colitis with rectally administered Escherichia coli Nissle 1917 (EcN). BMC Complement Altern Med, 10, 2010, 13.
87. Oliva, S., Di Nardo, G., Ferrari, F., et al. Randomised clinical trial: the effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis. Aliment Pharmacol Ther 35 (2012), 327–334.
88. Shanahan, F., Collins, S.M., Pharmabiotic manipulation of the microbiota in gastrointestinal disorders, from rationale to reality. Gastroenterol Clin North Am 39 (2010), 721–726.
89. Wildt, S., Nordgaard, I., Hansen, U., et al. 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. J Crohns Colitis 5 (2011), 115–121.
90. Kruis, W., Schutz, E., Fric, P., et al. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 11 (1997), 853–858.
91. Rembacken, B.J., Snelling, A.M., Hawkey, P.M., et al. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 354 (1999), 635–639.
92. Kruis, W., Fric, P., Pokrotnieks, J., et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53 (2004), 1617–1623.
93. Zocco, M.A., dal Verme, L.Z., Cremonini, F., et al. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 23 (2006), 1567–1574.
94. Huynh, H.Q., deBruyn, J., Guan, L., et al. Probiotic preparation VSL#3 induces remission in children with mild to moderate acute ulcerative colitis: a pilot study. Inflamm Bowel Dis 15 (2009), 760–768.
95. Sandborn, W.J., Pouchitis following ileal pouch-anal anastomosis: definition, pathogenesis, and treatment. Gastroenterology 107 (1994), 1856–1860.
96. Ruseler-van Embden, J.G., Schouten, W.R., van Lieshout, L.M., Pouchitis: result of microbial imbalance?. Gut 35 (1994), 658–664.
97. Kuisma, J., Mentula, S., Jarvinen, H., et al. Effect of Lactobacillus rhamnosus GG on ileal pouch inflammation and microbial flora. Aliment Pharmacol Ther 17 (2003), 509–515.
98. Gionchetti, P., Rizzello, F., Helwig, U., et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 124 (2003), 1202–1209.
99. Gionchetti, P., Rizzello, F., Venturi, A., et al. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology 119 (2000), 305–309.
100. Mimura, T., Rizzello, F., Helwig, U., et al. Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut 53 (2004), 108–114.
101. Pronio, A., Montesani, C., Butteroni, C., et al. Probiotic administration in patients with ileal pouch-anal anastomosis for ulcerative colitis is associated with expansion of mucosal regulatory cells. Inflamm Bowel Dis 14 (2008), 662–668.
102. Landy, J., Hart, A., Commentary: 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 38 (2013), 1405–1406.
103. Sanders, M.E., Akkermans, L.M., Haller, D., et al. Safety assessment of probiotics for human use. Gut Microbes 1 (2010), 164–185.
104. Whelan, K., Myers, C.E., Safety of probiotics in patients receiving nutritional support: a systematic review of case reports, randomized controlled trials, and nonrandomized trials. Am J Clin Nutr 91 (2010), 687–703.
105. Shanahan, F., A commentary on the safety of probiotics. Gastroenterol Clin North Am 41 (2012), 869–876.
106. Guenther, K., Straube, E., Pfister, W., et al. Severe sepsis after probiotic treatment with Escherichia coli Nissle 1917. Pediatr Infect Dis J 29 (2010), 188–189.
107. Besselink, M.G., van Santvoort, H.C., Buskens, E., et al., Dutch Acute Pancreatitis Study Group. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 371 (2008), 651–659.
108. Gong, D., Gong, X., Wang, L., et al. Involvement of reduced microbial diversity in inflammatory bowel disease. Gastroenterol Res Pract, 2016, 2016, 6951091.
109. Knoll, R.L., Forslund, K., Kultima, J.R., et al. Gut microbiota differs between children with inflammatory bowel disease and healthy siblings in taxonomic and functional composition: a metagenomic analysis. Am J Physiol Gastrointest Liver Physiol 312 (2017), G327–G339.
110. Bermúdez-Humarán, L.G., Motta, J.P., Aubry, C., et al. Serine protease inhibitors protect better than IL-10 and TGF-β anti-inflammatory cytokines against mouse colitis when delivered by recombinant lactococci. Microb Cell Fact, 14, 2015, 26.
111. Shigemori, S., Shimosato, T., Applications of genetically modified immunobiotics with high immunoregulatory capacity for treatment of inflammatory bowel diseases. Front Immunol, 8, 2017, 22.
112. Van Tol, E.A.F., Holt, L., Ling Li, F., et al. Bacterial cell wall polymers promote intestinal fibrosis by direct stimulation of myofibroblasts. Am J Physiol 277 (1999), G245–G255.