Probiotics and the gut microbiota in intestinal health and disease

Nature Reviews Gastroenterology and Hepatology

Volumn 7, Issue 9, 2010, Pages 503-514

  Gareau, Mélanie G ^a   Sherman, Philip M ^a   Walker, W Allan ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROBIOTIC AGENT;

DIARRHEA; ENTERITIS; GASTROINTESTINAL DISEASE; GASTROINTESTINAL TRACT; HUMAN; MICROBIOLOGY; REVIEW;

DIARRHEA; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATORY BOWEL DISEASES; PROBIOTICS;

EID: 79952108387     PISSN: 17595045     EISSN: 17595053     Source Type: Journal    
DOI: 10.1038/nrgastro.2010.117     Document Type: Article

References (131)

1. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323 (2009).
2. Eckburg, P B. et al. Diversity of the human intestinal microbial flora. Science 308, 1635-1638 (2005).
3. Forsythe, P, Sudo, N., Dinan, T., Taylor, V H. & Bienenstock, J., Mood and gut feelings. Brain Behav. Immun. 24, 9-16 (2010).
4. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010).
5. Ley, R. E., Peterson, D. A. & Gordon, J. I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837-848 (2006).
6. Chen, J., Cai, W. & Feng, Y., Development of intestinal bifidobacteria and lactobacilli in breast-fed neonates. Clin. Nutr. 26, 559-566 (2007).
7. Conroy, M. E., Shi, H. N. & Walker, W. A. The longterm health effects of neonatal microbial flora. Curr. Opin. Allergy Clin. Immunol. 9, 197-201 (2009).
8. Taylor, S. N., Basile, L. A., Ebeling, M. & Wagner, C. L. Intestinal permeability in preterm infants by feeding type: mother’s milk versus formula. Breastfeed. Med. 4, 11-15 (2009).
9. Martin, R. et al. Human milk is a source of lactic acid bacteria for the infant gut. J. Pediatr. 143, 754-758 (2003).
10. Rautava, S., Salminen, S. & Isolauri, E. Specific probiotics in reducing the risk of acute infections in infancy-a randomised, double-blind, placebocontrolled study. Br. J. Nutr. 101, 1722-1726 (2009).
11. Turnbaugh, P J. & Gordon, J. I. The core gut microbiome, energy balance and obesity. J. Physiol. 587, 4153-4158 (2009).
12. Friswell, M. K. et al. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS ONE 5, 4 (2010).
13. Mariat, D. et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 9, 123 (2009).
14. Vael, C. & Desager, K. The importance of the development of the intestinal microbiota in infancy. Curr. Opin. Pediatr. 21, 794-800 (2009).
15. Hoffmann, C. et al. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Infect. Immun. 77, 4668-4678 (2009).
16. Hill, D. A. et al. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 3, 148-158 (2010).
17. De Palma, G. et al. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 10, 63 (2010).
18. Larsen, N. et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLOS ONE 5, 85 (2010).
19. Turnbaugh, P J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480-484 (2009).
20. Tannock, G. W. Molecular analysis of the intestinal microflora in IBD. Mucosal Immunol. 1 (Suppl. 1), S15-S18 (2008).
21. Swidsinski, A., Loening-Baucke, V., Verstraelen, H., Osowska, S. & Doerffel, Y. Biostructure of fecal microbiota in healthy subjects and patients with chronic idiopathic diarrhea. Gastroenterology 135, 568-579 (2008).
22. Willing, B. et al. Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn’s disease. Inflamm. Bowel Dis. 15, 653-660 (2009).
23. Seksik, P et al. Search for localized dysbiosis in Crohn’s disease ulcerations by temporal temperature gradient gel electrophoresis of 16S RNA. J. Clin. Microbiol. 43, 4654-658 (2005).
24. Mileti, E., Matteoli, G., Iliev, I. D. & Rescigno, M. Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS ONE 4, 56 (2009).
25. Sherman, P M., Ossa, J. C. & Johnson-Henry, K. Unraveling mechanisms of action of probiotics. Nutr. Clin. Pract. 24, 10-14 (2009).
26. Ford, A. C., Talley, N. J., Schoenfeld, P S., Quigley, E. M. & Moayyedi, P., Efficacy of antidepressants and psychological therapies in irritable bowel syndrome: systematic review and meta-analysis. Gut 58, 367-378 (2009).
27. Spiller, R. & Garsed, K. Postinfectious irritable bowel syndrome. Gastroenterology 136, 1979-1988 (2009).
28. O’Mahony, L. et al. Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128, 541-551 (2005).
29. Whorwell, P J. et al. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am. J. Gastroenterol. 101, 1581-1590 (2006).
30. Agrawal, A. et al. Clinical trial: the effects of a fermented milk product containing Bifidobacterium lactis DN-173-010 on abdominal distension and gastrointestinal transit in irritable bowel syndrome with constipation. Aliment. Pharmacol. Ther. 29, 104-114 (2008).
31. Guyonnet, D. et al. Effect of a fermented milk containing Bifidobacterium animalis DN-173 010 on the health-related quality of life and symptoms in irritable bowel syndrome in adults in primary care: a multicentre, randomized, double-blind, controlled trial. Aliment. Pharmacol. Ther. 26, 475-486 (2007).
32. Moayyedi, P et al. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 59, 325-332 (2010).
33. Brenner, D. M., Moeller, M. J., Chey, W. D. & Schoenfeld, P. S. The utility of probiotics in the treatment of irritable bowel syndrome: a systematic review. Am. J. Gastroenterol. 104, 1033-1049 (2009).
34. Soderholm, J. D. et al. Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G1257-G1263 (2002).
35. Gareau, M. G., Jury, J., MacQueen, G., Sherman, P. M. & Perdue, M. H. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56, 1522-1528 (2007).
36. O’Mahony, S. M. et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry 65, 263-267 (2009).
37. Soderholm, J. D. et al. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology 123, 1099-1108 (2002).
38. Zareie, M. et al. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 55, 1553-1560 (2006).
39. Rousseaux, C. et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat. Med. 13, 35-37 (2007).
40. Verdu, E. F. et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 55, 182-190 (2006).
41. Verdu, E. F. et al. Lactobacillus paracasei normalizes muscle hypercontractility in a murine model of postinfective gut dysfunction. Gastroenterology 127, 826-837 (2004).
42. Kamiya, T. et al. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 55, 191-196 (2006).
43. Ait-Belgnaoui, A. et al. Lactobacillus farciminis treatment attenuates stress-induced overexpression of Fos protein in spinal and supraspinal sites after colorectal distension in rats. Neurogastroenterol. Motil. 21, 567-569 (2009).
44. Mankertz, J. & Schulzke, J. D. Altered permeability in inflammatory bowel disease: pathophysiology and clinical implications. Curr. Opin. Gastroenterol. 23, 379-383 (2007).
45. Shanahan, F. & Bernstein, C. N. The evolving epidemiology of inflammatory bowel disease. Curr. Opin. Gastroenterol. 25, 301-305 (2009).
46. Sokol, H. et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl Acad. Sci. USA 105, 16731-16736 (2008).
47. Darfeuille-Michaud, A. et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology 127, 412-421 (2004).
48. Barnich, N. et al. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J. Clin. Invest. 117, 1566-1574 (2007).
49. Isaacs, K. & Herfarth, H. Role of probiotic therapy in IBD. Inflamm. Bowel Dis. 14, 1597-1605 (2008).
50. Pronio, A. 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, 662-668 (2008).
51. Bibiloni, R. et al. VSL probiotic-mixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenterol. 100, 1539-1546 (2005).
52. Hansen, R., Thomson, J. M., El Omar, E. M. & Hold, G. L. The role of infection in the aetiology of inflammatory bowel disease. J. Gastroenterol. 45, 266-276 (2010).
53. Marteau, P., Bacterial flora in inflammatory bowel disease. Dig. Dis. 27 (Suppl. 1), 99-103 (2009).
54. Ingrassia, I., Leplingard, A. & Darfeuille-Michaud, A., Lactobacillus casei DN-114 001 inhibits the ability of adherent-invasive Escherichia coli isolated from Crohn’s disease patients to adhere to and to invade intestinal epithelial cells. Appl. Environ. Microbiol. 71, 2880-2887 (2005).
55. Johnson-Henry, K. C. et al. Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J. Infect. Dis. 191, 2106-2117 (2005).
56. Wu, X. et al. Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G295-G306 (2008).
57. Ewaschuk, J. B. et al. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G1025-G1034 (2008).
58. Ukena, S. N. et al. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. ONE 2, 8 (2007).
59. Mennigen, R. et al. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G1140-G1149 (2009).
60. Miyauchi, E., Morita, H. & Tanabe, S., Lactobacillus rhamnosus alleviates intestinal barrier dysfunction in part by increasing expression of zonula occludens-1 and myosin light-chain kinase in vivo. J. Dairy Sci. 92, 2400-2408 (2009).
61. Tien, M. T. et al. Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J. Immunol. 176, 1228-1237 (2006).
62. Kamada, N. et al. Nonpathogenic Escherichia coli strain Nissle 1917 inhibits signal transduction in intestinal epithelial cells. Infect. Immun. 76, 214-220 (2008).
63. Roselli, M. et al. Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of gammadeltaT and regulatory Tcells of intestinal intraepithelial lymphocytes. Inflamm. Bowel Dis. 15, 1526-1536 (2009).
64. Hacini-Rachinel, F. et al. CD4+ T cells and Lactobacillus casei control relapsing colitis mediated by CD T cells. J. Immunol. 183, 5477-5486 (2009).
65. Kwon, H. K. et al. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc. Natl Acad. Sci. USA 107, 2159-2164 (2010).
66. Chen, C. C., Louie, S., Shi, H. N. & Walker, W. A. Preinoculation with the probiotic Lactobacillus acidophilus early in life effectively inhibits murine Citrobacter rodentium colitis. Pediatr. Res. 58, 1185-1191 (2005).
67. Im, E., Choi, Y. J., Pothoulakis, C. & Rhee, S. H. Bacillus polyfermenticus ameliorates colonic inflammation by promoting cytoprotective effects in colitic mice. J. Nutr. 139, 1848-1854 (2009).
68. Carol, M. et al. Modulation of apoptosis in intestinal lymphocytes by a probiotic bacteria in Crohn’s disease. J. Leukoc. Biol. 79, 917-922 (2006).
69. Llopis, M. et al. Lactobacillus casei downregulates commensals’ inflammatory signals in Crohn’s disease mucosa. Inflamm. Bowel Dis. 15, 275-283 (2009).
70. Schultz, M. et al. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 8, 71-80 (2002).
71. Jijon, H. et al. DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology 126, 1358-1373 (2004).
72. Pagnini, C. et al. Probiotics promote gut health through stimulation of epithelial innate immunity. Proc. Natl Acad. Sci. USA 107, 454-459 (2010).
73. Madsen, K. et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121, 580-591 (2001).
74. Conte, M. P. et al. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut 55, 1760-1767 (2006).
75. Miele, 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, 437-443 (2009).
76. Huynh, H. Q. et al. Probiotic preparation VSL#3 induces remission in children with mild to moderate acute ulcerative colitis: a pilot study. Inflamm. Bowel Dis. 15, 760-768 (2009).
77. Guandalini, S. et al. VSL#3 improves symptoms in children with irritable bowel syndrome: a multicenter, randomized, placebo-controlled, double-blind, crossover study. J. Pediatr. Gastroenterol. Nutr. 51, 24-30 (2010).
78. Fedorak, R. N., Understanding why probiotic therapies can be effective in treating IBD. J. Clin. Gastroenterol. 42 (Suppl. 3), S111-S115.
79. Petrosyan, M., Guner, Y S., Williams, M., Grishin, A. & Ford, H. R., Current concepts regarding the pathogenesis of necrotizing enterocolitis. Pediatr. Surg. Int. 25, 309-318.
80. Morowitz, M. J., Poroyko, V., Caplan, M., Alverdy, J. & Liu, D. C. Redefining the role of intestinal microbes in the pathogenesis of necrotizing enterocolitis. Pediatrics 125, 777-785 (2010).
81. Cotten, C. M. et al. Prolonged duration of initial empirical antibiotic treatment is associated with increased rates of necrotizing enterocolitis and death for extremely low birth weight infants. Pediatrics 123, 58-66 (2009).
82. Wang, Y et al. RNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J. 3, 944-954 (2009).
83. Alfaleh, K., Anabrees, J. & Bassler, D. Probiotics reduce the risk of necrotizing enterocolitis in preterm infants: a meta-analysis. Neonatology 97, 93-99 (2009).
84. Deshpande, G., Rao, S., Patole, S. & Bulsara, M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 125, 921-930 (2010).
85. Chou, I. C. et al. Lack of effects of oral probiotics on growth and neurodevelopmental outcomes in preterm very low birth weight infants. J. Pediatr. 156, 393-396 (2010).
86. Lin, H. C. et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics 122, 693-700 (2008).
87. Manzoni, P et al. Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birth-weight neonates: a randomized trial. JAMA 302, 1421-1428 (2009).
88. Rouge, C. et al. Oral supplementation with probiotics in very-low-birth-weight preterm infants: a randomized, double-blind, placebocontrolled trial. Am. J. Clin. Nutr. 89, 1828-1835 (2009).
89. Luoto, R., Matomaki, J., Isolauri, E. & Lehtonen, L. Incidence of necrotizing enterocolitis in very-low-birth-weight infants related to the use of Lactobacillus GG. Acta Paediatr. 99, 1135-1138 (2010).
90. Khailova, L. et al. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G940-G949 (2009).
91. Lin, P W., Nasr, T. R., Berardinelli, A. J., Kumar, A. & Neish, A. S. The probiotic Lactobacillus GG may augment intestinal host defense by regulating apoptosis and promoting cytoprotective responses in the developing murine gut. Pediatr. Res. 64, 511-516 (2008).
92. McFarland, L. V., Update on the changing epidemiology of Clostridium difficile-associated disease. Nat. Clin. Pract. Gastroenterol. Hepatol. 5, 40-48 (2008).
93. Leffler, D. A. & Lamont, J. T. Treatment of Clostridium difficile-associated disease. Gastroenterology 136, 1899-1912 (2009).
94. McFarland, L. V., Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am. J. Gastroenterol. 101, 812-822.
95. Pillai, A. & Nelson, R. Probiotics for treatment of Clostridium difficile-associated colitis in adults. Cochrane Database of Systematic Reviews, Issue 1. Art no.: CD004611. doi:10.1002/14651858.CD004611.pub2. (2008).
96. Miller, M. The fascination with probiotics for Clostridium difficile infection: lack of evidence for prophylactic or therapeutic efficacy. Anaerobe 15, 281-284 (2009).
97. Tung, J. M., Dolovich, L. R. & Lee, C. H. Prevention of Clostridium difficile infection with Saccharomyces boulardii: A systematic review. Can. J. Gastroenterol. 23, 817-821 (2009).
98. McFarland, L. V. Antibiotic-associated diarrhea: epidemiology, trends and treatment. Future Microbiol. 3, 563-578 (2008).
99. Lonnermark, E. et al. Intake of Lactobacillus plantarum reduces certain gastrointestinal symptoms during treatment with antibiotics. J. Clin. Gastroenterol. 44, 106-112 (2010).
100. Ruszczynski, M., Radzikowski, A. & Szajewska, H. Clinical trial: effectiveness of Lactobacillus rhamnosus (strains E/N, Oxy and Pen) in the prevention of antibiotic-associated diarrhoea in children. Aliment. Pharmacol. Ther. 28, 154-161 (2008).
101. McFarland, L. V., Systematic review and metaanalysis of Saccharomyces boulardii in adult patients. World J. Gastroenterol. 16, 2202-2222.
102. Chen, C. C. et al. Probiotics have clinical, microbiologic, and immunologic efficacy in acute infectious diarrhea. Pediatr. Infect. Dis. J. 29, 135-138 (2010).
103. Pedone, C. A., Arnaud, C. C., Postaire, E. R., Bouley, C. F. & Reinert, P Multicentric study of the effect of milk fermented by Lactobacillus casei on the incidence of diarrhoea. Int. J. Clin. Pract. 54, 568-571 (2000).
104. Pedone, C. A., Bernabeu, A. O., Postaire, E. R., Bouley, C. F. & Reinert, P. The effect of supplementation with milk fermented by Lactobacillus casei (strain DN-114 001) on acute diarrhoea in children attending day care centres. Int. J. Clin. Pract. 53, 179-184 (1999).
105. Szajewska, H. & Mrukowicz, J. Z. Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J. Pediatr. Gastroenterol. Nutr. 33 (Suppl. 2), S17-S25 (2001).
106. Van Niel, C. W., Feudtner, C., Garrison, M. M. & Christakis, D. A. Lactobacillus therapy for acute infectious diarrhea in children: a meta-analysis. Pediatrics 109, 678-684 (2002).
107. Huang, J. S., Bousvaros, A., Lee, J. W., Diaz, A. & Davidson, E. J. Efficacy of probiotic use in acute diarrhea in children: a meta-analysis. Dig. Dis. Sci. 47, 2625-2634 (2002).
108. Szajewska, H., Skorka, A. & Dylag, M. Metaanalysis: Saccharomyces boulardii for treating acute diarrhoea in children. Aliment. Pharmacol. Ther. 25, 257-264 (2007).
109. Szajewska, H., Skorka, A., Ruszczynski, M. & Gieruszczak-Bialek, D. Meta-analysis: Lactobacillus GG for treating acute diarrhoea in children. Aliment. Pharmacol. Ther. 25, 871-881.
110. Wine, E., Gareau, M. G., Johnson-Henry, K. & Sherman, P M. Strain-specific probiotic (Lactobacillus helveticus) inhibition of Campylobacter jejuni invasion of human intestinal epithelial cells. FEMS Microbiol. Lett. 300, 146-152 (2009).
111. Corr, S. C. et al. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc. Natl Acad. Sci. USA 104, 7617-7621 (2007).
112. Konstantinov, S. R. et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl Acad. Sci. USA 105, 19474-19479.
113. Johnson-Henry, K. C., Hagen, K. E., Gordonpour, M., Tompkins, T A. & Sherman, P M. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol. 9, 356-367 (2007).
114. Mondel, M. et al. Coli treatment mediates antimicrobial human beta-defensin synthesis and fecal excretion in humans. Mucosal Immunol. 2, 166-172 (2009).
115. Sherman, P. M. et al. Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect. Immun. 73, 5183-5188 (2005).
116. Johnson-Henry, K. C., Donato, K. A., Shen-Tu, G., Gordanpour, M. & Sherman, P. M. Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7- induced changes in epithelial barrier function. Infect. Immun. 76, 1340-1348 (2008).
117. Gareau, M. G., Wine, E., Reardon, C. & Sherman, P. M. Probiotics prevent death caused by Citrobacter rodentium infection in neonatal mice. J. Infect. Dis. 201, 81-91 (2010).
118. O’Mahony, C. et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog. 4, 2 (2008).
119. Steidler, L. et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289, 1352-1355 (2000).
120. Braat, H. et al. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin. Gastroenterol. Hepatol. 4, 754-759 (2006).
121. Sturm, A. & Dignass, A. U., Epithelial restitution and wound healing in inflammatory bowel disease. World J. Gastroenterol. 14, 348-353 (2008).
122. Vandenbroucke, K. et al. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology 127, 502-513 (2004).
123. Lih-Brody, L. et al. Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig. Dis. Sci. 41, 2078-2086 (1996).
124. Carroll, I. M. et al. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G729-G738 (2007).
125. Hamady, Z. Z. et al. Xylan-regulated delivery of human keratinocyte growth factor-2 to the inflamed colon by the human anaerobic commensal bacterium Bacteroides ovatus. Gut 59, 461-469 (2010).
126. De Groote, M. A., Frank, D. N., Dowell, E., Glode, M. P. & Pace, N. R., Lactobacillus rhamnosus GG bacteremia associated with probiotic use in a child with short gut syndrome. Pediatr. Infect. Dis. J. 24, 278-280 (2005).
127. Land, M. H. et al. Lactobacillus sepsis associated with probiotic therapy. Pediatrics 115, 178-181 (2005).
128. Barton, L. L., Rider, E. D. & Coen, R. W. Bacteremic infection with Pediococcus: vancomycin-resistant opportunist. Pediatrics 107, 775-776 (2001).
129. van Minnen, L. P et al. Modification of intestinal flora with multispecies probiotics reduces bacterial translocation and improves clinical course in a rat model of acute pancreatitis. Surgery 141, 470-480 (2007).
130. Besselink, M. G. et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 371, 651-659 (2008).
131. Sorokulova, I., Preclinical testing in the development of probiotics: a regulatory perspective with Bacillus strains as an example. Clin. Infect. Dis. 46 (Suppl. 2), S92-S95 (2008).