Probiotics: The scientific evidence in the context of inflammatory bowel disease

Critical Reviews in Food Science and Nutrition

Volumn 57, Issue 9, 2017, Pages 1759-1768

  Celiberto, Larissa Sbaglia ^a   Bedani, Raquel ^b   Rossi, Elizeu Antonio ^a   Cavallini, Daniela Cardoso Umbelino ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Inflammatory bowel disease; microbiota; probiotics; ulcerative colitis

Indexed keywords

DRUG PRODUCTS; IMMUNE SYSTEM;

ANTI-INFLAMMATORIES; BACTERIAL STRAINS; INFLAMMATORY BOWEL DISEASE; MICROBIOTAS; POSSIBLE MECHANISMS; PROBIOTICS; SCIENTIFIC EVIDENCE; ULCERATIVE COLITIS;

DISEASES;

PROBIOTIC AGENT;

BACTERIUM; CLASSIFICATION; HUMAN; INFLAMMATORY BOWEL DISEASES; INTESTINE FLORA;

BACTERIA; GASTROINTESTINAL MICROBIOME; HUMANS; INFLAMMATORY BOWEL DISEASES; PROBIOTICS;

EID: 85014930373     PISSN: 10408398     EISSN: 15497852     Source Type: Journal    
DOI: 10.1080/10408398.2014.941457     Document Type: Article

References (132)

1. Abdin, A., and Saeid, E. M., (2008). An experimental study on ulcerative colitis as a potential target for probiotic therapy by Lactobacillus acidophilus with or without “olsalazine.” J. Crohn's. Colitis. 2:296–303. http://dx.doi.org/10.1016/j.crohns.2008.04.002
2. Alfaleh, K., Anabrees, J., and Bassler, D., (2010). Probiotics reduce the risk of necrotizing enterocolitis in preterm infants:A meta-analysis. Neonatology. 97:93–99. doi:10.1159/000235684
3. Ahmed, J., Reddy, B. S., Molbak, L., et al. (2013). Impact of probiotics on colonic microflora in patients with colitis:A prospective double blind randomized crossover study. Inter. J. Surg. 11(10):1131–1136 http://dx.doi.org/10.1016/j.ijsu.2013.08.019
4. Appleyard, C., Hernández, G., and Ríos-Bedoya, C. F., (2004). Basic epidemiology of inflammatory bowel disease in Puerto Rico. Inflamm. Bowel. Dis. 10:106–111.
5. Arumugam, M., Raes, J., Pelletier, E., et al. (2011). Enterotypes of the human gut microbiome. Nature. 473:174–180. doi:10.1038/nature09944
6. Assumpção, I. R., Rodrigues, M., and Barbieri, D., (1999). Tratamento da retocolite ulcerativa inespecífica em criança com enemas contendo butirato. Relato de caso. Arqu Gastroenterol. 36(4):238–243. http://dx.doi.org/10.1590/S0004-28031999000400012
7. Bardocz, S., Grant, G., Brown, D. S., et al. (1993). Polyamines in food:Implications for growth and health. J. Nutr. Biochem. 4:66–71. http://dx.doi.org/10.1016/0955-2863(93)90001-D
8. Bibiloni, R., Fedorak, R. N., Tannok, G. W., et al. (2005). VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenter. 100:1539–1546. doi:10.1111/j.1572-0241.2005.41794.x
9. Biondo-Simões, M. L. P., Mandelli, K. K., Pereira, M. S. C., et al. (2003). Opções terapêuticas para as doenças inflamatórias intestinais:revisão. Rev. Bras. Coloproctol. 23(3):172–182.
10. Bloomfield, S. F., Stanwell-Smith, R., Crevel, R. W., et al. (2006). Too clean, or not too clean:the hygiene hypothesis and home hygiene. Clin. Exper. Allergy. 36:402–425. doi:10.1111/j.1365-2222.2006.02463.x
11. British Society of Gastroenterology. (2003). Guidelines for the management of inflammatory bowel disease. BSG, London.
12. Bron, P. A., Van Baarlen, A., and Kleerebezem, M., (2011). Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat. Rev.— Microbiol. 10:66–78. doi:10.1038/nrmicro2690
13. Bouma, G., and Strober, W., (2003). The immunological and genetic basis of inflammatory bowel disease. Nat. Rev Immunol. 3:521–533. doi:10.1038/nri1132
14. Boyle, R. J., Bath-Hextall, F. J., Leonardi-Bee, J., et al. (2009). Probiotics for the treatment of eczema:A systematic review. Clin. Exper. Allergy. 39:1117–1127. doi:10.1111/j.1365-2222.2009.03305.x
15. Buller, H., Chin, S., Kirschner, B., et al. (2002). Inflammatory bowel disease in children and adolescents:Working Group Report of the First World Congress of Pediatric Gastroenterology, Hepatology, and Nutrition. J. Ped. Gastroenterol. Nutr. 35(2):151–158.
16. Campos, F. G., Habr-Gama, A., Plopper, C., et al. (1999). Ácidos graxos de cadeira curta e doenças colorretais. Rev. Bras. Coloproctol. 19(1):11–16.
17. Caporaso, J. G., Lauber, C. L., Christian, L. L., et al. (2012). Moving pictures of the human microbiome. Genome Biol. 12:R50. http://genomebiology.com/2011/12/5/R50
18. Cavallini, D. C. U., Abdalla, D. S. P., Vendramini, R. C., et al. (2009b). Effects of isoflavone-supplemented soy yogurt on lipid parameters and atherosclerosis development in hypercholesterolemic rabbits:A randomized double-blind study. Lipids Health Dis. 8:40. doi:10.1186/1476-511X-8-40
19. Cavallini, D. C. U., Bedani, R., Pauly, N. D., et al. (2009a). Effects of probiotic bacteria, isoflavones and simvastatin on lipid profile and atherosclerosis in cholesterol-fed rabbits. Lipids Health Dis. 8:1. doi:10.1186/1476-511X-8-1
20. th Probiotics & Prebiotics New Foods, Rome.
21. Cavallini, D. C. U., Suzuki, J. Y., Abdalla, D. S. P., et al. (2011). Influence of a probiotic soy product on fecal microbiota and its association with cardiovascular risk factors in an animal model. Lipids Health Dis. 10:126. doi:10.1186/1476-511X-10-126
22. th Probiotics & Prebiotics New Foods, Rome.
23. Champagne, C. P., Ross, R. P., Saarela, M., et al. (2011). Recommendations for viability assessment of probiotics as concentrated cultures and in food matrices. Inter. J. Food Microbiol. 149:185–193. doi:10.1016/j.ijfoodmicro.2011.07.005
24. Chen, L. L., Zou, Y. Y., Lu, F. G., et al. (2013). Efficacy profiles for different concentrations of Lactobacillus acidophilus in experimental colitis. World J. Gastroenterol. 19:5347–5256. doi:10.3748/wjg.v19.i32.5347
25. Clavel, T., and Haller, D., (2007). Bacteria and host-derived mechanisms to control intestinal epithelial cell homeostasis:Implications for chronic inflammation. Inflamm. Bowel. Dis. 13:1153–1164. doi:10.1002/ibd.20174
26. Conte, M. P., Schippa, S., Zamboni, I., et al. (2006). Gut-associated bacterial microbiota in pediatric patients with inflammatory bowel disease. Gut. 55(12):1760–1767. doi:10.1136/gut.2005.078824
27. Cornish, J. A., Tan, E., Teare, J., et al. (2007). A meta-analysis on the influence of inflammatory bowel disease on pregnancy. Gut. 56:830–837. doi:10.1136/gut.2006.108324
28. Cui, H., Chen, C., Wang, J., et al. (2004). Effects of probiotic on intestinal mucosa of patients with ulcerative colitis. World J. Gastroenterol. 10(10):1521–1525. http://www.wjgnet.com/1007-9327/10/1521.asp
29. Daniel, C., Poiret, S., Goudercourt, D., et al. (2006). Selecting lactic acid bacteria for their safety and functionality by use of a mouse colitis model. Appl. Environ. Microbiol. 72(9):5799–5805. doi:10.1128/AEM.00109-06
30. Darfeuille-Michaud, A., Boudeau, J., Bulois, P., et al. (2004). High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterol. 127:412–421. doi:10.1053/j.gastro.2004.04.061
31. DeBusk, R. M., Fogarty, C. P., Ordovas, J. M., et al. (2005). Nutritional genomics in practice where do we begin? J. Am. Diet. Assoc. 105:589–598. doi:10.1016/j.jada.2005.01.002
32. De Ross, N. M., Katan, M. B., (2000). Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis:a review of papers published between 1988 and 1998. Am. J. Clin. Nutr. 71:405–411.
33. Deshpande, G., Rao, S., Patole, S., et al. (2010). Update meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pedriatics. 125:921–930. doi:10.1542/peds.2009-1301
34. Dionne, S., Ruemmele, F. M., and Seidman, E. G., (1999). Immunopathogenesis of inflammatory bowel disease:Role of cytokines and immune cell-enterocyte interactions. In:Inflammatory Bowel Diseases, Vol. 2, pp. 41–62. Bristian, B. R., and Walker-Smith, J. A., Ed., Nestlé Nutrition Workshop Series.
35. D'Oliveira, R., Mayberry, J. F., Newcombe, R., et al. (1984). International comparison of mortality from inflammatory bowel disease in the Latin-speaking countries Venezuela, Italy, and France. Digestion. 29:239–241.
36. Dorhout, B., Van Faassen, A., Van Beusekom, C. M., et al. (1997). Oral administration of deuterium-labelled polyamines to sucking rat pups:luminal uptake, metabolic fate and effects on gastrointestinal maturation. Br. J. Nutr. 78:639–54. http://dx.doi.org/10.1079/BJN19970180
37. Duchmann, R., Kaiser, I., Herhann, E., et al. (1995). Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease. Clin. Exper. Immunol. 102:448–455.
38. Duchmann, R., May, E., Heike, M., et al. (1999). T cell specifity and cross reactivity towards enterobacteria, Bacteroides, Bifidobacterium, and antigen from resident intestinal flora in humans. Gut. 44(6):812–818. doi:10.1136/gut.44.6.812
39. Dufour, C., Dandrifosse, G., Forget, P., et al. (1988). Spermine and spermidine induce intestinal maturation in the rat. Gastroenterology. 95:112–6.
40. Ekbom, A., Helmick, C., Zack, M., et al. (1991). The epidemiology of inflammatory bowel disease:a large, population-based study in Sweden. Gastroenterology. 100(2):350–358.
41. Eckburg, P. B., Bik, E. M., Bernstein, C. N., et al. (2005). Diversity of the human intestinal microbial flora. Science. 308(5728):1635–1638. doi:10.1126/science.1110591
42. Fedorak, R. N., and Madsen, K. L., (2004). Probiotics and the management of inflammatory bowel disease. Inflamm. Bowel. Dis. 10(3):286–299.
43. Food and Agriculture Organization/World Health Organization. (2002). Working Group Report on Drafting Guidelines, pp. 60. Evaluation of Probiotics in Food, London, Ontario, Canada.
44. Fujimori, S., Gudis, K., Mitsui, K., et al. (2009). 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. 25:520–525. doi:10.1016/j.nut.2008.11.017
45. Geier, M. S., Butler, R. N., Giffard, P. M., et al. (2007). Lactobacillus fermentum BR11, a potention new probiotic, alleviates symtoms of colitis induced by dextran sulphate sodium (DSS) in rats. Inter. J. Food Microbiol. 114:267–274. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.09.018
46. Girishkumar, B., Henry, D. E., Srinivasan, K., et al. (2012). Beneficial effect of a probiotic Lactobacillus fermentum CFR 2195 in trinitrobenzenesulfonate induced colitis in rat. Ann. Food Sci. Technol. 13(2):231–239.
47. Green, J. R., Lobo, A. J., Holdsworth, C. D., et al. (1998). Balsalazide is more effective and better tolerated than mesalamine in the treatment of acute ulcerative colitis. Gastroenterology. 114:15–22.
48. Grody, W. W., (2003). Molecular genetic risk screening. Ann. Rev. Med. 54:473–490. doi:10.1146/annurev.med.54.101601.152127
49. Guarner, F., Casellas, F., Borruel, N., et al. (2002). Role of microecology in chronic inflammatory bowel diseases. Eur. J. Clin. Nutr. 56(4):S34–S38. doi:10.1038/sj.ejcn.1601662
50. Haller, D., Antoine, J. M., Bengmark, S., et al. (2010). Guidance for substantiating the evidence for beneficial effects of probiotics:probiotics in chronic inflammatory bowel disease and the functional disorder irritable bowel syndrome. Am. Soc. Nutr. 690s–699s. doi:10.3945/jn.109.113746
51. Hanauer, S. B., (2006). Inflammatory bowel disease:Epidemiology, pathogenesis, and therapeutic opportinities. Inflamm. Bowel. Dis. 12:S3–S9.
52. Holubar, S. D., Cima, R. R., Sandborn, W. J., et al. (2010). Treatment and prevention of pouchitis after ileal pouch-anal anastomosis for chronic ulcerative colitis. Cochrane Database Systematic Review. 6. doi:10.1002/14651858.CD001176.pub2
53. Hove, H., and Mortesen, P. B., (1995). Influence of intestinal inflammation (IBD) and small and large bowel length on fecal short-chain fatty acids and lactate. Dig. Dis. Sci. 40:1372–1380.
54. Howarth, G. S., (2008). Inflammatory bowel disease, a dysregulated host-microbiota interaction:are probiotics a new therapeutic option? J. Gastroenterol. Hepatol. 23:1775–1784. doi:10.1111/j.1440-1746.2008.05685.x
55. Hudcovic, T., Kozakova, H., Kolynska, J., et al. (2009). Monocolonization with Bacteroides ovatus protects immunodeficient SCID mice from mortality in chronic intestinal inflammation caused by long lasting dextran sodium sulfate treatment. Physiol. Research. 58(1):101–110.
56. Irvine, E., Farrokhyar, F., and Swarbrick, E. T., (2001). A critical review of epidemiological studies in inflammatory bowel disease. Scand. J. Gastroenterol. 36:2–15.
57. Jewel, D. P., (1998). Ulcerative colitis. In:Sleisenger & Fordtran's Gastrointestinal and Liver Disease-Pathophysiology, Diagnosis and Management. Vol. 2, pp. 1735–1761. Feldman, M., Scharschmidt, B. F., and Sleisenger, M. H., Eds., Philadelphia.
58. Juillerat, P., Pittet, V., Bulliard, J. L., et al. (2008). Prevalence of inflammatory bowel disease in the Canton of Vaud (Switzerland):A population-based cohort study. J. Crohn's. Colitis. 2:131–141. doi:10.1016/j.crohns.2007.10.006
59. Kale-Pradhan, P. B., Jassal, H. K., Wilhelm, S. M., (2010). Role of Lactobacillus in the prevention of antibiotic-associated diarrhea:A meta analysis. Pharmacotherapy. 30:119–126. doi:10.1592/phco.30.2.119
60. Kaouass, M., Deloyer, P., Wery, I., et al. (1996). Analysis of structural and biochemical events occurring in the small intestine after dietary polyamine ingestion in suckling rats. Dig. Dis. Sci. 41:1434–1444.
61. Kaser, A., Zeissig, S., Blumberg, R. S., (2010). Inflammatory Bowel Disease. Annual. Rev. Immunol. 28:573–621.
62. Kato, K., Mizuno, S., Umesaki, Y., et al. (2004). Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Alim. Pharmacol. Ther. 20(10):1133–1141. doi:10.1111/j.1365-2036.2004.02268.x
63. Koloski, N. A., Bret, L., and Radford-Smith, G., (2008). Hygiene hypothesis in inflammatory bowel disease:A critical review of the literature. World J. Gastroenterol. 14:165–173. doi:10.3748/wjg.14.165
64. Krishnan, A., and Korzenik, J. R., (2002). Inflammatory bowel disease and environmental influences. Gastroenterol. Clin. North Am. 31:21–39.
65. Kronbluth, A., Sachar, D. K., and Salomon, P., (1998). Crohn's disease. In:Sleisenger & Fordtran's Gastrointestinal and Liver Disease:Pathophysiology, Diagnosis, Management, Vol. 6, pp. 1708–1734. Feldman, M., Scharschmidt, B. F., and Sleisenger, M. H., Eds., Philadelphia.
66. Lepage, P., Häsler, R., Spehlmann, M. E., et al. (2011). Twin Study Indicates Loss of Interaction Between Microbiota and Mucosa of Patients With Ulcerative Colitis. Gastroenterology. 141:227–236. http://dx.doi.org/10.1053/j.gastro.2011.04.011
67. Liu, Y. W., Su, Y.W., Ong, W. K., et al. (2011). Oral administration of Lactobacillus plantarum K68 ameliorates DSS-induced ulcerative colitis in BALB/c mice via the anti-inflammatory and immunomodulatory activities. Int. Immunopharmacol. 11:2159–2166. doi:10.1016/j.intimp.2011.09.013
68. Luther, J., Dave, M., Higgins, P. D. R., et al. (2010). Association Between Helicobacter pylori Infection and Inflammatory Bowel Disease:A Meta-analysis and Systematic Review of the Literature. Inflamm. Bowel. Dis. 16(6):1077–1084. doi:10.1002/ibd.21116
69. Lyra, A., Lahtinen, S., and Ouwehand, A. C., (2012). Gastrointestinal benefits of probiotics:clinical evidence. In:Lactic Acid Bacteria:Microbiological and Functional Aspects, pp. 509–523, Lahtinen, S., Ouwehand, A. C., and Salminen, S., Eds., CRC, Boca Raton.
70. Mahadevan, U., Sandborn, W. J., Li, D. K., et al. (2007). Pregnancy outcomes in women with inflammatory bowel disease:A large community-based study of Northern California. Gastroenterology. 33:1106–1112. doi:10.1053/j.gastro.2007.07.019
71. Makharia, G. K., Sood, A., Midha, V., et al. (2008). A randomized, double-blind, placebo-controlled trial of a probiotic preparation, VSL#3, for the treatment of mild to moderate active ulcerative colitis. Gastroenteroly. 134(4):A–99. doi:10.1016/S0016-5085(08)60463-1
72. Manichanh, C., Rigottier‐Gois, L., Bonnaud, E., et al. (2006). Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut. 55(2):205–211. doi:10.1136/gut.2005.073817
73. Matsumoto, S., Hara, T., Hori, T., et al. (2005). Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clin. Exp. Immunol. 140:417–426. doi:10.1111/j.1365-2249.2005.02790.x
74. Matsumoto, M., Kurihara, S., Kibe, R., et al. (2011). Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production. PLoS One. 6(8):e23652.
75. Matsumoto, S., Okabe, Y., Setoyama, H., et al. (1998). Inflammatory bowel disease- like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut. 43:71–78. doi:10.1136/gut.43.1.71
76. Matsumoto, M., Ohishi, H., and Benno, Y., (2001). Impact of LKM512 yogurt on improvement of intestinal environment of the elderly. FEMS Immunol. Med. Microbiol. 31:181–186. doi:10.1111/j.1574-695X.2001.tb00518.x
77. Medina, M., Izquierdo, E., Ennahar, S., et al. (2007). Differential immunomodulatory properties of Bifidobacterium logum strains:relevance to probiotic selection and clinical applications. Clin. Exp. Immun. 150:531–538. doi:10.1111/j.1365-2249.2007.03522.x
78. Miele, E., Pascarella, F., Giannetti, E., et al. (2009). Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am. J. Gastroenterol. 10:437–443. doi:10.1038/ajg.2008.118
79. Moayyedi, P., Ford, A. C, Talley, N. J., et al. (2010). The efficacy of probiotics in the treatment of irritable bowel syndrome:a systematic review. Gut. 59:325–332. doi:10.1136/gut.2008.167270
80. Mondot, S., Kang, S., Furet, J. P., et al. (2011). Highlighting New Phylogenetic Specificities of Crohn's Disease Microbiota. Inflamm. Bowel. Dis. 17(1):185–192. doi:10.1002/ibd.21436
81. Müller, M., and Kersten, S., (2003). Nutrigenomics:goals and strategies. Nature Rev–Genetics. 4:315–322.
82. Nanda-Kumar, N. S., Balamurugan, R., Jayakanthan, K., et al. (2008). Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulphate. J. Gastroenterol. Hepatology. 23:1834–1839.
83. −/− mice. Inflamm. Bowel. Dis. 18(8):1434–1446. doi:10.1002/ibd.22848
84. Neut, C., Bulois, P., Desreumaux, P., et al. (2002). Changes in the bacterial flora of the neoterminal ileum after ileocolonic resection for Crohn's disease. Am. J. Gastroenterol. 97:939–946. doi:10.1111/j.1572-0241.2002.05613.x
85. Ng, S. C., Plamondon, S., Kamm, M. A., et al. (2010). Immunosuppressive effects via human intestinal dendritic cells of probiotic bacteria and steroids in the treatment of acute ulcerative colitis. Inflamm. Bowel. Dis. 16(8):1286–1298. doi:10.1002/ibd.21222
86. Noor, S. O., Ridgway, K., Scovell, L., et al. (2010). Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota. BMC Gastroenterol. 12:134–142. doi:10.1186/1471-230X-10-134
87. Ocón, B., Anzola, A., Ortega-Gonzalez, M., et al. (2013). Active hexose-correlated compound and Bifidobacterium longum BB536 exert symbiotic effects in experimental colitis. European. J. Nutr. 52(2):457–466. doi:10.1007/s00394-012-0347-z
88. O'Hara, A. M., O'Reagan, P., Fanning, A., et al. (2006). Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarus. Immunology. 118:202–215. doi:10.1111/j.1365-2567.2006.02358.x
89. O'Hara, A. M., and Shanahan, F., (2007). Mechanisms of action of probiotics in intestinal diseases. Scientific World J. 7:31–46. http://dx.doi.org/10.1100/tsw.2007.26
90. Oliveira, F. M., Emerick, A. P. C., and Soares, E. G., (2010). Aspectos epidemiológicos das doenças intestinais inflamatórias na macrorregião de saúde leste do Estado de Minas Gerais. Ciência & Saúde Coletiva. 15(1):1031–1037. http://dx.doi.org/10.1590/S1413-81232010000700009
91. Osman, N., Adawi, D., Molin, G., et al. (2006). Bifidobacterium infantis strains with and without a combination of oligofructose and inulin (OFI) attenuate inflammation in DSS-induced colitis in rats. BMC Gastroenterol. 6:6–31. http://www.biomedcentral.com/1471-230X/6/31
92. Ott, S. J., and Schreiber, S., (2004). Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 53:685–693. doi:10.1136/gut.2003.025403
93. Pearson, C., (2004). Inflammatory bowel disease. Clin. Adv. Nutr. 100(9):86–90.
94. Persson, P. G., Ahlbom, A., and Hellers, G., (1992). Diet and inflammatory bowel disease:a case-control study. Epidemiology. 3:47–52.
95. Peran, L., Camuesco, D., Comalada, M., et al. (2006). Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int. J. Colorectal. Dis. 21:737–746. doi:10.1007/s00384-005-0773-y
96. Podolsky, D. K., (2002). Inflammatory bowel disease. New. Eng. J. Medicine. 347:417–429.
97. Qin, J., Li, R., Raes, J., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 464:59–65. doi:10.1038/nature08821
98. Rachmilewitz, D., Katakura, K., Karmeli, F., et al. (2004). Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology. 126:520–528. doi:10.1053/j.gastro.2003.11.019
99. Rimbach, G., Boesch-Saadatmandi, C., Frank, J., et al. (2008). Dietary isoflavones in the prevention of cardiovascular disease–A molecular perspective. Food Chem. Toxicol. 46:1308–1319. http://dx.doi.org/10.1016/j.fct.2007.06.029
100. Rioux, K. P., and Fedorak, R. N., (2006). Probiotics in the treatment of inflammatory bowel disease. J. Clin. Gastroenterol. 40:260–263.
101. Roediger, W., (1980). The colonic epithelium in ulcerative colitis:an energy-deficiency disease. The Lancet. 2:712–715.
102. Rolfe, R. D., (2000). The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 130:396S–402S.
103. Sadlack, B., Merz, H., Schorle, H., et al. (1993). Ulcerative colitis-like disease in mice with disrupted interleukin-2 gene. Cell Press. 17:253–261. doi:10.1016/0092-8674(93)80067-O
104. Sartor, R. B., (2006). Mechanisms of disease:pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3:390–407. doi:10.1038/ncpgasthep0528
105. Scheppach, W., Sommer, H., Kirchner, T., et al. (1992). Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology. 103:51.
106. Schnitzler, F., Fidder, H., Ferrante, M., et al. (2011). Outcome of Pregnancy in Women with Inflammatory Bowel Disease Treated with Antitumor Necrosis Factor Therapy. Inflamm. Bowel. Dis. 17(9):1846–1854. doi:10.1002/ibd.21583
107. Segain, J. P., Raingeard de la Blétière, D., Bourreille, A., et al. (2000). Butyrate inhibits inflammatory responses through NFКB inhibition:implications for Crohn's disease. Gut. 47:397–403. doi:10.1136/gut.47.3.397
108. Shanahan, F., (2000). Probiotics and inflammatory bowel disease:Is there a scientific rationale? lnflamm. Bowel. Dis. 6(2):107–115.
109. Shanahan. (2002). Crohn´s disease. The Lancet. 359:62–69.
110. Shen, J., Ran, H. Z., Yin, M. H., et al. (2009). Meta-analysis:the effect and adverse events of Lactobacilli versus placebo in maintenance therapy for Crohn disease. Int. Med. J. 39:103–109. doi:10.1111/j.1445-5994.2008.01791.x
111. Sivieri, K., Spinardi-Barbisan, A. L. T., Barbisan, L. F., et al. (2008). Probiotic Enterococcus faecium CRL 183 inhibit chemically induced colon cancer in male Wistar rats. Eur. Food Res. Technol. 228:231–237. doi:10.1007/s00217-008-0927-6
112. Smeltzer, S. C., and Bare, B. G., (2002). Tratado de enfermagem médico- cirúrgica. Guanabara Koogan. Rio de Janeiro.
113. Sokol, H., Seksik, P., Furet, J. P., et al. (2009). Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel. Dis. 15:1183–1189. doi:10.1002/ibd.20903
114. Sonnenberg, A., (1986). Geographic variation in the incidence of and mortality from inflammatory bowel disease. Dis. Colon. & Rectum. 29:854–861.
115. Sood, A., Midha, V., Makharia, G. K., et al. (2009). The probiotic preparation VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis. Clin. Gastroenterol. Hepatol. 7:1202–1209. doi:10.1016/j.cgh.2009.07.016
116. Souza, M. H. L. P., Troncon, L. E. A., Rodrigues, C. M., et al. (2002). Evolução da ocorrência (1980–1999) da Doença de Crohn e da Retocolite Ulcerativa Idiopática e análise das suas características clínicas em um hospital universitário do Sudeste do Brasil. Arq. Gastroenterol. 39(2):98–105. http://dx.doi.org/10.1590/S0004-28032002000200006.
117. Steinwurz, F., (1998). Epidemiologia, aspectos clínicos e evolutivos da doença de Crohn. Arq. Gastroenterol. 35:237–239.
118. Stolaki, M., De Vos, W., Kleerebezem, M., et al. (2012). Lactic acid bacteria in the gut. In:Lactic Acid Bacteria:Microbiological and Functional Aspects, pp. 385–401, Lahtinen, S., Ouwehand, A. C., Salminen, S., and von Wright, A., Eds., CRC, Boca Raton.
119. Sydora, B. C., Tavernini, M. M., Doyle, J. S. G., et al. (2005). Association with selected bacteria does not cause enterocolitis in IL-10 gene-deficient mice despite a systemic immune response. Dig. Dis. Sci. 50(5):905–913. doi:10.1007/s10620-005-2663-0
120. Swidsinski, A., Ladhoff, A., Pernthaler, A., et al. (2002). Mucosal flora in inflammatory bowel disease. Gastroenterology. 122:44–54.
121. Szajewska, H., Ruszczynski, M., and Radzikowsky, A., (2006). Probiotics in the prevention of antibiotic-associated diarrhea in children:a meta analysis of randomized controlled trials. J. Pedriatics. 149:367–372. doi:10.1016/j.jpeds.2006.04.053
122. Takaishi, H., Matsuki, T., Nakazawa, A., et al. (2008). Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int. J. Med. Microbiol. 298(5–6):463–472. http://dx.doi.org/10.1016/j.ijmm.2007.07.016
123. Tamboli, C. P., Neut, C., and Desreumaux, P., (2004). Dysbiosis in inflammatory bowel disease. Gut. 51:1–4.
124. Uronis, J. M., Arthur, J. C., Keku, T., et al. (2011). Gut microbial diversity is reduced by the probiotic VSL#3 and correlates with decreased TNBS-induced colitis. Inflamm. Bowel. Dis. 17(1):289–297. doi:10.1002/ibd.21366
125. Van Heel, D. A., McGovern, D. P. B., and Jewell, D. P., (2001). Crohn´s disease:genetic susceptibility, bacteria, and innate immunity. The Lancet. 441:1902–1904. doi:10.1016/S0140-6736(00)05091-1
126. Van Heel, D. A., Udalova, I., Silva, A., et al. (2002). Inflammatory bowel disease is associated with a TNF polymorphism that affects an interaction between the OCT1 and NF-Kb transcription factors. Hum. Mol. Gen. 11:1281–1289. doi:10.1093/hmg/11.11.1281
127. Vendramini, A. P., (2002). Efeito da ingestão de um produto de soja fermentado com Enterococcus faecium e Lactobacillus helveticus na produção de citocinas, óxido nítrico e peróxido de hidrogênio, Dissertação (Mestrado em Análises Clínicas). Faculdade de Ciências Farmacêuticas de Araraquara/UNESP.
128. Venturi, A., Gionchetti, P., Rizzello, F., et al. (1999). Impact on the composition of the faecal flora by a new probiotic preparation:preliminary data on maintenance treatment of patients with ulcerative colitis. Alim. Pharmacol. Ther. 13:1103–1108. doi:10.1046/j.1365-2036.1999.00560.x
129. Waidmann, M., Bechtold, O., Frick, J. S., et al. (2003). Bacteroides vulgatus protects against Escherichia coli-induced colitis in gnotobiotic interleukin-2-deficient mice. Gastroenterology. 125(1):162–177. doi:10.1016/S0016-5085(03)00672-3
130. Wildt, A., Nordgaard, I., Hansen, U., et al. (2011). A randomized 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. Crohn's. Colitis. 5:115–121. doi:10.1016/j.crohns.2010.11.004
131. Willing, B., Halfvarson, J., Dicksved, J., et al. (2009). Twin studies reveal specific imbalances in the mucosa‐associated microbiota of patients with ileal Crohn's disease. Inflamm. Bowel. Dis. 15(5):653–660. doi:10.1002/ibd.20783
132. Zhou, F. X., Chen, L., Liu, X. W., et al. (2012). Lactobacillus crispatus M206119 exacerbates murine DSS-colitis by interfering with inflammatory responses. World J. Gastroenterol. 18(19):2344–2356. doi:10.3748/wjg.v18.i19.2344