Protection and restitution of gut barrier by probiotics: Nutritional and clinical implications

Current Nutrition and Food Science

Volumn 9, Issue 2, 2013, Pages 99-107

  Rao, Radha Krishna ^a   Samak, Geetha ^b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b DVS College of Arts and Science   (India)

Author keywords

Enteric bacteria; Epithelium; Intestine; Signaling; Tight junction

Indexed keywords

ADENYLATE KINASE; CALCIUM; CASEIN KINASE II; CLAUDIN; CYCLIC AMP; JUNCTIONAL ADHESION MOLECULE; MITOGEN ACTIVATED PROTEIN KINASE; OCCLUDIN; PROBIOTIC AGENT; RHO KINASE; TIGHT JUNCTION PROTEIN; TRICELLULIN;

ACTIN FILAMENT; ALCOHOL LIVER DISEASE; APOPTOSIS; BACTERIAL TRANSLOCATION; BIFIDOBACTERIUM LONGUM INFANTIS; CELIAC DISEASE; CELL MIGRATION; CELL PROLIFERATION; CELL PROTECTION; CELL STRAIN CACO 2; CHOLESTASIS; CROHN DISEASE; DIARRHEA; DIGESTIVE SYSTEM; ELECTRIC RESISTANCE; EMOTIONAL STRESS; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; EX VIVO STUDY; FIRST DEGREE RELATIVE; FOOD PROCESSING; GASTROINTESTINAL MUCOSA; GENE EXPRESSION; GLUCONACETOBACTER; GLUCONACETOBACTER XYLINUS; HANSENIASPORA; HUMAN; IMMUNE SYSTEM; INTERSTITIUM; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; INTRACELLULAR SIGNALING; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS BREVIS; LACTOBACILLUS CASEI; LACTOBACILLUS FERMENTUM; LACTOBACILLUS PLANTARUM; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LEUCONOSTOC MESENTEROIDES; MACROMOLECULE; MENTAL STRESS; NECROTIZING ENTEROCOLITIS; NONHUMAN; OXIDATIVE STRESS; PARENTERAL NUTRITION; PEDIOCOCCUS PENTOSACEUS; PICHIA; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES BOULARDII; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SHELF LIFE; STAPHYLOCOCCUS XYLOSUS; STREPTOCOCCUS SALIVARIUS; STREPTOCOCCUS THERMOPHILUS; SYSTEMIC CIRCULATION; THERMAL INJURY; TIGHT JUNCTION; ULCERATIVE COLITIS; ZYGOSACCHAROMYCES;

ANIMALIA; ENTEROBACTERIACEAE;

EID: 84878645943     PISSN: 15734013     EISSN: 22123881     Source Type: Journal    
DOI: 10.2174/1573401311309020004     Document Type: Review

References (121)

1. de Vrese M, Schrezenmeir J. Probiotics, prebiotics and synbiotics. Adv Biochem Eng Biotechnol 2008; 111: 1-66.
2. Caramia G. Probiotics: From metchnikoff to the current preventive and therapeutic possibilities. Pediatr Med Chir 2004; 26: 19-33.
3. Bengmark, S. Pro-and synbiotics to prevent sepsis in major surgery and severe emergencies. Nutrients 2012; 4: 91-111.
4. Boirivant M, Strober W. The mechanism of action of probiotics. Curr Opin Gastroenterol 2007; 23: 679-92.
5. Anderson JM, Van Itallie CM. Tight junctions and the molecular basis for regulation of paracellular permeability. Am J Physiol 1995; 269: G467-75.
6. Dignass AU. Mechanisms and modulation of intestinal epithelial repair. Inflamm Bowel Dis 2001; 7: 68-77.
7. Duggan C, Gannon J, Walker, WA. Protective nutrients and functional foods for the gastrointestinal tract. Am J Clin Nutr 2002; 75: 789-808.
8. Gibson PR. Increased gut permeability in Crohn's disease: is TNF the link? Gut 2004; 53: 1724-5.
9. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, Turner JR. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by upregulating myosin light chain kinase expression. Am J Pathol 2005; 166: 409-19.
10. Welsh F, Farmery S, MacLennan K, et al. Gut barrier function in malnourished patients. Gut 1998; 42: 396-401.
11. Rupani B, Caputo FJ, Watkins AC, et al. Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock. Surgery 2007; 141: 481-9.
12. Viswanathan VK, Koutsouris A, Lukic S, et al. Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infect Immun 2004; 72: 3218-27.
13. Wilmore DW, Smith RJ, O'Dwyer ST, Jacobs DO, Ziegler TR, Wang XD. The gut: A central organ after surgical stress. Surgery 1988. 104: 917-23.
14. Carneiro-Filho BA, Lima IP, Araujo DH, et al. Intestinal barrier function and secretion in methotrexate-induced rat intestinal mucositis. Dig Dis Sci 2004; 49: 65-72.
15. Illig KA, Ryan CK, Hardy DJ, Rhodes J, Locke W, Sax HC. Total parenteral nutrition-induced changes in gut mucosal function: atrophy alone is not the issue. Surgery 1992; 112: 631-7.
16. Yoshida S, Matsui M, Shirouzu Y, Fujita H, Yamana H, Shirouzu K. Effects of glutamine supplements and radiochemotherapy on systemic immune and gut barrier function in patients with advanced esophageal cancer. Ann Surg 1998; 227: 485-91.
17. Ferrier L, Mazelin L, Cenac N, et al. Stress-induced disruption of colonic epithelial barrier: role of interferon-gamma and myosin light chain kinase in mice. Gastroenterology 2003; 125: 795-804.
18. Anderson JM, Van Itallie CM. Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 2009; 1: a002584.
19. Le S, Christopher RW, David R, Raleigh, Dan Y, Jerrold RT. Tight junction pore and leak pathways: a dynamic duo. Ann Rev Physiol 2011; 73: 283-309.
20. Wittchen ES, Haskins J, Stevenson BR. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J Biol Chem 1999; 274: 35179-85.
21. Madara JL, Stafford J, Barenberg D, Carlson S. Functional coupling of tight junctions and microfilaments in T84 monolayers. Am J Physiol 1988; 254: G416-23.
22. Wittchen ES, Haskins J, Stevenson BR. Exogenous expression of the amino-terminal half of the tight junction protein ZO-3 perturbs junctional complex assembly. J Cell Biol 2000; 151: 825-36.
23. Jain S, Suzuki T, Seth A, Samak G, Rao R. Protein kinase Czeta phosphorylates occludin and promotes assembly of epithelial tight junctions. Biochem J 2011. 437: 289-99.
24. Mitic LL, Anderson JM. Molecular architecture of tight junctions. Annu Rev Physiol 1998; 60: 121-42.
25. Suzuki T, Elias BC, Seth A, et al. PKC eta regulates occludin phosphorylation and epithelial tight junction integrity. Proc Natl Acad Sci USA 2009; 106: 61-6.
26. Basuroy S, Sheth P, Kuppuswamy D, Balasubramanian S, Ray RM, Rao RK. Expression of kinase-inactive c-Src delays oxidative stress-induced disassembly and accelerates calcium-mediated reassembly of tight junctions in the Caco-2 cell monolayer. J Biol Chem 2003; 278: 11916-24.
27. Sheth P, Samak G, Shull JA, Seth A, Rao R. Protein phosphatase 2A plays a role in hydrogen peroxide-induced disruption of tight junctions in Caco-2 cell monolayers. Biochem J 2009; 421: 59-70.
28. Rao R. Occludin phosphorylation in regulation of epithelial tight junctions. Ann NY Acad Sci 2009; 1165: 62-8.
29. Zahraoui A, Joberty G, Arpin M, et al. A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J Cell Biol 1994; 124: 101-15.
30. Denker BM, Saha C, Khawaja S, Nigam SK, Involvement of a heterotrimeric G protein alpha subunit in tight junction biogenesis. J Biol Chem 1996; 271: 25750-3.
31. Sheth P, Basuroy S, Li C, Naren AP, Rao RK. Role of phosphatidylinositol 3-kinase in oxidative stress-induced disruption of tight junctions. J Biol Chem 2003; 278: 49239-45.
32. Samak G, Narayanan D, Jaggar JH, Rao R. CaV1.3 channels and intracellular calcium mediate osmotic stress-induced N-terminal c-Jun kinase activation and disruption of tight junctions in Caco-2 Cell Monolayers. J Biol Chem 2011; 286: 30232-43.
33. Duffey ME, Hainau B, Ho S, Bentzel CJ. Regulation of epithelial tight junction permeability by cyclic AMP. Nature 1981; 294: 451-3.
34. Zhang L, Li J, Young LH, Caplan MJ. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci USA 2006; 103: 17272-7.
35. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology 2001; 121: 566-79.
36. Stuart RO, Nigam SK. Regulated assembly of tight junctions by protein kinase C. Proc Natl Acad Sci USA 1995; 92: 6072-6.
37. Samak G, Suzuki T, Bhargava A, Rao RK. c-Jun NH2-terminal kinase-2 mediates osmotic stress-induced tight junction disruption in the intestinal epithelium. Am J Physiol Gastrointest Liver Physiol 2010; 299: G572-84.
38. Basuroy S, Seth A, Elias B, Naren AP, Rao R. MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem J 2006; 393: 69-77.
39. Resta-Lenert S, Barrett KE. Probiotics and commensals reverse TNF-alpha-and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 2006; 130: 731-46.
40. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 2007; 132: 562-75.
41. Yan F, Polk DB. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 2002; 277: 50959-65.
42. Yan F, Polk DB. Probiotics as functional food in the treatment of diarrhea. Curr Opin Clin Nutr Metab Care 2006; 9: 717-21.
43. Madsen K, Cornish A, Soper P, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 2001; 121: 580-91.
44. Gauhea A, Györgya P, Hoover JRE. Bifidus factor. IV. Preparations obtained from human milk. Arch Biochem Biophys 1954; 48: 214-24.
45. Borthakur A, Gill RK, Tyagi S. The probiotic Lactobacillus acidophilus stimulates chloride/hydroxyl exchange activity in human intestinal epithelial cells. J Nutr 2008; 138: 1355-9.
46. Ahrne S, Hagslatt, JM-L. Effect of lactobacilli on paracellular permeability in the gut. Nutrients 2011; 3: 104-17.
47. Seth A, Yan F, Polk DB, Rao RK. Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKCand MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 2008; 294: G1060-9.
48. Forsyth CB, Farhadi A, Jakate SM, Tang Y, Shaikh M, Keshavarzian A. Lactobacillus GG treatment ameliorates alcoholinduced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 2009; 43: 163-72.
49. Johnson-Henry KC, Donato KA, Shen-Tu G, Gordanpour M, Sherman PM. Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function. Infect Immun 2008; 76: 1340-8.
50. Schultz M, Veltkamp C, Dieleman LA, et al. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis 2002; 8: 71-80.
51. Mao Y, Nobaek S, Kasravi B, et al. The effects of Lactobacillus strains and oat fiber on methotrexate-induced enterocolitis in rats. Gastroenterology 1996; 111: 334-44.
52. Karczewski J, Troost FJ, Konings I, et al., Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 2010; 298: G851-9.
53. Ko JS, Yang HR, Chang JY, Seo JK. et al., Lactobacillus plantarum inhibits epithelial barrier dysfunction and interleukin-8 secretion induced by tumor necrosis factor-alpha. World J Gastroenterol 2007; 13: 1962-5.
54. 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 2009; 92: 2400-8.
55. White JS, Hoper M, Parks RW, Clements WD, Diamond T, Bengmark S. The probiotic bacterium Lactobacillus plantarum species 299 reduces intestinal permeability in experimental biliary obstruction. Lett Appl Microbiol 2006; 42: 19-23.
56. Qin H, Zhongwei Zhang Z, Xiaomin Hang X, Yanqun Jiang Y. Plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol 2009; 9: 63.
57. Parassol N, Freitas M, Thoreux K, Dalmasso G, Bourdet-Sicard R, Rampal P. Lactobacillus casei DN-114 001 inhibits the increase in paracellular permeability of enteropathogenic Escherichia coliinfected T84 cells. Res Microbiol 2005; 156: 256-62.
58. Llopis M, Antolín M, Guarner F, Salas A, Malagelada, J-R. Mucosal colonisation with Lactobacillus casei mitigates barrier injury induced by exposure to trinitronbenzene sulphonic acid. Gut 2005; 54: 955-9.
59. Llopis M, Antolin M, Carol M, et al. Lactobacillus casei downregulates commensals' inflammatory signals in Crohn's disease mucosa. Inflamm Bowel Dis 2009; 15: 275-83.
60. Zakostelska Z, Kverka M, Klimesova K, et al. Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS One 2011; 60: e27961.
61. Zareie M, Johnson-Henry K, Jury J, et al. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 2006; 55: 1553-60.
62. Eutamene H, Lamine F, Chabo C, et al. Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats. J Nutr 2007; 137: 1901-7.
63. Lebeer S, Vanderleyden J, De Keersmaecker SC. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 2008; 72: 728-64
64. Ewaschuk JB, Diaz H, Meddings L, et al. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol 2008; 295: G1025-34.
65. Wang Z, Xiao G, Yao Y, Guo S, Lu K, Sheng Z. The role of Bifidobacteria in gut barrier function after thermal injury in rats. J Trauma 2006; 61: 650-7.
66. Khailova L, Dvorak K, Arganbright KM, et al. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2009. 297: G940-9.
67. Qiao H, Duffy LC, Griffiths E, et al. Immune responses in rhesus rotavirus-challenged BALB/c mice treated with bifidobacteria and prebiotic supplements. Pediatr Res 2002. 51: 50-5.
68. Shu, Q, Gill, H.S. A dietary probiotic (Bifidobacterium lactis HN019) reduces the severity of Escherichia coli O157:H7 infection in mice. Med Microbiol Immunol 2001; 189: 147-52.
69. Mennigen R, Bruewer M. Effect of probiotics on intestinal barrier function. Ann NY Acad Sci 2009. 1165: 183-9.
70. Mennigen R, Nolte K, Rijcken E, 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 2009; 296: G1140-9.
71. Girardin M, Seidman EG, Indications for the use of probiotics in gastrointestinal diseases. Digest Dis 2011; 29: 574-87.
72. Herbrecht R, Nivoix Y. Saccharomyces cerevisiae fungemia: an adverse effect of Saccharomyces boulardii probiotic administration. Clin Infect Dis 2005; 40: 1635-7.
73. X. Wu X, Vallance VA, Boyer L, et al. Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. Am J Physiol Gastrointest Liver Physiol 2008; 294: G295-306.
74. Bai YH, Pak SC, Lee SH, et al. Assessment of a bioactive compound for its potential antiinflammatory property by tight junction permeability. Phytother Res 2005; 19: 1009-12.
75. Generoso SV, Viana M, Santos R, et al. Saccharomyces cerevisiae strain UFMG 905 protects against bacterial translocation, preserves gut barrier integrity and stimulates the immune system in a murine intestinal obstruction model. Arch Microbiol 2010; 192: 477-84.
76. Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol 2007; 9: 804-16.
77. Sya N, Ukena SN, Singh A, Dringenberg U, et al. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PloS one 2007; 2: e1308.
78. Veltman K, Hummel S, Cichon C, Sonnenborn U, Schmidt MA. Identification of specific miRNAs targeting proteins of the apical junctional complex that simulate the probiotic effect of E. coli Nissle 1917 on T84 epithelial cells. Int J Biochem Cell Biol 2012; 44: 341-9.
79. Trebichavsk- I, Splíchal I. Probiotics manipulate host cytokine response and induce antimicrobial peptides. Folia Microbiol (Praha), 2006; 51: 507-10.
80. Candela M, Perna F, Carnevali P, et al. Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 2008; 125: 286-92.
81. Kravtsov EG, Yermolayev AV, Anokhina IV, Yashina NV, Chesnokova VL, Dalin MV. Adhesion characteristics of lactobacillus is a criterion of the probiotic choice. Bull Exp Biol Med 2008; 145: 232-4.
82. Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 2009; 139: 1619-25.
83. Putaala H, Salusjärvi T, Nordström M, et al. Effect of four probiotic strains and Escherichia coli O157:H7 on tight junction integrity and cyclo-oxygenase expression. Res Microbiol 2008; 159: 692-8.
84. Segawa S, Fujiya M, Konishi H, et al. Probiotic-derived polyphosphate enhances the epithelial barrier function and maintains intestinal homeostasis through integrin-p38 MAPK pathway. PLoS One 2011; 6: e23278.
85. Erkkilä S, Suihko ML, Eerola S, Petäjä E, Mattila-Sandholm T. Dry sausage fermented by Lactobacillus rhamnosus strains. Int J Food Microbiol 2001; 64: 205-10.
86. Carissa M. Thomas CM, Hong T, van Pijkeren JP, et al. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 2012; 7: e31951.
87. Vinderola G, Perdigón G, Duarte J, Farnworth E, Matar C. Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity. Cytokine 2006; 36: 254-60.
88. Aquilanti L, Carbini A, Strappati R, et al. Characterisation of Lactobacillus helveticus strains producing antihypertensive peptides by RAPD and inverse-PCR of IS elements. Benef Microbes 2010; 1: 229-42.
89. Sutyak KE, Wirawan RE, Aroutcheva AA, Chikindas ML. Isolation of the Bacillus subtilis antimicrobial peptide subtilosin from the dairy product-derived Bacillus amyloliquefaciens. J Appl Microbiol 2008; 104: 1067-74.
90. Zhang L, Li N, Caicedo R, Neu J. Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 2005; 135: 1752-6
91. Ohland CL, Macnaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 2010; 298: G807-19.
92. Anderson RC, Cookson AL, McNabb WC, et al. Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol 2010; 10: 316.
93. Arvola T, Laiho K, Torkkeli S, et al. Prophylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: a randomized study. Pediatrics 1999; 104: e64.
94. Armuzzi A, Cremonini F, Ojetti V, et al. Effect of Lactobacillus GG supplementation on antibiotic-associated gastrointestinal side effects during Helicobacter pylori eradication therapy: A pilot study. Digestion 2001; 63: 1-7.
95. Armuzzi A, Cremonini F, Bartolozzi F, et al. The effect of oral administration of Lactobacillus GG on antibiotic-associated gastrointestinal side-effects during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2001; 15: 163-9.
96. Gotteland, M, Cruchet S, Verbeke S. Effect of Lactobacillus ingestion on the gastrointestinal mucosal barrier alterations induced by indometacin in humans. Aliment Pharmacol Ther 2001; 15: 11-7.
97. Koebnick C, Wagner I, Leitzmann P, Stern U, Zunft HJ. Probiotic beverage containing Lactobacillus casei Shirota improves gastrointestinal symptoms in patients with chronic constipation. Can J Gastroenterol 2003; 17: 655-9.
98. Huynh HQ, 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 2009; 15: 760-8.
99. Schultz M. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm Bowel Dis 2008; 14: 1012-8.
100. Gupta P, Andrew H, Kirschner BS, Guandalini S. Is lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study. J Pediatr Gastroenterol Nutr 2000. 31: 453-7.
101. Pessi T, Sütas Y, Hurme M, Isolauri E., Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy 2000; 30: 1804-8.
102. Bin-Nun A, Bromiker R, Wilschanski M, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr 2005; 147: 192-6.
103. Gruenwald J, Graubaum HJ, Harde A. Effect of a probiotic multivitamin compound on stress and exhaustion. Adv Ther 2002; 19: 141-50.
104. Kim HS, Park H, Cho IY, Paik HD, Park E. Dietary supplementation of probiotic Bacillus polyfermenticus, Bispan strain, modulates natural killer cell and T cell subset populations and immunoglobulin G levels in human subjects. J Med Food 2006; 9: 321-7.
105. Kajander K, Hatakka K, Poussa T, Färkkilä M, Korpela R. A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment Pharmacol Ther 2005; 22: 387-94.
106. Hun L. Bacillus coagulans significantly improved abdominal pain and bloating in patients with IBS. Postgrad Med 2009; 121:119-24.
107. Hammer HF. Gut microbiota and inflammatory bowel disease. Dig Dis 2011; 29: 550-3.
108. Meijer BJ, Dieleman LA. Probiotics in the treatment of human inflammatory bowel diseases: Update 2011. J Clin Gastroenterol 2011; 45: S139-44.
109. O'Sullivan MA, O'Morain CA. Bacterial supplementation in the irritable bowel syndrome. A randomised double-blind placebocontrolled crossover study. Dig Liver Dis 2000; 32: 294-301.
110. Bausserman M, Michail S. The use of Lactobacillus GG in irritable bowel syndrome in children: A double-blind randomized control trial. J Pediatr 2005; 147: 197-201.
111. Butterworth AD, Thomas AG, Akobeng AK. Probiotics for induction of remission in Crohn's disease. Cochrane Database Syst Rev 2008: CD006634.
112. Elli M, Callegari ML, Ferrari S, et al. Survival of yogurt bacteria in the human gut. Appl Environ Microbiol 2006; 72: 5113-7.
113. Dufresne CJ, Farnworth ER. A review of latest research findings on the health promotion properties of tea. J Nutr Biochem 2001; 12: 404-21.
114. Lopitz-Otsoa F, Rementeria A, Elguezabal N, Garaizar J. Kefir: a symbiotic yeasts-bacteria community with alleged healthy capabilities. Rev Iberoam Micol 2006; 23: 67-74.
115. Fleming HP, McFeeters RF, Humphries EG. A fermentor for study of sauerkraut fermentation. Biotechnol Bioeng 1988; 31: 189-97.
116. Cheigh HS, Park KY. Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Crit Rev Food Sci Nutr 1994; 34: 175-203.
117. Gardiner GE, Ross RP, Collins JK, Fitzgerald G, Stanton C. Development of a probiotic cheddar cheese containing humanderived Lactobacillus paracasei strains. Appl Environ Microbiol 1998; 64: 2192-9.
118. Heyman M, Menard S. Probiotic microorganisms: how they affect intestinal pathophysiology. Cell Mol Life Sci 2002; 59: 1151-65.
119. Shimakawa Y, Matsubara S, Yuki N, Ikeda M, Ishikawa F. Evaluation of Bifidobacterium breve strain Yakult-fermented soymilk as a probiotic food. Int J Food Microbiol 2003; 81: 131-6.
120. Vuyst LD, Falony G, Leroy F. Probiotics in fermented sausages. Meat Sci 2008; 80: 75-8.
121. Nikawa H, Makihira S, Fukushima H, et al. Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci. Int J Food Microbiol 2004; 95: 219-23.