Probiotics, immunity and exercise: A review

Exercise Immunology Review

Volumn 15, Issue , 2009, Pages 107-126

  West, N P ^a,b,c   Pyne, D B ^c   Peake, J M ^d,e   Cripps, Allan W ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c AUSTRALIAN INSTITUTE OF SPORT   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e QUEENSLAND ACADEMY OF SPORT   (Australia)

Author keywords

Exercise immunology; Gastrointestinal illness; Immunity; Intestinal microbial flora; Probiotics

Indexed keywords

MUCIN; PROBIOTIC AGENT; YOGHURT;

ADULT; ANIMAL; CELLULAR IMMUNITY; CLINICAL TRIAL; CROSSOVER PROCEDURE; CYTOLOGY; DIARRHEA; DOUBLE BLIND PROCEDURE; DRUG EFFECT; EXERCISE; FEMALE; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOLOGY; INTESTINE ABSORPTION; INTESTINE MUCOSA; LYMPHOID TISSUE; MALE; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; RESPIRATORY TRACT INFECTION; REVIEW; SECRETION; STOMACH MUCOSA; URINARY TRACT INFECTION;

ANIMALS; CLINICAL TRIALS AS TOPIC; CROSS-OVER STUDIES; DIARRHEA; DOUBLE-BLIND METHOD; EXERCISE; FEMALE; GASTRIC MUCOSA; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; IMMUNITY, CELLULAR; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; LYMPHOID TISSUE; MALE; MUCINS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RESPIRATORY TRACT INFECTIONS; STRESS, PHYSIOLOGICAL; URINARY TRACT INFECTIONS; YOGURT; YOUNG ADULT;

EID: 74049085410     PISSN: 10775552     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (111)

1. Alberda C, Gramlich L, Meddings J, Field C, McCargar L, Kutsogiannis D, Fedorak R, and Madsen K. Effects of probiotic therapy in critically ill patients: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr 85: 816-823, 2007. (Pubitemid 46393515)
2. Allen SJ, Okoko B, Martinez E, Gregorio G, and Dans LF. Probiotics for treating infectious diarrhoea. Cochrane Database Syst Rev CD003048, 2004.
3. Allgrove JE, Gomes E, Hough J, and Gleeson M. Effects of exercise intensity on salivary antimicrobial proteins and markers of stress in active men. Journal of Sports Sciences 26: 653-661, 2008. (Pubitemid 351419896)
4. Arunachalam K, Gill HS, and Chandra RK. Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr 54: 263-267, 2000. (Pubitemid 30156738)
5. Barrett B, Harahan B, Brown D, Zhang Z, and Brown R. Sufficiently important difference for common cold: severity reduction. Ann Fam Med 5: 216-223, 2007. (Pubitemid 46889998)
6. Berg A, Muller HM, Rathmann S, and Deibert P. The gastrointestinal system - an essential target organ of the athlete's health and physical performance. Exerc Immunol Rev 5: 78-95, 1999. (Pubitemid 29340642)
7. Bergen WG, and Wu G. Intestinal nitrogen recycling and utilization in health and disease. J Nutr 139: 821-825, 2009.
8. Bethell DR, and Huang J. Recombinant human lactoferrin treatment for global health issues: iron deficiency and acute diarrhea. Biometals 17: 337-342, 2004. (Pubitemid 38987159)
9. Bishop NC, and Gleeson M. Acute and chronic effects of exercise on markers of mucosal immunity. Front Biosci 14: 4444-4456, 2009.
10. Brandtzaeg P. Do salivary antibodies reliably reflect both mucosal and systemic immunity? Ann N Y Acad Sci 1098: 288-311, 2007. (Pubitemid 47092533)
11. Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JK, Doherty JM, Mills JC, and Colonna M. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457: 722-725, 2009.
12. Cerutti A. The regulation of IgA class switching. Nat Rev Immunol 8: 421-434, 2008. (Pubitemid 351733417)
13. Chiang BL, Sheih YH, Wang LH, Liao CK, and Gill HS. Enhancing immunity by dietary consumption of a probiotic lactic acid bacterium (Bifidobacterium lactis HN019): optimization and definition of cellular immune responses. Eur J Clin Nutr 54: 849-855, 2000.
14. Christensen HR, Frokiaer H, and Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168: 171-178, 2002. (Pubitemid 34014116)
15. Christensen HR, Larsen CN, Kaestel P, Rosholm LB, Sternberg C, Michaelsen KF, and Frokiaer H. Immunomodulating potential of supplementation with probiotics: a dose-response study in healthy young adults. FEMS Immunol Med Microbiol 47: 380-390, 2006. (Pubitemid 44035888)
16. Clancy RL, Gleeson M, Cox A, Callister R, Dorrington M, D'Este C, Pang G, Pyne D, Fricker P, and Henriksson A. Reversal in fatigued athletes of a defect in interferon gamma secretion after administration of Lactobacillus acidophilus. Br J Sports Med 40: 351-354, 2006.
17. Corthesy B, Gaskins HR, and Mercenier A. Cross-talk between probiotic bacteria and the host immune system. J Nutr 137: 781S-790S, 2007. (Pubitemid 46397518)
18. Cox AJ, Pyne DB, Saunders PU, Callister R, and Gleeson M. Cytokine responses to treadmill running in healthy and illness-prone athletes. Med Sci Sports Exerc 39: 1918-1926, 2007. (Pubitemid 350073354)
19. Cox AJ, Pyne DB, Saunders PU, and Fricker PA. Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. Br J Sports Med 2008.
20. Cummings JH, Antoine JM, Azpiroz F, Bourdet-Sicard R, Brandtzaeg P, Calder PC, Gibson GR, Guarner F, Isolauri E, Pannemans D, Shortt C, Tuijtelaars S, and Watzl B. PASSCLAIM - gut health and immunity. Eur J Nutr 43 Suppl 2: II118-II173, 2004.
21. Davison G, Allgrove J, and Gleeson M. Salivary antimicrobial peptides (LL-37 and alpha-defensins HNP1-3), antimicrobial and IgA responses to prolonged exercise. Eur J Appl Physiol 106: 277-284, 2009.
22. de Vrese M, and Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 111: 1-66, 2008.
23. de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, Ott S, Hampe J, Schreiber S, Heller K, and Schrezenmeir J. Probiotic bacteria reduced duration and severity but not the incidence of common cold episodes in a double blind, randomized, controlled trial. Vaccine 24: 6670-6674, 2006.
24. Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y, and Roy D. Immunomodulatory effects of probiotics in the intestinal tract. Curr Issues Mol Biol 10: 37-54, 2008. (Pubitemid 351756577)
25. Delzenne NM, and Cani PD. [Gut microflora is a key player in host energy homeostasis]. Med Sci (Paris) 24: 505-510, 2008.
26. Diop L, Guillou S, and Durand H. Probiotic food supplement reduces stress-induced gastrointestinal symptoms in volunteers: a double-blind, placebo-controlled, randomized trial. Nutr Res 28: 1-5, 2008.
27. Dubin RF, Robinson SK, and Widdicombe JH. Secretion of lactoferrin and lysozyme by cultures of human airway epithelium. Am J Physiol Lung Cell Mol Physiol 286: L750-755, 2004. (Pubitemid 38365060)
28. Eutamene H, Lamine F, Chabo C, Theodorou V, Rochat F, Bergonzelli GE, Corthesy-Theulaz I, Fioramonti J, and Bueno L. Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats. J Nutr 137: 1901-1907, 2007. (Pubitemid 47292737)
29. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, Backer J, Looijervan Langen M, and Madsen KL. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol 295: G1025-1034, 2008.
30. Genton L, van Gemert W, Pichard C, and Soeters P. Physiological functions should be considered as true end points of nutritional intervention studies. Proc Nutr Soc 64: 285-296, 2005. (Pubitemid 41160755)
31. Gill HS, Rutherfurd KJ, Cross ML, and Gopal PK. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 74: 833-839, 2001. (Pubitemid 33101806)
32. Gleeson M. Assessing immune function changes in exercise and diet intervention studies. Curr Opin Clin Nutr Metab Care 8: 511-515, 2005. (Pubitemid 41192326)
33. Gleeson M. Mucosal immunity and respiratory illness in elite athletes. Int J Sports Med 21 Suppl 1: S33-43, 2000. (Pubitemid 30342603)
34. Gleeson M, Hall ST, McDonald WA, Flanagan AJ, and Clancy RL. Salivary IgA subclasses and infection risk in elite swimmers. Immunol Cell Biol 77: 351-355, 1999. (Pubitemid 29370107)
35. Gleeson M, Pyne DB, and Callister R. The missing links in exercise effects on mucosal immunity. Exerc Immunol Rev 10: 107-128, 2004.
36. Guarino A, Lo Vecchio A, and Canani RB. Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol 25: 18-23, 2009.
37. Haaland DA, Sabljic TF, Baribeau DA, Mukovozov IM, and Hart LE. Is regular exercise a friend or foe of the aging immune system? A systematic review. Clin J Sport Med 18: 539-548, 2008.
38. Haller D, Bode C, Hammes WP, Pfeifer AM, Schiffrin EJ, and Blum S. Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 47: 79-87, 2000. (Pubitemid 30430415)
39. Hamer M, Wolvers D, and Albers R. Using stress models to evaluate immuno-modulating effects of nutritional intervention in healthy individuals. J Am Coll Nutr 23: 637-646, 2004. (Pubitemid 40096754)
40. Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, Gionchetti P, Campieri M, Kamm MA, Knight SC, and Stagg AJ. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53: 1602-1609, 2004. (Pubitemid 39434103)
41. Hayday AC, and Peakman M. The habitual, diverse and surmountable obstacles to human immunology research. Nat Immunol 9: 575-580, 2008. (Pubitemid 351712624)
42. Heerdt BG, Houston MA, and Augenlicht LH. Short-chain fatty acid-initiated cell cycle arrest and apoptosis of colonic epithelial cells is linked to mitochondrial function. Cell Growth Differ 8: 523-532, 1997. (Pubitemid 27273063)
43. Horn P, Kalz A, Lim CL, Pyne D, Saunders P, Mackinnon L, Peake J, and Suzuki K. Exercise-recruited NK cells display exercise-associated eHSP-70. Exerc Immunol Rev 13: 100-111, 2007.
44. Hrncir T, Stepankova R, Kozakova H, Hudcovic T, and Tlaskalova-Hogenova H. Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: studies in germ-free mice. BMC Immunol 9: 65, 2008.
45. Ishikawa H, Tanaka K, Maeda Y, Aiba Y, Hata A, Tsuji NM, Koga Y, and Matsumoto T. Effect of intestinal microbiota on the induction of regulatory CD25+ CD4+ T cells. Clin Exp Immunol 153: 127-135, 2008. (Pubitemid 351809336)
46. Jain PK, McNaught CE, Anderson AD, MacFie J, and Mitchell CJ. Influence of synbiotic containing Lactobacillus acidophilus La5, Bifidobacterium lactis Bb 12, Streptococcus thermophilus, Lactobacillus bulgaricus and oligofructose on gut barrier function and sepsis in critically ill patients: a randomised controlled trial. Clin Nutr 23: 467-475, 2004. (Pubitemid 39107024)
47. Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Jarvenpaa S, Kautiainen H, Julkunen I, Vapaatalo H, and Korpela R. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14: 2029-2036, 2008. (Pubitemid 351795822)
48. Kekkonen RA, Vasankari TJ, Vuorimaa T, Haahtela T, Julkunen I, and Korpela R. The effect of probiotics on respiratory infections and gastrointestinal symptoms during training in marathon runners. Int J Sport Nutr Exerc Metab 17: 352-363, 2007. (Pubitemid 47359006)
49. Kelly D, Conway S, and Aminov R. Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol 26: 326-333, 2005. (Pubitemid 40732666)
50. Kelsall B. Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol 1: 460-469, 2008.
51. Kendall CW, Emam A, Augustin LS, and Jenkins DJ. Resistant starches and health. J AOAC Int 87: 769-774, 2004.
52. Klein A, Friedrich U, Vogelsang H, and Jahreis G. Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. Eur J Clin Nutr 62: 584-593, 2008. (Pubitemid 351663397)
53. Klingberg TD, and Budde BB. The survival and persistence in the human gastrointestinal tract of five potential probiotic lactobacilli consumed as freeze-dried cultures or as probiotic sausage. Int J Food Microbiol 109: 157-159, 2006.
54. Koretz RL. Death, morbidity and economics are the only end points for trials. Proc Nutr Soc 64: 277-284, 2005.
55. Kudsk KA. Current aspects of mucosal immunology and its influence by nutrition. Am J Surg 183: 390-398, 2002. (Pubitemid 34442503)
56. Lenoir-Wijnkoop I, Sanders ME, Cabana MD, Caglar E, Corthier G, Rayes N, Sherman PM, Timmerman HM, Vaneechoutte M, Van Loo J, and Wolvers DA. Probiotic and prebiotic influence beyond the intestinal tract. Nutr Rev 65: 469-489, 2007. (Pubitemid 351804339)
57. Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, Zhang Y, Shen J, Pang X, Zhang M, Wei H, Chen Y, Lu H, Zuo J, Su M, Qiu Y, Jia W, Xiao C, Smith LM, Yang S, Holmes E, Tang H, Zhao G, Nicholson JK, Li L, and Zhao L. Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A 105: 2117-2122, 2008. (Pubitemid 351439474)
58. Lillehoj ER, and Kim KC. Airway mucus: its components and function. Arch Pharm Res 25: 770-780, 2002. (Pubitemid 43066562)
59. Mack DR, Ahrne S, Hyde L, Wei S, and Hollingsworth MA. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52: 827-833, 2003. (Pubitemid 36613489)
60. Mack DR, Michail S, Wei S, McDougall L, and Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol 276: G941-950, 1999. (Pubitemid 29214108)
61. Mackinnon LT. Chronic exercise training effects on immune function. Med Sci Sports Exerc 32: S369-376, 2000. (Pubitemid 30482636)
62. Macpherson AJ. IgA adaptation to the presence of commensal bacteria in the intestine. Curr Top Microbiol Immunol 308: 117-136, 2006. (Pubitemid 47400299)
63. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, and De Simone C. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121: 580-591, 2001. (Pubitemid 32822573)
64. Marcos A, Warnberg J, Nova E, Gomez S, Alvarez A, Alvarez R, Mateos JA, and Cobo JM. The effect of milk fermented by yogurt cultures plus Lactobacillus casei DN-114001 on the immune response of subjects under academic examination stress. Eur J Nutr 43: 381-389, 2004. (Pubitemid 40064275)
65. McFarland LV. Meta-analysis of probiotics for the prevention of traveler's diarrhea. Travel Med Infect Dis 5: 97-105, 2007. (Pubitemid 46222221)
66. Meyer AL, Elmadfa I, Herbacek I, and Micksche M. Probiotic, as well as conventional yogurt, can enhance the stimulated production of proinflammatory cytokines. J Hum Nutr Diet 20: 590-598, 2007. (Pubitemid 350142240)
67. Meyer AL, Micksche M, Herbacek I, and Elmadfa I. Daily intake of probiotic as well as conventional yogurt has a stimulating effect on cellular immunity in young healthy women. Ann Nutr Metab 50: 282-289, 2006. (Pubitemid 43829820)
68. Michel C, Kravtchenko TP, David A, Gueneau S, Kozlowski F, and Cherbut C. In vitro prebiotic effects of Acacia gums onto the human intestinal microbiota depends on both botanical origin and environmental pH. Anaerobe 4: 257-266, 1998. (Pubitemid 29353671)
69. Mondel M, Schroeder BO, Zimmermann K, Huber H, Nuding S, Beisner J, Fellermann K, Stange EF, and Wehkamp J. Probiotic E. coli treatment mediates antimicrobial human beta-defensin synthesis and fecal excretion in humans. Mucosal Immunol 2: 166-172, 2009.
70. Montalto M, Maggiano N, Ricci R, Curigliano V, Santoro L, Di Nicuolo F, Vecchio FM, Gasbarrini A, and Gasbarrini G. Lactobacillus acidophilus protects tight junctions from aspirin damage in HT-29 cells. Digestion 69: 225-228, 2004. (Pubitemid 39140468)
71. Muns G. Effect of long-distance running on polymorphonuclear neutrophil phagocytic function of the upper airways. Int J Sports Med 15: 96-99, 1994. (Pubitemid 24068423)
72. Ndagijimana M, Laghi L, Vitali B, Placucci G, Brigidi P, and Guerzoni ME. Effect of a synbiotic food consumption on human gut metabolic profiles evaluated by (1)H Nuclear Magnetic Resonance spectroscopy. Int J Food Microbiol 2009.
73. Nichols AW. Probiotics and athletic performance: a systematic review. Curr Sports Med Rep 6: 269-273, 2007. (Pubitemid 47235584)
74. O'Hara AM, O'Regan P, Fanning A, O'Mahony C, Macsharry J, Lyons A, Bienenstock J, O'Mahony L, and Shanahan F. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118: 202-215, 2006. (Pubitemid 43727425)
75. Olguin F, Araya M, Hirsch S, Brunser O, Ayala V, Rivera R, and Gotteland M. Prebiotic ingestion does not improve gastrointestinal barrier function in burn patients. Burns 31: 482-488, 2005. (Pubitemid 40724487)
76. Olivares M, Paz Diaz-Ropero M, Gomez N, Sierra S, Lara-Villoslada F, Martin R, Miguel Rodriguez J, and Xaus J. Dietary deprivation of fermented foods causes a fall in innate immune response. Lactic acid bacteria can counteract the immunological effect of this deprivation. J Dairy Res 73: 492-498, 2006. (Pubitemid 44624080)
77. Paineau D, Carcano D, Leyer G, Darquy S, Alyanakian MA, Simoneau G, Bergmann JF, Brassart D, Bornet F, and Ouwehand AC. Effects of seven potential probiotic strains on specific immune responses in healthy adults: a double-blind, randomized, controlled trial. FEMS Immunol Med Microbiol 53: 107-113, 2008. (Pubitemid 351659718)
78. Pals KL, Chang RT, Ryan AJ, and Gisolfi CV. Effect of running intensity on intestinal permeability. J Appl Physiol 82: 571-576, 1997. (Pubitemid 27090185)
79. Perdigon G, Alvarez S, Rachid M, Aguero G, and Gobbato N. Immune system stimulation by probiotics. J Dairy Sci 78: 1597-1606, 1995.
80. Petrof EO, Kojima K, Ropeleski MJ, Musch MW, Tao Y, De Simone C, and Chang EB. Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 127: 1474- 1487, 2004.
81. Pregliasco F, Anselmi G, Fonte L, Giussani F, Schieppati S, and Soletti L. A new chance of preventing winter diseases by the administration of synbiotic formulations. J Clin Gastroenterol 42 Suppl 3 Pt 2: S224-233, 2008.
82. Pyne DB, and Gleeson M. Effects of intensive exercise training on immunity in athletes. Int J Sports Med 19 Suppl 3: S183-191; discussion S191-184, 1998.
83. Pyne DB, McDonald WA, Gleeson M, Flanagan A, Clancy RL, and Fricker PA. Mucosal immunity, respiratory illness, and competitive performance in elite swimmers. Med Sci Sports Exerc 33: 348-353, 2001. (Pubitemid 32209651)
84. Resta-Lenert S, and Barrett K. Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130: 731-746, 2006. (Pubitemid 43374524)
85. Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, and Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 6: 507- 514, 2005.
86. Rochet V, Rigottier-Gois L, Sutren M, Krementscki MN, Andrieux C, Furet JP, Tailliez P, Levenez F, Mogenet A, Bresson JL, Meance S, Cayuela C, Leplingard A, and Dore J. Effects of orally administered Lactobacillus casei DN-114 001 on the composition or activities of the dominant faecal microbiota in healthy humans. Br J Nutr 95: 421-429, 2006.
87. Roessler A, Friedrich U, Vogelsang H, Bauer A, Kaatz M, Hipler UC, Schmidt I, and Jahreis G. The immune system in healthy adults and patients with atopic dermatitis seems to be affected differently by a probiotic intervention. Clin Exp Allergy 38: 93- 102, 2008.
88. Rosenthal KL. Tweaking Innate Immunity: the Promise of Innate Immunologicals As Anti-infectives. Can J Infect Dis Med Microbiol 17: 307-314, 2006. (Pubitemid 44898670)
89. Rosignoli P, Fabiani R, De Bartolomeo A, Fuccelli R, Pelli MA, and Morozzi G. Genotoxic effect of bile acids on human normal and tumour colon cells and protection by dietary antioxidants and butyrate. Eur J Nutr 47: 301-309, 2008.
90. Rosignoli P, Fabiani R, De Bartolomeo A, Spinozzi F, Agea E, Pelli MA, and Morozzi G. Protective activity of butyrate on hydrogen peroxide-induced DNA damage in isolated human colonocytes and HT29 tumour cells. Carcinogenesis 22: 1675- 1680, 2001.
91. Salvi S, and Holgate ST. Could the airway epithelium play an important role in mucosal immunoglobulin A production? Clin Exp Allergy 29: 1597-1605, 1999. (Pubitemid 30012417)
92. Sazawal S, Hiremath G, Dhingra U, Malik P, Deb S, and Black RE. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infect Dis 6: 374-382, 2006. (Pubitemid 43737276)
93. Smith K, McCoy KD, and Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 19: 59-69, 2007. (Pubitemid 46810285)
94. Spanhaak S, Havenaar R, and Schaafsma G. The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur J Clin Nutr 52: 899-907, 1998. (Pubitemid 29008371)
95. Spence L, Brown WJ, Pyne DB, Nissen MD, Sloots TP, McCormack JG, Locke AS, and Fricker PA. Incidence, etiology, and symptomatology of upper respiratory illness in elite athletes. Med Sci Sports Exerc 39: 577-586, 2007. (Pubitemid 46555783)
96. Takahashi I, Nochi T, Yuki Y, and Kiyono H. New horizon of mucosal immunity and vaccines. Curr Opin Immunol 21: 352-358, 2009.
97. Tao Y, Drabik K, Waypa T, Musch M, Alverdy J, Schneewind O, Chang E, and Petrof E. Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. Am J Physiol Cell Physiol 290: C1018-1030, 2006.
98. Tiollier E, Chennaoui M, Gomez-Merino D, Drogou C, Filaire E, and Guezennec CY. Effect of a probiotics supplementation on respiratory infections and immune and hormonal parameters during intense military training. Mil Med 172: 1006-1011, 2007. (Pubitemid 47427672)
99. Topping DL, Fukushima M, and Bird AR. Resistant starch as a prebiotic and synbiotic: state of the art. Proc Nutr Soc 62: 171-176, 2003.
100. Tuohy KM, Gougoulias C, Shen Q, Walton G, Fava F, and Ramnani P. Studying the human gut microbiota in the trans-omics era - focus on metagenomics and metabonomics. Curr Pharm Des 15: 1415-1427, 2009.
101. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, and Gordon JI. A core gut microbiome in obese and lean twins. Nature 457: 480-484, 2009.
102. Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 169: 1901-1909, 2006. (Pubitemid 351181952)
103. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, and Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal hostmicrobial interface. Proc Natl Acad Sci U S A 105: 20858-20863, 2008.
104. van der Baan B. Ciliary function. Acta Otorhinolaryngol Belg 54: 293-298, 2000.
105. Ventura M, O'Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, and O'Toole PW. Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7: 61-71, 2009.
106. Vizoso Pinto MG, Schuster T, Briviba K, Watzl B, Holzapfel WH, and Franz CM. Adhesive and chemokine stimulatory properties of potentially probiotic Lactobacillus strains. J Food Prot 70: 125-134, 2007. (Pubitemid 46191875)
107. West NP, Pyne DB, Kyd JM, Renshaw GMC, Fricker P, and Cripps AW. The effect of exercise on innate mucosal immunity. British Journal of Sports Medicine 2008.
108. West NP, Pyne DB, Renshaw G, and Cripps AW. Antimicrobial peptides and proteins, exercise and innate mucosal immunity. FEMS Immunol Med Microbiol 48: 293-304, 2006. (Pubitemid 44736567)
109. Wilson ID, and Nicholson JK. The role of gut microbiota in drug response. Curr Pharm Des 15: 1519-1523, 2009.
110. Winkler P, de Vrese M, Laue C, and Schrezenmeir J. Effect of a dietary supplement containing probiotic bacteria plus vitamins and minerals on common cold infections and cellular immune parameters. Int J Clin Pharmacol Ther 43: 318-326, 2005. (Pubitemid 40974738)
111. Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, and 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 9: 804-816, 2007. (Pubitemid 46231983)