Probiotics: Immunomodulation and evaluation of safety and efficacy

Nutrition Reviews

Volumn 64, Issue 1, 2006, Pages 1-14

  Ezendam, Janine ^a   Van Loveren, Henk ^a,b  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Efficacy and safety evaluation; Immunomodulation; Probiotics

Indexed keywords

BB 12; DSM 122460; DSM 15158; DSM 9843; GAMMA INTERFERON; HN 001; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; LC 7055; MESALAZINE; NISSLE 1917; PROBIOTIC AGENT; YOGHURT;

ALLERGIC DISEASE; ANTIBODY TITER; ANTIMICROBIAL ACTIVITY; ASTHMA; ATOPIC DERMATITIS; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BREVE; CELLULAR IMMUNITY; CLINICAL TRIAL; COLITIS; CROHN DISEASE; DIET SUPPLEMENTATION; DISEASE DURATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; ENTERITIS; ESCHERICHIA COLI; FOOD AND DRUG ADMINISTRATION; HUMAN; ILEITIS; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOREGULATION; IN VITRO STUDY; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS DEBRUEKKII BULGARICUS; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; MILK ALLERGY; MOUSE STRAIN; MULTIPLE SCLEROSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROPIONIBACTERIUM FREUDENREICHII; RANDOMIZATION; REVIEW; RHEUMATOID ARTHRITIS; RHINITIS; RISK ASSESSMENT; STREPTOCOCCUS THERMOPHILUS; TH1 CELL; TH2 CELL; ULCERATIVE COLITIS;

ANIMALS; CONSUMER PRODUCT SAFETY; DISEASE MODELS, ANIMAL; EVIDENCE-BASED MEDICINE; HUMANS; IMMUNE SYSTEM; IMMUNE SYSTEM DISEASES; IMMUNITY, MUCOSAL; IMMUNOLOGIC FACTORS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS; RISK ASSESSMENT; TREATMENT OUTCOME;

ANIMALIA; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BREVE; ESCHERICHIA COLI; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; PROPIONIBACTERIUM FREUDENREICHII; STREPTOCOCCUS THERMOPHILUS;

EID: 33644557349     PISSN: 00296643     EISSN: 00296643     Source Type: Journal    
DOI: 10.1301/nr.2006.jan.1-14     Document Type: Review

References (72)

1. Schrezenmeir J, Vrese M. Probiotics, prebiotics, and synbiotics - approaching a definition. Am J Clin Nutr. 2001;73(suppl 2):361S-364S.
2. De Waard R, Claassen E, Bokken GC, Buiting B, Garssen J, Vos JG. Enhanced immunological memory responses to Listeria monocytogenes in rodents, as measured by delayed-type hypersensitivity (DTH), adoptive transfer of DTH, and protective immunity, following Lactobacillus casei Shirota ingestion. Clin Diagn Lab Immunol. 2003;10:59-65.
3. De Waard R, Garssen J, Snel J, et al. Enhanced antigen-specific delayed-type hypersensitivity and immunoglobulin G2b responses after oral administration of viable Lactobacillus casei YIT9029 in Wistar and Brown Norway rats. Clin Diagn Lab Immunol. 2001;8:762-767.
4. Alvarez S, Herrero C, Bru E, Perdigon G. Effect of Lactobacillus casei and yogurt administration on prevention of Pseudomonas aeruginosa infection in young mice. J Food Prot. 2001;64:1768-1774.
5. Hatakka K, Savilahti E, Ponka A, et al. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ. 2001;322:1327.
6. Weizman Z, Asli G, Alsheikh A. Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics. 2005;115:5-9.
7. Madsen KL. The use of probiotics in gastrointestinal disease. Can J Gastroenterol. 2001;15:817-822.
8. Shanahan F. Probiotics and inflammatory bowel disease: from fads and fantasy to facts and future. Br J Nutr. 2002;88(suppl 1):S5-S9.
9. Marteau P, Seksik P, Jian R. Probiotics and intestinal health effects: a clinical perspective. Br J Nutr. 2002;88(suppl 1):S51-S57.
10. Isolauri E, Sutas Y, Kankaanpaa P, Arvilommi H, Salminen S. Probiotics: effects on immunity. Am J Clin Nutr. 2001;73(suppl 2):444S-450S.
11. Matsuzaki T. Immunomodulation by treatment with Lactobacillus casei strain Shirota. Int J Food Microbiol. 1998;41:133-140.
12. Cross ML, Stevenson LM, Gill HS. Anti-allergy properties of fermented foods: an important immunoregulatory mechanism of lactic acid bacteria? Int Immunopharmacol. 2001;1:891-901.
13. Hessle C, Hanson LA, Wold AE. Lactobacilli from human gastrointestinal mucosa are strong stimulators of IL-12 production. Clin Exp Immunol. 1999;116:276-282.
14. Miettinen M, Matikainen S, Vuopio-Varkila J, et al. Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect Immun. 1998;66:6058-6062.
15. Murosaki S, Yamamoto Y, Ito K, et al. Heat-killed Lactobacillus plantarum L-137 suppresses naturally fed antigen-specific IgE production by stimulation of IL-12 production in mice. J Allergy Clin Immunol. 1998;102:57-64.
16. Cross ML, Mortensen RR, Kudsk J, Gill HS. Dietary intake of Lactobacillus rhamnosus HNOO1 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med Microbiol Immunol (Berl). 2002;191:49-53.
17. Pohjavuori E, Viljanen M, Korpela R, et al. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow's milk allergy. J Allergy Clin Immunol. 2004;114:131-136.
18. Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S. Probiotics in the management of atopic eczema. Clin Exp Allergy. 2000;30:1604-1610.
19. Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet. 2001;357:1076-1079.
20. Kalliomaki M, Salminen S, Poussa T, Arvilommi H, Isolauri E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet. 2003;361:1869-1871.
21. Rosenfeldt V, Benfeldt E, Nielsen SD, et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol. 2003;111:389-395.
22. Rosenfeldt V, Benfeldt E, Valerius NH, Paerregaard A, Michaelsen KF. Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. J Pediatr. 2004;145:612-616.
23. Majamaa H, Isolauri E. Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol. 1997;99:179-185.
24. Pessi T, Sutas Y, Hurme M, Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy. 2000;30:1804-1808.
25. Wheeler JG, Bogle ML, Shema SJ, et al. Impact of dietary yogurt on immune function. Am J Med Sci. 1997;313:120-123.
26. Wheeler JG, Shema SJ, Bogle ML, et al. Immune and clinical impact of Lactobacillus acidophilus on asthma. Ann Allergy Asthma Immunol. 1997;79:229-233.
27. Aldinucci C, Bellussi L, Monciatti G, et al. Effects of dietary yoghurt on immunological and clinical parameters of rhinopathic patients. Eur J Clin Nutr. 2002;56:1155-1161.
28. Helin T, Haahtela S, Haahtela T. No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study. Allergy. 2002;57:243-246.
29. Sepp E, Julge K, Vasar M, Naaber P, Bjorksten B, Mikelsaar M. Intestinal microflora of Estonian and Swedish infants. Acta Paediatr. 1997;86:956-961.
30. Bjorksten B, Naaber P, Sepp E, Mikelsaar M. The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy. 1999;29:342-346.
31. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001;107:129-134.
32. Saavedra JM, Abi-Hanna A, Moore N, Yolken RH. Long-term consumption of infant formulas containing live probiotic bacteria: tolerance and safety. Am J Clin Nutr. 2004;79:261-267.
33. US Food and Drug Administration. Agency Response Letter. GRAS Notice No. GRN 000049. Available online at: http://www.cfsan.fda.gov/∼rdb/opa-g049. html. Accessed December 7, 2005.
34. Wagner RD, Warner T, Roberts L, Farmer J, Balish E. Colonization of congenitally immunodeficient mice with probiotic bacteria. Infect Immun. 1997;65:3345-3351.
35. Matricardi PM. Probiotics against allergy: data, doubts, and perspectives. Allergy. 2002;57:185-187.
36. Matsuzaki T, Nagata Y, Kado S, Uchida K, Hashimoto S, Yokokura T. Effect of oral administration of Lactobacillus casei on alloxan-induced diabetes in mice. APMIS. 1997;105:637-642.
37. Matsuzaki T, Nagata Y, Kado S, et al. Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. APMIS. 1997;105:643-649.
38. Matsuzaki T, Yamazaki R, Hashimoto S, Yokokura T. The effect of oral feeding of Lactobacillus casei strain Shirota on immunoglobulin E production in mice. J Dairy Sci. 1998;81:48-53.
39. von der Weid T, Bulliard C, Schiffrin EJ. Induction by a lactic acid bacterium of a population of CD4(+) T cells with low proliferative capacity that produce transforming growth factor beta and interleukin-10. Clin Diagn Lab Immunol. 2001;8:695-701.
40. Sheil B, McCarthy J, O'Mahony L, et al. Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut. 2004;53:694-700.
41. Kato I, Endo-Tanaka K, Yokokura T. Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci. 1998;63:635-644.
42. Butler DM, Malfait AM, Maini RN, Brennan FM, Feldmann M. Anti-IL-12 and anti-TNF antibodies synergistically suppress the progression of murine collagen-induced arthritis. Eur J Immunol. 1999;29:2205-2212.
43. Baharav E, Mor F, Halpern M, Weinberger A. Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. J Nutr. 2004;134:1964-1969.
44. Toivanen P. From reactive arthritis to rheumatoid arthritis. J Autoimmun. 2001;16:369-371.
45. Hatakka K, Martio J, Korpela M, et al. Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis - a pilot study. Scand J Rheumatol. 2003;32:211-215.
46. Maassen CB, van Holten JC, Balk F, et al. Orally administered Lactobacillus strains differentially affect the direction and efficacy of the immune response. Vet Q. 1998;20(suppl 3):S81-S83.
47. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417-429.
48. Fabia R, Ar'Rajab A, Johansson ML, et al. The effect of exogenous administration of Lactobacillus reuteri R2LC and oat fiber on acetic acid-induced colitis in the rat. Scand J Gastroenterol. 1993;28:155-162.
49. Osman N, Adawi D, Ahrne S, Jeppsson B, Molin G. Modulation of the effect of dextran sulfate sodiuminduced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium. Dig Dis Sci. 2004;49:320-327.
50. Kennedy RJ, Hoper M, Deodhar K, Kirk SJ, Gardiner KR. Probiotic therapy fails to improve gut permeability in a hapten model of colitis. Scand J Gastroenterol. 2000;35:1266-1271.
51. Kruis W, Fric P, Pokrotnieks J, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut. 2004;53:1617-1623.
52. Rembacken BJ, Snelling AM, Hawkey PM, Chalmers DM, Axon AT. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet. 1999;354:635-639.
53. Mimura T, Rizzello F, Helwig U, et al. Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut. 2004;53:108-114.
54. Prantera C, Scribano ML, Falasco G, Andreoli A, Luzi C. Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn's disease: a randomised controlled trial with Lactobacillus GG. Gut. 2002;51:405-409.
55. Anderson KV. Toll signaling pathways in the innate immune response. Curr Opin Immunol. 2000;12:13-19.
56. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol. 2001;2:675-680.
57. Sturm A, Rilling K, Baumgart DC, et al. Escherichia coli Nissle 1917 distinctively modulates T-cell cycling and expansion via toll-like receptor 2 signaling. Infect Immun. 2005;73:1452-1465.
58. Rachmilewitz D, Katakura K, Karmeli F, et al. Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology. 2004;126:520-528.
59. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-β-bearing regulatory cells. J Immunol. 2005;174:3237-3246.
60. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3:984-993.
61. Christensen HR, Frokiaer H, Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol. 2002;168:171-178.
62. Mohamadzadeh M, Olson S, Kalina WV, et al. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A. 2005;102:2880-2885.
63. Hart AL, Lammers K, Brigidi P, et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut. 2004;53:1602-1609.
64. Braat H, van den Brande J, van Tol E, Hommes D, Peppelenbosch M, van Deventer S. Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. Am J Clin Nutr. 2004;80:1618-1625.
65. Pelto L, Isolauri E, Lilius EM, Nuutila J, Salminen S. Probiotic bacteria down-regulate the milk-induced inflammatory response in milk-hypersensitive subjects but have an immunostimulatory effect in healthy subjects. Clin Exp Allergy. 1998;28:1474-1479.
66. Feord J. Lactic acid bacteria in a changing legislative environment. Antonie Van Leeuwenhoek. 2002;82:353-360.
67. von Wright A. Regulating safety of probiotics - the European approach. Curr Pharm Des. 2005;11:17-23.
68. Food and Agriculture Organization of the United Nations/World Health Organization. Guidelines for the Evaluation of Probiotics in Food: Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. Available at: ftp://ftp.fao.org/es/esn/food/wgreport2.pdf. Accessed December 7, 2005.
69. Salminen S, von Wright A, Morelli L, et al. Demonstration of safety of probiotics - a review. Int J Food Microbiol. 1998;44:93-106.
70. He F, Morita H, Ouwehand AC, et al. Stimulation of the secretion of pro-inflammatory cytokines by Bifidobacterium strains. Microbiol Immunol. 2002;46:781-785.
71. European Commission Scientific Committee on Food. Report of the Scientific Committee on Food on the Revision of Essential Requirements of Infant Formulae and Follow-on Formulae. Available online at: http://europa.eu.int/ comm/food/fs/sc/scf/out199_en.pdf. Accessed December 7, 2005.
72. Agostoni C, Axelsson I, Braegger C, et al. Probiotic bacteria in dietetic products for infants: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr. 2004;38:365-374.