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Effects of gender and age on immune responses of human peripheral blood mononuclear cells to probiotics: A large scale pilot study

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The journal of nutrition, health & aging

Abstract

Background

Despite the widely accepted concept that probiotics confer miscellaneous benefits to hosts, the controversies surrounding these health-promoting claims cannot be ignored. These controversies hinder development and innovation in this field.

Results

To clarify the effects of age and gender on probiotic-induced immune responses, we recruited 1613 Taiwanese individuals and calculated the ratio of IFN-γ to IL-10 production after each individual’s PBMCs were stimulated by six probiotic strains (L. paracasei BRAP01, L. acidophilus AD300, B. longum BA100, E. faecium BR0085, L. rhamnosus AD500 and L. reuteri BR101). Our results indicated that gender and age have only minor effects on the immune modulation of probiotics. Additionally, we showed that L. paracasei BRAP01 and L. acidophilus AD300 are the two dominant strains inducing IFN-γ/IL-10 production in Taiwanese individuals and that L. reuteri BR101 was the most effective stimulator of IL-10/IFN-γ. Additionally, a significant inverse relationship between the ability of L. paracasei BRAP01 and L. rhamnosus AD500 to stimulate IFN-γ/IL-10 or IL-10/IFN-γ production was also observed.

Conclusions

Our results indicated that age and gender have only minor effects on the immune modulation abilities of probiotics.

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References

  1. Shen, D., et al., Human gut microbiota: dysbiosis and manipulation. Front Cell Infect Microbiol, 2012. 2: p. 123.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Amara, A.A. and A. Shibl, Role of Probiotics in health improvement, infection control and disease treatment and management. Saudi Pharm J, 2015. 23(2): p. 107–14.

    Article  CAS  PubMed  Google Scholar 

  3. Ozdemir, O., Various effects of different probiotic strains in allergic disorders: an update from laboratory and clinical data. Clin Exp Immunol, 2010. 160(3): p. 295–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zajac, A.E., A.S. Adams, and J.H. Turner, A systematic review and meta-analysis of probiotics for the treatment of allergic rhinitis. Int Forum Allergy Rhinol, 2015. 5(6): p. 524–32.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Inoue, Y., et al., Effects of oral administration of Lactobacillus acidophilus L-92 on the symptoms and serum cytokines of atopic dermatitis in Japanese adults: a doubleblind, randomized, clinical trial. Int Arch Allergy Immunol, 2014. 165(4): p. 247–54.

    Article  CAS  PubMed  Google Scholar 

  6. Brouwer, M.L., et al., No effects of probiotics on atopic dermatitis in infancy: a randomized placebo-controlled trial. Clin Exp Allergy, 2006. 36(7): p. 899–906.

    Article  CAS  PubMed  Google Scholar 

  7. Cuello-Garcia, C.A., et al., Probiotics for the prevention of allergy: A systematic review and meta-analysis of randomized controlled trials. J Allergy Clin Immunol, 2015.

    Google Scholar 

  8. Matsui, E., No Effect of Probiotics on Respiratory Allergies: A Seven-Year Followup of a Randomized Controlled Trial in Infancy. Pediatrics, 2014. 134 Suppl 3: p. S141–2.

    Article  PubMed  Google Scholar 

  9. Abrahamsson, T.R., et al., No effect of probiotics on respiratory allergies: a sevenyear follow-up of a randomized controlled trial in infancy. Pediatr Allergy Immunol, 2013. 24(6): p. 556–61.

    Article  PubMed  Google Scholar 

  10. Fiocchi, A., et al., World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics. World Allergy Organ J, 2015. 8(1): p. 4.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ferolla, S.M., et al., Probiotics as a complementary therapeutic approach in nonalcoholic fatty liver disease. World J Hepatol, 2015. 7(3): p. 559–65.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Vitetta, L., et al., Probiotics, prebiotics and the gastrointestinal tract in health and disease. Inflammopharmacology, 2014. 22(3): p. 135–54.

    Article  PubMed  Google Scholar 

  13. Morrow, L.E. and M.H. Kollef, Probiotics in the intensive care unit: why controversies and confusion abound. Crit Care, 2008. 12(3): p. 160.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Theodorakopoulou, M., et al., Controversies in the management of the critically ill: the role of probiotics. Int J Antimicrob Agents, 2013. 42 Suppl: p. S41–4.

    Article  CAS  PubMed  Google Scholar 

  15. Zhang, Z., C. Liu, and X. Guo, [Safety of probiotics—a review]. Wei Sheng Wu Xue Bao, 2008. 48(2): p. 257–61.

    CAS  PubMed  Google Scholar 

  16. Haghighat, L. and N.F. Crum-Cianflone, The potential risks of probiotics among HIV-infected persons: Bacteraemia due to Lactobacillus acidophilus and review of the literature. Int J STD AIDS, 2015.

    Google Scholar 

  17. Doron, S. and D.R. Snydman, Risk and safety of probiotics. Clin Infect Dis, 2015. 60 Suppl 2: p. S129–34.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Becker, Y., Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy—a review. Virus Genes, 2006. 33(2): p. 235–52.

    CAS  PubMed  Google Scholar 

  19. Oreja-Guevara, C., et al., TH1/TH2 Cytokine profile in relapsing-remitting multiple sclerosis patients treated with Glatiramer acetate or Natalizumab. BMC Neurol, 2012. 12: p. 95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Espindola, O.M., et al., High IFN-gamma/IL-10 expression ratio and increased frequency of persistent human T-cell lymphotropic virus type 1-infected clones are associated with human T-cell lymphotropic virus type 1-associated myelopathy/tropical spastic paraparesis development. Intervirology, 2015. 58(2): p. 106–14.

    Article  CAS  PubMed  Google Scholar 

  21. Paul, J., S. Karmakar, and T. De, TLR-mediated distinct IFN-gamma/IL-10 pattern induces protective immunity against murine visceral leishmaniasis. Eur J Immunol, 2012. 42(8): p. 2087–99.

    Article  CAS  PubMed  Google Scholar 

  22. Sharma, R., et al., Improvement in Th1/Th2 immune homeostasis, antioxidative status and resistance to pathogenic E. coli on consumption of probiotic Lactobacillus rhamnosus fermented milk in aging mice. Age (Dordr), 2014. 36(4): p. 9686.

    Article  Google Scholar 

  23. Won, T.J., et al., Modulation of Th1/Th2 balance by Lactobacillus strains isolated from Kimchi via stimulation of macrophage cell line J774A.1 in vitro. J Food Sci, 2011. 76(2): p. H55–61.

    Article  CAS  PubMed  Google Scholar 

  24. Stewart, C.A., et al., Interferon-dependent IL-10 production by Tregs limits tumor Th17 inflammation. J Clin Invest, 2013. 123(11): p. 4859–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Teng, M.W., et al., Multiple antitumor mechanisms downstream of prophylactic regulatory T-cell depletion. Cancer Res, 2010. 70(7): p. 2665–74.

    Article  CAS  PubMed  Google Scholar 

  26. Baba, N., et al., Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J Leukoc Biol, 2008. 84(2): p. 468–76.

    Article  CAS  PubMed  Google Scholar 

  27. Finamore, A., et al., Lactobacillus rhamnosus GG and Bifidobacterium animalis MB5 induce intestinal but not systemic antigen-specific hyporesponsiveness in ovalbuminimmunized rats. J Nutr, 2012. 142(2): p. 375–81.

    Article  CAS  PubMed  Google Scholar 

  28. Kwon, H.K., et al., Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A, 2010. 107(5): p. 2159–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lavasani, S., et al., A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One, 2010. 5(2): p. e9009.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Man, A.L., et al., Age-associated modifications of intestinal permeability and innate immunity in human small intestine. Clin Sci (Lond), 2015.

    Google Scholar 

  31. Yaqoob, P., Ageing, immunity and influenza: a role for probiotics? Proc Nutr Soc, 2014. 73(2): p. 309–17.

    Article  PubMed  Google Scholar 

  32. Moro-Garcia, M.A., et al., Oral supplementation with Lactobacillus delbrueckii subsp. bulgaricus 8481 enhances systemic immunity in elderly subjects. Age (Dordr), 2013. 35(4): p. 1311–26.

    Article  CAS  Google Scholar 

  33. Yonekura, S., et al., Effects of daily intake of Lactobacillus paracasei strain KW3110 on Japanese cedar pollinosis. Allergy Asthma Proc, 2009. 30(4): p. 397–405.

    Article  PubMed  Google Scholar 

  34. Cross, M.L., et al., Dietary intake of Lactobacillus rhamnosus HNOO1 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med Microbiol Immunol, 2002. 191(1): p. 49–53.

    Article  CAS  PubMed  Google Scholar 

  35. Iliev, I.D., et al., Immunostimulatory oligodeoxynucleotide containing TTTCGTTT motif from Lactobacillus rhamnosus GG DNA potentially suppresses OVA-specific IgE production in mice. Scand J Immunol, 2008. 67(4): p. 370–6.

    Article  CAS  PubMed  Google Scholar 

  36. Karimi, K., et al., A Lactobacillus rhamnosus strain induces a heme oxygenase dependent increase in Foxp3+ regulatory T cells. PLoS One, 2012. 7(10): p. e47556.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Imani Fooladi, A.A., et al., Th1 Cytokine Production Induced by Lactobacillus acidophilus in BALB/c Mice Bearing Transplanted Breast Tumor. Jundishapur J Microbiol, 2015. 8(4): p. e17354.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Azevedo, M.S., et al., Lactobacillus acidophilus and Lactobacillus reuteri modulate cytokine responses in gnotobiotic pigs infected with human rotavirus. Benef Microbes, 2012. 3(1): p. 33–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Smits, H.H., et al., Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol, 2005. 115(6): p. 1260–7.

    Article  CAS  PubMed  Google Scholar 

  40. Razmpoosh, E., et al., Probiotics as beneficial agents in the management of diabetes mellitus: a systematic review. Diabetes Metab Res Rev, 2015.

    Google Scholar 

  41. Mohammadi, A.A., et al., The effects of probiotics on mental health and hypothalamic-pituitary-adrenal axis: A randomized, double-blind, placebo-controlled trial in petrochemical workers. Nutr Neurosci, 2015.

    Google Scholar 

  42. Sawas, T., et al., Patients Receiving Prebiotics and Probiotics Before Liver Transplantation Develop Fewer Infections Than Controls: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol, 2015.

    Google Scholar 

  43. Abrahamsson, T.R., et al., Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol, 2007. 119(5): p. 1174–80.

    Article  CAS  PubMed  Google Scholar 

  44. Forsberg, A., et al., Pre-and post-natal Lactobacillus reuteri supplementation decreases allergen responsiveness in infancy. Clin Exp Allergy, 2013. 43(4): p. 434–42.

    Article  CAS  PubMed  Google Scholar 

  45. Ho, Y.H., et al., Daily intake of probiotics with high IFN-gamma/IL-10 ratio increases the cytotoxicity of human natural killer cells: a personalized probiotic approach. J Immunol Res, 2014. 2014: p. 721505.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Research and Development, Bio Ray Biotech Inc., Kaohsiung, Taiwan, 80466, R.O.C.

    Y.-H. Ho, Y.-T. Huang, Y.-C. Lu, S.-Y. Lee, M.-F. Tsai, S.-P. Hung & Ting-Yuan Hsu

  2. 5F., No.466, Bo’ai 1st Rd., Gushan Dist., Kaohsiung City, 80466, Taiwan, R.O.C.

    Ting-Yuan Hsu

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  1. Y.-H. Ho
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  2. Y.-T. Huang
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Ho, YH., Huang, YT., Lu, YC. et al. Effects of gender and age on immune responses of human peripheral blood mononuclear cells to probiotics: A large scale pilot study. J Nutr Health Aging 21, 521–526 (2017). https://doi.org/10.1007/s12603-016-0818-7

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  • DOI: https://doi.org/10.1007/s12603-016-0818-7

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