1887

Abstract

Giardiasis, caused by the protozoan , is one of the most common intestinal diseases worldwide and constitutes an important problem for the public health systems of various countries. Kefir is a probiotic drink obtained by fermenting milk with ‘kefir grains’, which consist mainly of bacteria and yeasts that coexist in a complex symbiotic association. In this work, we studied the ability of kefir to protect mice from infection, and characterized the host immune response to this probiotic in the context of the intestinal infection. Six- to 8-week-old C75BL/6 mice were separated into four groups: controls, kefir mice (receiving 1 : 100 dilution of kefir in drinking water for 14 days), mice (infected orally with 4×10 trophozoites of at day 7) and –kefir mice (kefir-treated -infected mice), and killed at 2 or 7 days post-infection. Kefir administration was able to significantly reduce the intensity of infection at 7 days post-infection. An increase in the percentage of CD4 T cells at 2 days post-infection was observed in the Peyer’s patches (PP) of mice belonging to the group compared with the control and kefir groups, while the percentage of CD4 T cells in PP in the –kefir group was similar to that of controls. At 2 days post-infection, a reduction in the percentage of B220-positive major histocompatibility complex class II medium cells in PP was observed in infected mice compared with the other groups. At 7 days post-infection, -infected mice showed a reduction in RcFcϵ-positive cells compared with the control group, suggesting a downregulation of the inflammatory response. However, the percentages of RcFcϵ-positive cells did not differ from controls in the kefir and –kefir groups. An increase in IgA-positive cells was observed in the lamina propria of the kefir group compared with controls at 2 days post-infection. Interestingly, the diminished number of IgA-positive cells registered in the group at 7 days post-infection was restored by kefir feeding, although the increase in IgA-positive cells was no longer observed in the kefir group at that time. No significant differences in CXCL10 expression were registered between groups, in concordance with the absence of inflammation in small-intestinal tissue. Interestingly, a slight reduction in CCL20 expression was observed in the group, suggesting that might downregulate its expression as a way of evading the inflammatory immune response. On the other hand, a trend towards an increase in TNF-α expression was observed in the kefir group, while the –kefir group showed a significant increase in TNF-α expression. Moreover, kefir-receiving mice (kefir and –kefir groups) showed an increase in the expression of IFN-γ, the most relevant Th1 cytokine, at 2 days post-infection. Our results demonstrate that feeding mice with kefir reduces infection and promotes the activation of different mechanisms of humoral and cellular immunity that are downregulated by parasitic infection, thus contributing to protection.

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2013-12-01
2024-04-19
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References

  1. Amorós I., Alonso J. L., Cuesta G. 2010; Cryptosporidium oocysts and Giardia cysts on salad products irrigated with contaminated water. J Food Prot 73:1138–1140[PubMed]
    [Google Scholar]
  2. Anderle P., Rumbo M., Sierro F., Mansourian R., Michetti P., Roberts M. A., Kraehenbuhl J. P. 2005; Novel markers of the human follicle-associated epithelium identified by genomic profiling and microdissection. Gastroenterology 129:321–327 [View Article][PubMed]
    [Google Scholar]
  3. Benyacoub J., Pérez P. F., Rochat F., Saudan K. Y., Reuteler G., Antille N., Humen M., De Antoni G. L., Cavadini C. other authors 2005; Enterococcus faecium SF68 enhances the immune response to Giardia intestinalis in mice. J Nutr 135:1171–1176[PubMed]
    [Google Scholar]
  4. Besirbellioglu B. A., Ulcay A., Can M., Erdem H., Tanyuksel M., Avci I. Y., Araz E., Pahsa A. 2006; Saccharomyces boulardii and infection due to Giardia lamblia. Scand J Infect Dis 38:479–481 [View Article][PubMed]
    [Google Scholar]
  5. Calzada F., Cerda-García-Rojas C. M., Meckes M., Cedillo-Rivera R., Bye R., Mata R. 1999; Geranins A and B, new antiprotozoal A-type proanthocyanidins from Geranium niveum. J Nat Prod 62:705–709 [View Article][PubMed]
    [Google Scholar]
  6. Cotton J. A., Beatty J. K., Buret A. G. 2011; Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol 41:925–933 [View Article][PubMed]
    [Google Scholar]
  7. de Moreno de LeBlanc A., Matar C., Farnworth E., Perdigón G. 2007; Study of immune cells involved in the antitumor effect of kefir in a murine breast cancer model. J Dairy Sci 90:1920–1928 [View Article][PubMed]
    [Google Scholar]
  8. Dekker J., Collett M., Prasad J., Gopal P. 2007; Functionality of probiotics - potential for product development. Forum Nutr 60:196–208 [View Article][PubMed]
    [Google Scholar]
  9. FAO/WHO 2002; 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.
    [Google Scholar]
  10. Farnworth E. 2005; Kefir – a complex probiotic. Food Sci Technol Bull 2:1–17
    [Google Scholar]
  11. Faubert G. 2000; Immune response to Giardia duodenalis. Clin Microbiol Rev 13:35–54 [View Article][PubMed]
    [Google Scholar]
  12. Galdeano C. M., Perdigón G. 2006; The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 13:219–226 [View Article][PubMed]
    [Google Scholar]
  13. Gardner T. B., Hill D. R. 2001; Treatment of giardiasis. Clin Microbiol Rev 14:114–128 [View Article][PubMed]
    [Google Scholar]
  14. Garrote G. L., Abraham A. G., De Antoni G. L. 2001; Chemical and microbiological characterisation of kefir grains. J Dairy Res 68:639–652 [View Article][PubMed]
    [Google Scholar]
  15. Goyal N., Shukla G. 2013; Probiotic Lactobacillus rhamnosus GG modulates the mucosal immune response in Giardia intestinalis-infected BALB/c mice. Dig Dis Sci 58:1218–1225 [View Article][PubMed]
    [Google Scholar]
  16. Goyal N. R., Tiwari R. P., Shukla G. 2011; Lactobacillus rhamnosus GG as an effective probiotic for murine giardiasis. Interdiscip Perspect Infect Dis 2011:795219 [View Article][PubMed]
    [Google Scholar]
  17. Goyal N., Rishi P., Shukla G. 2013; Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study. World J Microbiol Biotechnol 29:1049–1057 [View Article][PubMed]
    [Google Scholar]
  18. Hawrelak J. 2003; Giardiasis: pathophysiology and management. Altern Med Rev 8:129–142[PubMed]
    [Google Scholar]
  19. Humen M. A. 2009 Interacción de Giardia intestinalis con el hospedador efecto antagónico de probióticos intestinales PhD thesis, Universidad Nacional de La Plata; Argentina:
    [Google Scholar]
  20. Humen M. A., De Antoni G. L., Benyacoub J., Costas M. E., Cardozo M. I., Kozubsky L., Saudan K. Y., Boenzli-Bruand A., Blum S. other authors 2005; Lactobacillus johnsonii La1 antagonizes Giardia intestinalis in vivo. Infect Immun 73:1265–1269 [View Article][PubMed]
    [Google Scholar]
  21. Ito T., Carson W. F. IV, Cavassani K. A., Connett J. M., Kunkel S. L. 2011; CCR6 as a mediator of immunity in the lung and gut. Exp Cell Res 317:613–619 [View Article][PubMed]
    [Google Scholar]
  22. Langford T. D., Housley M. P., Boes M., Chen J., Kagnoff M. F., Gillin F. D., Eckmann L. 2002; Central importance of immunoglobulin A in host defense against Giardia spp. Infect Immun 70:11–18 [View Article][PubMed]
    [Google Scholar]
  23. Lee M.-Y., Ahn K.-S., Kwon O.-K., Kim M.-J., Kim M.-K., Lee I.-Y., Oh S.-R., Lee H.-K. 2007; Anti-inflammatory and anti-allergic effects of kefir in a mouse asthma model. Immunobiology 212:647–654 [View Article][PubMed]
    [Google Scholar]
  24. Li E., Zhou P., Petrin Z., Singer S. M. 2004; Mast cell-dependent control of Giardia lamblia infections in mice. Infect Immun 72:6642–6649 [View Article][PubMed]
    [Google Scholar]
  25. Liu M., Guo S., Hibbert J. M., Jain V., Singh N., Wilson N. O., Stiles J. K. 2011; CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine Growth Factor Rev 22:121–130[PubMed]
    [Google Scholar]
  26. Lopitz-Otsoa F., Rementeria A., Elguezabal N., Garaizar J. 2006; Kefir: a symbiotic yeasts–bacteria community with alleged healthy capabilities. Rev Iberoam Micol 23:67–74 [View Article][PubMed]
    [Google Scholar]
  27. Matowicka-Karna J., Dymicka-Piekarska V., Kemona H. 2009; IFN-γ, IL-5, IL-6 and IgE in patients infected with Giardia intestinalis. Folia Histochem Cytobiol 47:93–97 [View Article][PubMed]
    [Google Scholar]
  28. Medrano M., Racedo S. M., Rolny I. S., Abraham A. G., Pérez P. F. 2011; Oral administration of kefiran induces changes in the balance of immune cells in a murine model. J Agric Food Chem 59:5299–5304 [View Article][PubMed]
    [Google Scholar]
  29. Moreno G., Errea A., Van Maele L., Roberts R., Léger H., Sirard J. C., Benecke A., Rumbo M., Hozbor D. 2013; Toll-like receptor 4 orchestrates neutrophil recruitment into airways during the first hours of Bordetella pertussis infection. Microbes Infect 15:708–718 [View Article][PubMed]
    [Google Scholar]
  30. Roxström-Lindquist K., Ringqvist E., Palm D., Svärd S. G. 2005; Giardia lamblia-induced changes in gene expression in differentiated Caco-2 human intestinal epithelial cells. Infect Immun 73:8204–8208 [View Article][PubMed]
    [Google Scholar]
  31. Rumbo M., Sierro F., Debard N., Kraehenbuhl J. P., Finke D. 2004; Lymphotoxin beta receptor signaling induces the chemokine CCL20 in intestinal epithelium. Gastroenterology 127:213–223 [View Article][PubMed]
    [Google Scholar]
  32. Shah N. P. 2007; Functional cultures and health benefits. Int Dairy J 17:1262–1277 [View Article]
    [Google Scholar]
  33. Shukla G., Sidhu R. K. 2011; Lactobacillus casei as a probiotic in malnourished Giardia lamblia-infected mice: a biochemical and histopathological study. Can J Microbiol 57:127–135 [View Article][PubMed]
    [Google Scholar]
  34. Shukla G., Devi P., Sehgal R. 2008; Effect of Lactobacillus casei as a probiotic on modulation of giardiasis. Dig Dis Sci 53:2671–2679 [View Article][PubMed]
    [Google Scholar]
  35. Singer S. M., Nash T. E. 2000; T-cell-dependent control of acute Giardia lamblia infections in mice. Infect Immun 68:170–175 [View Article][PubMed]
    [Google Scholar]
  36. Smaldini P., Curciarello R., Candreva A., Rey M. A., Fossati C. A., Petruccelli S., Docena G. H. 2012; In vivo evidence of cross-reactivity between cow’s milk and soybean proteins in a mouse model of food allergy. Int Arch Allergy Immunol 158:335–346 [View Article][PubMed]
    [Google Scholar]
  37. Teruya K., Myojin-Maekawa Y., Shimamoto F., Watanabe H., Nakamichi N., Tokumaru K., Tokumaru S., Shirahata S. 2013; Protective effects of the fermented milk kefir on X-ray irradiation-induced intestinal damage in B6C3F1 mice. Biol Pharm Bull 36:352–359 [View Article][PubMed]
    [Google Scholar]
  38. Thoreux K., Schmucker D. L. 2001; Kefir milk enhances intestinal immunity in young but not old rats. J Nutr 131:807–812[PubMed]
    [Google Scholar]
  39. Travers M. A., Florent I., Kohl L., Grellier P. 2011; Probiotics for the control of parasites: an overview. J Parasitol Res 2011:610769 [View Article][PubMed]
    [Google Scholar]
  40. Vinderola C. G., Duarte J., Thangavel D., Perdigón G., Farnworth E., Matar C. 2005; Immunomodulating capacity of kefir. J Dairy Res 72:195–202 [View Article][PubMed]
    [Google Scholar]
  41. Vinderola G., Perdigón G., Duarte J., Farnworth E., Matar C. 2006; Effects of the oral administration of the products derived from milk fermentation by kefir microflora on immune stimulation. J Dairy Res 73:472–479 [View Article][PubMed]
    [Google Scholar]
  42. Vinderola G., Matar C., Perdigón G. 2007; Milk fermentation products of L. helveticus R389 activate calcineurin as a signal to promote gut mucosal immunity. BMC Immunol 8:19 [View Article][PubMed]
    [Google Scholar]
  43. Vitiñi E., Alvarez S., Medina M., Medici M., de Budeguer M. V., Perdigón G. 2000; Gut mucosal immunostimulation by lactic acid bacteria. Biocell 24:223–232[PubMed]
    [Google Scholar]
  44. WHO/PAHO 1992; Informal consultation on intestinal protozoal infections. Geneva: WHO;
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