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Lactobacillus rhamnosus intake can prevent the development of Candidiasis

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Abstract

Objective

This study aimed to investigate the influence of Lactobacillus rhamnosus intake on the development of candidiasis and cytokines release.

Material and methods

Candida suspensions were inoculated into the oral cavity of experimentally immunosuppressed mice for candidiasis induction. The animals were divided into experimental groups: candidiasis with no probiotic intake (F), candidiasis with probiotic intake during Candida inoculation (FP), and candidiasis with probiotic intake 14 days before inoculation with Candida (FPP); and control groups: (C), (CP), and (CPP) without inducing candidiasis with probiotic intake in the same manner as groups F, FP, and FPP, respectively. After these periods, samples were collected from the oral cavity for yeast counts and, after euthanasia, the tongues of the animals were removed for histological analysis. Sera samples were also collected for analysis of IL-1 beta, TNF-alpha, INF-gamma, IL-12, IL-4, and IL-10.

Results

FP group showed lower Candida counts in the oral cavity, and the presence of Candida was almost not detected in FPP group. In tissues, the counts of fungi were significantly lower in FPP group, followed by FP. Groups that consumed probiotics also had lower histological and inflammatory infiltrates compared to F. Cytokines analysis demonstrated low concentrations of TNF-α, IL-12, IL-4, and IL-10 in all the groups, and no statistical difference between them. The production of IL-6 could be better detected, and the experimental groups that consumed the probiotic showed significant lower levels of this cytokine.

Conclusions

The results suggest that L. rhamnosus intake, especially preventively, may avoid or decrease the development of candidiasis in immunosuppressed mice.

Clinical relevance

This work adds scientific evidences that probiotics intake can avoid the development of candidiasis.

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References

  1. FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations/World Health Organization, London

    Google Scholar 

  2. Kumar M, Babaei P, Ji B, Nielsen J (2016) Human gut microbiota and healthy aging: recent developments and future prospective. Nutr Healthy Aging 4(1):3–16. https://doi.org/10.3233/NHA-150002

    Article  PubMed  PubMed Central  Google Scholar 

  3. Iannitti T, Palmieri B (2010) Therapeutical use of probiotic formulations in clinical practice. Clin Nutr 29(6):701–725. https://doi.org/10.1016/j.clnu.2010.05.004

    Article  PubMed  Google Scholar 

  4. Al-Salami H, Caccetta R, Golocorbin-Kon S, Mikov M (2012). Probiotics applications in autoimmune diseases. In: Rigobelo EC(ed). Probiotics. InTech, Rijeka, pp 325–366

  5. Shteyer E, Wilschanski M (2008) Novel therapeutic modalities in pediatric inflammatory bowel disease. Isr Med Assoc J 10(11):816–820 http://www.ncbi.nlm.nih.gov/pubmed/19070296

    PubMed  Google Scholar 

  6. Gupta V, Garg R (2009) Probiotics. Indian J Med Microbiol 27(3):2002–2009. https://doi.org/10.4103/0255-0857.53201

    Google Scholar 

  7. Richardson M, Rautemaa R (2009) How the host fights against Candida infections. Front Biosci (Schol Ed) (1):246–257. http://www.ncbi.nlm.nih.gov/pubmed/19482700, S1. https://doi.org/10.2741/s24

  8. Pinto TMS, Neves ACC, Leão MVP, Jorge AOC (2008) Vinegar as an antimicrobial agent for control of Candida spp. in complete denture wearers. J Applied Oral Science (Online) 16(6):385–390. https://doi.org/10.1590/S1678-77572008000600006

    Article  Google Scholar 

  9. Querido SMR, Brito GN, Santos SSF, Leão MVP, Ito CYK, Jorge AOC (2011) Opportunistic microorganisms in patients undergoing antibiotic therapy for pulmonary tuberculosis. Braz J Microbiol 42(4):1321–1328. https://doi.org/10.1590/S1517-838220110004000012

    Article  PubMed  PubMed Central  Google Scholar 

  10. Silva CRG, Oliveira LD, Leão MVP, Jorge AOC (2014) Candida spp. adherence to oral epithelial cells and levels of IgA in children with orthodontic appliances. Braz Oral Res 28(1):28–32. https://doi.org/10.1590/S1806-83242013005000031

    Article  Google Scholar 

  11. Shalev E, Battino S, Weiner E, Colodner R, Keness Y (1996) Ingestion of yogurt containing Lactobacillus acidophilus compared with pasteurized yogurt as prophylaxis for recurrent candidal vaginitis and bacterial vaginosis. Arch Fam Med 5(10):593–596 http://www.ncbi.nlm.nih.gov/pubmed/8930233

    Article  PubMed  Google Scholar 

  12. Hatakka K, Ahola AJ, Yli-Knuuttila H, Richardson M, Poussa T, Meurman JH, Korpela R (2007) Probiotics reduce the prevalence of oral Candida in the elderly—a randomized controlled trial. J Dent Res 86(2):125–130. https://www.ncbi.nlm.nih.gov/pubmed/17251510

    Article  PubMed  Google Scholar 

  13. Dos Santos AL, Jorge AOC, Santos SSF, Silva CRG, Leão MVP (2009) Influence of probiotics on Candida presence and IgA anti-Candida in the oral cavity. Braz J Microbiol 40(4):960–964. https://doi.org/10.1590/S1517-838220090004000030

    Article  PubMed  PubMed Central  Google Scholar 

  14. Mendonça FHBP, Santos SSF, Faria IS, Silva CRG, Jorge AOC, Leão MVP (2012) Effects of probiotics bacteria on Candida presence and IgA anti-Candida in the oral cavity of elderly. Braz Dent J 23(5):534–538. https://doi.org/10.1590/S0103-64402012000500011

    Article  PubMed  Google Scholar 

  15. Villena J, Salva S, Agüero G, Alvarez S (2011) Immunomodulatory and protective effect of probiotic Lactobacillus casei against Candida albicans infection in malnourished mice. Microbiol Immunol 55(6):434–445. https://doi.org/10.1111/j.1348-0421.2011.00334.x

    Article  PubMed  Google Scholar 

  16. Oliveira VM, Santos SS, Silva CR, Jorge AO, Leão MV (2016) Lactobacillus is able to alter the virulence and the sensitivity profile of Candida albicans. J Appl Microbiol 121(6):1737–1744. https://doi.org/10.1111/jam.13289

    Article  PubMed  Google Scholar 

  17. Charan J, Kantharia ND (2013) How to calculate sample size in animal studies? J Pharmacol Pharmacother 4(4):303–306. https://doi.org/10.4103/0976-500X.119726

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dongari-Bagtzoglou A, Kashleva H, Dwivedi P, Diaz P, Vasilakos J (2009) Characterization of mucosal Candida albicans biofilms. PLoS One 4(11):e7967. https://doi.org/10.1371/journal.pone.0007967.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Rossoni RD, Fuchs BB, de Barros PP, Velloso MD, Jorge AO, Junqueira JC, Mylonakis E (2017) Lactobacillus paracasei modulates the immune system of Galleria mellonella and protects against Candida albicans infection. PLoS One 12(3):e0173332. https://doi.org/10.1371/journal.pone.0173332

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wagner RD, Johnson SJ (2012) Probiotic lactobacillus and estrogen effects on vaginal epithelial gene expression responses to Candida albicans. J Biomed Sci 19(1):58. https://doi.org/10.1186/1423-0127-19-58

    Article  PubMed  PubMed Central  Google Scholar 

  21. Habil N, Murrani WA, Beal J, Foey AD (2011) Probiotic bacterial strains differentially modulate macrophage cytokine production in a strain-dependent and cell subset-specific manner. Benef Micro 2(4):283–293. https://doi.org/10.3920/BM2011.0027

    Article  Google Scholar 

  22. Gozalbo D, Maneu V, Gil ML (2014) Role of IFN-gamma in immune response to Candida albicans infections. Front Biosci (Landmark Ed) 19:1279–1290 http://www.ncbi.nlm.nih.gov/pubmed/24896350

    Article  Google Scholar 

  23. Zhang H, Chen H, Niu J, Wang Y, Xie L (2009) Role of adaptive immunity in the pathogenesis of Candida albicans keratitis. Invest Ophthalmol Vis Sci 50(6):2653–2659. https://doi.org/10.1167/iovs.08-3104.

    Article  PubMed  Google Scholar 

  24. Uddin MN, Siddig A, Oettinger CW, D’Souza MJ (2011) Potentiation of pro-inflammatory cytokine suppression and survival by microencapsulated dexamethasone in the treatment of experimental sepsis. J Drug Target 19(9):752–760. https://doi.org/10.3109/1061186X.2011.561856

    Article  PubMed  Google Scholar 

  25. Morgan DJ, Davis DM (2017) Distinct effects of dexamethasone on human natural killer cell responses dependent on cytokines. Front Immunol 8:432. https://doi.org/10.3389/fimmu.2017.00432

    Article  PubMed  PubMed Central  Google Scholar 

  26. Samaranayake YH, Samaranayake LP (2001) Experimental oral candidiasis in animal models. Clin Microbiol Rev 14(2):398–429. https://doi.org/10.1128/CMR.14.2.398-429.2001

    Article  PubMed  PubMed Central  Google Scholar 

  27. Metwalli KH, Khan SA, Krom BP, Jabra-Rizk MA (2013) Streptococcus mutans, Candida albicans, and the human mouth: a sticky situation. PLoS Pathog 9(10):e1003616. https://doi.org/10.1371/journal.ppat.1003616

    Article  PubMed  PubMed Central  Google Scholar 

  28. Traynor TR, Huffnagle GB (2001) Role of chemokines in fungal infections. Med Mycol 39:41–50. http://mmy.oxfordjournals.org/content/39/1/41.1.long. https://doi.org/10.1080/mmy.39.1.41.50

    Article  PubMed  Google Scholar 

  29. Huang W, Na L, Fidel PL, Schwarzenberger P (2004) Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 190(3):624–631. https://doi.org/10.1086/422329

    Article  PubMed  Google Scholar 

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Funding

The work was supported by Fundação de Amparo à Pesquisa de São Paulo (FAPESP).

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Authors and Affiliations

  1. Bioscience Basic Institute, University of Taubaté, Av. Tiradentes, 500 Bom Conselho, Taubaté, SP, 12030-180, Brazil

    Mariella Vieira Pereira Leão, Célia Regina Gonçalves e Silva & Silvana Soleo Ferreira dos Santos

  2. Department of Biosciences and Oral Diagnosis, Institute of Science and Technology, Univ. Estadual Paulista, UNESP, Av. Eng. Francisco José Longo, 777 Jardim Sao Dimas, São José dos Campos, SP, 12245-000, Brazil

    Talita Angelina Aureliano Tavares, Juliana Campos Junqueira, Luciane Dias de Oliveira & Antonio Olavo Cardoso Jorge

Authors
  1. Mariella Vieira Pereira Leão
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  2. Talita Angelina Aureliano Tavares
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  3. Célia Regina Gonçalves e Silva
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  4. Silvana Soleo Ferreira dos Santos
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  6. Luciane Dias de Oliveira
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  7. Antonio Olavo Cardoso Jorge
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Correspondence to Mariella Vieira Pereira Leão.

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The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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For this type of study, formal consent was not required.

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Leão, M.V.P., Tavares, T.A.A., Gonçalves e Silva, C.R. et al. Lactobacillus rhamnosus intake can prevent the development of Candidiasis. Clin Oral Invest 22, 2511–2518 (2018). https://doi.org/10.1007/s00784-018-2347-8

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  • DOI: https://doi.org/10.1007/s00784-018-2347-8

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