Background: Oral candidiasis is a frequent form of candidiasis, caused by Candida species, in particular, Candida albicans (C. albicans). The transition of C. albicans from yeast to hyphae allows its attachment to epithelial cells, followed by biofilm formation, invasion, and tissue damage. Hence, we investigated the effect of Streptococcus salivarius subspecies thermophilus (S thermophilus) on the growth as well as biofilm and germ-tube formation of C. albicans both in vitro and in vivo in a murine model. Methods: This experimental study was performed in the Department of Medical Mycology and Parasitology, School of Medicine, in collaboration with the Central Research Laboratory and the Comparative Biomedical Center, Shiraz University of Medical Sciences, Shiraz, Iran (2017 to 2018). The inhibitory activity of S. thermophilus against Candida species growth was evaluated using the broth microdilution method, and the inhibition of C. albicans biofilm formation was measured using the XTT assay. The inhibition of C. albicans germ-tube formation by S. thermophilus was evaluated using the plate assay and fluorescence microscopy. The experimental activity of the probiotic bacterium was assessed by culture and histopathological methods in six groups of five mice, comprising those treated with four concentrations of probiotics, fluconazole, and distilled water. The one-way analysis of variance, followed by a Tukey post hoc test, was used and a P value of less than 0.05 was considered significant. Results: S. thermophilus inhibited Candida species growth at concentrations of 16 to 512 µg/mL. This probiotic inhibited the formation of C. albicans biofilms and germ tubes in a dose-dependent manner. S. thermophilus significantly reduced the colony-forming units in the mice receiving 30 mg/mL of this probiotic treatment compared with the control group (P=0.024). The histopathological analysis showed that Candida colonization was diminished in the mice following the administration of the probiotic. Conclusion: Given the inhibitory activity of S. thermophilus against the growth, transition, and biofilm formation of C. albicans, it could be used in the management of oral candidiasis. |
- Morelli L, Capurso L. FAO/WHO guidelines on probiotics: 10 years later. J Clin Gastroenterol. 2012;46 Suppl:S1-2. doi: 10.1097/MCG.0b013e318269fdd5. PubMed PMID: 22955349.
- Chen CC, Kong MS, Lai MW, Chao HC, Chang KW, Chen SY, et al. Probiotics have clinical, microbiologic, and immunologic efficacy in acute infectious diarrhea. Pediatr Infect Dis J. 2010;29:135-8. doi: 10.1097/inf.0b013e3181b530bf. PubMed PMID: 20135748.
- Haukioja A. Probiotics and oral health. Eur J Dent. 2010;4:348-55. PubMed PMID: 20613927; PubMed Central PMCID: PMCPMC2897872.
- Meurman JH, Stamatova IV. Probiotics: Evidence of Oral Health Implications. Folia Med (Plovdiv). 2018;60:21-9. doi: 10.1515/folmed-2017-0080. PubMed PMID: 29668457.
- Jiang Q, Stamatova I, Kari K, Meurman JH. Inhibitory activity in vitro of probiotic lactobacilli against oral Candida under different fermentation conditions. Benef Microbes. 2015;6:361-8. doi: 10.3920/BM2014.0054. PubMed PMID: 25380800.
- Kraft-Bodi E, Jorgensen MR, Keller MK, Kragelund C, Twetman S. Effect of Probiotic Bacteria on Oral Candida in Frail Elderly. J Dent Res. 2015;94:181S-6S. doi: 10.1177/0022034515595950. PubMed PMID: 26202995.
- Mendonca FH, Santos SS, Faria Ida S, Goncalves e Silva CR, Jorge AO, Leao MV. Effects of probiotic bacteria on Candida presence and IgA anti-Candida in the oral cavity of elderly. Braz Dent J. 2012;23:534-8. doi: 10.1590/s0103-64402012000500011. PubMed PMID: 23306230.
- Ishijima SA, Hayama K, Burton JP, Reid G, Okada M, Matsushita Y, et al. Effect of Streptococcus salivarius K12 on the in vitro growth of Candida albicans and its protective effect in an oral candidiasis model. Appl Environ Microbiol. 2012;78:2190-9. doi: 10.1128/AEM.07055-11. PubMed PMID: 22267663; PubMed Central PMCID: PMCPMC3302625.
- Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, et al. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev. 2005;29:435-63. doi: 10.1016/j.femsre.2005.04.008. PubMed PMID: 16125007.
- Ogawa A, Furukawa S, Fujita S, Mitobe J, Kawarai T, Narisawa N, et al. Inhibition of Streptococcus mutans biofilm formation by Streptococcus salivarius FruA. Appl Environ Microbiol. 2011;77:1572-80. doi: 10.1128/AEM.02066-10. PubMed PMID: 21239559; PubMed Central PMCID: PMCPMC3067281.
- Iyer R, Tomar S, Maheswari TU, Singh R. Streptococcus thermophilus strains: Multifunctional lactic acid bacteria. International Dairy Journal. 2010;20:133-41. doi: 10.1016/j.idairyj.2009.10.005.
- Mehta M, Dave M. Candidiasis-review of risk factor. IJCR. 2018;10:67838-40.
- Manik A, Bahl R. A review on oral candidal infection. Journal of Advanced Medical and Dental Sciences Research. 2017;5:54.
- Sharifynia S, Badali H, Sharifi Sorkherizi M, Shidfar MR, Hadian A, Shahrokhi S, et al. In Vitro Antifungal Susceptibility Profiles of Candida albicans Complex Isolated from Patients with Respiratory Infections. Acta Med Iran. 2016;54:376-81. PubMed PMID: 27306344.
- Soll DR. The role of phenotypic switching in the basic biology and pathogenesis of Candida albicans. J Oral Microbiol. 2014;6. doi: 10.3402/jom.v6.22993. PubMed PMID: 24455104; PubMed Central PMCID: PMCPMC3895265.
- Tsui C, Kong EF, Jabra-Rizk MA. Pathogenesis of Candida albicans biofilm. Pathog Dis. 2016;74:ftw018. doi: 10.1093/femspd/ftw018. PubMed PMID: 26960943; PubMed Central PMCID: PMCPMC5975230.
- Kolenbrander PE, Palmer RJ, Jr., Periasamy S, Jakubovics NS. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol. 2010;8:471-80. doi: 10.1038/nrmicro2381. PubMed PMID: 20514044.
- Dongari-Bagtzoglou A, Kashleva H, Dwivedi P, Diaz P, Vasilakos J. Characterization of mucosal Candida albicans biofilms. PLoS One. 2009;4:e7967. doi: 10.1371/journal.pone.0007967. PubMed PMID: 19956771; PubMed Central PMCID: PMCPMC2776351.
- Diaz PI, Strausbaugh LD, Dongari-Bagtzoglou A. Fungal-bacterial interactions and their relevance to oral health: linking the clinic and the bench. Front Cell Infect Microbiol. 2014;4:101. doi: 10.3389/fcimb.2014.00101. PubMed PMID: 25120959; PubMed Central PMCID: PMCPMC4114182.
- Bamford CV, d’Mello A, Nobbs AH, Dutton LC, Vickerman MM, Jenkinson HF. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect Immun. 2009;77:3696-704. doi: 10.1128/IAI.00438-09. PubMed PMID: 19528215; PubMed Central PMCID: PMCPMC2737996.
- Boris S, Barbes C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2000;2:543-6. doi: 10.1016/s1286-4579(00)00313-0. PubMed PMID: 10865199.
- Forster TM, Mogavero S, Drager A, Graf K, Polke M, Jacobsen ID, et al. Enemies and brothers in arms: Candida albicans and gram-positive bacteria. Cell Microbiol. 2016;18:1709-15. doi: 10.1111/cmi.12657. PubMed PMID: 27552083.
- Mukherjee PK, Chandra J, Retuerto M, Sikaroodi M, Brown RE, Jurevic R, et al. Oral mycobiome analysis of HIV-infected patients: identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathog. 2014;10:e1003996. doi: 10.1371/journal.ppat.1003996. PubMed PMID: 24626467; PubMed Central PMCID: PMCPMC3953492.
- Devine DA, Marsh PD. Prospects for the development of probiotics and prebiotics for oral applications. J Oral Microbiol. 2009;1. doi: 10.3402/jom.v1i0.1949. PubMed PMID: 21523212; PubMed Central PMCID: PMCPMC3077007.
- Kohler GA, Assefa S, Reid G. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect Dis Obstet Gynecol. 2012;2012:636474. doi: 10.1155/2012/636474. PubMed PMID: 22811591; PubMed Central PMCID: PMCPMC3395238.
- Ujaoney S, Chandra J, Faddoul F, Chane M, Wang J, Taifour L, et al. In vitro effect of over-the-counter probiotics on the ability of Candida albicans to form biofilm on denture strips. J Dent Hyg. 2014;88:183-9. PubMed PMID: 24935148.
- Association WM. WMA Declaration of Helsinki-Ethical principles for medical research involving human subjects. 2016.
- Dell RB, Holleran S, Ramakrishnan R. Sample size determination. ILAR J. 2002;43:207-13. doi: 10.1093/ilar.43.4.207. PubMed PMID: 12391396; PubMed Central PMCID: PMCPMC3275906.
- Meurman JH, Stamatova I. Probiotics: contributions to oral health. Oral Dis. 2007;13:443-51. doi: 10.1111/j.1601-0825.2007.01386.x. PubMed PMID: 17714346.
- Biyari S, Fozouni L. The inhibitory effect of probiotic bacteria against drug-resistant Candida species isolated from the oral cavity of the elderly. Shiraz E-Medical Journal. 2018;19:e62026. doi: 10.5812/semj.62026.
- Rodrigues LR, Teixeira JA, van der Mei HC, Oliveira R. Isolation and partial characterization of a biosurfactant produced by Streptococcus thermophilus A. Colloids Surf B Biointerfaces. 2006;53:105-12. doi: 10.1016/j.colsurfb.2006.08.009. PubMed PMID: 16987640.
- Koll P, Mandar R, Marcotte H, Leibur E, Mikelsaar M, Hammarstrom L. Characterization of oral lactobacilli as potential probiotics for oral health. Oral Microbiol Immunol. 2008;23:139-47. doi: 10.1111/j.1399-302X.2007.00402.x. PubMed PMID: 18279182.
- Shirtliff ME, Peters BM, Jabra-Rizk MA. Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett. 2009;299:1-8. doi: 10.1111/j.1574-6968.2009.01668.x. PubMed PMID: 19552706; PubMed Central PMCID: PMCPMC4406406.
- Tang H, Ren J, Yuan J, Zeng B, Wei H. An in vitro assessment of inhibitory effect of 16 strains of probiotics on the germination of Candida albicans. African Journal of Microbiology Research. 2010;4:1251-6.
- Elahi S, Pang G, Ashman R, Clancy R. Enhanced clearance of Candida albicans from the oral cavities of mice following oral administration of Lactobacillus acidophilus. Clin Exp Immunol. 2005;141:29-36. doi: 10.1111/j.1365-2249.2005.02811.x. PubMed PMID: 15958067; PubMed Central PMCID: PMCPMC1809411.
|