In-vitro Antifungal Activities of Kombucha Tea Culture Supernatant Combined with Voriconazole against Vulvovaginal Candidiasis Clinical Isolates

Authors

  • Rasha H. Bassyouni Medical Microbiology and Immunology Department, Faculty of Medicine, Fayoum University, Fayoum 63514, Egypt.
  • Fatma AboElnaga Ahmed Medical Microbiology and Immunology Department, Faculty of Medicine, Fayoum University, Fayoum 63514, Egypt.
  • Ahmed A. Ismaiel Botany and Microbiology Department, Faculty of Science, Zagazig University, Zagazig 44519, Egypt.
  • Abdelsamie Abdelmoneim Obstetric and Gynecology Department, Faculty of Medicine, Fayoum University, Fayoum 63514, Egypt.
  • Haitham Badran Obstetric and Gynecology Department, Faculty of Medicine, Fayoum University, Fayoum 63514, Egypt.
  • Mazen A. El Zahry Obstetrics and Gynecology Department, Faculty of Medicine, Azhar University, Cairo 11651, Egypt.
  • Reham Ali Dwedar Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Cairo 12613, Egypt.
  • Ahmed Ashraf Wegdan Medical Microbiology and Immunology Department, Faculty of Medicine, Fayoum University, Fayoum 63514, Egypt.

DOI:

https://doi.org/10.31584/jhsmr.2023933

Keywords:

antimicrobial, biofilm, Kombucha tea culture, voriconazole, vulvovaginal candidiasis

Abstract

Objective: To investigate the antifungal activity of voriconazole, with and without Kombucha tea culture, against Candida strains isolated from vulvovaginal candidiasis.
Material and Methods: The study included 150 females, within child-bearing periods, complaining of valvovaginal candidiasis. Candida strains were isolated, and identified by conventional microbiological methods; and confirmed by Viteck-2 System. The sensitivity of the isolates to voriconazole was performed, via the Disc diffusion method. Resistant strains were then subjected to minimum inhibitory concentrations (MIC) investigation of voriconazole alone, and in combination with a Kombucha tea culture via the broth micro-dilution method in concentrations ranging from 0.0048 to 10 µg/ml. The ability of voriconazole, with and without Kombucha, to eradicate Candida biofilms were investigated using a crystal violet absorbance assay.
Results: Eighty-nine strains were isolated. From these 60 isolates showed variable resistance patterns (57 were voriconazole resistant, and 3 had dose-dependent susceptability). Kombucha significantly decreased the MIC50 of voriconazole against all strains from 5 to 0.625 µg/ml (p-value<0.01); additionally, MIC90 were reduced from 10 to 1.25 µg/ml (p-value =0.000). Voriconazole at a concentration of 0.156 μg/ml succeeded in eradicating biofilms formed by 18 strains after adding a Kombucha tea supernatant versus zero strains when using Voriconazole alone.
Conclusion: Kombucha Black tea cultures could be promising antifungal agents in the treatment of vulvovaginal candidiasis.

References

Larsen B, Monif GR. Understanding the bacterial flora of the female genital tract. Clin Infect Dis 2001;32:e69-77.

Faraji R, Rahimi MA, Rezvanmadani F, Hashemi M. Prevalence of vaginal candidiasis infection in diabetic women. African J Microbiol 2012;6:2773-8.

Pereira LC, Correia, AF, Silva ZDL, Resende CN, Brandão F, Almeida RM, et al. Vulvovaginal candidiasis and current perspectives: new risk factors and laboratory diagnosis by using MALDI TOF for identifying species in primary infection and recurrence. Eur J Clin Microbiol Infect Dis 2021;40:1681–93.

Gonçalves B, Ferreira C, Alves CT, Henriques M , Azeredo J, Silva S. Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors. Crit Rev Microbiol 2016;42:905–27.

Sobel JD. Recurrent vulvovaginal candidiasis. Am J Obstet Gynecol 2016;214:15–21.

Alizadeh M, Kolecka A, Boekhout T, Zarrinfar H, GhanbariNahzag MA, Badiee P, et al. Identification of Candida species isolated from vulvovaginitis using matrix assisted laser desorption ionization-time of flight mass spectrometry. Curr Med Mycol 2017;3:21-5.

Siddiqi R, Mendiratta DK, Rukadikar A, Gadre S. Study of virulence markers and antifungal susceptibility by vitek-2 in various Candida species isolated from cases of vulvovaginal candidiasis. Int J Curr Microbiol App Sci 2017:6:3593–605.

Pfaller MA, Messer SA, Boyken LB, Rice C, Tendolkar S, Hollis RJ, et al. Global trends in the antifungal susceptibility of Cryptococcus neoformans (1990 to 2004). J Clin Microbiol 2005;43:2163–7.

Pfaller MA, Castanheira M, Lockhart SR, Jones RN. Candida glabrata: multidrug resistance and increased virulence in a major opportunistic fungal pathogen. Curr Fungal Infect Rep 2012;6:154–64.

Jackson ST, Mullings AM, Ranford L, Miller A. The epidemiology of mycotic vulvovaginitis and the use of Antifungal agents in suspected mycotic vulvovaginitis and its implications for clinical practice. West Indian Med J 2005;54:192-5.

Sardi JCO, Scorzoni L, Bernardi AM, Almeida F, Mendes Giannini, MJS. Candida species: current epidemiology, pathology biofilm formation, natural anti-fungal products and new therapeutic options. J Med Microbiol 2013;62:10-24.

Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, Gómez-Llorente C, Gil A. Probiotic mechanisms of action. Ann Nutr Metab 2012;61:160–74.

Al-Mohammadi AR, Ismaiel AA, Ibrahim RA, Moustafa AH, Abou Zeid A, Enan G. Chemical constitution and antimicrobial activity of kombucha fermented beverage. Molecules 2021;26:5026.

Watawana MI. Jayawardena N, Gunawardhana CB, Waisundara VY. Health, wellness, and safety aspects of the consumption of kombucha. J Chem 2015;11:1–11.

Ivanišová E, Meňhartová K, Terentjeva M, Harangozo Ľ, Kántor A, Kačániová M. The evaluation of chemical, antioxidant, antimicrobial and sensory properties of kombucha tea beverage. J Food Sci Technol 2020;57:1840-6.

Battikh H, Bakhrouf A. Ammar E. Antimicrobial effect of Kombucha analogues. LWT Food Sci Technol 2012;47:71–7.

Clinical and Laboratory Standards Institute. Reference method for antifungal disk diffusion susceptibility testing of nondermatophyte filamentous fungi; approved guideline. Villanova: CLSI; 2010;

Ramage G, Vande-Walle K, Wickes BL, López-Ribot JL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 2001;45:2475–9.

Capoci IRG, Bonfim-Mendonça PS, Arita GS, Pereira RRA, Consolaro MEL, Bruschi ML, et al. Propolis Is an Efficient Fungicide and Inhibitor of Biofilm Production by Vaginal Candida albicans. Evid Based Complement Alternat Med 2015;9:287693

Rodrigues LB, Santos LR, Tagliari VZ, Rizzo NN, Trenhago G, Oliveira AP, et al. Quantification of biofilm production on polystyrene by Listeria, Escherichia coli and Staphylococcus areus isolated from a poultry slaughterhouse. Braz J Microbiol 2010;41:1082-5.

Ismaiel AA, Bassyouni RH. Kamel Z, Gabr SM. Detoxification of Patulin by Kombucha tea culture. CyTA - J Food 2016;14:271-9.

Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts. 4th ed. Wayne: CLSI; 2017

Fracchia L, Cavallo M, Allegrone G, Martinotti MG. A Lactobacillus-derived biosurfactant inhibits biofilm formation of human pathogenic Candida albicans biofilm producers. Appl Microbiol Biotechnol 2010;2:827-37.

Deghrigue M, Chriaa J, Battikh H, Abid K, Bakhrouf A. Antiproliferative and antimicrobial activities of kombucha tea. Afr J Microbiol Res 2013;7:3466–70

Khan M, Ahmed J, Gul A, Ikram A, Lalani FK. Antifungal susceptibility testing of vulvovaginal Candida species among women attending antenatal clinic in tertiary care hospitals of Peshawar. Infect Drug Resist 2018;11:447-56.

Adesiji Y.O, Ndukwe N, Okanlawon BM. Isolation and Antifungal Sensitivity to Candida isolates in young females. Cent Eur J Med 2011;62:172-6.

Waikhom SD, Afeke I, Kwawu GS, Mbroh HK, Osei GY, Louis B, et al. Prevalence of vulvovaginal candidiasis among pregnant women in the Ho municipality, Ghana: species identification and antifungal susceptibility of Candida isolates. BMC Pregnancy Childbirth 2020;20:266. doi: 10.1186/s12884-020-02963-3.

Wang Y, Yang Q, Chen L, Liu L, Hao R,Zhang T, et al. Cross-resistance between voriconazole and fluconazole for non-albicans Candida infection: a case-case-control study. Eur J Clin Microbiol Infect Dis 2017;36:2117-26.

Mendling W, Brasch J, Cornely OA, Effendy I, Friese, K. Ginter-Hanselmayer G, et al. Guideline: vulvovaginal candidosis (AWMF 015/072), S2k (excluding chronic mucocutaneous candidosis). Mycoses 2015;58(Suppl 1):1–15.

Cetojevic-Simin DD, Bogdanovic GM, Cvetkovic DD, Velicanski AS. Antiproliferative and antimicrobial activity of traditional Kombucha and Satureja montana L. Kombucha. JBUON 2008;13:395-401.

Kıvanç M, Er S. Biofilm formation of Candida Spp. isolated from the vagina and antibiofilm activities of lactic acid bacteria on these Candida isolates. Afr Health Sci 2020;20: 641–8.

Wu X, Zhang S, Li H, Shen L, Dong C, Sun Y, et al. Biofilm formation of Candida albicans facilitates fungal infiltration and persister cell formation in vaginal candidiasis. Front Microbiol 2020;11:1117.

Galdiero, de Alteriis E, De Natale A, D’Alterio A, Siciliano A, Guida M, et al. Eradication of Candida albicans persister cell biofilm by the membranotropic peptide gH625. Sci Rep 2020; 10:1–12.

EL-Azizi M, Farag N, Khardori N. Antifungal activity of amphotericin B and voriconazole against the biofilms and biofilm-dispersed cells of Candida albicans employing a newly developed in vitro pharmacokinetic model. Ann Clin Microbiol Antimicrob 2015;14:21.

Fernandes T, Silva S, Henriques M. Effect of voriconazole on Candida tropicalis biofilms: relation with ERG genes expression. Mycopathologia 2016;181:643-51.

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Published

2023-05-23

How to Cite

1.
Bassyouni RH, Ahmed FA, Ismaiel AA, Abdelmoneim A, Badran H, Zahry MAE, Dwedar RA, Wegdan AA. In-vitro Antifungal Activities of Kombucha Tea Culture Supernatant Combined with Voriconazole against Vulvovaginal Candidiasis Clinical Isolates. J Health Sci Med Res [Internet]. 2023 May 23 [cited 2024 Dec. 23];41(4):e2023933. Available from: https://he01.tci-thaijo.org/index.php/jhsmr/article/view/263805

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