Drug Resistance and Biofilm Formation in Candida Species of Vaginal Origin
-
Tahereh Alikhani
,
Roshanak Daie Ghazvini
,
Mehdi Mirzaii
,
Seyed Jamal Hashemi
,
Mozhgan Fazli
,
Zahra Rafat
,
Davoud Roostaei
,
Pegah Ardi
,
Hasti Kamali Sarvestani
,
Mahdi Zareei
Abstract
Background: Candida species are normal vaginal flora in healthy women, which can cause vulvovaginal candidiasis (VVC). The formation of biofilm is a cause of drug resistance in Candida species of vaginal origin. We aimed to specify Candida species cause VVC, detect their biofilm-forming ability, and antifungal susceptibility pattern.
Methods: Overall 150 vaginal samples were collected from suspected cases of referring to Bahar Hospital of Shahroud, Iran between Jan 2018 and Jan 2019. Samples were cultured on Sabouraud dextrose agar (SDA), Chrome gar Candida and Corn meal agar (CMA). PCR-RFLP was performed to confirm the identification. Biofilm formation of the identified species was measured by the Crystal Violet method. The susceptibility to fluconazole, clotrimazole, and miconazole was determined based on the CLSI document M27-A3.
Results: Of 50 women (33.3%) were suffering from VVC. C.albicans was the predominant species isolated in this study (n=39, 78%) followed by C. glabratia (n=11, 22%). In addition, in 25 (50%) of positive samples, biofilm formation was determined. The mean MIC of fluconazole and clotrimazole for C. albicans was 5.02 μg /mL and 3.92 μg /mL, respectively. Furthermore, the mean MIC related to these drugs for C. glabrata was 12.45 μg / mL and 4.1μg / mL, respectively. The mean diameter of miconazole inhibition zone for C. albicans and C. glabra isolates was 25.13 mm and 24.5mm, respectively and all of them were susceptible to this drug.
Conclusion: C.albicans was the predominant Candida species isolated from patients with VVC and also was the predominant biofilm producer species.
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3. Mendling, W., & Brasch, J. (2012). Guideline vulvovaginal candidosis (2010) of the german society for gynecology and obstetrics, the working group for infections and infectimmunology in gynecology and obstetrics, the german society of dermatology, the board of german dermatologists and the german speaking mycological society. Mycoses, 55:1-13.
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7. Redding, S., Smith, J., Farinacci, G., Rinaldi, M., Fothergill, A., Rhine-Chalberg, J., & Pfaller, M. (1994). Resistance of Candida albicans to fluconazole during treatment of oropharyngeal candidiasis in a patient with AIDS: documentation by in vitro susceptibility testing and DNA subtype analysis. Clinical Infectious Diseases, 18(2):240-2
8. Donlan, R., Murga, R., Carpenter, J., Brown, E., Besser, R., & Fields, B. (2001). Monochloramine disinfection of biofilm‐associated Legionella pneumophila in a potable water model system. Legionella, 406-10.
9. Sobel JD (1986) Recurrent vulvovaginal candidiasis. A prospective study of the efficacy of maintenance ketoconazole therapy. N Engl J:1455-8.
10. Kumamoto CA (2005) A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci: 5576-81.
11. Inci M, Atalay MA, KOÇ AN, et al (2012). Investigating virulence factors of clinical Candida isolates in relation to atmospheric conditions and genotype. Turk J Med Sci, 42(2): 1476-83.
12. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Meis JF, Gould IM, Fu W, Colombo AL, Rodriguez-Noriega E (2007). Results from the ARTEMIS DISK Global Antifungal Surveillance study, 1997 to 2005: an 8.5-year analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol. 1;45(6):1735-45.
13. Hazen KC, Baron EJ, Colombo AL, et al (2003). Comparison of the susceptibilities of Candida spp. to fluconazole and voriconazole in a 4-year global evaluation using disk diffusion. J Clin Microbiol: 5623-5632.
14. Pfaller M, Diekema D, Gibbs D, et al (2009). Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: 10.5-year analysis of susceptibilities of noncandidal yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol.: 1;47(1):117-23.
15. Klimko N, Kozlova Y, Khostelidi S, et al (2015). The burden of serious fungal diseases in Russia. Mycoses .58:58-62.
16. Sherry L, Kean R, McKloud E, O'Donnell LE, Metcalfe R, Jones BL, Ramage G. (2017). Biofilms formed by isolates from recurrent vulvovaginal candidiasis patients are heterogeneous and insensitive to fluconazole. Antimicrob Agents Chemother: e01065-17.
17. Giacomazzi J, Baethgen L, Carneiro LC, Millington MA, Denning DW, Colombo AL, Pasqualotto AC, in association with the LIFE program (2016). The burden of serious human fungal infections in Brazil. Mycoses. 59(3):145-50.
18. Jung HS, Ehlers MM, Lombaard H, Redelinghuys MJ, Kock MM (2017). Etiology of bacterial vaginosis and polymicrobial biofilm formation. Crit Rev Microbiol. 43(6):651-67.
19. Hardy L, Cerca N, Jespers V, Vaneechoutte M., Crucitti T (2017). Bacterial biofilms in the vagina. Res Microbiol. 168(9-10):865-74.
20. Akbarzdeh M, Bonyadpour B, Pakshir K (2010). Causes and clinical symptoms of vaginal candidiasis in patients referring to selective clinics of Shiraz University of Medical Sciences. Arak Med Uni J. 13(3):12-20.
21Nazeri M, Mesdaghinia E, Moravej SA, Atabakhshiyan R, Soleymani F (2012). Prevalence of vulvovaginal candidiasis and frequency of candida species in women. J Maz Uni Med. 21(86):254-62.
22. Gonçalves, B., Ferreira, C., Alves, C. T., Henriques, M., Azeredo, J., & Silva, S. (2012). Prevalence of vaginal candidiasis infection in diabetic women. Afr. J. Microbiol. Res :2773-2778.
23. Gonçalves B, Ferreira C, Alves CT, et al (2016). Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors. Crit Rev Microbiol: 42(6), 905-927.
24. Ramage G, López-Rib JL (2005). Techniques for antifungal susceptibility testing of Candida albicans biofilms. Antifungal Agents: 71-79.
25. Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009). Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Sabouraudia. 7:681-9.
26. Mohammadi R, Mirhendi H, Rezaei-Matehkolaei A, Ghahri M, Shidfar MR, Jalalizand N, Makimura K. (2013). Molecular identification and distribution profile of Candida species isolated from Iranian patients. Med Mycol J. 51(6):657-63.
27. Rafat Z, Hashemi SJ, Ahamdikia K, Daie-Ghazvini R, Bazvandi F (2017). Study of skin and nail Candida species as a normal flora based on age groups in healthy persons in Tehran-Iran. J Mycol Med. 27(4): 501-5.
28. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al (2020). Fungal Isolates of the Respiratory Tract in Symptomatic Patients Hospitalized in Pulmonary Units: A Mycological and Molecular Epidemiologic Study. J Multidiscip Healthc. 13 : 661-9.
29. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al (2020). Epidemiology, laboratory diagnosis and clinical aspects of fungal pulmonary infections in 384 patients hospitalized in pulmonary units in Guilan province, Iran. Iran J Microbiol. 12(4) : 353-63.
2. Sobel, J. D. (1992). Pathogenesis and treatment of recurrent vulvovaginal candidiasis. Clinical Infectious Diseases, 14(1): 148-53.
3. Mendling, W., & Brasch, J. (2012). Guideline vulvovaginal candidosis (2010) of the german society for gynecology and obstetrics, the working group for infections and infectimmunology in gynecology and obstetrics, the german society of dermatology, the board of german dermatologists and the german speaking mycological society. Mycoses, 55:1-13.
4. Oriel, J. D., Partridge, B. M., Denny, M. J., & Coleman, J. C. (1972). Genital yeast infections. Br Med J, 4(5843): 761-4.
5. Sobel, J. D. (1985). Epidemiology and pathogenesis of recurrent vulvovaginal candidiasis. American journal of obstetrics and gynecology, 152(7):924-35.
6. Linda, O., & Eckert, M. D. (2006). Acute vulvovaginitis. N Engl J Med, 355(12): 1244-52.
7. Redding, S., Smith, J., Farinacci, G., Rinaldi, M., Fothergill, A., Rhine-Chalberg, J., & Pfaller, M. (1994). Resistance of Candida albicans to fluconazole during treatment of oropharyngeal candidiasis in a patient with AIDS: documentation by in vitro susceptibility testing and DNA subtype analysis. Clinical Infectious Diseases, 18(2):240-2
8. Donlan, R., Murga, R., Carpenter, J., Brown, E., Besser, R., & Fields, B. (2001). Monochloramine disinfection of biofilm‐associated Legionella pneumophila in a potable water model system. Legionella, 406-10.
9. Sobel JD (1986) Recurrent vulvovaginal candidiasis. A prospective study of the efficacy of maintenance ketoconazole therapy. N Engl J:1455-8.
10. Kumamoto CA (2005) A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci: 5576-81.
11. Inci M, Atalay MA, KOÇ AN, et al (2012). Investigating virulence factors of clinical Candida isolates in relation to atmospheric conditions and genotype. Turk J Med Sci, 42(2): 1476-83.
12. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Meis JF, Gould IM, Fu W, Colombo AL, Rodriguez-Noriega E (2007). Results from the ARTEMIS DISK Global Antifungal Surveillance study, 1997 to 2005: an 8.5-year analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol. 1;45(6):1735-45.
13. Hazen KC, Baron EJ, Colombo AL, et al (2003). Comparison of the susceptibilities of Candida spp. to fluconazole and voriconazole in a 4-year global evaluation using disk diffusion. J Clin Microbiol: 5623-5632.
14. Pfaller M, Diekema D, Gibbs D, et al (2009). Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: 10.5-year analysis of susceptibilities of noncandidal yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol.: 1;47(1):117-23.
15. Klimko N, Kozlova Y, Khostelidi S, et al (2015). The burden of serious fungal diseases in Russia. Mycoses .58:58-62.
16. Sherry L, Kean R, McKloud E, O'Donnell LE, Metcalfe R, Jones BL, Ramage G. (2017). Biofilms formed by isolates from recurrent vulvovaginal candidiasis patients are heterogeneous and insensitive to fluconazole. Antimicrob Agents Chemother: e01065-17.
17. Giacomazzi J, Baethgen L, Carneiro LC, Millington MA, Denning DW, Colombo AL, Pasqualotto AC, in association with the LIFE program (2016). The burden of serious human fungal infections in Brazil. Mycoses. 59(3):145-50.
18. Jung HS, Ehlers MM, Lombaard H, Redelinghuys MJ, Kock MM (2017). Etiology of bacterial vaginosis and polymicrobial biofilm formation. Crit Rev Microbiol. 43(6):651-67.
19. Hardy L, Cerca N, Jespers V, Vaneechoutte M., Crucitti T (2017). Bacterial biofilms in the vagina. Res Microbiol. 168(9-10):865-74.
20. Akbarzdeh M, Bonyadpour B, Pakshir K (2010). Causes and clinical symptoms of vaginal candidiasis in patients referring to selective clinics of Shiraz University of Medical Sciences. Arak Med Uni J. 13(3):12-20.
21Nazeri M, Mesdaghinia E, Moravej SA, Atabakhshiyan R, Soleymani F (2012). Prevalence of vulvovaginal candidiasis and frequency of candida species in women. J Maz Uni Med. 21(86):254-62.
22. Gonçalves, B., Ferreira, C., Alves, C. T., Henriques, M., Azeredo, J., & Silva, S. (2012). Prevalence of vaginal candidiasis infection in diabetic women. Afr. J. Microbiol. Res :2773-2778.
23. Gonçalves B, Ferreira C, Alves CT, et al (2016). Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors. Crit Rev Microbiol: 42(6), 905-927.
24. Ramage G, López-Rib JL (2005). Techniques for antifungal susceptibility testing of Candida albicans biofilms. Antifungal Agents: 71-79.
25. Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009). Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Sabouraudia. 7:681-9.
26. Mohammadi R, Mirhendi H, Rezaei-Matehkolaei A, Ghahri M, Shidfar MR, Jalalizand N, Makimura K. (2013). Molecular identification and distribution profile of Candida species isolated from Iranian patients. Med Mycol J. 51(6):657-63.
27. Rafat Z, Hashemi SJ, Ahamdikia K, Daie-Ghazvini R, Bazvandi F (2017). Study of skin and nail Candida species as a normal flora based on age groups in healthy persons in Tehran-Iran. J Mycol Med. 27(4): 501-5.
28. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al (2020). Fungal Isolates of the Respiratory Tract in Symptomatic Patients Hospitalized in Pulmonary Units: A Mycological and Molecular Epidemiologic Study. J Multidiscip Healthc. 13 : 661-9.
29. Rafat Z, Hashemi SJ, Ashrafi K, Nikokar I, Jafari A, Foroushani AR, et al (2020). Epidemiology, laboratory diagnosis and clinical aspects of fungal pulmonary infections in 384 patients hospitalized in pulmonary units in Guilan province, Iran. Iran J Microbiol. 12(4) : 353-63.
| Files | ||
| Issue | Vol 51 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v51i4.9253 | |
| Keywords | ||
| Vulvovaginal candidiasis Biofilm Candida albicans Azole antifungals | ||
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How to Cite
1.
Alikhani T, Daie Ghazvini R, Mirzaii M, Hashemi SJ, Fazli M, Rafat Z, Roostaei D, Ardi P, Kamali Sarvestani H, Zareei M. Drug Resistance and Biofilm Formation in Candida Species of Vaginal Origin. Iran J Public Health. 2022;51(4):913-918.
