Determining the Frequency and Antifungal Drug Resistance Patterns of Candida Species Isolated from Patients with Vaginitis in Health and Treatment Centers in Zanjan City

Document Type : Original Article

Authors

1 Department of Parasitology and Mycology, School of Medicine, Zanjan University of Medical Sciences, Zanjan, Iran

2 Department of Medical Laboratory Sciences, School of Paramedical Sciences, Zanjan University of Medical Sciences, Zanjan, Iran

3 Department of Biostatistics and Epidemiology, School of Medicine, Zanjan University of Medical Sciences, Zanjan, Iran

4 Zanjan University of Medical Sciences, Zanjan, Iran

Abstract

Introduction: The management of Candida-related infectious diseases and the recognition of drug susceptibility patterns in each region depend on local epidemiological studies and population structure of each region. The present study was carried out with the aim of identifying the common species associated with VVC and determining their antifungal susceptibility profile.
Materials and Methods: In this study, 140 clinical isolates of Candida species were collected from people with vaginitis referred to a number of health centers in Zanjan, Iran. The collected samples were identified and differentiated using CHROMagar Candida. Antifungal susceptibility tests for fluconazole, itraconazole and ketoconazole was performed by broth microdilution method, and the results were statistically analyzed using SPSS software.
Results: Overall, 41 Candida species were isolated from vaginal discharge samples. C. glabrata was the most frequent with 23 isolates (56.1%), followed by C. albicans (16 isolates, 39%) and C. tropicalis (2 isolates, 4.9%) respectively. Candida isolates showed high resistance to azoles, so that 11 isolates (26.8%) were resistant to fluconazole. Also, the resistance to itraconazole and ketoconazole was found to be 58.5% and 65.9%, respectively.
Conclusions: In this study C. glabrata had the highest prevalence and it shows the change in the pattern of Candida
infections towards non-albicans species. The occurrence of high drug resistance to azoles is one of the problems facing vaginal candidiasis, which leads to recurrent and treatment-resistant infections.

Keywords

1. Martins N, Ferreira IC, Barros L, Silva S, Henriques
M. Candidiasis: predisposing factors, prevention,
diagnosis and alternative treatment. Mycopathologia.
2014;177:223-40.
2. Xie HY, Feng D, Wei DM, Mei L, Chen H, Wang X,
et al. Probiotics for vulvovaginal candidiasis in non‐
pregnant women. Cochrane Database Syst Rev.
2017(11).
3. Mølgaard-Nielsen D, Svanström H, Melbye M, Hviid
A, Pasternak B. Association between use of oral
fluconazole during pregnancy and risk of spontaneous
abortion and stillbirth. Jama. 2016;315(1):58-67.
4. Jr PLF. Distinct protective host defenses against oral
and vaginal candidiasis. Med Mycol. 2002;40(4):359-
75.
5. Sobel JD. Recurrent vulvovaginal candidiasis. Am J
Obstet Gynecol. 2016;214(1):15-21.
6. Kennedy MA, Sobel JD. Vulvovaginal candidiasis
caused by non-albicans Candida species: new insights.
Curr Infect Dis Rep 2010;12:465-70.
7. Makanjuola O, Bongomin F, Fayemiwo SA. An
update on the roles of non-albicans Candida species in
vulvovaginitis. J Fungi. 2018;4(4):121.
8. Hamad M, Kazandji N, Awadallah S, Allam H.
Prevalence and epidemiological characteristics of
vaginal candidiasis in the UAE. Mycoses.
2014;57(3):184-90.
9. Denning DW, Kneale M, Sobel JD, Rautemaa-
Richardson R. Global burden of recurrent
vulvovaginal candidiasis: a systematic review. Lancet
Infect Dis. 2018;18(11):e339-e47.
10. Sharma C, Muralidhar S, Xu J, Meis JF, Chowdhary
A. Multilocus sequence typing of Candida africana
from patients with vulvovaginal candidiasis in New
Delhi, India. Mycoses. 2014;57(9):544-52.
11. Dan M, Poch F, Levin D. High rate of vaginal
infections caused by non-C. albicans Candida species
among asymptomatic women. Med Mycol J.
2002;40(4):383-6.
12. Pfaller M, Diekema D. Epidemiology of invasive
candidiasis: a persistent public health problem. Clin
Microbiol Rev. 2007;20(1):133-63.
13. Sasani E, Rafat Z, Ashrafi K, Salimi Y, Zandi M,
Soltani S, et al .Vulvovaginal candidiasis in Iran: A
systematic review and meta-analysis on the
epidemiology, clinical manifestations, demographic
characteristics, risk factors, etiologic agents and
laboratory diagnosis. Microb Pathog.
2021;154:104802.
14. Willems HM, Ahmed SS, Liu J, Xu Z, Peters BM.
Vulvovaginal candidiasis: a current understanding and
burning questions. J Fungi. 2020;6(1):27.
15. Nyirjesy P. Vulvovaginal candidiasis and bacterial
vaginosis. Infect Dis Clin North Am. 2008;22(4):637-
52.
16. Neal CM, Martens MG. Clinical challenges in
diagnosis and treatment of recurrent vulvovaginal
candidiasis. SAGE Open Med.
2022;10:20503121221115201.
17. Bitew A, Abebaw Y. Vulvovaginal candidiasis:
species distribution of Candida and their antifungal
susceptibility pattern. BMC Womens Health.
2018;18(1):1-10.
18. Powell AM, Gracely E, Nyirjesy P. Non-albicans
Candida vulvovaginitis: treatment experience at a
tertiary care vaginitis center. J Low Genit Tract Dis.
2016;20(1):85-9.
19. Wayne PA. Reference method for broth dilution
antifungal susceptibility testing of yeasts, approved
standard. CLSI document M27-A3, 2008; 2nd edition.
20. Wayne PA. Reference method for broth dilution
antifungal susceptibility testing of yeasts, approved
standard. CLSI document M27-S4, 2012; Fourth
informational supplement.
21. Jeanmonod R, Jeanmonod D, Christopherson N,
Spivey R. Vaginal candidiasis (vulvovaginal
candidiasis). StatPearls. 2019.
22. moghadasi b, shams ghahfarokhi m, zeini f, razaghi
abyaneh m. In vitro Antifungal Effects of
Ketoconazole against Clinical Isolates of Candida
from Vulvovaginal Candidiasis. Daneshvar Med.
2009;16(78):75-82.
23. Falahati M, Sharifinia S, Foroumadi AR, Bolouri F,
Akhlagh L, Yazdan Parast A, et al. Drug Resistance
Pattern in Candida Species Isolated from Vaginitis.
Razi Med Sci. 2009;16(0):40-5.
24. Fouladi B, Rajabibazl M, Fazaeli A, Hashemzadeh
Chaleshtori M. Identification of candida species in
patients with vulvovaginitis presenting different clinical symptoms. J Adv Med Biomed Res.
015;23(98):53-67.
25. Foxman B, Muraglia R, Dietz J-P, Sobel JD, Wagner
J. Prevalence of recurrent vulvovaginal candidiasis in
5 European countries and the United States: results
from an internet panel survey. J Low Genit Tract Dis.
2013;17(3):340-5.
26. Panchal PA, Katara RK, Mehta RC, Soni ST, Nanera
A, Trivedi NA, Desai KJ, Vegad MM.
Microbiological study of various candida species and
its antifungal sensitivity testing isolated from
antenatal women with vaginitis, in tertiary care
teaching hospital, western india. Int J Microbiol Res.
2013 1;5(6):486.
27. Simhan HN, Caritis SN, Krohn MA, Hillier SL.
Elevated vaginal pH and neutrophils are associated
strongly with early spontaneous preterm birth. Am J
Obstet Gynecol. 2003 Oct;189(4):1150-4.
28. Vermitsky J-P, Self MJ, Chadwick SG, Trama JP,
Adelson ME, Mordechai E, et al. Survey of vaginal-
flora Candida species isolates from women of
different age groups by use of species-specific PCR
detection. J Clin Microbiol. 2008;46(4):1501-3.
29. Quan M. Vaginitis: diagnosis and management.
Postgrad Med. 2010;122(6):117-27.
30. Ray D, Goswami R, Banerjee U, Dadhwal V,
Goswami D, Mandal P, et al. Prevalence of Candida
glabrata and its response to boric acid vaginal
suppositories in comparison with oral fluconazole in
patients with diabetes and vulvovaginal candidiasis.
Diabetes Care. 2007;30(2):312-7.
31. Farr A, Effendy I, Frey Tirri B, Hof H, Mayser P,
Petricevic L, et al. Guideline: vulvovaginal candidosis
(AWMF 015/072, level S2k). Mycoses.
2021;64(6):583-602.
32. Nelson M, Wanjiru W, Margaret MW. Prevalence of
vaginal candidiasis and determination of the
occurrence of Candida species in pregnant women
attending the antenatal clinic of Thika District
Hospital, Kenya. Open J Med Microbiol. 2013;2013.
23. Jasim ST. The relationship between vulvovaginal
candidiasis and some predisposing factors in
prevalence among Baghdad women. Syst Rev
Pharm. 2020;11(12):1318-22.
34. Van de Wijgert JH, Verwijs MC, Turner AN,
Morrison CS. Hormonal contraception decreases
bacterial vaginosis but oral contraception may
increase candidiasis: implications for HIV
transmission. Aids. 2013;27(13):2141-53.
35. Yano J, Sobel JD, Nyirjesy P, Sobel R, Williams VL,
Yu Q, et al. Current patient perspectives of
vulvovaginal candidiasis: incidence, symptoms,
management and post-treatment outcomes. BMC
Womens Health. 2019;19:1-9.
36. Anderson MR, Klink K, Cohrssen A. Evaluation of
vaginal complaints. JAMA. 2004 Mar
17;291(11):1368-79.
37. Lowe NK, Neal JL, Ryan-Wenger NA. Accuracy of
the clinical diagnosis of vaginitis compared to a DNA
probe laboratory standard. Obstet Gynecol.
2009;113(1):89.
38. Mylonas I, Bergauer F. Diagnosis of vaginal
discharge by wet mount microscopy: a simple and
underrated method. Obstet Gynecol Surv.
2011;66(6):359-68.
39. Marchaim D, Lemanek L, Bheemreddy S, Kaye KS,
Sobel JD. Fluconazole-resistant Candida albicans
vulvovaginitis. Obstet Gynecol. 2012
Dec;120(6):1407-14.
40. Leusink P, van de Pasch S, Teunissen D, Laan ET,
Lagro-Janssen AL. The relationship between
vulvovaginal candidiasis and provoked vulvodynia: a
systematic review. J Sex Med. 2018;15(9):1310-21.
41. Nurbhai M, Grimshaw J, Watson M, Bond CM,
Mollison JA, Ludbrook A. Oral versus intra‐vaginal
imidazole and triazole anti‐fungal treatment of
uncomplicated vulvovaginal candidiasis (thrush).
Cochrane Database Syst Rev. 2007(4).
42. Pappas PG, Kauffman CA, Andes DR, Clancy CJ,
Marr KA, Ostrosky-Zeichner L, et al. Clinical practice
guideline for the management of candidiasis: 2016
update by the Infectious Diseases Society of America.
Clin Infect Dis. 2016;62(4):e1-e50.
43. Sobel J, Sobel R. Current treatment options for
vulvovaginal candidiasis caused by azole-resistant
Candida species. Expert Opin Pharmacother
2018;19(9):971-7.
44. Pericolini E, Gabrielli E, Ballet N, Sabbatini S,
Roselletti E, Cayzeele Decherf A, et al. Therapeutic
activity of a Saccharomyces cerevisiae-based
probiotic and inactivated whole yeast on vaginal
candidiasis. Virulence. 2017;8(1):74-90.