Epidemiologic Evaluation of Candida Species in Vaginal Swab Specimens: An 11-Year Retrospective Study

Abstract

Objective: Candida species may be part of the normal vulvovaginal flora, and hence their isolation in vaginal cultures does not necessarily indicate infection. However, vulvovaginal candidiasis (VVC) is a clinical condition particularly prevalent among women of reproductive age. The aim of this study was to investigate the epidemiology of Candida species isolated from vaginal swab samples (VSS) in the microbiology laboratory. Materials and Methods: This study was designed retrospectively at a university hospital in Istanbul, with a bed capacity of 950, between August 2012 and August 2023. A total of 7050 vaginal swab culture results were analyzed in the microbiology laboratory. VSSs were cultured on CHROMagar™ Candida (CHROMagar, Paris, France) to isolate fungal pathogens. Automated systems such as the VITEK 2 (bioMérieux, France) system or MALDI-TOF mass spectrometry (Bruker, United States) were employed for undetermined colonies on this medium. The study evaluated the results of 2594 vaginal swab cultures and identified Candida species.  Results: The rate of Candida species in VSS cultures was 36.79%. The mean age of the patients was 36.1 years (range: 0–85 years), with 97.8% falling within the category of young adults. The highest prevalence of VVC was in patients 29–38 years of age (48%). Candida albicans accounted for 70.7%, non-albicans Candida for 26.4%, and growth of more than one Candida species for 2.8%. The most frequently observed non-albicans species was Candida glabrata, accounting for 23.1% of the isolates. Conclusions: C. albicans was the predominant species in VSSs. However, the emergence of C. glabrata as a significant non-albicans species is a serious concern due to its potential for azole resistance.

Keywords

• Candida albicans
• non-albicans Candida
• vaginal candidiasis
• vaginal swab culture

Vajinal Sürüntü Örneklerindeki Candida Türlerinin Epidemiyolojik Değerlendirmesi: 11 Yıllık Retrospektif Bir Çalışma

Öz

Amaç: Candida türleri normal vulvovajinal floranın bir parçası olabilir ve bu nedenle vajinal kültürlerde izole edilmeleri mutlaka enfeksiyona işaret etmez. Bununla birlikte, vulvovajinal kandidiyazis özellikle üreme çağındaki kadınlarda yaygın olan klinik bir durumdur. Bu çalışmanın amacı, mikrobiyoloji laboratuvarına gönderilen vajinal sürüntü kültürlerinden izole edilen Candida türlerinin epidemiyolojisini incelemektir. Materyal ve Metot: Bu çalışma Ağustos 2012-Ağustos 2023 tarihleri arasında İstanbul'da 950 yatak kapasiteli bir üniversite hastanesinde retrospektif olarak gerçekleştirilmiştir. Toplam 7050 vajinal sürüntü örneği kültürü mikrobiyoloji laboratuvarında analiz edilmiştir. Mantar patojenlerinin izolasyonu için kültür besiyeri olarak CHROMagar™ Candida (CHROMagar, Paris, France) kullanılmıştır. Bu besiyerinde belirlenemeyen kolonilerin tanımlanması için VITEK 2 (bioMérieux, Fransa) sistemi veya MALDI-TOF mass spectrometry (Bruker, United States) gibi otomatize sistemler kullanılmıştır. Çalışmada, Candida türlerinin tanımlandığı 2594 vajinal sürüntü kültürünün sonuçları değerlendirilmiştir. Bulgular: Vaginal sürüntü kültürlerinden Candida türlerinin izolasyon oranı %36.79’dır. Hastaların ortalama yaşı 36.1 (aralık: 0-85 yıl) olup, %97.8'i genç yetişkin kategorisinde yer almaktadır. En yüksek vulvovaginal kandidiyazis prevalansı 29-38 yaş arasındaki hastalarda görülmüştür (%48). Candida albicans %70,7, non-albicans Candida %26.4 ve birden fazla türde Candida üremesi %2.8 oranında görülmüştür. En sık gözlenen non-albicans Candida türü, izolatların %23.1'ini oluşturan Candida glabrata olmuştur. C. albicans ve non-albicans Candida izolasyon oranlarında çalışma periyodu süresince anlamlı bir değişiklik gözlenmemiştir. Sonuç: On bir yıllık süreçte C. albicans vajinal sürüntü örneklerinde baskın tür olarak kalmıştır. Bununla birlikte non-albicans Candida türlerinden C. glabrata'nın baskın tür olarak ortaya çıkması, azol direnci potansiyeli nedeniyle tedavi güçlüğü açısından endişe kaynağıdır.

Anahtar Kelimeler

• Candida albicans
• non-albicans Candida
• vajinal kandidiyazis
• vajinal sürüntü kültürü

References

1. Sun Z, Ge X, Qiu B, et al. Vulvovaginal candidiasis and vaginal microflora interaction: Microflora changes and probiotic therapy. Front Cell Infect Microbiol. 2023;13. doi:10.3389/fcimb.2023.1123026
2. Willems HME, Ahmed SS, Liu J, Xu Z, Peters BM. Vulvovaginal candidiasis: A current understanding and burning questions. Journal of Fungi. 2020;6(1). doi:10.3390/jof6010027
3. Gonçalves B, Ferreira C, Alves CT, Henriques M, Azeredo J, Silva S. Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors. Crit Rev Microbiol. 2016;42(6). doi:10.3109/1040841X.2015.1091805
4. Gandhi AB, Purandare A, Athota K, et al. Vulvovaginal candidiasis: Epidemiology, treatment and prevention strategies. Indian Journal of Obstetrics and Gynecology Research. 2022;9(3). doi:10.18231/j.ijogr.2022.063
5. Farr A, Effendy I, Frey Tirri B, et al. Guideline: Vulvovaginal candidosis (AWMF 015/072, level S2k). Mycoses. 2021;64(6). doi:10.1111/myc.13248
6. Arechavala A, Negroni R, Santiso G, Depardo R, Bonvehí P. Chronic recurrent vulvovaginitis is not only due to Candida. Rev Iberoam Micol. 2021;38(3). doi:10.1016/j.riam.2021.03.002
7. Kennedy MA, Sobel JD. Vulvovaginal Candidiasis caused by non-albicans Candida species: New insights. Curr Infect Dis Rep. 2010;12(6). doi:10.1007/s11908-010-0137-9
8. Kalaiarasan K, Singh R, Chaturvedula L. Fungal profile of vulvovaginal candidiasis in a tertiary care hospital. Journal of Clinical and Diagnostic Research. 2017;11(3). doi:10.7860/JCDR/2017/23578.9475

9. Yano J, Sobel JD, Nyirjesy P, et al. Current patient perspectives of vulvovaginal candidiasis: Incidence, symptoms, management and post-treatment outcomes. BMC Womens Health. 2019;19(1). doi:10.1186/s12905-019-0748-8
10. Benedict K, Singleton AL, Jackson BR, Molinari NAM. Survey of incidence, lifetime prevalence, and treatment of self-reported vulvovaginal candidiasis, United States, 2020. BMC Womens Health. 2022;22(1). doi:10.1186/s12905-022-01741-x
11. Brandolt TM, Klafke GB, Gonçalves CV, et al. Prevalence of Candida spp. in cervical-vaginal samples and the in vitro susceptibility of isolates. Brazilian Journal of Microbiology. 2017;48(1):145-150. doi:10.1016/j.bjm.2016.09.006
12. Pereira LC, Correia AF, da Silva ZDL, 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. European Journal of Clinical Microbiology and Infectious Diseases. 2021;40(8). doi:10.1007/s10096-021-04199-1
13. Jacob L, John M, Kalder M, Kostev K. Prevalence of vulvovaginal candidiasis in gynecological practices in Germany: A retrospective study of 954,186 patients. Curr Med Mycol. 2018;4(1):6-11. doi:10.18502/cmm.4.1.27
14. Aroca JJ, Martínez PR, Esteban LMM, González AMF, García-Arata I, Menchero SP. Epidemiology and etiology of vulvovaginal candidiasis in spanish and immigrants’ women in fuenlabrada (madrid). Revista Espanola de Quimioterapia. 2020;33(3):187-192. doi:10.37201/req/099.2019
15. Mushi MF, Olum R, Bongomin F. Prevalence, antifungal susceptibility and etiology of vulvovaginal candidiasis in sub-Saharan Africa: A systematic review with meta-analysis and meta-regression. Med Mycol. 2022;60(7). doi:10.1093/mmy/myac037
16. Shanmugam N, Balasundharam A, Thomas IN, et al. A Cross-Sectional Clinical Investigation of Organisms Causing Vaginal Discharge in Patients in Rural Tamil Nadu, India. Cureus. Published online 2023. doi:10.7759/cureus.33979
17. Sasani E, Rafat Z, Ashrafi K, 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. doi:10.1016/j.micpath.2021.104802
18. Huang SH, Hsu HC, Lee TF, et al. Prevalence, Associated Factors, and Appropriateness of Empirical Treatment of Trichomoniasis, Bacterial Vaginosis, and Vulvovaginal Candidiasis among Women with Vaginitis. Microbiol Spectr. 2023;11(3). doi:10.1128/spectrum.00161-23
19. Malak A, Aydın KM, Gulen D, Kaya AD, Taşdemir N, Varol G. Vulvovajinal Kandidiyazis: Risk Faktörleri ve İnfeksiyon Etkenlerinin Dağılımı. Sağlık Bilimlerinde Değer. 2024;14(1). doi:10.33631/sabd.1359836
20. Hösükoǧlu FG, Ekşi F, Erinmez M, Uǧur MG. An Epidemiologic Analysis of Vulvovaginal Candidiasis and Antifungal Susceptibilities. Infectious Microbes and Diseases. 2022;4(3). doi:10.1097/IM9.0000000000000095
21. Chaabaawi A, Sucu M, Karakoyun AS, Ünal N, Kara E, İlkit M. Gebelerde Candida Vajinitinin Epidemiyolojisi. Turk Mikrobiyol Cemiy Derg. 2022;52(2):109-118. doi:10.54453/tmcd.2022.82621
22. Karakoç ZÇ. Vajinitlerde Etiyoloji Değişiyor mu? Tek Merkez Verilerinin Paylaşımı. Muğla Sıtkı Koçman Üniversitesi Tıp Dergisi. 2021;8(1):18-22. doi:10.47572/muskutd.769354
23. Bashir G, Altaf I, Khurshid R, Ahmed T, Ali A, Zaffar S. Identification and pattern of antifungal susceptibility of Candida species isolated from cases of vaginitis in a tertiary care hospital in India. Iran J Microbiol. 2023;15(2). doi:10.18502/ijm.v15i2.12484
24. Vermitsky JP, Self MJ, Chadwick SG, 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). doi:10.1128/JCM.02485-07
25. Bitew A, Abebaw Y. Vulvovaginal candidiasis: Species distribution of Candida and their antifungal susceptibility pattern. BMC Womens Health. 2018;18(1). doi:10.1186/s12905-018-0607-z
26. John N, Rahima S, Raji T, Santhosh P, Kidangazhiathmana A, Sukumarakurup S. Clinicoetiological study on vaginal discharge among sexually active women attending a tertiary center in North Kerala, India. Indian J Sex Transm Dis AIDS. 2023;44(1). doi:10.4103/ijstd.ijstd_65_21
27. Anh DN, Hung DN, Tien TV, et al. Prevalence, species distribution and antifungal susceptibility of Candida albicans causing vaginal discharge among symptomatic non-pregnant women of reproductive age at a tertiary care hospital, Vietnam. BMC Infect Dis. 2021;21(1). doi:10.1186/s12879-021-06192-7
28. Kumar S, Goyal R, Kumar A. Determination of vulvovaginal candidiasis in tertiary care hospital. Asian Journal of Pharmaceutical and Clinical Research. Published online 2022. doi:10.22159/ajpcr.2022.v15i8.44302
29. Waikhom SD, Afeke I, Kwawu GS, 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(1). doi:10.1186/s12884-020-02963-3
30. Aslani N, Kokabi R, Moradi F, Abbasi K, Vaseghi N, Afsarian MH. Characterization of Candida species isolated from vulvovaginal candidiasis by MALDI-TOF with in vitro antifungal susceptibility profiles. Curr Med Mycol. 2021;7(4). doi:10.18502/cmm.7.4.8405