Skip to main content

Advertisement

Log in

Epidemiology and Antifungal Susceptibilities of Yeasts Causing Vulvovaginitis in a Teaching Hospital

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Vulvovaginal candidiasis is one of the most common mycosis. However, the information about antifungal susceptibilities of the yeasts causing this infection is scant. We studied 121 yeasts isolated from 118 patients with vulvovaginal candidiasis. The isolates were identified by phenotypic and molecular methods, including four phenotypic methods described to differentiate Candida albicans from C. dubliniensis. Antifungal susceptibility testing was performed according to CLSI documents M27A3 and M27S4 using the drugs available as treatment option in the hospital. Diabetes, any antibacterial and amoxicillin treatment were statistically linked with vulvovaginal candidiasis, while oral contraceptives were not considered a risk factor. Previous azole-based over-the-counter antifungal treatment was statistically associated with non-C.albicans yeasts infections. The most common isolated yeast species was C. albicans (85.2 %) followed by C. glabrata (5 %), Saccharomyces cerevisiae (3.3 %), and C. dubliniensis (2.5 %). Fluconazole- and itraconazole-reduced susceptibility was observed in ten and in only one C. albicans strains, respectively. All the C. glabrata isolates showed low fluconazole MICs. Clotrimazole showed excellent potency against all but seven isolates (three C. glabrata, two S. cerevisiae, one C. albicans and one Picchia anomala). Any of the strains showed nystatin reduced susceptibility. On the other hand, terbinafine was the less potent drug. Antifungal resistance is still a rare phenomenon supporting the use of azole antifungals as empirical treatment of vulvovaginal candidiasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Sobel JD. Vulvovaginitis. When Candida becomes a problem. Dermatol Clin 1998;16:763–8, xii.

  2. Nyirjesy P, Sobel JD. Vulvovaginal candidiasis. Obstet Gynecol Clin North Am. 2003;30:671–84.

    Article  PubMed  Google Scholar 

  3. Pappas PG, Kauffman CA, Andes D, et al. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis. 2009;48:503–35.

    Article  CAS  PubMed  Google Scholar 

  4. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20:133–63.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Pappas PG, Rex JH, Lee J, et al. A prospective observational study of candidemia: epidemiology, therapy, and influences on mortality in hospitalized adult and pediatric patients. Clin Infect Dis. 2003;37:634–43.

    Article  PubMed  Google Scholar 

  6. Lockhart SR, Messer SA, Gherna M, et al. Identification of Candida nivariensis and Candida bracarensis in a large global collection of Candida glabrata isolates: comparison to the literature. J Clin Microbiol. 2009;47:1216–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Diekema DJ, Messer SA, Boyken LB, et al. In vitro activity of seven systemically active antifungal agents against a large global collection of rare Candida species as determined by CLSI broth microdilution methods. J Clin Microbiol. 2009;47:3170–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Bauters TG, Dhont MA, Temmerman MI, Nelis HJ. Prevalence of vulvovaginal candidiasis and susceptibility to fluconazole in women. Am J Obstet Gynecol. 2002;187:569–74.

    Article  CAS  PubMed  Google Scholar 

  9. Holland J, Young ML, Lee O, Chen A. Vulvovaginal carriage of yeasts other than Candida albicans. Sex Transm Infect. 2003;79:249–50.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Mathema B, Cross E, Dun E, et al. Prevalence of vaginal colonization by drug-resistant Candida species in college-age women with previous exposure to over-the-counter azole antifungals. Clin Infect Dis. 2001;33:E23–7.

    Article  CAS  PubMed  Google Scholar 

  11. Gomez-Lopez A, Alastruey-Izquierdo A, Rodriguez D, et al. Prevalence and susceptibility profile of Candida metapsilosis and Candida orthopsilosis: results from population-based surveillance of candidemia in Spain. Antimicrob Agents Chemother. 2008;52:1506–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Lachance MA, Boekhout T, Scorzetti G, Fell JW, Kurtzman CP. The yeasts a taxonomic study. London. Editorial: Elsevier; 2013.

    Google Scholar 

  13. Staib P, Morschhauser J. Chlamydospore formation in Candida albicans and Candida dubliniensis an enigmatic developmental programme. Mycoses. 2007;50:1–12.

    Article  PubMed  Google Scholar 

  14. Khan ZU, Ahmad S, Mokaddas E, Chandy R. Tobacco agar, a new medium for differentiating Candida dubliniensis from Candida albicans. J Clin Microbiol. 2004;42:4796–8.

    Article  PubMed Central  PubMed  Google Scholar 

  15. Slifkin M. Tween 80 opacity test responses of various Candida species. J Clin Microbiol. 2000;38:4626–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Alves SH, Milan EP, de Laet SP, Oliveira LO, Santurio JM, Colombo AL. Hypertonic sabouraud broth as a simple and powerful test for Candida dubliniensis screening. Diagn Microbiol Infect Dis. 2002;43:85–6.

    Article  CAS  PubMed  Google Scholar 

  17. Donnelly SM, Sullivan DJ, Shanley DB, Coleman DC. Phylogenetic analysis and rapid identification of Candida dubliniensis based on analysis of ACT1 intron and exon sequences. Microbiology. 1999;145(Pt 8):1871–82.

    Article  CAS  PubMed  Google Scholar 

  18. White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego, Calif: Academic press, Inc.; 1990. p. 315–22.

    Chapter  Google Scholar 

  19. Romeo O, Criseo G. First molecular method for discriminating between Candida africana, Candida albicans, and Candida dubliniensis by using HPW1 gene. Diagn Microbiol Infect Dis. 2008;62:230–3.

    Article  CAS  PubMed  Google Scholar 

  20. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press; 1998.

    Google Scholar 

  21. Echeverria-Irigoyen MJ, Eraso E, Cano J, Gomariz M, Guarro J, Quindos G. Saccharomyces cerevisiae vaginitis: microbiology and in vitro antifungal susceptibility. Mycopathologia. 2011;172:201–5.

    Article  CAS  PubMed  Google Scholar 

  22. Haynes KA, Westerneng TJ. Rapid identification of Candida albicans, C. glabrata, C. parapsilosis and C. krusei by species-specific PCR of large subunit ribosomal DNA. J Med Microbiol. 1996;44:390–6.

    Article  CAS  PubMed  Google Scholar 

  23. Li YL, Leaw SN, Chen JH, Chang HC, Chang TC. Rapid identification of yeasts commonly found in positive blood cultures by amplification of the internal transcribed spacer regions 1 and 2. Eur J Clin Microbiol Infect Dis. 2003;22:693–6.

    Article  CAS  PubMed  Google Scholar 

  24. Garcia-Effron G, Canton E, Peman J, Dilger A, Roma E, Perlin DS. Assessment of two new molecular methods for identification of Candida parapsilosis sensu lato species. J Clin Microbiol. 2011;49:3257–61.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Enache-Angoulvant A, Guitard J, Grenouillet F, et al. Rapid discrimination between Candida glabrata, Candida nivariensis, and Candida bracarensis by use of a singleplex PCR. J Clin Microbiol. 2011;49:3375–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts. Third edition. Document M27-A3. 2008.

  27. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeast: fourth informational supplement—CLSI document M27-S4-Wayne, PA. 2012.

  28. Sobel JD, Faro S, Force RW, et al. Vulvovaginal candidiasis: epidemiologic, diagnostic, and therapeutic considerations. Am J Obstet Gynecol. 1998;178:203–11.

    Article  CAS  PubMed  Google Scholar 

  29. Ilkit M, Guzel AB. The epidemiology, pathogenesis, and diagnosis of vulvovaginal candidosis: a mycological perspective. Crit Rev Microbiol. 2011;37:250–61.

    Article  PubMed  Google Scholar 

  30. Xu J, Schwartz K, Bartoces M, Monsur J, Severson RK, Sobel JD. Effect of antibiotics on vulvovaginal candidiasis: a MetroNet study. J Am Board Fam Med. 2008;21:261–8.

    Article  PubMed  Google Scholar 

  31. Sobel JD. Management of recurrent vulvovaginal candidiasis: unresolved issues. Curr Infect Dis Rep. 2006;8:481–6.

    Article  PubMed  Google Scholar 

  32. Blignaut E, Messer S, Hollis RJ, Pfaller MA. Antifungal susceptibility of South African oral yeast isolates from HIV/AIDS patients and healthy individuals. Diagn Microbiol Infect Dis. 2002;44:169–74.

    Article  CAS  PubMed  Google Scholar 

  33. 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;46:1501–3.

    Article  PubMed Central  PubMed  Google Scholar 

  34. Spinillo A, Capuzzo E, Gulminetti R, Marone P, Colonna L, Piazzi G. Prevalence of and risk factors for fungal vaginitis caused by non-albicans species. Am J Obstet Gynecol. 1997;176:138–41.

    Article  CAS  PubMed  Google Scholar 

  35. Saporiti AM, Gomez D, Levalle S, et al. Vaginal candidiasis: etiology and sensitivity profile to antifungal agents in clinical use. Rev Argent Microbiol. 2001;33:217–22.

    CAS  PubMed  Google Scholar 

  36. Richter SS, Galask RP, Messer SA, Hollis RJ, Diekema DJ, Pfaller MA. Antifungal susceptibilities of Candida species causing vulvovaginitis and epidemiology of recurrent cases. J Clin Microbiol. 2005;43:2155–62.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Mujica MT, Finquelievich JL, Jewtuchowicz V, Iovannitti CA. Prevalence of Candida albicans and Candida non-albicans in clinical samples during 1999–2001. Rev Argent Microbiol. 2004;36:107–12.

    CAS  PubMed  Google Scholar 

  38. Giusiano G, Rojas F, Toma-Vanacore S, Mangiaterra M. Frequency and antifungal profile of Candida isolated from vaginal exudates of preadolescent girls. Enferm Infecc Microbiol Clin. 2009;27:428.

    Article  PubMed  Google Scholar 

  39. Garcia HM, Garcia SD, Copolillo EF, et al. Prevalence of vaginal candidiasis in pregnant women. Identification of yeasts and susceptibility to antifungal agents. Rev Argent Microbiol. 2006;38:9–12.

    PubMed  Google Scholar 

  40. Corsello S, Spinillo A, Osnengo G, et al. An epidemiological survey of vulvovaginal candidiasis in Italy. Eur J Obstet Gynecol Reprod Biol. 2003;110:66–72.

    Article  PubMed  Google Scholar 

  41. Buscemi L, Arechavala A, Negroni R. Study of acute vulvovaginitis in sexually active adult women, with special reference to candidosis, in patients of the Francisco J. Muniz Infectious Diseases Hospital. Rev Iberoam Micol. 2004;21:177–81.

    PubMed  Google Scholar 

  42. Arechavala AI, Bianchi MH, Robles AM, Santiso G, Negroni R. Identification and susceptibility against fluconazole and albaconazole of 100 yeasts’ strains isolated from vaginal discharge. Rev Iberoam Micol. 2007;24:305–8.

    Article  PubMed  Google Scholar 

  43. Schaberg DR, Culver DH, Gaynes RP. Major trends in the microbial etiology of nosocomial infection. Am J Med. 1991;91:72S–5S.

    Article  CAS  PubMed  Google Scholar 

  44. Paulitsch A, Weger W, Ginter-Hanselmayer G, Marth E, Buzina W. A 5-year (2000–2004) epidemiological survey of Candida and non-Candida yeast species causing vulvovaginal candidiasis in Graz, Austria. Mycoses. 2006;49:471–5.

    Article  CAS  PubMed  Google Scholar 

  45. Kalkanci A, Guzel AB, Khalil II, Aydin M, Ilkit M, Kustimur S. Yeast vaginitis during pregnancy: susceptibility testing of 13 antifungal drugs and boric acid and the detection of four virulence factors. Med Mycol. 2012;50:585–93.

    Article  CAS  PubMed  Google Scholar 

  46. Borman AM, Szekely A, Linton CJ, Palmer MD, Brown P, Johnson EM. Epidemiology, antifungal susceptibility, and pathogenicity of Candida africana isolates from the United Kingdom. J Clin Microbiol. 2013;51:967–72.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Cross EW, Park S, Perlin DS. Cross-Resistance of clinical isolates of Candida albicans and Candida glabrata to over-the-counter azoles used in the treatment of vaginitis. Microb Drug Resist. 2000;6:155–61.

    Article  CAS  PubMed  Google Scholar 

  48. Ribeiro MA, Dietze R, Paula CR, Da Matta DA, Colombo AL. Susceptibility profile of vaginal yeast isolates from Brazil. Mycopathologia. 2001;151:5–10.

    Article  CAS  PubMed  Google Scholar 

  49. Sobel JD, Wiesenfeld HC, Martens M, et al. Maintenance fluconazole therapy for recurrent vulvovaginal candidiasis. N Engl J Med. 2004;351:876–83.

    Article  CAS  PubMed  Google Scholar 

  50. Guitard J, Angoulvant A, Letscher-Bru V, et al. Invasive infections due to Candida norvegensis and Candida inconspicua: report of 12 cases and review of the literature. Med Mycol. 2013;51(8):795–799.

  51. Arikan S, Ostrosky-Zeichner L, Lozano-Chiu M, et al. In vitro activity of nystatin compared with those of liposomal nystatin, amphotericin B, and fluconazole against clinical Candida isolates. J Clin Microbiol. 2002;40:1406–12.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Carrillo-Munoz AJ, Quindos G, Tur C, et al. In-vitro antifungal activity of liposomal nystatin in comparison with nystatin, amphotericin B cholesteryl sulphate, liposomal amphotericin B, amphotericin B lipid complex, amphotericin B desoxycholate, fluconazole and itraconazole. J Antimicrob Chemother. 1999;44:397–401.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported in part by grants CAI+D prog. RH and PEIS 2011 both from the Universidad Nacional del Litoral to G.G.E. and S.G., respectively. C. Dudiuk has a predoctoral fellowship from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guillermo Garcia-Effron.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gamarra, S., Morano, S., Dudiuk, C. et al. Epidemiology and Antifungal Susceptibilities of Yeasts Causing Vulvovaginitis in a Teaching Hospital. Mycopathologia 178, 251–258 (2014). https://doi.org/10.1007/s11046-014-9780-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-014-9780-2

Keywords

Navigation