Top

Published in:

01-09-2017 | General Gynecology

Emergence of Candida glabrata in vulvovaginal candidiasis should be attributed to selective pressure or virulence ability?

Authors: Sandra Sayuri Nakamura-Vasconcelos, Adriana Fiorini, Pamela Delvas Zanni, Patrícia de Souza Bonfim-Mendonça, Janine Ribeiro Godoy, Adriana Araújo Almeida-Apolonio, Marcia Edilaine Lopes Consolaro, Terezinha Inez Estivalet Svidzinski

Published in: Archives of Gynecology and Obstetrics | Issue 3/2017

Abstract

Purpose

Vulvovaginal candidiasis (VVC) is one of the most frequent female genital disorders and Candida glabrata is the second most common agent. Current study was aimed to study the susceptibility to antifungal agents of C. glabrata isolated from vaginal samples and some virulence attributes in order to better understand why this species is emerging as the main VVC agents.

Methods

A total of 60 C. glabrata vaginal isolates were included in this study. Firstly they were screened by susceptibility tests to antifungal agents. The isolates that showed sensitivity or resistance to fluconazole were evaluated for their virulence potential, including ability to adhere to polystyrene and vaginal ring, cell surface hydrophobicity (CSH) and capacity to form biofilm.

Results

Candida glabrata isolates varied significantly in adherence capacity, biofilm formation and CSH. However, it was possible to observe that isolates resistant to fluconazole adhered more efficiently to the vaginal ring and were statistically more able to form biofilm.

Conclusion

These results allow hypothesizing that C. glabrata is an emergent agent in VVC probably because the treatment with fluconazole selects this species. But once adhered, yeasts remain on biotic or abiotic surfaces causing colonization or VVC symptomatology.

Liu XP, Fan SR, Peng YT, Zhang HP (2014) Species distribution and susceptibility of Candida isolates from patient with vulvovaginal candidiasis in Southern China from 2003 to 2012. J Mycol Med. doi:10.1016/j.mycmed.2014.01.060 PubMed

Kumari F, Banerjee T, Kumar P, Pandey S, Tilak R (2013) Emergence of non-albicans Candida among candidal vulvovaginitis cases and study of their potential virulence factors, from a tertiary care center, North India. Indian J Pathol Microbiol. doi:10.4103/0377-4929.118703 PubMed

Ogouyèmi-Hounto A, Adisso S, Djamal J, Sanni R, Amangbegnon R, Biokou-Bankole B et al (2014) Place of vulvovaginal candidiasis in the lower genital tract infections and associated risk factors among women in Benin. J Mycol Med. doi:10.1016/j.mycmed.2014.01.003 PubMed

Maria C, Zahra R, Sara P (2013) Prevalence of cervical-vaginal infections in the pap-smear samples in Iran. Glob J Health Sci. doi:10.5539/gjhs.v6n1p201 PubMedPubMedCentral

Gunther LSA, Martins HPR, Gimenes F, Abreu ALPD, Consolaro MEL, Svidzinski TIE (2014) Prevalence of Candida albicans and non-albicans isolates from vaginal secretions: comparative evaluation of colonization, vaginal candidiasis and recurrent vaginal candidiasis in diabetic and non-diabetic women. Sao Paulo Med J 132(2):116–120CrossRefPubMed

Babin D, Kotigadde S, Rao PS, Rao TV, Babin MD (2013) Clinico-mycological profile of vaginal candidiasis in a tertiary care hospital in Kerala. Int J Res Biol Sci 3:55–59

Hamad M, Kazandji N, Awadallah S, Allam H (2014) Prevalence and epidemiological characteristics of vaginal candidiasis in the UAE. Mycoses. doi:10.1111/myc.12141 PubMed

Fan SR, Liu XP, Li JW (2008) Clinical characteristics of vulvovaginal candidiasis and antifungal susceptibilities of Candida species isolates among patients in southern China from 2003 to 2006. J Obstet Gynaecol Res. doi:10.1111/j.1447-0756.2008.00817.x PubMed

Martins HPR, Da Silva MC, Paiva LCF, Svidzinski TIE, Consolaro MEL (2012) Efficacy of fluconazole and nystatin in the treatment of vaginal Candida species. Acta Derm Venereol. doi:10.2340/00015555-1194 PubMed

10.

Kennedy MA, Sobel JD (2010) Vulvovaginal candidiasis caused by non-albicans Candida species: new insights. Curr Infect Dis Rep. doi:10.1007/s11908-010-0137-9 PubMed

11.

Ragunathan L, Poongothai GK, Sinazer AR, Kannaiyan K, Gurumurthy H, Jaget N et al (2014) Phenotypic characterization and antifungal susceptibility pattern to fluconazole in Candida species isolated from vulvovaginal candidiasis in a tertiary care hospital. J Clin Diagn Res 8(5):DC01–DC04. doi:10.7860/JCDR/2014/7434.4311 PubMedPubMedCentral

12.

Alfouzan W, Dhar R, Ashkanani H, Gupta M, Rachel C, Khan ZU (2015) Species spectrum and antifungal susceptibility profile of vaginal isolates of Candida in Kuwait. J Mycol Med 25(1):23–28. doi:10.1016/j.mycmed.2014.10.021 CrossRefPubMed

13.

Payne MS, Cullinane M, Garland SM, Tabrizi SN, Donath SM, Bennett CM et al (2015) Detection of Candida spp. in the vagina of a cohort of nulliparous pregnant women by culture and molecular methods: is there an association between maternal vaginal and infant oral colonisation? Aust N Z J Obstet Gynaecol 56(2):179–184. doi:10.1111/ajo.12409 (Epub 2015 Oct 5) CrossRefPubMed

14.

Wang FJ, Zhang D, Liu ZH, Wu WX, Bai HH, Dong HY (2016) Species distribution and in vitro antifungal susceptibility of vulvovaginal Candida isolates in China. Chin Med J (Engl) 129(10):1161–1165. doi:10.4103/0366-6999.181964 CrossRef

15.

Alczuk SDSD, Bonfim-Mendonca PS, Rocha-Brischiliari SC, Shinobu-Mesquita CS, Martins HPR, Gimenes F et al (2015) Effect of highly active antiretroviral therapy on vaginal Candida spp. isolation in HIV-infected compared to HIV-uninfected women. Rev Inst Med Trop Sao Paulo 57(2):169–174. doi:10.1590/S0036-46652015000200012 CrossRefPubMedCentral

16.

Consolaro MEL, Albertoni TA, Yoshida CS, Mazucheli J, Peralta RM, Svidzinski TIE (2004) Correlation of Candida species and symptoms among patients with vulvovaginal candidiasis in Maringá, Paraná, Brazil. Rev Iberoam Micol 21:202–205

17.

Irie MMT, Consolaro MEL, Guedes TE, Donatti L, Patussi VE, Svidzinski TIE (2006) A simplified technique for evaluating the adherence of yeasts to human vaginal epithelial cells. J Clin Lab Anal 20:195–203CrossRef

18.

Camacho DP, Consolaro MEL, Patussi EV, Donatti L, Gasparetto A, Svidzinski TIE (2007) Vaginal yeast adherence to the combined contraceptive vaginal ring (CCVR). Contraception 76:439–443CrossRefPubMed

19.

Paiva LCF, Donatti L, Patussi EV, Svizdinski TIE, Consolaro MEL (2010) Scanning electron and confocal scanning laser microscopy imaging of the ultrastructure and viability of vaginal Candida albicans and non-albicans species adhered to an intrauterine contraceptive device. Microsc Microanal. doi:10.1017/S1431927610093773 PubMed

20.

Bonfim-Mendonça PS, Ratti BA, Godoy JSR, Negri M, Lima NCA, Fiorini A et al (2014) β-Glucan induces reactive oxygen species production in human neutrophils to improve the killing of Candida albicans and Candida glabrata isolates from vulvovaginal candidiasis. PLoS One. doi:10.1371/journal.pone.0107805 PubMedCentral

21.

Institute CaLS (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts M27-A3, 3rd edn. Clinical and Laboratory Standards Institute, Wayne

22.

European Committee on Antimicrobial Susceptibility (2010) T. EUCAST clinical breakpoints, Verfügbar unter. http://www.eucast.org/clinical_breakpoints. Accessed 18 Oct 2012

23.

Raut J, Rathod V, Karuppayil SM (2010) Cell surface hydrophobicity and adhesion: a study on fifty clinical isolates of Candida albicans. Nihon Ishinkin Gakkai Zasshi 51:131–136CrossRefPubMed

24.

Negri M, Gonçalves VM, Silva SC, Henriques M, Azeredo J, Oliveira R (2010) Crystal violet staining to quantity Candida adhesion to epithelial cells. Br J Biomed Sci. doi:10.1080/09674845.2010.11730308 PubMed

25.

Santander MP (2016) Identificación y sensibilidad antifúngica in vitro de Candida spp. de origen vaginal a fluconazol, clotrimazol y nistatina. Quimioterapia 29:151–154

26.

Santos ER, Forno CFD, Hernandez MG, Kubiça TF, Venturini TP, Chassot F et al (2014) Susceptibility of Candida spp. isolated from blood cultures as evaluated using the M27-A3 and new M27-S4 approved breakpoints. Rev Inst Med Trop São Paulo 56:477–482CrossRefPubMedPubMedCentral

27.

Goswami D, Goswami R, Banerjee U, Dadhwal V, Miglani S, Lattif AA et al (2006) Pattern of Candida species isolated from patients with diabetes mellitus and vulvovaginal candidiasis and their response to single dose oral fluconazole therapy. J Infect 52:111–117CrossRefPubMed

28.

Dalben-Dota KF, Faria MGI, Bruschi ML, Pelloso SM, Consolaro MEL, Svidzinski TIE (2010) Antifungal activity of propolis extract against yeasts isolated from vaginal exudates. J Altern Complement Med. doi:10.1089/acm.2009.0281 PubMed

29.

Gonçalves B, Ferreira C, Alves CT, Henriques M, Azeredo J, Silva S (2016) Vulvovaginal candidiasis: epidemiology, microbiology and risk factors. Crit Rev Microbiol. doi:10.3109/1040841X.2015.1091805 PubMed

30.

Gómez-Molero E, Boer AD, Dekker HL, Moreno-Martínez A, Kraneveld EA, Chauhan N et al (2015) Proteomic analysis of hyperadhesive Candida glabrata clinical isolates reveals a core wall proteome and differential incorporation of adhesins. FEMS Yeast Res. doi:10.1093/femsyr/fov098 PubMed

31.

Doyle RJ (2000) Contribution of the hydrophobic effect to microbial infection. Microbes Infect 4:391–400CrossRef

32.

Camacho DP, Gasparetto A, Svidzinski TIE (2007) The effect of chlorhexidine and gentian violet on the adherence of Candida spp. to urinary catheters. Mycopathologia 163:261–266CrossRefPubMed

33.

Paiva LCF, Vidigal PG, Donatti L, Svidzinski TIE, Consolaro MEL (2012) Assessment of in vitro biofilm formation by Candida species isolates from vulvovaginal candidiasis and ultrastructural characteristics. Micron. doi:10.1016/j.micron.2011.09.013 PubMed

34.

Vitali A, Vavala E, Marzano V, Leone C, Castagnola M, Lavarone F et al (2016) Cell wall composition and biofilm formation of azoles-susceptible and-resistant Candida glabrata strains. J Chemother. doi:10.1080/1120009X.2016.1199507 PubMed

35.

Samaranayake LP, Fidel PL, Sweet SP, Teanpaisan R, Coogan MM, Blignaut E et al (2002) Fungal infections associated with HIV infection. Oral Dis 8:151–160CrossRefPubMed

36.

El-Kirat-Chatel S, Beaussart A, Derclaye S, Alsteens D, Kucharikova S, Dijck PV et al (2015) Force nanoscopy of hydrophobic interactions in the fungal pathogen Candida glabrata. ACS Nano. doi:10.1021/nn506370f PubMed

37.

Seneviratne CJ, Jin LJ, Samaranayake YH, Samaranayake LP (2008) Cell density and cell aging as factors modulating antifungal resistance of Candida albicans biofilms. Antimicrob Agents Chemother. doi:10.1128/AAC.00541-08 PubMedPubMedCentral

38.

Rodrigues CF, Silva S, Henriques M (2013) Candida glabrata: a review of its features and resistance. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-013-2009-3 PubMed

Title: Emergence of Candida glabrata in vulvovaginal candidiasis should be attributed to selective pressure or virulence ability?
Authors: Sandra Sayuri Nakamura-Vasconcelos
Adriana Fiorini
Pamela Delvas Zanni
Patrícia de Souza Bonfim-Mendonça
Janine Ribeiro Godoy
Adriana Araújo Almeida-Apolonio
Marcia Edilaine Lopes Consolaro
Terezinha Inez Estivalet Svidzinski
Publication date: 01-09-2017
Publisher: Springer Berlin Heidelberg
Published in: Archives of Gynecology and Obstetrics / Issue 3/2017
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI: https://doi.org/10.1007/s00404-017-4465-y

At a glance: The STEP trials

Springer Medicine

Emergence of Candida glabrata in vulvovaginal candidiasis should be attributed to selective pressure or virulence ability?

Abstract

Purpose

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 3/2017

“Per vaginam” topical use of hormonal drugs in women with symptomatic deep endometriosis: a narrative literature review

Hysterectomy technique and risk of pelvic organ prolapse repair: a Danish nationwide cohort study

Application of testosterone supplementation in semen to improve sperm motility in asthenozoospermic males

Is there any relationship between adipocytokines and angiogenesis factors to address endothelial dysfunction and platelet aggregation in untreated patients with preeclampsia?

Prophylactic use of Bakri balloon for reduction of hemorrhage at cesarean for placenta previa: addition and clarification

Polycystic ovary syndrome, adipose tissue and metabolic syndrome