Abstract
Candida yeasts are the most frequent in the vaginal content. This yeast may be a normal microbiota but also causes candidiasis. In symptomatic cases, primary candidiasis (VVC) or recurrence (RVVC) can be considered. This study aims to compare the frequency and in vitro sensitivity profile of Candida species isolated in the vaginal content with the different stages of the presence of yeasts. A total of 258 non-pregnant patients with/without VVC were prospectively screened at a teaching Health Centre of the Faculty of Medicine, in the University of Sao Paulo. The vaginal isolates were identified by traditional and molecular methods. Yeasts were isolated in 160 women. 34% were asymptomatic, 34% with vulvovaginal candidiasis (VVC), and 32% recurrent vulvovaginal candidiasis (RVVC). C. albicans was the most frequent species with 50.1% (82/160), followed by C. parapsilosis 13.7%(22/160), C. glabrata 12.5% (20/160), and C. tropicalis (6.2%). Analysis by the group showed that, in the asymptomatic group, eight yeast species were isolated, C. albicans 44.5% (24/54), C. glabrata 20% (11/54), C. parapsilosis and Rhodotorula rubra being the most frequent. In the VVC group, 11 yeast species were identified. Most isolates were C. albicans 68.5% (37/54), C. tropicalis 7.5% (4/54), and C. parapsilosis 5.5% (3/54). In the RVVC group, ten species were identified, the most frequent being C. albicans 38.5% (20/52), C. parapsilosis 17% (9/52), C. glabrata 4% (8/52), and C. tropicalis 6% (3/52). Less frequent species, such as C. haemulonii and Trichosporon spp, were isolated in the VVC and RVVC groups, C. kefyr was isolated in the three groups studied, and Rhodotorula spp was isolated in the control and RVVC groups. Candida metapsilosis was present in two isolates from the RVVC group. Most isolates were considered sensitive to the tested antifungals. Less sensitivity was seen for caspofungin. In this study, we were able to verify that the most common species of yeasts found in vaginal secretion were isolated in the three groups studied; however, there was the diversity of species in VVC and RVVC. Cryptic species C. haemulonii and were isolated in symptomatic patients. High levels of MICs, some of the antifungals tested, in the control group, draw attention in the group of asymptomatic women. We would like to emphasize that this research aims to assist clinicians and gynecologists, as well as assist in the epidemiological studies of candidiasis, in our country, how to draw attention to the profile of sensitivity/resistance to antifungals.
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References
Pappas PG, Kauffman CA, Andes DR, Clancy CJ, Marr KA, Ostrosky-Zeichner L, Reboli AC, Schuster MG, Vazquez JA, Walsh TJ, Zaoutis TE, Sobel JD. Clinical practice guideline for the management of candidiasis: 2016 update by the infectious diseases society of America. Clin Infect Dis. 2016;62(4):e1-50.
Beigi RH, Meyn LA, Moore DM, Krohn MA, Hillier SL. Vaginal yeast colonization in non-pregnant women: a longitudinal study. Obstet Gynecol. 2004;104:926–30.
Guzel AB, Ilkit M, Burgut R, Urunsak IF, Ozgunen FT. An evaluation of risk factors in pregnant women with Candida vaginitis and the diagnostic value of simultaneous vaginal and rectal sampling. Mycopathologia. 2011;172(1):25–36.
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):905–27.
Fan SR, Liao QP, Liu XP, Liu ZH, Zang D. Vaginal allergic response in women with vulvovaginal candidiasis. Int J Gynecol Obstet. 2008;101(1):27–30.
Achkar JM, Fries BC. Candida infections of the genitourinary tract. Clin Microbiol Rev. 2010;23(2):253–73.
Blostein F, Levin-Sparenberg E, Wagner J, Foxman B. Recurrent vulvovaginal candidiasis. Ann Epidemiol. 2017;27(9):575–82.
Pirotta MV, Suzanne MG. Genital Candida species detected in samples from women in Melbourne, Australia, before and after treatment with antibiotics. J Clin Microbiol. 2006;44(9):3213–7.
Fontecha G, Montes K, Ortiz B, Galindo C, Braham S. Identification of cryptic species of four Candida complexes in a culture collection. J Fungi (Basel). 2019;5(4):117.
Dannaoui E, Espinel-Ingroff A. Antifungal susceptibly testing by concentration gradient strip etest method for fungal isolates: a review. J Fungi. 2019;5:108.
Kurtzman CP, Fell JW, Boekhout T. The yeasts, a taxonomic study, 5th. Burllington: Elsevier; 2011. p. 2354.
Mannarelli BM, Kurtzman CP. Rapid identification of Candida albicans and other human pathogenic yeasts by using short oligonucleotides in a PCR. J Clin Microbiol. 1998;36:1634–41.
Van Den Ende AHGG, de Hoog GS. Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana. Stud Mycol. 1999;43:151–216.
Merseguel KB, Nishikaku AS, Rodrigues AM, Padovan AC, Ferreira RC, Azevedo Melo AS, Briones MR, Colombo AL. Genetic diversity of medically important and emerging Candida species causing invasive infection. BMC Infect Dis. 2015;13:15–57.
White TJ, Bruns S, Lee S, Taylor J. 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 applications. New York: Academic Press Inc; 1990. p. 315–22.
Clinical Laboratory Standards Institute. Performance Standards for Antifungal Susceptibility Testing of Yeasts. Wayne, PA: CLSI; 2017 [1st Edition, M60].
Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts. Wayne, PA: CLSI; 2002 [Approved Standard, Second edition, M27-A2].
Yano J, Sobel JD, Nyirjesv P, Sobel R, Williams VL, Yu Q, Noverr MC, Fidel PL Jr. Current patient perspectives of vulvovaginal candidiasis: incidence, symptoms, management and post-treatment outcomes. BMC Womens Health. 2019;19(1):48.
Kantarcioglu AS, Ÿucel A. Phospholipase and protease activities in clinical Candida isolates with reference to the sources of strains. Mycoses. 2002;45:160–5.
Landers DV, Wiesenfeld HC, Heine RP, Krohn MA, Hillier SL. Predictive value of the clinical diagnosis of lower genital tract infection in women. Am J Obst Gynecol. 2004;190:1004–10.
Moreira D, Paula CR. Vulvovaginal candidiasis. Int J Gynec Obst. 2006;92:266–7.
Amouri I, Sellami H, Borji N, Abbes S, Sellami A, Cheikhrouhou F, Maazoun L, Khaled S, Khrouf S, Boujelben Y, Ayadi A. Epidemiological survey of vulvovaginal candidosis in Sfax. Tunisia Mycoses. 2011;54(5):e499-505.
Chatzivasileiou P, Vyzantiadi TA. Vaginal yeast colonisation: from a potential harmless condition to clinical implications and management approaches—a literature review. Mycoses. 2019;62(8):638–50.
Denning DW, Kneale M, Sobel JD, Rautemaa-Richardson R. Global burden of recurrent vulvovaginal candidiasis: a systematic review. Lancet Infect Dis. 2018;18(11):e339–47.
Cassone A. Vulvovaginal Candida albicans infections: pathogenesis, immunity and vaccine prospects. BJOG Int J Obst Gynaecol. 2015;122(6):785–94.
Hashemi SE, et al. Species distribution and susceptibility profiles of Candida species isolated from vulvovaginal candidiasis, emergence of C. lusitaniae. Curr Med Mycol. 2019;5(4):26.
Holland J, Young ML, Lee O, Chen SCA. Vulvovaginal carriage of yeasts others than Candida albicans. Sex Transm Infect. 2003;79:249–50.
Lockhart SR, Messer SA, Pfaller MA, Diekema DJ. Geographic distribution and antifungal susceptibility of the newly described species Candida orthopsilosis and Candida metapsilosis in comparison to the closely related species Candida parapsilosis. J Clin Microb. 2008;46:2659–64.
Tavanti A, Davidson AD, Gow NAR, Maiden MCJ, Odds FC. Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis Groups II and III. J Clin Microbiol. 2005;43(1):284–292.
Arastehfar A, Khodavaisy S, Daneshnia F, Najafzadeh MJ, Mahmoudi S, Charsizadeh A, Salehi MR, Zarrinfar H, Raeisabadi A, Dolatabadi S, Zare Shahrabadi Z, Zomorodian K, Pan W, Hagen F, Boekhout T. Molecular identification, genotypic diversity, antifungal susceptibility, and clinical outcomes of infections caused by clinically underrated yeasts, Candida orthopsilosis, and Candida metapsilosis: an Iranian multicenter study (2014–2019). Front Cell Infect Microbiol. 2019;30:264.
Zhu Y, Shan Y, Fan S, Li J, Liu X. Candida parapsilosis sensu stricto and the closely related species Candida orthopsilosis and Candida metapsilosis in Vulvovaginal Candidiasis. Mycopathologia. 2015;179(1–2):111–8.
Kasper, L, Katja S, Bernhard H. Intracellular survival of Candida glabrata in macrophages: immune evasion and persistence. FEMS Yeast Res. 2015;15(5): fov042.
de Almeida JN, et al. Candida haemulonii complex species, Brazil, January 2010–March 2015. Emerg Infect Dis. 2016;22(3):561.
Fontecha G, et al. Identification of cryptic species of four Candida complexes in a culture collection. J Fungi. 2019;5(4):117.
Boatto HF, Cavalcanti SDB, Del Negro GMB, Girão MJBC, Francisco EC, Ishida K, Gompertz OF. Candida duobushaemulonii: an emerging rare pathogenic yeast isolated from recurrent vulvovaginal candidiasis in Brazil. Mem Inst Oswaldo Cruz. 2016;111:407–10.
Muñoz JF, Gade L, Chow NA, Loparev VN, Juieng P, Berkow EL, Farrer RA, Litvinteseva AP, Cuom CA. Genomic insights into multidrug-resistance, mating and virulence in Candida auris and related emerging species. Nat Commun. 2018;9(1):5346.
Kathuria S, et al. Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization–time of flight mass spectrometry and DNA sequencing and its antifungal susceptibility profile variability by Vitek 2, CLSI broth microdilution, and Etest method. J Clin Microbiol. 2015;53(6):1823–30.
Mendling W, Brasch J. 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. 2012;55(1–13):42.
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Acknowledgments by the authors to the São Paulo State Research Support Foundation—FAPESP: 2008/58830-0 and Coordination for the Improvement of Higher Education Personnel, for a doctoral scholarship.
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Moreira, D., Ruiz, L.S., Leite-Jr, D.P. et al. Difference Between the Profiles Presented by Yeasts that Colonize the Vaginal Mucosa or Cause Primary or Recurrent Candidiasis. Mycopathologia 186, 411–421 (2021). https://doi.org/10.1007/s11046-021-00556-y
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DOI: https://doi.org/10.1007/s11046-021-00556-y