VULVOVAGINAL CANDIDIASIS (VVC) is common, affecting up to 75% of women in their lifetime.1,2 VVC may be asymptomatic3 but can cause significant morbidity including vaginal discharge, itching, vulvovaginal soreness, dysuria, and dyspareunia.2,4,5 Up to 50% of women suffer recurrent episodes.2 VVC is associated with multiple precipitating factors including diabetes mellitus, pregnancy, and immune deficiency syndromes.2,6 Other suggested precipitating factors include high dose oral combined oral contraceptives, spermicides, and nonsexual factors such as consumption of cranberry juice, douching, and wearing panty-liners or pantyhose.2,5,7–9 Studies show VVC to be more common in black women.8,10
There is debate about the role of sexual transmission in the etiology of VVC.1,2 VVC is associated with onset of sexual activity, the frequency of vaginal sex,7,11 receptive orogenital sex,7,8,11 and numbers of heterosexual partners.12 Genetic fingerprinting has identified congruent strains of Candida albicans in male partners of symptomatic women,13 suggesting that it can be heterosexually transmitted.
There is evidence that agents such as genital herpes, trichomoniasis, syphilis, and human papillomavirus can be transmitted sexually between women.14–20 There is also debate about whether bacterial vaginosis (BV) is sexually transmissible between women.21–23 VVC is commonly diagnosed in women who have sex with women in clinic settings,24,25 but it is not known whether VVC can be sexually transmitted between women. In this study, we explore risk factors for VVC in women who have sex with women.
Materials and Methods
A questionnaire was offered to new patients at 2 sexual health clinics for lesbians and bisexual women in London, UK.14 Eight hundred three women completed the questionnaire out of an estimated 1000 attenders. The questionnaire was self-completed before consultation with clinic staff, and gathered data about demographic variables, partner history (lifetime and past year), and sexual practice. Seven hundred eight women (88%) had a full genitourinary screen.
Examination and testing comprised Gram-stained high vaginal preparations and culture for identification of candida species (albicans and nonalbicans).26 Cervical and urethral Gram-stained smear and cultures were taken for Neisseria gonorrhoeae, cervical swab for Chlamydia trachomatis by ELISA, and high vaginal samples for Trichomonas vaginalis by wet preparation. BV was diagnosed using Amsel criteria. Screening for treponemal disease used the Venereal Disease Research Laboratory test and the Treponema pallidum hemagglutination assay. Herpes simplex cultures were performed as clinically indicated and genital warts were diagnosed by visual inspection. Pelvic inflammatory disease was diagnosed on clinical examination with a raised white cell count.
The mechanism by which candida becomes symptomatic is not well understood,13 so we have combined symptomatic and asymptomatic women for analysis. Univariate analysis explored the associations of candidiasis on Gram stain and/or culture with sexual history, sexual practice, and demographic variables. We used Mantel Haenzel Odds Ratios, with Mantel Haenzel Score tests for trend with ordered categorical variables, Pearson χ2 tests for nominal variables, and Fisher exact χ2 tests where numbers in any one category were fewer than 5 subjects. Most variables were examined as categorical variables. Variables reaching statistical significance at the level of P <0.1 were included in a multivariate model. A logistic regression model was built up in a stepwise fashion by using the Likelihood Ratio test and by observing change in odds ratios.
The demographic features of the 708 women who had a full genitourinary examination are shown in Table 1. Most identified as lesbian rather than bisexual, most came from London (where the clinics were situated) and most fell into the category of white British/Irish/European.
One hundred thirty women were diagnosed with VVC on Gram stain and/or high vaginal culture, giving a prevalence of 18.4% (CI 15.5%–21.2%) in this clinic population. This includes both symptomatic and asymptomatic women. Fifteen women with VVC were coinfected with BV (11.5%). One woman was coinfected with trichomoniasis (0.8%) and 1 with gonorrhea (0.8%).
Numbers of female partners in the last year, vaginal penetration with fingers, sexual identity, age, employment status, and history of pregnancy were associated with a diagnosis of VVC at a level of P <0.1 in univariate analysis (see Table 2). No associations were found with demographic variables, sexual history with men, vaginal douching, lubricant use, or other sexual practices between women including orogenital sex or the use of sex toys. There was a trend toward increased VVC in younger age groups; numbers of female partners in the last year was correlated with age.
Number of female sexual partners in the last year, age, sexual identity, employment status, history of pregnancy, and vaginal penetration with fingers were included in the multivariate model. All of these variables except numbers of female sexual partners in the last year became nonsignificant in the multivariate model. Vaginal penetration with fingers was retained in the final model, because this variable modified the odds ratio for numbers of female sexual partners. Multivariate analysis using logistic regression showed an independent association of VVC with 2 or more female sexual partners within the last year (see Table 3).
This study seems to be the first to suggest a link between sexual activity between women and symptomatic or asymptomatic VVC. The sexual transmission of candida species between women is biologically plausible: Candida may be present in reservoirs in the vagina, mouth, and rectum27 and sexual practice between women includes activities such as orogenital contact and the sharing of sex toys that may facilitate cross-infection.28,29 Having greater numbers of female sexual partners is likely to increase exposure to candida, whether this is symptomatic or asymptomatic in partners. Other studies have found associations of sexually transmitted infections with numbers of female sexual partners: Both herpes simplex Type 1 seroprevalence and BV are associated with numbers of female sexual partners.20–22,30 One study describes associations of BV with specific sexual practices between women (the sharing of sex toys and oroanal contact).22
Sexual health surveys are vulnerable to inaccuracies such as recall bias and social desirability bias.31 However, this study is strengthened by its use of laboratory data rather than self-reported diagnoses.1 Associations with specific sexual practices were difficult to explore because data on the time elapsed from each specific sexual behavior were not available, “occasionally” and “often” are imprecise terms, and some sexual activities were almost universally reported (see Table 2). We found no trend with greater numbers of female partners: measuring cumulative incidence of candidiasis over the last year rather than point prevalence would have been a more accurate outcome, but self-reporting is unreliable,2 and longitudinal data collection was not possible in this cross-sectional survey. Data for numbers of female partners over the past year were highly skewed, with most respondents reporting 1 female partner.
We have accounted for a wide range of sociodemographic and behavioral confounders in the multivariate model, but there may be other confounding factors such as frequency of sex, taking antibiotics, or having diabetes. This article suggests a novel hypothesis: partner studies, robust epidemiologic studies, and qualitative investigation of sexual behavior would help to clarify the etiology of candidiasis in women who have sex with women.
This study of lesbians and bisexual women shows that VVC is associated with greater numbers of female sexual partners in the last year. This finding raises the possibility that candida species could be sexually transmitted between women.
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