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ORIGINAL RESEARCH |
From the Centers for Disease Control and Prevention, Atlanta, Georgia; National Institute for Child Health and Human Development, Bethesda, Maryland; Brown University, Providence, Rhode Island; Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, New York; Johns Hopkins University, Baltimore, Maryland; and Wayne State University, Detroit, Michigan.
Address reprint requests to: Ann Duerr, MD, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Division of Reproductive Health, HIV Section, Mailstop K-34, 4770 Buford Highway NE, Atlanta, GA 30341-3717; E-mail: aduerr{at}cdc.gov.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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METHODS: Data were from 856 HIV-infected women and 421 at-risk uninfected women observed semiannually at four study sites from April 1993 through February 1999. At enrollment women were 15–55 years old and had no acquired immunodeficiency syndrome–defining conditions. Three definitions for vulvovaginal candidiasis of differing severity were constructed using data from vaginal Candida culture and Gram stains scored for yeast and three signs on pelvic examination (vulvovaginal edema, erythema, or discharge): 1) culture or Gram stain positivity plus at least one clinical sign, 2) culture or Gram stain positivity plus at least two clinical signs, and 3) visible yeast on Gram stain plus at least one clinical sign.
RESULTS: The prevalence and cumulative incidence of each definition of vulvovaginal candidiasis were greater among HIV-infected women than among women not infected with HIV (P < .01 for all comparisons). Stratified by status at the preceding visit, vulvovaginal candidiasis was most likely among women with prior vulvovaginal candidiasis, least likely among women without earlier Candida colonization, and intermediately likely among women with preceding subclinical Candida colonization. Among HIV-infected women, lower CD4 count and higher HIV viral load were associated with vulvovaginal candidiasis. Several other factors were independently associated with vulvovaginal candidiasis, with strong associations for diabetes mellitus and pregnancy in particular. Vulvovaginal candidiasis was not more severe among HIV-infected women.
CONCLUSION: Vulvovaginal candidiasis occurred with higher incidence and greater persistence, but not greater severity, among HIV-infected women.
Both vaginal colonization by Candida species and vulvovaginitis associated with Candida occur more frequently among human immunodeficiency virus (HIV)–infected women, especially those with moderate to severe immune compromise.1–7 The Centers for Disease Control and Prevention (CDC) included vulvovaginal candidiasis among category B conditions, those for which clinical course or management is complicated by HIV infection.8 The CDC revised classification system indicates that vulvovaginal candidiasis associated with HIV is especially persistent, frequent, or poorly responsive to therapy. Similarly, the World Health Organization classifies vulvovaginal candidiasis that is chronic or poorly responsive to therapy as being associated with intermediate (moderate) HIV disease.9
Most studies of vulvovaginal candidiasis and HIV to date have been cross-sectional,1–5,7 have enrolled relatively few HIV-infected women, lacked appropriate matched controls, or have been restricted to specialized subpopulations such as women who are pregnant1 or have symptoms of vulvovaginitis.6 To redress this deficiency, we have used data from a large prospective study of women with or at risk for HIV infection to investigate the relative occurrence of vulvovaginal candidiasis in HIV-infected versus uninfected women. We also examined whether the vaginal yeast infections that occur among these two groups of women differ qualitatively.
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MATERIALS AND METHODS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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We constructed three definitions of vulvovaginal candidiasis using the following data: 1) the presence of yeast in the vagina as measured by vaginal culture for Candida and a Gram stain of vaginal flora and 2) data on the presence of three signs on examination noted by a study clinician: vulvovaginal edema, erythema, or abnormal discharge. The three definitions were as follows: 1) vulvovaginal candidiasis 1, yeast on culture and/or Gram stain plus at least one sign; 2) vulvovaginal candidiasis 2, yeast on culture and/or Gram stain plus two or more signs; and 3) vulvovaginal candidiasis 3, budding yeast or hyphae on Gram stain plus at least one sign. At any given visit, a woman could meet one or more definitions of vulvovaginal candidiasis. These definitions represent vulvovaginal candidiasis of differing severity. Women with vulvovaginal candidiasis 2 are required to have more signs than those meeting only the definition of vulvovaginal candidiasis 1. As a group, women with vulvovaginal candidiasis 3 likely have a higher quantity of yeast present (as evidenced by the ability to detect yeast on Gram stain) than women meeting only the definition of vulvovaginal candidiasis 1 or vulvovaginal candidiasis 2 because not all of the latter necessarily have yeast detected on Gram stain.
Because signs attributed to vulvovaginal candidiasis could be due to other conditions, we evaluated the role of three coexisting genital tract conditions in our risk models: bacterial vaginosis, trichomoniasis, and genital ulcers. Bacterial vaginosis was identified through Gram stains of vaginal specimens using a scoring system based on the relative frequencies of Lactobacillus sp, Gardnerella vaginalis, Bacteroides sp, and Mobiluncus sp morphotypes.11 Trichomoniasis was initially defined as the presence of trichomonads by wet mount (visits one to three); culture (in modified Diamond medium) was introduced for all women at visit four. Vulvar, vaginal, and cervical ulcers were visually identified by a study clinician on examination. Evaluations for gonorrhea and chlamydia were discontinued after visit five because of their very low occurrence, and these conditions were excluded from the analysis. Women with symptomatic vaginal or cervical infections at the time of the study visit were either treated or referred for treatment.
Human immunodeficiency virus status was ascertained through enzyme-linked immunosorbent assay and Western blot. We used three CD4 + T lymphocyte groups to categorize the level of immune system compromise: less than 200 cells per microliter, severe; 200–499, moderate; and 500 or more, least immunocompromised. When testing followed phlebotomy by more than 2 days, groups were determined by CD4 percentage instead of count, with cut points of 14% and 29%.8 Human immunodeficiency virus load was determined via a third-generation, branched deoxyribonucleic acid signal amplification assay (Chiron Corp., Emeryville, CA) with a lower quantification limit of 50 copies per milliliter. Mindful of the possible links between medical therapy and vulvovaginal candidiasis, we classified systemic and vaginal drugs using a published drug index12 with a view to possible class-level associations with vulvovaginal candidiasis. We focused on three classes of drugs: antiretrovirals, systemic antifungals, and systemic antibacterials. Antiretroviral regimens were classified as highly active antiretroviral combination therapy, other antiretroviral therapy, or no antiretrovirals; highly active antiretroviral combination therapy comprised regimens of multiple drugs with clinical evidence of effective and sustained viral suppression. Regimen classifications were adapted from US Department of Health and Human Services guidelines for preferred or alternative combinations,13 with unclassed regimens included if they were believed to have a high likelihood of exhibiting the same properties. Antiretroviral regimens not considered as highly effective (usually one- or two-drug regimens) were classified as antiretroviral therapy. Systemic antifungals included fluconazole, ketoconazole, and itraconazole. Insofar as our sample included women with Candida infection at other mucosal sites, systemic antifungals may not have been taken to treat vaginal Candida infection. We also included data on use of topical antifungals, as reported by the woman. Systemic antibacterials (eg, amoxicillin) included broad-spectrum antibacterials plus some narrow-spectrum antimicrobials with activity against common genital tract infections but excluded most antiparasitics and antimycobacterials. In addition to these drug classes, we considered antimycobacterials (eg, isoniazid), antiprotozoals (eg, atovaquone), and antivirals (eg, acyclovir). Additionally, we used data on diabetes therapies to identify women with that disease.
Pregnancy was ascertained through a urine test administered at the study site. Menses was considered recent if the last reported date was within 14 days of the gynecologic examination. Other factors considered included number of vaginal yeast infections in the previous 6 months (self-report); presence of a cervix; delivery in the past 8 weeks; number of pregnancies and live births; douching in the past 48 hours; and use of hormonal contraceptives, spermicides, diaphragms, or intrauterine devices.
We also accounted for potential links between vulvovaginal candidiasis prevalence and several sexual and drug-related factors, including trading sex for drugs or money; number of male partners; frequency of vaginal sex; consistency of condom use in vaginal sex; detection of sperm on Gram stain; number of female sex partners; frequency of sex with women; and use of tobacco, crack, and intravenous drugs.
Cumulative incidence of vulvovaginal candidiasis was estimated over the course of this study using the Kaplan-Meier product-limit survival estimator.14 Logistic models provided estimates of overall prevalence via methods that compensated for within-subject correlation across multiple observations.15 These prevalence estimates and odds ratios (ORs) averaged the characteristics of study participants over the course of the study. Inferences were based on standard errors estimated by robust methods using an m-dependent working correlation structure, which assumes that the correlation depends only on how far apart two visits were in time.15 Computations were performed in SAS 7 (SAS Institute Inc., Cary, NC).
Under the HER Study design, we were able to ascertain vulvovaginal candidiasis status every 6 months. For each pair of visits separated by 6 months, vulvovaginal candidiasis at the second visit was designated as persistence if it was preceded by vulvovaginal candidiasis, escalation if preceded by subclinical colonization, and acquisition if preceded by noncolonization. We estimated the association of vulvovaginal candidiasis at the current visit with vulvovaginal candidiasis status at the preceding visit by including previous vulvovaginal candidiasis status as an additional predictor in the multivariable model.
We evaluated each of the candidate predictors for vulvovaginal candidiasis individually. These initial models adjusted only for HIV status, study site, risk cohort (injection drug use, heterosexual sex), and visit number. Predictors were retained as candidates for subsequent multivariable models if they demonstrated at least a moderate association with vulvovaginal candidiasis (P < .2).
Multivariable models were then built using variables identified in this process plus several preselected variables thought to be related to clinical course and management of vulvovaginal candidiasis. Seven preselected predictors—use of antibacterial drugs, pregnancy, diabetes, self-reported vaginal yeast infections, bacterial vaginosis, trichomoniasis, and genital ulcers—were thus included in the final model by design. Additional predictors were retained if they demonstrated statistical evidence of an association with vulvovaginal candidiasis. After selection of a multivariable model we checked for effect modification of HIV status on the other predictors. Then, we explored associations of vulvovaginal candidiasis with risk factors in HIV-infected women, looking at two characteristics of the stage of HIV disease (CD4 group and viral load) and two HIV-related medical therapies (antiretrovirals and systemic antifungals).
Finally, we examined the risk of more severe vaginal yeast infections among women with vulvovaginal candidiasis 1. This was accomplished using multivariable models that estimated the risk of vulvovaginal candidiasis 2 or vulvovaginal candidiasis 3 among women with vulvovaginal candidiasis 1.
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RESULTS |
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For the 1277 women in our analysis (Table 1
), mean age over all study visits was 37 years, with no difference by HIV status. (More complete demographic information on the cohort at enrollment is included in Smith et al.10) Human immunodeficiency virus–uninfected women were more likely to report postsecondary education and recent menstrual periods and to be pregnant. No significant differences were seen for bacterial vaginosis, trichomoniasis, or diabetes. Human immunodeficiency virus–infected women were more likely to have genital ulcers on examination and to report recent vaginal yeast infections and current antibacterial use. Human immunodeficiency virus–infected women showed moderate immune compromise (as indicated by CD4 count) at almost half their visits; at the remaining visits, women were evenly divided between the highest and lowest CD4 groups. Human immunodeficiency virus–infected women reported highly active antiretroviral combination therapy use at 8% and other antiretroviral use at 35%. After 1995, however, highly active antiretroviral combination therapy use was reported at 19% of visits, whereas other antiretroviral regimens were reported at 34%. Human immunodeficiency virus–infected women reported use of systemic antifungals at 10% of visits.
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). After 4.5 years of follow-up the cumulative incidence of vulvovaginal candidiasis 1 was 64.5% among HIV-infected women who did not have vulvovaginal candidiasis 1 at the baseline visit. The 4.5-year cumulative incidences among HIV-infected women of vulvovaginal candidiasis 2 and vulvovaginal candidiasis 3 were 28% and 38.1%, respectively. The cumulative incidence of each condition at 4.5 years was roughly ten to 20 percentage points lower among HIV-uninfected women.
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). The average prevalences of vulvovaginal candidiasis 2 and vulvovaginal candidiasis 3 were lower and differed significantly by HIV status (P < .01 for each) (Table 2).
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). These differences in frequency were significant even when corrected for multiple comparisons (P < .01). Furthermore, HIV infection was associated with increased prevalence of vulvovaginal candidiasis 1 at a given visit, regardless of the woman’s status at the preceding visit: HIV-infected women had 1.74 times the odds for acquisition, escalation, or persistence relative to HIV-uninfected women (95% confidence interval [CI] 1.45, 2.09). Results for vulvovaginal candidiasis 2 and vulvovaginal candidiasis 3 were similar (vulvovaginal candidiasis 2: OR 1.60; 95% CI 1.15, 2.23; vulvovaginal candidiasis 3: OR 1.58; 95% CI 1.24, 2.00). Similar results were obtained in a multivariable model that adjusted for other risk factors for vulvovaginal candidiasis. Persistent cases occurred more frequently than escalated cases, which in turn occurred more frequently than acquired cases, and the HIV-associated risk seen after stratifying on the woman’s vulvovaginal candidiasis status at the previous visit remained after adjusting for other factors (data not shown).
Regardless of the definition used, vulvovaginal candidiasis was elevated among HIV-infected women. The HIV-associated ORs for vulvovaginal candidiasis 1, vulvovaginal candidiasis 2, and vulvovaginal candidiasis 3 were 1.88 (95% CI 1.58, 2.25), 1.68 (1.23, 2.28), and 1.63 (1.29, 2.06), respectively, after adjustment for antibacterial use, age, education, genital tract infections, recent menses, diabetes, and pregnancy. Only bacterial vaginosis appeared to act as an HIV effect modifier.
In a model that considered HIV-infected women separately, those with a CD4 count below 200 cells per microliter showed higher prevalence of vulvovaginal candidiasis (all definitions) (Table 3). Among women with CD4 counts of 200–499 cells per microliter, only vulvovaginal candidiasis 1 was significantly more prevalent (Table 3). Use of highly active antiretroviral combination therapy or less active antiretroviral regimens was not associated with prevalence of vulvovaginal candidiasis. Reported use of systemic antifungal agents was associated with decreased prevalence of vulvovaginal candidiasis 1.
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In addition to the HIV-specific items listed above, the model evaluated the independent effect of risk factors not specific to HIV (Table 3). Bacterial vaginosis and recent menses were independently associated with reduced odds for having vulvovaginal candidiasis 1, 2, or 3. Odds of vulvovaginal candidiasis 1 and 2 decreased with age and education and increased with trichomoniasis. Genital ulcers, self-reported recent vaginal yeast infections, and pregnancy were each associated with increased odds of vulvovaginal candidiasis 1, 2, or 3, and diabetes was associated with increased risk of vulvovaginal candidiasis 1 and vulvovaginal candidiasis 3. No other predictor listed in Materials and Methods demonstrated an independent association with vulvovaginal candidiasis—not race, antibacterial drugs, contraceptive practices (including use of hormonal contraceptives), sexual behaviors, or nontherapeutic drug use. Neither reported current use of topical antifungals nor reported use of antifungal cream after a prior episode (data not shown) was significantly associated with current vulvovaginal candidiasis.
Finally, we examined whether vaginal yeast infections are more severe among HIV-infected women. Among women who had yeast on either culture or Gram stain and had at least one clinician-reported sign (ie, among women with vulvovaginal candidiasis 1), the risk of more symptomatic vulvovaginitis (the presence of two or more signs or vulvovaginal candidiasis 2) was not elevated among HIV-infected women (adjusted OR 0.97, P = .86). Similarly, among women with vulvovaginal candidiasis 1, the risk of extensive yeast overgrowth (vulvovaginal candidiasis 3) was essentially equal in HIV-infected and HIV-uninfected women (adjusted OR = 0.96, P = .77).
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DISCUSSION |
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Our analysis used three definitions of vulvovaginal candidiasis based on Candida culture, the presence of yeast on Gram stain, and signs of vulvovaginitis. Using an alternative definition of vulvovaginal candidiasis, a cross-sectional analysis of baseline HER Study data found no significant difference in the prevalence of vulvovaginal candidiasis between HIV-infected and HIV-uninfected women.16 In that analysis, vulvovaginal candidiasis was defined as a positive Candida culture plus abnormal discharge and vaginal erythema or edema. Using that more restrictive definition, Candida vulvovaginitis was found in only 3.1% of HIV-infected women and 1.8% of HIV-uninfected women. Two other cross-sectional studies reported a positive association of vulvovaginal candidiasis with HIV and HIV-associated immune compromise, using two other definitions of vulvovaginal candidiasis: 1) positive Candida culture plus either clinician-reported abnormal white discharge or at least one self-reported symptom2 and 2) presence of budding yeast or hyphae on potassium hydroxide mounts of vaginal specimens.3
The increased risk of vulvovaginal candidiasis in women with low CD4 counts has been attributed to defective cell-mediated immunity, as seen in immunosuppressed patients who have increased risk for chronic mucocutaneous candidiasis and recurrent Candida vulvovaginitis.17,18 Other researchers have reported slightly larger association between antibacterial use and vulvovaginal candidiasis prevalence than reported here, but the associations did not achieve statistical significance in these studies either.1,3 Their findings and ours are consistent with a beneficial response to therapy among HIV-infected women and no significant risk for vulvovaginal candidiasis in women taking antibacterial agents.
The observational nature of our study limited some aspects of the analysis. Because we had incomplete data on the occurrence and treatment of symptomatic vulvovaginitis between visits, we were unable to include such episodes in our analysis. The study did not systematically collect data on response to treatment for vulvovaginal candidiasis. Although vulvovaginal candidiasis prevalence was not significantly decreased in either HIV-infected or HIV-uninfected women who reported topical antifungal use, topical therapy for vulvovaginal candidiasis is available over the counter and could have been used for conditions that were not really vulvovaginal candidiasis. It was not possible for us to analyze precisely the effectiveness of topical therapy for vulvovaginal candidiasis.
Despite these limitations, several strengths of this large, prospective design permitted a substantially improved understanding of the association of HIV status with vulvovaginal candidiasis. These include the following: a large number of HIV-infected and HIV-uninfected women; follow-up over several years; the fact that the HIV-infected and HIV-uninfected women were from the same communities and were matched at enrollment by HIV risk behavior; the fact that the study visits were not symptom driven; and the use of several definitions of vulvovaginal candidiasis, which allowed us to examine severity as well as incidence and prevalence. In addition, the detailed data collection at each study visit allowed us to control for both HIV-related covariates (CD4 count, viral load, and the use of antiretroviral and systemic antifungal agents) and covariates not related to HIV (such as coexistence of bacterial vaginosis, trichomoniasis, or genital ulcers; age; diabetes; and pregnancy).
Many practitioners have interpreted the inclusion of vulvovaginal candidiasis as a category B condition to mean that a patient with unknown HIV risk and recurrent vaginitis symptoms may have a sentinel event for HIV. Our results, however, do not support the use of vulvovaginal candidiasis status as a reliable sentinel for HIV. First, vulvovaginal candidiasis is common in HIV-uninfected women. Second, although it is more common in untreated HIV-infected women than in HIV-uninfected women, the increase is not substantial among women with high CD4 counts or low viral load. Although women with very low CD4 and high viral load have higher rates of vulvovaginal candidiasis, they are likely to manifest other, more classically AIDS-related sentinel conditions as well. Finally, among women with vulvovaginal candidiasis, the condition does not appear to differ substantively in severity between HIV-infected and HIV-uninfected women.
In conclusion, the results of this analysis will be useful clinically in helping to anticipate those HIV-infected women most likely to experience vulvovaginal candidiasis. These include women with low CD4 counts or high HIV viral loads. Our findings also imply that vulvovaginal candidiasis risk may be modulated by antiretroviral therapy; a decrease in vulvovaginal candidiasis risk can be expected for women whose immune function improves on highly active antiretroviral combination therapy but not for those without substantial CD4 increases. We also found high rates for vulvovaginal candidiasis among women with vulvovaginal candidiasis (or subclinical Candida colonization) within the past 6 months. Our data on treatment of women with vulvovaginal candidiasis are not definitive. Nonetheless, a high persistence rate was seen among HIV-infected women, even those who report intercurrent use of topical antifungals or current systemic antifungal use. This high persistence (or reinfection) rate implies that careful follow-up of HIV-infected women after treatment is warranted.
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APPENDIX |
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Footnotes |
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The authors acknowledge the editorial support of Tyris Shaw and anonymous reviewers.
* HER Study group members are listed in the Appendix. 
doi: 10.1016/S0029-7844(02)02729-1
Received July 15, 2002. Received in revised form October 7, 2002. Accepted October 17, 2002.
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REFERENCES |
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2. Duerr A, Sierra MF, Feldman J, Clarke LM, Ehrlich I, DeHovitz J. Immune compromise and the prevalence of Candida vulvovaginitis in human immunodeficiency virus-infected women. Obstet Gynecol 1997;90:252–6.[Abstract]
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