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Prevalence, Incidence, and Persistence or Recurrence of Trichomoniasis among Human Immunodeficiency Virus (HIV)–Positive Women and among HIV-Negative Women at High Risk for HIV Infection

  1. Susan Cu-Uvin1,
  2. Ko Hyejin1,
  3. Denise J. Jamieson2,
  4. Joseph W. Hogan1,
  5. Paula Schuman3,
  6. Jean Anderson4,
  7. S. Klein Robert5, and
  8. HIV Epidemiology Research Study (HERS) Group
  1. 1Brown University, Providence, Rhode Island
  2. 2Centers for Disease Control and Prevention, Atlanta, Georgia
  3. 3Wayne State University, Detroit, Michigan
  4. 4Johns Hopkins University, Baltimore, Maryland
  5. 5Montefiore Medical Center and Albert Einstein College of Medicine, Bronx, New York
  1. Reprints or correspondence: Dr. Susan Cu-Uvin, The Miriam Hospital, 164 Summit Ave., Providence, RI 02906 (scu-uvin{at}lifespan.org).
 
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Abstract

Trichomoniasis has been implicated in the acquisition and transmission of human immunodeficiency virus (HIV) infection. The prevalence, incidence, and persistence or recurrence of trichomoniasis were assessed among HIV-positive women and among HIV-negative women at high risk for HIV infection. A total of 871 HIV-seropositive women and 439 HIV-seronegative women enrolled in the HIV Epidemiology Study (HERS) were seen biannually. The prevalence of trichomoniasis was 9.4%–29.5% among HIV-seropositive women and 8.2%–23.4% among HIV-seronegative women. Prevalence decreased over time, did not vary according to HIV status or CD4 cell count, and was higher among women who reported crack use (P = .02) or cigarette use (P = .02), women who had bacterial vaginosis (P = .02), and those who were black (compared with white women, P < .001). There were no differences, according to HIV status or CD4 cell count, in the adjusted incidence, unadjusted incidence, or persistence or recurrence of trichomoniasis. HIV infection does not make a woman more likely to have prevalent, incident, or persistent or recurrent trichomoniasis.

Trichomonas vaginalis, which is transmitted primarily by sexual contact, causes vaginitis, adverse gynecologic sequelae (e.g., pelvic inflammatory disease), and obstetric sequelae (e.g., premature rupture of membranes) in women [1–3]. A recent study, however, reported that treatment of pregnant women who had asymptomatic trichomoniasis did not prevent premature delivery [4]. The T. vaginalis parasite infects >200 million people worldwide annually [1]. The reported rates of trichomoniasis prevalence are 5%–13% among women in the general population and 40%–60% among women who are commercial sex workers [3, 5]. In the HIV Epidemiology Research Study (HERS), the prevalence of trichomoniasis at baseline, as determined by wet mount analysis, was 12% among 871 HIV-positive women and 10% among 439 HIV-negative women at high risk for HIV infection (hereafter known as “high-risk HIV-negative women”). The HERS, a multicenter, longitudinal cohort study of women either living with or at risk for HIV infection, was designed to study the biological, behavioral, and social determinants of progression of HIV disease [6].

T. vaginalis infection is common among HIV-infected women and high-risk HIV-uninfected women [6–8], and it has been implicated in the acquisition and transmission of HIV. Laga et al. [9] found an increased risk of HIV acquisition among female sex workers in Zaire who had trichomoniasis. Cohen et al. [10] reported increased shedding of HIV in the semen of men with Trichomonas urethral infection. Even in symptom-free women, trichomoniasis causes punctate hemorrhages (e.g., strawberry cervix) and elicits a local cellular response, which may increase both the number of cells susceptible to HIV and the shedding of HIV by the genital tract. Even if Trichomonas organisms amplify HIV transmission by only a small degree, the risk of HIV transmission attributable to Trichomonas infection may be substantial because infection with such organisms is common [11].

There is concern that, compared with HIV-negative women, HIV-infected women may have higher incidence and persistence and greater severity of genital tract infections. However, little is known about the course of trichomoniasis and other infections of the lower genital tract among women with HIV infection. Only vulvovaginal candidiasis that is persistent, frequent, or poorly responsive to therapy has been specified by the Centers for Disease Control and Prevention (CDC; Atlanta) as belonging to category B in the revised classification of HIV disease [12], which means that the condition is (1) attributed to HIV infection, (2) indicative of a defect in cell-mediated immunity, or (3) considered to have a clinical course or management that is complicated by HIV infection. Whether other genitourinary infections are exacerbated by HIV infection needs to be further studied

Despite the clinical and public health importance of trichomoniasis, there has been little information published on trichomoniasis in HIV-infected women. In the present report, we examine the prevalence, incidence, and persistence or recurrence of trichomoniasis during a 5.5-year period, in addition to the risk factors associated with such infection, in a large cohort of HIV-infected women and a well-matched high-risk comparison group.

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Patients and Methods

From April 1993 through January 1995, the HERS recruited 871 HIV-seropositive women and 439 high-risk HIV-seronegative women from 4 sites in the United States (Bronx, NY; Baltimore, MD; Detroit, MI; and Providence, RI). The study protocol was approved by the institutional review boards at each study site and by the CDC. A detailed description of the selection of participants and the design of the HERS has been reported elsewhere [13]. Participants were recruited through flyers distributed in community gathering places, notices placed in community newspapers, letters sent to physicians caring for women who either have HIV infection or are at risk for HIV infection, meetings with the staff of drug treatment centers, invitations extended to participants in earlier behavioral or clinical studies, and word-of-mouth publicity generated by participants in other HIV studies. HIV-negative women were recruited during the same period, by use of resources that were the same as or comparable to those used in the recruitment of HIV-infected women. Appropriate informed consent was obtained from participants, and clinical research was conducted in accordance with guidelines for human experimentation, as specified by the US Department of Health and Human Services and the study authors' institutions.

Individuals were enrolled in the HERS if they were 16–55 years of age and if they (1) had a history of injection drug use (since 1985), (2) had reported having >5 sexual partners in their lifetime, (3) had engaged in sex with a male injection drug user or a person either known or suspected of having HIV infection, or (4) had traded sex for drugs or money. HIV-infected women who had any AIDS-defining clinical illness were excluded. Participants consented to a standardized interview and a physical examination that included pelvic examination and collection of blood, urine, and genital tract specimens every 6 months.

Pelvic examinations were performed at scheduled visits and were not symptom driven. Trichomoniasis was diagnosed on the basis of detection of trichomonads on wet mount analysis. Culture for Trichomonas species (in modified Diamond's media) was performed consistently, beginning at the time of study visit 4. Neisseria gonorrhoeae was diagnosed by culture, and Chlamydia trachomatis was identified by direct fluorescent antibody testing. Vaginal and anal cultures for Candida organisms were performed. A swab specimen obtained from the posterior fornix underwent Gram staining on a slide, and bacterial vaginosis was diagnosed when a score of 7 of 10 was assigned on the basis of the Gram-stain scoring system of Nugent et al. [14]. Screening for syphilis was done by use of the rapid plasma reagin test, and the fluorescent Treponema antibody absorption test was done for confirmation of the result. Routine testing for N. gonorrhoeae, C. trachomatis, and syphilis was discontinued after visit 3 because of the low prevalence of such infections among the study participants [6]. Women who had trichomoniasis or any other genital tract infection diagnosed were referred to their primary health care providers for treatment. The HERS was an observational study and did not provide treatment.

We analyzed data obtained during the first 12 study visits. Univariate associations, at baseline, between demographic, behavioral, clinical, or laboratory variables and patient HIV status were quantified using odds ratios. Because culture for Trichomonas organisms was not routinely performed until study visit 4, summary statistics reported in table 1 and baseline multivariate analysis by Trichomonas infection status relied on a simple imputation method for estimation of the prevalence of a positive culture result. To do this, we computed site-specific sensitivity and specificity values for wet mount analysis (which was performed during all study visits) and then estimated the number of positive culture results by use of the formula nc + ·, where pw is the prevalence of trichomoniasis, as determined by wet mount analysis; where nw is the number of women with Trichomonas organisms detected by wet mount analysis; and where nc is the number of women whose cultures were positive for Trichomonas species. Calculation of the sensitivity and specificity values associated with wet mount analysis was done with the use of data obtained at all visits, under the assumption that both values were constant across all visits but differed by site.

Table 1
Table 1

Baseline characteristics of 1310 women evaluated in the HIV Epidemiology Research Study, according to HIV status.

The prevalence of trichomoniasis at baseline in the HERS, according to wet mount analysis only, has been published elsewhere [6]. In contrast, the baseline data presented in our report were calculated by use of the imputations described above. Our calculation provides a more accurate assessment of the baseline prevalence rate, because wet mount analysis has a sensitivity of ∼60% for the detection of Trichomonas organisms, compared with culture [15].

Actual rates of incidence and either recurrence or persistence of trichomoniasis were calculated, according to HIV status, on the basis of culture results obtained at visits 5–12. “Incident infection” was defined by culture that was negative for Trichomonas species at one study visit being followed by culture that was positive for Trichomonas species at the subsequent visit. We did not have reliable data on treatments for trichomoniasis given between study visits, to distinguish infection that was persistent (i.e., continuous infection) from infection that was recurrent (i.e., relapse or reinfection after treatment). Therefore, women who had trichomoniasis detected on consecutive visits were considered to have either persistence or recurrence.

To investigate specific covariate effects on prevalence, we used logistic regression for repeated binary outcomes and fitted the models by use of generalized estimating equations. HIV-positive women were classified into 3 groups according to their CD4 cell count categories: <200 cells/mm3, 200–500 cells/mm3, and >500 cells/mm3. Also included as covariates were race, sexual behavior, drug and alcohol use, presence of bacterial vaginosis, and a positive result of culture for Candida species. For the prevalence model, the underlying log odds of prevalence of Trichomonas infection were assumed to follow a linear time trend, which allowed for the use of all culture data obtained during visit 1. For modeling of incidence and either recurrence or persistence, we used logistic regression formulations of Markov transition models [16]. All analyses were performed using SAS software, version 7 (SAS Institute), on a Sun Ultra Workstation. Logistic regressions and transition models were fit using Proc Genmond in SAS.

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Results

The mean patient age at baseline was 35 years. Other baseline characteristics of the 2 groups of women are presented in table 1. HIV-seropositive women were significantly less likely to have had sex with men, to have had ⩾2 sexual partners, and to have used crack during the past 6 months, and they were more likely to have used condoms, to have received a positive result of culture for Candida species, and to have developed trichomoniasis. The groups were similar with regard to alcohol use, cigarette use, injection drug use, and having traded sex for drugs or money during the past 6 months (data not shown).

On multivariate analysis, trichomoniasis at baseline was significantly associated with current injection drug use (55% among users vs. 15% among nonusers; adjusted OR, 6.67; 95% CI, 4.82–8.51), crack use during the past 6 months (34% among users vs. 20% among nonusers; adjusted OR, 2.05; 95% CI, 1.48–2.61), and alcohol use during the past 6 months (78% among users vs. 45% among nonusers; adjusted OR, 4.39; 95% CI, 3.13–5.65). Trichomoniasis was also associated with the presence of bacterial vaginosis (74% among those with bacterial vaginosis vs. 35% among those without bacterial vaginosis; adjusted OR, 5.22; 95% CI, 3.77–6.67) and with a positive result of culture for Candida species (37% among those with a positive result vs. 29% among those with a negative result; adjusted OR, 1.41; 95% CI, 1.04–1.78).

During the 5.5-year evaluation period, the prevalence of trichomoniasis was 9.4%–29.5% among HIV-seropositive women and 8.2%–23.4% among HIV-seronegative women, and it decreased over time. The results of multivariate analysis are shown in table 2. The rate of decrease did not vary significantly according to HIV status or CD4 cell count. Factors that were independently associated with prevalent trichomoniasis (i.e, a case for which culture was positive for Trichomonas organisms at the time of a study visit) included black race, crack use, cigarette use during the past 6 months, and presence of bacterial vaginosis.

Table 2
Table 2

Multivariate analysis of risk factors for prevalent trichomoniasis among 1310 participants in the HIV Epidemiology Research Study.

There was no significant difference in either the incidence or the persistence or recurrence of trichomoniasis among HIV-seropositive women, compared with high-risk HIV-seronegative women (table 3). Among HIV-seropositive women, there also was no difference observed on the basis of CD4 cell count. For study visits 5–12, the average rate of incidence of trichomoniasis was 0.07 per 6-month cycle of study visits among both HIV-seropositive women and high-risk HIV-seronegative women. The average rate of persistent or recurrent trichomoniasis was 0.52 for HIV-seropositive women and 0.46 for HIV-seronegative women.

Table 3
Table 3

Adjusted odds ratios for incident and either persistent or recurrent trichomoniasis in 1310 participants in the HIV Epidemiology Research Study.

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Discussion

We found no differences, according to patient HIV status or CD4 cell count, in the prevalence, incidence, or persistence or recurrence of Trichomonas infection during a >5-year period. This finding suggests that, for women, HIV infection does not result in an increased risk of contracting trichomoniasis.

Risk factors for prevalent trichomoniasis included black race, crack use, cigarette use, and the presence of bacterial vaginosis. We saw no effect of HIV-associated immunodeficiency on the risk for Trichomonas infection, except at baseline. Such risk appeared to depend, to a substantial degree, on behavioral factors.

Similar findings have been reported previously. Minkoff et al. [7] reported that T. vaginalis infection (as detected by culture) was present in 58 [20.4%] of 284 HIV-infected women and in 163 [24.2%] of 673 HIV-uninfected women (P = .23) evaluated and that no difference was noted in the prevalence of such infection in these groups of women, according to CD4 cell count. They also found no difference in the 1-year incidence of trichomoniasis by HIV status (incidence, 10.3% [for HIV-positive women] vs. 9.2% [for HIV-negative women]; OR, 1.13; 95% CI, 0.57–2.25). Smoking, drug use, and more sexual partners during the past year were all associated with acquisition of nonviral sexually transmitted diseases, including trichomoniasis.

An uncontrolled study by Bersoff-Matcha et al. [8] reported an 11% point prevalence for trichomoniasis (as detected by wet mount analysis) among HIV-seropositive women, a finding that is similar to the baseline findings noted in the HERS, previously published [6]. In a study performed at a public health clinic in Los Angeles, Trichomonas infection was the most frequently identified sexually transmitted disease reported (in 17.4% of 212 HIV-infected women) [17]. In that study, the crude rate of trichomoniasis was highest in women who were black, who had a history of trading sex for drugs or money, who used crack or cocaine, or who had ⩾4 sex partners. In our study, we found that black race and crack use were associated with an increase in the risk for trichomoniasis. Another study from Africa reported that trichomoniasis was present in 40 [18.6%] of 215 HIV-positive pregnant women and in 21 [10.2%] of 206 HIV-negative pregnant women (OR, 2.0; 95% CI, 1.1–3.6) [18], and, on multivariate analysis, only maternal HIV status was a risk factor for trichomoniasis. The present study and the aforementioned reports highlight (1) the high rates of trichomoniasis among HIV-infected women and those who are at risk for HIV infection, and (2) the behaviors associated with increased risk.

Bacterial vaginosis frequently coexists with trichomoniasis [19, 20], so our finding that trichomoniasis was more prevalent among women with bacterial vaginosis was not surprising. Other sexually transmitted diseases, such as gonorrhea or chlamydia, are also frequently seen in association with trichomoniasis, but these conditions were rarely observed in the HERS.

The major strengths of the HERS were its large sample size of demographically and behaviorally similar cohorts of HIV-positive women and HIV-negative women and its prolonged follow-up period. In addition, the fact that pelvic examinations were not symptom driven but, rather, were performed during scheduled study visits decreased the chance of trichomoniasis not being detected in asymptomatic women. However, because we did not have reliable data on possible treatment for trichomoniasis or response to treatment, we could not distinguish persistent infection from recurrent infection. It also should be noted that our findings may not apply to women at low risk for HIV infection.

Trichomoniasis frequently occurred among the HIV-positive women and the high-risk HIV-negative women in this study, more than three-fourths of whom had been sexually active with a man during the 6 months before the study. Screening for and treatment of trichomoniasis among HIV-positive women and high-risk HIV-negative women may contribute to the prevention of HIV transmission.

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acknowledgments

We gratefully acknowledge the assistance of Chien-hsun Li in data management and statistical computing.

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Footnotes

  • Financial support: Centers for Disease Control and Prevention cooperative agreements (nos. U64/CCU106795, U64/CCU206798, U64/CCU306802, and U64/CCU506831).

  • Received October 5, 2001.
  • Revision received January 22, 2002.
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  1. Clin Infect Dis. (2002) 34 (10): 1406-1411. doi: 10.1086/340264
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