Sexually Transmitted Diseases:
Prevalence and Correlates of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis infections, and Bacterial Vaginosis Among a Cohort of Young Injection Drug Users in Baltimore, Maryland
Plitt, Sabrina S. PhD*; Garfein, Richard S. PhD†; Gaydos, Charlotte A. DrPH‡; Strathdee, Steffanie A. PhD§; Sherman, Susan G. PhD*; Taha, Taha E. PhD*
From the *Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; the †Division of HIV/AIDS Prevention, Centers for Disease Control, Atlanta, Georgia; the ‡Department of Medicine, Johns Hopkins University, Baltimore, Maryland; and the §Division of International Health and Cross Cultural Medicine, University of California, San Diego, California
The authors acknowledge the staff at the Ferne Johnson Clinic for their extraordinary effort in the conduct of this study and the DUIT participants for their time and commitment. A special thank you to Karen Hobelmann and Marie Bailey-Kloch.
The authors acknowledge all DUIT investigators for their contribution to the design and conduct of DUIT: Elizabeth Golub (Johns Hopkins University, Baltimore), Lawrence Ouellet, and Susan Bailey (University of Illinois Chicago); Sharon Hudson and Peter Kerndt (Health Research Association, Los Angeles); Mary Latka and David Vlahov (New York Academy of Medicine, NY); and Holly Hagan and Hanne Thiede (Public Health Seattle and King County, Seattle).
The authors acknowledge the staff of the International Chlamydia Laboratory for their help with staff training, ordering of supplies, and processing and testing of specimens, especially Paul Stamper, Billie-Jo Wood, and Mellisa Theodore. Also thanks to Jeff Yuenger and Julie Giles for their help with the processing and reading of BV smears. In addition, the authors thank Carla Latney from the Baltimore City Health Department.
Sabrina Plitt was supported by a Health Research Studentship from the Alberta Heritage Foundation for Medical Research.
Correspondence: Richard S. Garfein, PhD, Division of HIV/AIDS Prevention, Epidemiology Branch, Centers for Disease Control and Prevention, 1600 Clifton Road, MS-E45, Atlanta, GA 30333. E-mail: firstname.lastname@example.org.
Received for publication September 28, 2004, and accepted December 16, 2004.
Objectives: Injection drug users (IDUs) consistently demonstrate high-risk behaviors for sexually transmitted infections (STIs). This study examines STI prevalence and correlates among young IDUs.
Study: This cross-sectional study recruited IDUs aged 18 to 30 years. Participants completed a behavioral risk assessment and were tested for chlamydia, gonorrhea, and trichomoniasis by nucleic acid amplification methods. Women were also tested for bacterial vaginosis (BV). Gender-specific analyses were done comparing infected with noninfected participants using chi-square, Mann-Whitney tests, and logistic regression.
Results: Of the 115 (35.3%) women and 211 (64.7%) men in the study, STI prevalence, respectively, was: chlamydia, 5.3% and 3.3%; gonorrhea, 3.5% and 0%; and trichomoniasis, 8.6% and 1.9%. Most (68.0%) participants had 2 or more sex partners in the past 3 months, of whom fewer than half consistently used condoms. Independent correlates for prevalent STIs included douching (adjusted odds ratio [AOR], 4.9; 95% confidence interval [CI], 1.5–23.6) for women and anal sex with female partners (AOR, 6.3; 95% CI, 1.5–25.8) for men. BV prevalence was 56.3% and was associated with douching (OR, 2.5; 95% CI, 1.1–5.7).
Conclusions: Despite high sexual risk, STI prevalence among young IDUs was similar to that of the general population. BV prevalence was high, suggesting that future STI assessments among female IDUs should include BV.
STUDIES CONSISTENTLY DEMONSTRATE THAT injection drug users (IDUs) practice sex behaviors that place them at high risk for sexually transmitted infections (STIs).1,2 However, information on nonbloodborne STIs among drug users is sparse, and most studies are based on a small number of IDUs captured in samples from clinics or drug treatment programs, which typically represent older, longer-term injectors. Recent studies of younger IDUs involving community-based samples show a high prevalence of sexual practices that could expose them to STIs.2,3 One study found that even among young IDUs who had a high prevalence of unprotected sex, the prevalence of gonorrhea and chlamydia were relatively low2; however, little is known about the prevalence of other STIs in this population.
The public health consequences of STIs are heightened among IDU populations as a result of the potentiation of HIV transmission and acquisition by both ulcerative and nonulcerative STIs.4–8 These consequences of STI–HIV coinfections are important among populations such as IDUs in whom the prevalence of HIV infection is greater than the general population and the probability of having HIV-positive sex partners is increased. In this study, we attempted to confirm a low prevalence of chlamydia and gonorrhea, estimate the prevalence of trichomoniasis and bacterial vaginosis (BV), and identify correlates of these infections among a cohort of young IDUs in Baltimore, Maryland.
Materials and Methods
Young adult IDUs were recruited for participation in this study from the Drug Users Intervention Trial (DUIT), a multicenter, randomized, controlled trial evaluating an intervention of cognitive–behavioral skills building to reduce sexual and injection risks associated with HIV and hepatitis C virus (HCV) infection. DUIT recruitment was conducted using community-based outreach, targeted sampling, and peer-driven sampling.9 The baseline assessment visit was designed to provide cross-sectional data on prevalence of multiple infections among young IDUs; therefore, recruitment and screening activities were conducted without regard for prevalent infection status. Participants were deemed eligible for DUIT if they were 15 to 30 years old, were not enrolled in other studies at the same time, planned to be in the area for the next 12 months, and had injected at least once in the 6 months before enrollment. All eligible participants were asked to complete a baseline survey and underwent HIV and HCV antibody screening with appropriate pretest counseling according to Centers for Disease Control and Prevention (CDC) guidelines.10
At the Baltimore site, between September 2002 until February 2003, all eligible participants for DUIT aged 18 to 30 years were subsequently asked if they wanted to join the STI substudy. Participants who agreed proceeded with informed consent and baseline assessment. At the end of the visit, participants were reimbursed for their time and travel costs, $20 for DUIT and $5 for the STI substudy. This research was approved by the Committee on Human Research at the Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, and the Institutional Review Board at the CDC, Atlanta, Georgia.
All participants were asked to complete the DUIT baseline questionnaire and an additional STI study questionnaire. The DUIT questionnaire was administered by audio computer-assisted self-interview (ACASI), which has been associated with higher reporting levels of sensitive behaviors among IDUs,11,12 as well as greater validity.13 In addition to demographic information, this questionnaire gathered information on sexual and drug use behaviors such as age at first intercourse, number of sex partners, frequency of condom use with steady or casual partners, type of sex (vaginal/oral/anal), type and frequency of drug use, self-reported description of sex partners, homosexual/bisexual behaviors, history of trading sex for money or drugs, and the frequency of “ask[ing] a sex client… to use a condom.” The majority of the sexual and drug use behavior variables referred to the previous 3-month period. A main steady sex partner referred to the sex partner to whom the participant felt was their closest or most important sex partner. Casual partners were defined as “nonsteady” or sex-trading partners.
Participants were also asked to complete a 1-page interviewer-administered questionnaire to collect information that was not captured by the DUIT baseline questionnaire such as lifetime sexual partners and history of STIs. In addition, douching practices of female participants were assessed by questions referring to douching frequency in the previous 6 months, date of last douche, reasons for douching, and type of douching solution used.
Two self-administered vaginal swabs were collected from women and 1 “first-catch” urine specimen was collected from men. Specimens were tested for chlamydia, gonorrhea, trichomoniasis, and, among women only, bacterial vaginosis as described subsequently.
Strand displacement amplification (SDA) was used to test for the presence of Chlamydia trachomatis and Neisseria gonorrhoeae DNA in urine samples and self-administered vaginal swabs. The ProbeTec ET system was used following the instructions provided by the manufacturer (Becton Dickinson, Sparks, MD). The presence of Trichomonas vaginalis DNA was tested by polymerase chain reaction (PCR) in urine and in self-administered vaginal swabs. This assay used 2 β-tubulin gene primers, BTUB-2 and BTUB-9.14 Previous studies have shown both the BD ProbeTec ET and the T. vaginalis PCR assay to have high sensitivity and specificity.14–16
Female participants were also tested for BV. Immediately after specimen collection, study staff rolled 1 of the vaginal swabs onto a microscope slide, fixed the smear, and allowed it to air dry. Once transported to the lab, these slides were Gram-stained, examined microscopically by trained laboratory staff, and given a score of zero to 10 based on the relative proportion of BV-associated organisms (i.e., large Gram-positive [Lactobacillus], small Gram-negative or Gram-variable rods [Gardnerella or Bacteroides], and curved Gram-variable rods [Mobiluncus]).17 Slides with a score of 7 or higher were diagnosed as BV, whereas scores of less than 4 were diagnosed as negative for BV. Any slide with a preliminary intermediate reading (i.e., a score of 4–6) was read by a second reader; the final BV score was determined when both readers came to a consensus. Compared with Amsel’s clinical criteria, the sensitivity and specificity of the Nugent criteria is 89% and 83%, respectively.18 In addition, the Nugent criteria have been shown to have high intra- and interobserver reliability.19
Experience shows that it can be difficult for IDUs to return for laboratory test results. To minimize participant burden and maximize the number of participants who would be given their test results, participants were asked to return 2 weeks after baseline to receive their results and posttest counseling for all tests in 1 visit. If positive for any STI or BV, participants were referred for medical evaluation and treatment, if required. A combination of reminder letters, telephone calls, and home visits were used to ensure that participants returned to receive their test results. Participants received monetary compensation for attending this results visit. As required by Maryland State Law, all cases of gonorrhea and chlamydia were reported by name, age, sex, and address to the Baltimore City Health Department, with the participant’s prior consent.
Prevalence was defined as the proportion of subjects with positive tests at their baseline visit. A 95% binomial confidence interval was calculated for each prevalence estimate. Given the observed differences in prevalence by gender, it was decided to stratify all further analyses by gender.
As a result of the small number of infections, data were collapsed for chlamydia, gonorrhea, or trichomoniasis and correlates were not identified for individual STIs. A separate analysis was carried out to assess correlates for BV. Descriptive statistics (e.g., chi-square, Fisher exact tests, Mann-Whitney tests) were used to analyze the distribution of categorical and continuous variables (e.g., demographics, sexual behaviors, drug use behaviors) between those infected and those not infected.
Multivariate logistic regression analyses were performed separately for men and women to identify significant independent effects of demographic, sexual behavior, and drug use variables on being positive for at least 1 of the STIs (i.e., chlamydia, gonorrhea, or trichomoniasis). Any variable associated with the outcome at P <0.15 in univariate analyses was entered into a logistic regression model to obtain adjusted estimates of the odds ratios (AOR) and 95% confidence intervals (CI). Race and age were assessed as possible confounders. If no meaningful changes were noted in the coefficients or the model, these variables were not included. Potential interactions were examined by adding product terms to the logistic regression model. Variables with zero cells could not be included in the logistic regression model. Statistical significance was determined using a significance of 0.05. All analyses were performed using Stata Version 7.0 (Stata Corp., College Station, TX).
Demographics, Drug Use, and Sexual Behaviors
Of 358 eligible individuals invited to join the STI substudy, 340 (95%) agreed to participate. Of the participants who consented, urine or vaginal swabs were received and tested for 326 (96%). Of the remaining 4%, specimens were either not collected from participants during their visit or were not properly transported for testing by the laboratory (e.g., leaked during transport).
Of these 326 participants, 115 (35.3%) were women and 211 (64.7%) were men (Table 1). In total, 75.6% of the sample was white, 14.4% were black, 2.2% Hispanic, 2.2% American Indian, 0.3% Asian, and 5.5% mixed races. The median age of the sample was 24 years (interquartile range [IQR] = 22–27). Twenty-five percent reported being homeless at least part of the time in the last 6 months. The seroprevalence of HIV was 1.7% among females and 2.4% among males.
In the previous 3 months, 71.7% of women and 62.7% of men injected daily (P = 0.10). For both sexes, the predominant drug used was heroin, whereas lower proportions reported injection of cocaine alone or with heroin (i.e., speedball). Crack smoking was reported by over half (53.7%); however, daily crack smoking was only reported for 2.2% of the population and did not differ by gender.
The median age of sexual debut of the sample was 14 years. Men had a higher median number of lifetime sexual partners than women (20 vs. 14.5, respectively; P = 0.02). Women were more likely than men to report bisexual/homosexual orientation (36.6% vs. 7.4%, respectively; P <0.001) and same-sex relationships in the past 3 months (27.3% vs. 10.6%, respectively; P <0.001).
Nearly all participants reported some sexual activity during the past 3 months. Women were significantly more likely to report having a steady sex partner in the 3 months before study entry than men (91.1% vs. 81.4%, respectively; P = 0.02). Only 13% of those with a main steady sex partner and 39.3% of those with casual partners reported consistent condom use for vaginal sex; these proportions did not differ significantly by gender. Women were more likely than men to report having a main steady sex partner who had ever injected drugs (74.0% vs. 42.7%, respectively; P <0.001). In the 3 months before study entry, 35.4% of women and 11.9% of men (P <0.001) had received money or drugs for sex, whereas 6.3% of women and 9.1% of men (P = 0.52) had paid someone to have sex. Women were more likely than men to consistently ask their sex trade partners to use condoms (70.7% vs. 36.7%; respectively; P = 0.004).
Sexually Transmitted Infection Prevalence
In total, 16.4% of women tested positive for chlamydia, gonorrhea, or trichomoniasis. In contrast, 5.2% of men tested positive for any of the 3 infections. In women, the prevalence of chlamydia, gonorrhea, and trichomoniasis was 5.3% (95% CI, 2.0–11.1%), 3.5% (95% CI, 0.95–8.6%), and 8.6% (95% CI, 4.2–15.3%), respectively (Table 2). Only 1 woman was coinfected with chlamydia and gonorrhea. The prevalence of chlamydia and trichomoniasis among men was 3.3% (95% CI, 2.3–6.6%) and 1.9% (95% CI, 0.5–4.7%). Among male participants, there were no cases of gonorrhea. The proportions of participants infected with gonorrhea and trichomoniasis were statistically higher among women than men. In addition, a higher proportion of women than men self-reported a previous infection with chlamydia (19.4% vs. 4.4%, P <0.001) and trichomonas (15.7% vs. 0.5%, P <0.001), respectively (data not shown).
All gonorrhea cases were among white participants, but there was no statistical difference in chlamydia prevalence by race. Among trichomoniasis cases, a significantly higher proportion of cases occurred in black than white participants (12.8% vs. 3.3%, P = 0.02). There were no significant differences in age between cases and noncases for any of the individual infections.
Sexually Transmitted Infection Correlates
Statistically significant correlates for being infected with any STI (chlamydia, gonorrhea, or trichomoniasis) were identified by univariate analyses for men and women separately. The median age was higher among women with at least 1 STI (25 years, IQR = 22–28 years) than among women with no STIs (23 years, IQR = 20–27 years), but this difference was not statistically significant (P = 0.08). The median age for men was 25 years in both groups (P = 0.23). The median age of first sexual intercourse was 14 years overall and did not differ by gender or STI infection status. There was also no difference in the median number of lifetime sexual partners between those with and without STIs among women (13.5, IQR = 5–30 vs. 14.5, IQR = 9–29; P = 0.38) or men (15, IQR = 11–20 vs. 20, IQR = 10–40; P = 0.42).
Women participants were less likely to be infected with at least 1 STI if they reported being in a same-sex relationship (0% vs. 32.3%, P = 0.006) and having a main steady sex partner who injected drugs (35.3% vs. 72.3%; P = 0.005) (Table 3). A greater proportion of women with STIs had douched in the past 6 months than women without an STI (81.3% vs. 56.5%; P = 0.09), although this difference was not statistically significant. This difference was greatest among those who had douched at least 6 times in the past 6 months. No other variables investigated for women were statistically significant. Among men, those with at least 1 STI were more likely to report having had anal sex with a female sex partner in the past 3 months than those with no STIs (72.7% vs. 31.0%, P = 0.007). No other variables investigated for men were statistically significant.
Multivariate analyses of women identified that having a steady sex partner who injected drugs (AOR, 0.3; 95% CI, 0.08–0.8) was an independent correlate for not being infected with at least 1 of the STIs (i.e., gonorrhea, chlamydia, or trichomoniasis), whereas having douched in the previous 6 months (AOR, 4.9; 95% CI, 1.1–23.6) was positively associated with infection. Among men, anal sex with female partners was positively associated with infection (AOR, 6.3; 95% CI, 1.5–25.8), whereas alcohol use was negatively associated with infection (AOR, 0.3; 95% CI, 0.07–1.0).
Bacterial Vaginosis: Prevalence and Correlates
Of the 112 female participants who had an BV smear, 63 (56.3%) were positive for BV, 6 (5.4%) were intermediate, and 43 (38.4%) were negative. Douching was the only factor found to be more common among those women with positive (or intermediate scores) BV smears than among those with negative smears (Table 4). Compared with women without BV, women with BV were more likely to have douched in the previous 6 months (67.2% vs. 44.7%; OR, 2.5; 95% CI, 1.1–5.7). Among women who douched in the previous 6 months, the median number of douches was higher (6 times [IQR = 6–12] vs. 4 times [IQR = 2–6]; OR, 1.1; 95% CI, 1.0–1.3) and the time since last douche was shorter (22 days [IQR = 6–34] vs. 34 days [IQR = 21–62]; OR, 0.98; 95% CI, 0.96–0.99) among those women with BV than those without BV. There was no difference between these groups in terms of type of douching solution (i.e., store-bought product or vinegar solution). No significant differences were found for douching variables after adjustment by age or race.
In this cohort of young IDUs, we observed high levels of sexual risk, including having multiple sex partners and low condom use, yet the prevalence of chlamydia, gonorrhea, and trichomoniasis were moderate to low. The high prevalence of sexual risk behaviors and BV among female participants is of concern as a result of the increased risk of HIV acquisition among women with BV infection.20
The prevalence of chlamydia and gonorrhea reported in this cohort was similar to those reported from other young drug-using populations.2,21–24 In a study of young IDUs by Latka et al. in the CIDUS-II multicenter study, the prevalence of chlamydia was 5.2% and did not differ by gender. Gonorrhea prevalence was 2% among women and 0.2% among men.2 Poulin et al. examined the prevalence of STIs among 738 drug users attending an STI prevention and needle exchange program in Quebec City, Canada. In that study, the prevalence of chlamydia was 5.3% for women and 3.3% for men; gonorrhea was 3.4% among women and 0% among men.24
In our study, there were no cases of chlamydia or gonorrhea among black women. These results were similar to those of a study conducted among female detainees in Baltimore city prisons in which white participants had a significantly higher proportion of chlamydia and gonorrhea infections than did black inmates.25 The black women in our study were significantly older than the white women, which may have led to our finding different prevalence by race, because both of these infections are associated with younger age.26 The prevalence of trichomoniasis was lower than that reported in other drug-using populations. Bachmann et al.21 reported a prevalence of 22% among women attending a residential drug treatment center in Alabama, whereas Lally et al.23 showed a prevalence of 43% among women at a substance abuse treatment center. We are unaware of any published reports of trichomoniasis prevalence conducted specifically among male drug users; however, research among men in Baltimore city sexually transmitted disease clinics (of which 7% were IDUs) indicated that 13% tested positive by urine PCR and/or culture.27 The lower prevalence of trichomonas infection reported from our sample compared with other studies is surprising considering that the use of PCR should have increased sensitivity to detect infections.14 One possible difference is that in those other studies, the populations were older than our participants; older age has been positively associated with trichomonas infection.27,28
Overall, the prevalence of STIs from this population of young IDUs is comparable to those from the general population. A 2002 Baltimore population-based study of 18 to 35 year olds showed that the prevalence of untreated chlamydia and gonorrhea was 3.0% and 5.3%, respectively, with the prevalence being higher among blacks than whites.29 A recent national survey of young adults reported a prevalence of chlamydia and gonorrhea of 4.7% and 0.4%, respectively, among females, and 3.7% and 0.4%, respectively, among males.30 The prevalence of trichomoniasis among women in the general population has been reported to be 5% to 10%, whereas the prevalence among asymptomatic men usually falls below 5%.31
In our study, the prevalence of chlamydia, gonorrhea, and trichomoniasis were all higher among women than men, a pattern seen in similar studies.22,24 Some of the other STI correlates such as decreased alcohol use and not having a sex partner who has injected drugs are difficult to explain; however, given the small number of infections and the large number of variables examined, some of these associations may have occurred by chance. The small sample size, as well as the combination of all STIs into a single outcome variable, may also explain our inability to identify correlates of STIs usually identified in the literature such as exchanging sex for money or drugs and precluded our ability to identify correlates that were specifically related to 1 of the STIs under study.
This sample had a high BV prevalence that was significantly associated with douching. The only other published report of BV prevalence among drug users indicated a similarly high percentage of 61%.21 The implications of BV are important among a population with high risk of HIV infection such as this one, because BV has been observed to potentiate the transmission of HIV.6–8 In addition, BV has also been associated with pelvic inflammatory disease and ectopic pregnancy.32,33 The association of BV with vaginal douching has been shown in other studies34–36; it is hypothesized that douching may upset the natural balance of genital flora thus leading to BV. One limitation of our cross-sectional design was the inability to establish temporality between douching and BV acquisition. However, when reasons for douching were examined, few women douched to relieve vaginal symptoms and BV was not associated with douching to relieve vaginal symptoms (1.5% vs. 5.3%, P = 0.30). Other correlates of BV described in the literature such as black race34 or use of oral contraceptives35 were not observed here. In our study, there was no statistically significant difference in the proportion of black women having douched in the previous 6 months (13 of 18: 72.2%) as compared with white women (47 of 82: 57.3%; P = 0.30), which could help explain why BV prevalence was not found to be associated with race. BV has also been associated in previous literature with the acquisition of a new sexual partner37; however, this variable could not be assessed in the current study. Further research of genital infections among female drug users should include assessments of BV.
In our study population, 60% of the women had douched over the past 6 months. This percentage is high given that the 1995 National Survey for Family Growth indicated that 27% of U.S. women of reproductive age douched38 and that black women, a group commonly associated with douching, represented only 17.4% of the women in our study population. Although research has not established a causal relationship between BV and douching, the association seen in this research and other literature34–37 suggests that further research should assess the importance and implications of counseling on the reduction of douching for female reproductive health.
This study was limited by low statistical power as a result of the low prevalence of infection, which led to difficulty identifying significant correlates. The baseline questionnaire did not collect information on sexual networks and sexual mixing patterns (e.g., concurrency) that have been shown to be highly correlated with STI risk.39 In addition, the questionnaire did not collect information on existing STI symptoms; however, any participant reporting symptoms during pre- or posttest counseling was referred for medical evaluation. All behavioral questions were limited to the previous 3-month period, which may have led to misclassification of behaviors.
The community-based recruitment method of this study hopefully provided an accurate reflection of young urban IDUs. However, the potential for selection bias exists in this study because those who chose to participate in the DUIT trial may not be representative of all young drug users in Baltimore. This bias may, in part, explain the low STI and HIV seroprevalence observed in the current study. However, the utilization of a variety of recruitment techniques and the similarity of our seroprevalence data with other studies of young drug users support the representativeness of our cohort.
Despite these limitations, we documented a high prevalence of sexual risk behaviors among young IDUs in Baltimore. Our data suggest that HIV sexual risk reduction messages need to be enhanced to prevent acquisition of HIV and STIs among young drug users. In addition, further research on the importance and implications of douching-prevention messages among women at high risk for HIV infection is recommended.
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