IN THE THIRD DECADE OF the HIV pandemic, what was once a uniformly and rapidly fatal disease has been transformed into a chronic illness by advances in the understanding of HIV pathogenesis and therapeutics. In contrast, despite expenditure of considerable effort and resources, new infections continue to occur and thus, HIV prevention remains a public health priority. In the late 1980s and 1990s,1,2widespread adoption of safer sex behaviors by persons at highest risk and, in particular, men who have sex with men (MSM) contributed to declining HIV and sexually transmitted disease (STD) rates. More recently, data from STD clinics, other high-prevalence venues, and STD surveillance data document increased rates of treatable STDs in MSM, serving as biologic confirmation of research reports of the apparent resurgence of risky sexual behaviors among a portion of this group.3–11 The reasons for the observed increases in behaviors linked to HIV transmission are complex and include changes in community norms, substance use, and decreasing fear of AIDS.12,13 There has been conjecture that improved health status and an associated sense of well-being associated with highly active antiretroviral therapy (HAART) may have also encouraged tendencies toward increased sexual risk-taking among some groups of both HIV-infected14 and HIV-negative MSM.15,16 That increases in sexual risk behaviors and STD rates among HIV-infected persons now contribute to increased HIV transmission is evidenced by data that indicate that the numbers of new HIV infections (as well as STDs) in the United States are no longer declining and are even increasing in certain populations10,17–19 Because not all exposures lead to infection, incident STDs among HIV-infected persons almost certainly underestimates the prevalence of risky sex among persons with HIV; however, the prevalence of these behaviors remains incompletely characterized.
Transmission of HIV to uninfected sexual partners is not the only consequence of risky sexual behavior by persons with HIV. The potential for transmission of medication-resistant virus to infected persons is a more recently appreciated threat supported by a number of recent reports.20–22 Promotion of safer sex for persons with known HIV could prevent not only new infections, but also transmission of ART-resistant HIV strains to persons already infected with the virus, an event that could reduce or even negate the effects of HAART.
In an attempt to reverse these trends in risky behaviors and stem the resurgence of HIV infections that may follow, public health officials have increasingly emphasized STD screening and provision of HIV prevention efforts for HIV-infected populations.23,24 As sites where HIV-infected persons are typically seen for regularly scheduled visits, HIV primary care clinics offer a potentially appealing environment in which to deliver HIV transmission prevention messages, as well as to conduct STD screening. However, because most reports of increasing STDs and risk-taking have been generated in STD clinics and study cohorts, there is a need to determine the prevalence and factors associated with risk-taking behaviors among patients attending HIV clinics. This study was conducted to describe sexual and substance use behaviors and their consequences (curable STDs) among men receiving continuing care for HIV in a university-based clinic.
From November 2001 to November 2002, male patients presenting to the University of Alabama at Birmingham (UAB) 1917 HIV Clinic were approached for study participation. All HIV-infected men receiving primary care at the 1917 Clinic who were willing and able to sign informed consent were eligible for participation. After the provision of written informed consent, patients were administered a survey in a private setting to collect data on HIV treatment history, history of STD, recent substance use, partner number and type (regular, casual, or new in the past 30 days and 6 months), specific sexual behaviors over the preceding 2 months, and the presence of symptoms. History of antibiotic use within the previous 4 weeks was also collected and includes antibiotics used for routine prophylaxis against opportunistic infections as well as antibiotics for other indications. After the survey, pharyngeal and rectal (MSM only) specimens for gonococcal and chlamydial culture were obtained and urine was collected for nucleic acid amplification testing for these organisms. Patients received $15 compensation for their time and trouble. The study protocol was approved by the UAB Institutional Review Board.
Specimen Collection and Laboratory Methods
For each participant, 2 specimens, 1 each for gonococcal and chlamydial culture, were collected from the pharynx and the rectum. Swabs from pharyngeal and rectal sites were immediately inoculated onto gonorrhea culture media (GC-Lec; Becton-Dickinson, Cockeysville, MD) for pharyngeal sites and Modified-Thayer-Martin for rectal sites or chlamydial cell culture transport media using methods described elsewhere.25,26 To test for genital Chlamydia trachomatis and Neisseria gonorrhoeae infections, initial void urine specimens were collected for nucleic acid amplification testing and processed according to the manufacturer’s instructions (LCX STD Specimen Collection and Transport Kit; Abbott Laboratories, Abbott Park, IL or Gen-Probe APTIMA Combo 2 Assay transcription-mediated amplification [TMA]; Gen-Probe Inc., San Diego, CA).
A dedicated phone line was available for patients to confidentially receive their laboratory results. Patients with positive tests who did not call for their test results were contacted and informed of the need for treatment. Patients infected with gonorrhea or chlamydia received treatment in accordance with the Centers for Disease Control and Prevention STD Treatment Guidelines.27,28 All positive gonorrhea and chlamydia test results were reported to the Alabama Department of Public Health. Partner notification and treatment were strongly encouraged.
Survey data were scanned directly into the database using TeleForm software. Descriptive statistics are presented as means (standard deviation) or medians (ranges) as indicated. Comparisons of proportions by sexual activity status or partner type were performed using chi-squared or Fisher exact tests. Comparison of continuous variables were performed using Student t test. Multivariate models of risk factors for unprotected sex were developed by stepwise logistic regression, including those predictors that were significant in the univariate analysis. Site-specific STD prevalence was calculated as the proportion of positive STDs as the numerator and number of men exposed at a particular site as the denominator. For all analyses, a P value of <0.05 was considered statistically significant.
During the study period, 385 men were approached for participation and 338 (87.8%) were enrolled. Reflecting the composition of the clinic, mean age was 41 years (range, 20–78 years), most men were white (58%) or black (38%), and they had lived with their HIV diagnosis a mean of 6 years (range, 0–23 years) (Table 1). Study participants had a mean of 13.5 years of education, the majority had never married (69%), and 76% reported a history of prior STDs other than HIV infection. At the time of interview, 76% were receiving HAART and the average CD4 lymphocyte count was 348 cells/mm3 with an average viral load of log10 2.52. The majority of men (77%) reported having sex with men and 23% reported sex with women only.
Sexual Activity and Substance Use
Levels of sexual activity varied substantially among clinic attendees. Nearly 30% of patients denied all sexual activity in the preceding 6 months, whereas 71.6% (N = 242) of men acknowledged sexual activity (Table 2). Drug and alcohol use tended to occur more often and more heavily among sexually active HIV clinic attendees than those who were not sexually active over the previous 6 months (Table 2). Over 80% of sexually active participants reported alcohol use within the last 6 months as compared with 70.8% of those who were inactive (P <0.05). Similarly, among the sexually active group, use of Viagra (14% vs. 6%), ecstasy (4% vs. 0), poppers (11% vs. 1%), and stimulants (“speed”) (5% vs. 0) were more common. When ecstasy, gamma hydroxybutyrate (GHB), poppers, and stimulants were combined to create an analytic category of “party drugs,” the relationship was strengthened, with 14.5% of sexually active participants reporting use of 1 or more of these drugs in the previous 6 months compared with 2.1% of those who denied sexual activity during this timeframe (P = 0.001).
During the 2 months before study enrollment, 203 men reported sexual activity with a total of 396 (67 female and 329 male) partners (median, 1.0), for whom each participant provided detailed information on their activities with up to 2 partners (n = 262). Of these men, 15.8% (32 of 203) reported 1 or more particularly high-risk activities such as exchanging sex for drugs or seeking partners at bathhouses, parks, sex clubs, or Internet chat rooms (data not shown).
Sexual Activity and HIV Status of Partner
Disclosure of participants’ HIV infection status varied by partner type. Overall, study participants were less likely to disclose their HIV status to other (ie, casual or new) partners as compared with self-defined regular partners, regardless of partner gender. Participants failed to disclose to 45.7% of other male partners, whereas 14.3% of regular male partners were reported to be unaware of the participants’ HIV infection (P <0.05). Similarly, participants with casual or new female sexual partners failed to disclose their infection status to over half of these partners, whereas they stated they had informed over 95% of their regular female partners of their HIV infection (P <0.05) (Table 3).
Sexual Activity and Site-Specific Exposures
Sites of sexual exposure varied among sexually active study participants. Approximately one third of the sexually active group (N = 63) reported exposure at only a single mucosal site: 28 (13.8%) oral only, 30 (14.8%) penile only, and 5 (2.5%) of 203 rectal only. The remaining 140 study participants reported exposure at 2 or more sites, including: 62 (30.5%) oral and penile; 25 (12.3%) oral and rectal; 36 (17.7%) oral, penile, and rectal; and 5 (2.5%) rectal and penile. Twelve participants (5.9%) reported partners over the previous 2 months but no site-specific sexual activity, 9 (4.4%) of whom reported participation in mutual masturbation only.
Sexual Activity and Condom Use
Condoms were used inconsistently by participants and also varied by partner gender, type, and site of exposure. Partner-specific 2-month sexual activity reports revealed that for vaginal sex, <100% condom use was reported with 15 (26%) of 58 female partners (Table 4). Of the females with whom condoms were not used 100% of the time, 60% (9 of 15) were HIV-negative or of unknown HIV status. Participants also reported active oral sex with 187 partners (31 females and 156 males), with condoms used 100% of the time with only 26 (14%). Sixty-four percent of partners with whom unprotected oral sex was reported were of HIV-negative or unknown serostatus (104 of 162) and 16.7% (27 of 162) were unaware of the participants’ HIV-positive status (Table 4).
Study participants also reported 80 partners with whom they had receptive rectal intercourse during the previous 2 months, performing this activity without a condom with 31 of 80 (39%) partners, 48% (15 of 31) of whom were HIV-negative or of unknown serostatus and 13% (4 of 31) who were unaware of the participants’ serostatus. Insertive rectal sex was reported with 97 partners, 35% (34 of 97) with whom condoms were not used 100% of the time. One fourth of these partners were HIV-negative or of unknown serostatus (26.5%), and 5.7% (2 of 35) of the men were unaware that they were engaging in this high-risk activity with an HIV-positive partner (Table 4).
Multivariate Analysis of Unprotected Sex
Men performing insertive rectal sex were 5 times less likely to use condoms when the partner was HIV-positive (odds ratio [OR], 5.14; 95% confidence interval [CI], 1.90–13.91) and were 4 times more likely to engage in this activity when using party drugs, including cocaine. Conversely, the practice of unprotected rectal sex was less common among patients on HAART therapy (OR, 0.34; 95% CI, 0.11–1.01). However, patients with higher CD4 counts were more likely to engage in this activity (OR, 1.20; 95% CI, 1.02–1.42) with risk increasing by 20% for every 100-unit increase in CD4 count. No risk factors were related to unprotected oral sex in a multivariate analysis.
Sexually Transmitted Disease Prevalence
Six percent of individuals reporting sexual activity within the last 6 months were infected with gonorrhea or chlamydia at the time of study enrollment. No infections were documented in participants who denied sexual activity over the 6 months before interview. Table 5 describes STD prevalence in HIV-infected men who acknowledged sex over the 2 months before study enrollment by site of exposure.
Our study reinforces the concept that clinics providing dedicated, comprehensive care for persons with HIV infection provide access to a group of patients in need of HIV prevention interventions and represent appropriate sites to explore for implementation of these activities. At the same time, integration of transmission prevention activities into these already busy clinics will be challenging, given the diversity of behaviors and associated factors found in clinic clients. For instance, at the time of our study, not all clinic clients were sexually active, and of those who were, 41.4% reported sex with only 1 partner. In contrast, 30.2% of HIV-infected primary care patients attending the clinic acknowledged sexual activity with multiple partners, many of whom were unaware of their partner’s HIV status. Furthermore, although this study was not designed to determine what proportion of sexually inactive men subsequently became active, we presume that at least some of those who did not report recent sexual activity at the time of interview would become so in the future and that others who acknowledged single partners would have sex with new partners in the future. The continuing nature of HIV care provided in this clinic and others like it lend itself to repeated sexual behavior assessments, screening when indicated, and delivery of risk reduction interventions to those with acknowledged risks.
Our data also suggest that there are a number of behaviors that might be targeted for intervention, including condom use, disclosure of HIV infection to sexual partners, and substance use as a potential modifier of decision-making. This diversity of behavior that might be targeted represents both opportunity and challenges for intervention efforts. It is likely that some behaviors may be more amenable to change than others. Furthermore, to address these diverse behaviors, a variety of interventions that can be tailored to the needs of the specific individual and their motivation to modify their own behavior will be needed.
Among male HIV clinic patients, we found that there were both MSM and heterosexual men engaging in risky sexual behaviors. We also found that the prevalence of behaviors that might lead to HIV transmission (ie, failure to use condoms or inform sexual partners of their HIV infection) also varied by partner type when subset by whether or not partners were characterized as regular and by the type of sexual activity patients engaged in. For instance, our data suggest that some degree of risk-based stratification may be influencing condom use among sexually active men receiving care in this clinic. Participants appeared more likely to forgo barrier protection with partners on whom they practice active oral sex (86.1%) as compared with receptive rectal intercourse (35.7%). Similarly, HIV-positive primary care patients reported that a greater proportion of partners with whom they engaged in unprotected active oral sex, a “lower-risk” activity, were HIV-negative or of unknown status (63.6%) compared with the partners with whom they practiced unprotected insertive rectal intercourse (26.5%), the activity that places the partner at highest risk for HIV acquisition. Understanding the ways in which HIV-positive individuals categorize specific sexual behaviors according to risk will be important for developing interventions targeted to specific behaviors.
Our data also appear to support the proposed association of substance use and sexual risk-taking among some HIV-infected men, suggesting another potential target for behavioral intervention. In a study conducted by Stueve and others,29 19% of 3075 young MSM with a main partner reported being “high” during last sexual contact and 25.0% of these men stated that they engaged in unprotected rectal intercourse. Among men with other, nonmain partners, 29.3% reported being high and 12.3% reported unprotected rectal intercourse. Being high was associated with unprotected receptive rectal intercourse with other partners (OR, 1.66; P = 0.02). Of particular concern among HIV-positive men is the growth in popularity of recreational or “party drugs” associated with specific social and sexual environments and networks.30 Our study found an association between sexual activity within the previous 6 months and the use of specific substances including Viagra, ecstasy, poppers, and speed. These “party drugs” have been noted in other studies to be potentiators of sexual risk-taking, and in particular, their use has been associated with increased rates of unprotected rectal intercourse.12,29,31 These findings are supported by data from this study, which demonstrated that the use of party drugs was associated with the practice of unprotected insertive rectal intercourse. Our data suggest that concurrently intervening on sexual risk behaviors and substance use may be a useful component of a successful intervention.
Testing for gonococcal and chlamydial infections in this study demonstrated a substantial prevalence of treatable STDs among persons with HIV. In addition to the individual morbidity associated with the infections themselves, STDs amplify both risk for HIV transmission to others and vulnerability to acquisition of other HIV strains. Confirmation of a these infections in more than 6% of clinic attendees reinforces recommendations for regular STD screening from the Centers for Disease Control and Prevention24,32 and Institute of Medicine.33
Several limitations of our study should be acknowledged. Although 23% of our clinic’s clients are female, logistic constraints lead us to focus this initial study on male clinic clients. Additional studies to characterize the prevalence of female HIV transmission behaviors are needed. In addition, although over 1 in 20 men attending the clinic were found to have treatable STDs, this estimate is likely to be conservative. Culture, which has been shown to be substantially less sensitive than nucleic acid amplification tests for detection of gonorrhea or chlamydia in genital tract specimens,34,35 is the only currently recommended method of detection of these infections at nongenital sites. Screening with more sensitive assays, as well as for other STDs, would likely demonstrate still higher rates. As the performance of nucleic acid amplification tests is better characterized, more infections are likely to be discovered at nongenital sites of sexual exposure.
In summary, we believe that this study supports HIV primary care clinics as potentially important sites to further investigate for delivery of interventions to reduce secondary transmission of HIV, to screen for STDs, and to implement efforts to stem spread of antiretroviral therapy-resistant HIV between persons already infected with HIV. Integration of such activities into these already busy clinics will not be a simple “1-size-fits-all” effort, but holds great promise both at the level of the individual and from a public health perspective, a challenge that has inspired recent funding initiatives by both the Centers for Disease Control and Prevention and the Department of Health and Human Services Health Resources and Services Administration.23,24,36 Through these initiatives, sexual behavior assessment, STD screening, and intervention for those at risk will be vigorously pursued as an adjunct to current efforts both to care for patients with HIV and to prevent further spread of the infection.
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