Reports since the mid-1990s have documented a resurgence of high-risk sex and sexually transmitted diseases (STDs) among men who have sex with men (MSM), 1–7 and new approaches to HIV prevention are urgently needed in this population. The US Centers for Disease Control and Prevention (CDC) recently announced the Serostatus Approach to Fighting the HIV Epidemic (SAFE) and the Advancing HIV Prevention Initiative. 8,9 These initiatives signal a change in the emphasis of HIV prevention, stressing the importance of prevention among persons already infected with HIV, intensified prevention among high-risk HIV-negative persons, and early HIV diagnosis.
Developing a system to identify persons in greatest need of prevention services during clinical encounters is a critical step in implementing the sort of prevention approach now being promoted by the CDC. To date, however, little operational research has been done to establish practical mechanisms to identify persons within identified risk groups at high risk for acquiring or transmitting HIV. Recent studies conducted in developed and developing nations have examined partner characteristics as risk factors for transmission and acquisition of STDs, including HIV infection, 10–16 and some reports have emphasized that many MSM engage in “negotiated safety,” altering their sexual behaviors based on their partners' HIV status. 17–21 These studies imply a need to integrate questions about partners and sexual behavior into clinical risk assessments. STD clinics are one important setting to identify persons in need of prevention interventions. Risk assessments used in these clinics vary widely but seldom include questions about sex partners' HIV status. 22
In 2001, we began systematically asking all MSM seen in our STD clinic about their use of condoms for anal sex, stratified by the HIV status of their sex partners. In adopting this approach, we sought to establish the feasibility of integrating more comprehensive questions about partner HIV status into routine sexual history taking so as to define the extent to which HIV-seropositive MSM seeking care in our STD clinic might be exposing others to HIV and to identify the group of HIV-negative MSM who might be at highest risk of acquiring HIV.
Study Population and Data Collection
The study population was composed of all MSM seen for new problem visits at the Public Health–Seattle and King County (PHSKC) STD Clinic between October 1, 2001 and March 31, 2003. All data were collected by clinicians as part of routine clinical encounters using a structured medical record form and were then recorded in the clinic's electronic medical record. (The PHSKC STD Clinic sexual history forms can be viewed at http://depts.washington.edu/cfar/researchtools.) Clinicians asked patients if they have had sex with men, women, or both men and women in the preceding year; if they have ever been tested for HIV; and the date and result of their most recent HIV test. In addition, MSM patients were asked whether they had anal sex in the preceding year with HIV-negative men, HIV-positive men, or men whose HIV status they did not know and whether they used condoms “always,” “usually,” “sometimes,” or “never” with partners of each HIV status category. These questions were asked separately for insertive and receptive anal intercourse. Finally, patients were asked if they have ever used methamphetamine, cocaine, ecstasy, or amyl nitrite (“poppers”) and whether they had ever engaged in anonymous sex. If they acknowledged any of these behaviors, they were asked when they last did so.
Definitions of Potential HIV Transmitters and Potentially HIV-Exposed Men
We defined potential HIV transmitters as men who acknowledged being infected with HIV and reported engaging in insertive or receptive anal sex without a condom (unprotected anal intercourse [UAI]) in the preceding year with at least 1 man who they knew to be HIV-negative or whose HIV status they did not know. Potentially HIV-exposed MSM were men who stated they were HIV-negative or had not been tested for HIV and who engaged in UAI in the preceding year with at least 1 man who they knew to be HIV-positive or whose HIV status they did not know.
Statistical Methods and Analysis
Only a single new problem visit was analyzed for each patient. To maximize the number of men newly diagnosed with HIV for analysis, if patients were seen more than once and tested positive for HIV, we included the visit at which they first tested HIV-positive in the analysis. Otherwise, we used the first patient visit for which data were sufficiently complete to allow determination of whether or not HIV-positive patients were potential transmitters or whether HIV-negative patients were potentially exposed or not exposed. Because data collection on last drug use was incomplete, we analyzed drug use variables as ever use versus never use.
Rectal gonorrhea and chlamydial infections were diagnosed by culture using modified Thayer-Martin medium and McCoy cell culture, 23 respectively. Clinic policy was to obtain rectal specimens on all MSM who acknowledged receptive anal intercourse in the preceding year. Urethral gonorrhea and chlamydial infection was diagnosed by Gram stain (gonorrhea only), culture of urethral specimens, or LCx ligase chain reaction assay (Abbott Diagnostics, Oak Park, IL) or Aptima Combo 2 (Gen-Probe, San Diego, CA) of urine specimens. Because the prevalence of asymptomatic urethral gonorrhea or chlamydial infection in MSM attending our clinic is low, 24 asymptomatic MSM are tested for urethral infection only if they present as contacts to gonorrhea or chlamydial infection or if they are found to have signs of urethritis on physical examination.
We compared continuous variables using t tests and dichotomous variables using logistic regression. To construct multivariate logistic regression models, we performed stepwise backward elimination of variables with P > 0.05. All statistical procedures were performed using the SAS statistical package (SAS Institute, Cary, NC).
This analysis was undertaken as a program evaluation. A certificate of exemption was obtained from the University of Washington Human Subjects Division.
Between October 1, 2001 and March 31, 2003, clinicians evaluated 2032 MSM at a total of 2826 new problem visits. Clinicians recorded self-reported HIV status for 1953 (96%) of these men, of whom 234 (12%) stated they were HIV-positive. Among the remaining 1719 men who denied already knowing that that they were HIV-positive, 1570 (91%) stated they were HIV-negative and 149 (9%) had never been tested.
Potential HIV Transmitters
Of the 234 HIV-positive MSM seen in the clinic, data were sufficiently complete to classify 217 (93%) as either potential transmitters or not potential transmitters. Of these 217 men, 93 (43%) were potential HIV transmitters, of whom 42 (47%) reported UAI with partners of unknown HIV status but not HIV-negative partners, 20 (22%) reporting having UAI with a partner who was HIV-negative but not with persons of unknown HIV status, and 27 (30%) reported having had UAI both with HIV-negative partners and with partners of unknown HIV status.
Table 1 compares the 93 potential HIV transmitters with 124 nontransmitters. In bivariate analysis, being a potential HIV transmitter was associated with history of >5 sex partners in the preceding year, anonymous sex in the preceding year, amyl nitrite use, methamphetamine use, and ecstasy use. Diagnosis with a bacterial STD was more common among potential transmitters but was not statistically significant. Potential transmitters and nontransmitters did not differ significantly by age, race, reason for clinic visit, anal sexual repertoire (insertive and receptive vs. insertive only or receptive only), or use of antiretroviral medications. In multivariate analysis, the only variables independently associated with being a potential transmitter were having >5 sex partners in the preceding year and a history of using methamphetamine.
Persons Potentially Exposed to HIV
Among 1719 MSM who denied knowing they were HIV-positive, data were sufficient to classify 1580 men (92%) as potentially exposed or not potentially exposed to HIV. Of these 1580 men, 433 patients (27%) were potentially exposed to HIV in the preceding 12 months. Table 2 compares these men with the 1147 men (73%) who were classified as not potentially exposed. In multivariate analysis, potential exposure to HIV was independently associated with having >5 sex partners in the preceding year, anonymous sex, diagnosis of a bacterial STD (gonorrhea, chlamydial infection, or primary or secondary syphilis) at time of the clinic visit, and a history of injection drug use.
Sexual Mixing and Repertoire of Anal Sexual Behavior
Complete information on anal sexual practices and partner HIV status information during the preceding 12 months was recorded for 1365 (79%) of the 1719 patients who reported not having been previously diagnosed HIV-positive at the time of their clinic visit and for 192 (82%) of the 234 men who reported being HIV-positive. Among men who acknowledged being HIV-positive, 25 (13%) had been diagnosed with HIV in the preceding year; the remaining 167 men had known their HIV status for more than a year. Table 3 presents data on anal sexual practices, condom use, and sexual mixing by HIV status for men who reported being HIV-negative or not having been tested for HIV and for the 167 men known to be HIV-positive for ≥1 year. There was substantial assortative mixing by HIV serostatus. For example, 96 (58%) of the 167 HIV-positive MSM reported having UAI with an HIV-positive partner compared with 85 (6%) of 1365 HIV-negative MSM who reported the same behavior. Conversely, 31 (19%) of 167 HIV-positive MSM reported UAI with an HIV-negative partner compared with 580 (42%) of 1365 HIV-negative MSM. Differences were much smaller in exposure to partners of unknown HIV status; 32% of HIV-positive men and 25% of HIV-negative men reported UAI with partners of unknown HIV status.
HIV Testing Results
Confidential HIV testing was done in 881 (56%) of the 1580 MSM not previously known to be HIV-positive; 35 (4%) tested positive. (Anonymous HIV testing was carried out in some men who did not undergo confidential HIV testing; these results could not be linked to charts for analysis.) Compared with those who were tested, those who declined confidential testing were more likely to report having previously been tested in the preceding year (75% vs. 55%, odds ratio [OR] = 2.4, 95% confidence interval [CI]: 1.9–3.0) but comparably likely to report having been potentially exposed to HIV (26% vs. 29%, OR = 0.89, 95% CI: 0.69–1.1).
Twenty-four (9.6%) of 251 potentially exposed MSM and 11 (1.7%) of 620 not potentially exposed men tested HIV-positive (OR = 5.8, 95% CI: 2.8–12.1). In bivariate analysis, testing HIV-positive was also significantly associated with diagnosis of bacterial STD at the same clinic visit (OR = 2.4, 95% CI: 1.2–4.9), injection drug use (OR = 3.6, 95% CI: 1.4–9.0), African-American race (OR = 2.8, 95% CI: 1.0–7.5), and methamphetamine use (OR = 2.3, 95% CI: 1.0–5.0). Use of amyl nitrite was more common among persons with newly diagnosed HIV, although this association was not significant (OR = 2.1, 95% CI: 0.97–4.4). Testing HIV-positive was not significantly associated with age, reason for clinic visit, numbers of sex partners, anonymous sex, ecstasy use, anal sexual repertoire (insertive and receptive vs. insertive or receptive only), or time since last HIV test (data not shown). In multivariate analysis, testing HIV-positive was associated only with potential exposure to HIV. Men who denied all UAI and those who reported having UAI with HIV-negative partners only had a comparable risk of testing HIV-positive; 7 (1.8%) of 388 MSM who denied any UAI in the preceding 12 months and 4 (1.7%) of 240 who acknowledged UAI only with HIV-negative partners in the preceding 12 months tested HIV-positive (OR = 0.92, 95% CI: 0.27–3.2).
Performance of Risk Assessment Criteria in Identifying New HIV Diagnoses
Table 4 presents the sensitivity, specificity, and positive predictive value (PPV) of various risk assessment criteria for identifying persons who tested HIV-positive for the first time (n = 35). Twelve-month risk assessments were more sensitive for HIV diagnosis than 2-month risk assessments. UAI in the preceding 12 months was 80% sensitive for identifying men with HIV but only 45% specific; most men (56%) reported having UAI in the prior 12 months. Incorporation of partner HIV status improved risk assessment specificity but decreased sensitivity; UAI with an HIV-positive partner or partner of unknown status (our criteria for potentially being exposed to HIV infection) was 69% sensitive and 73% specific for new HIV diagnosis and had a PPV of 9.5%.
New HIV prevention strategies among MSM are urgently needed. The CDC's 2001 HIV counseling and testing guidelines recommend a client-centered approach, with face-to-face pretest and posttest counseling. 25 The CDC also recommends risk screening of populations at high risk, with referral to prevention counseling based on risk screening results. Systematic risk assessment criteria for MSM have not been developed or evaluated, however, and, to date, STD clinic–based HIV prevention counseling has probably been relatively uniform in its application. The CDC is now advocating a more diversified approach to prevention, with enhanced integration of HIV testing into routine clinical care, and a new emphasis on applying prevention interventions to HIV-positive as well as HIV-negative persons. 8,9 Such a system might triage patients to interventions of variable content and intensity based on risk and HIV status. With this end in mind, we designed and implemented a new approach to assessing HIV risk among MSM in our STD clinic.
We found that clinicians could incorporate questions about sexual behavior stratified by partner HIV status into routine sexual histories and that substantial proportions of MSM attending our STD clinic acknowledge placing themselves or others at risk for acquiring HIV. UAI with an HIV-positive partner or with a partner of unknown HIV status was strongly associated with a new HIV diagnosis, and incorporating partner HIV status into a routine sexual history improved the specificity and predictive value of the HIV risk assessment with only a moderate loss in sensitivity. The information gained through such risk assessment provides a logical point of entry for subsequent risk reduction counseling and prevention interventions.
Although any UAI is typically used by clinicians as a marker of risk, several recent studies have reported that many MSM engage in “negotiated safety,” altering their condom use based on knowledge of their own and their partners' HIV status. 17–21 Our finding of higher rates of UAI in HIV-concordant partnerships is consistent with those observations. We also found that many MSM adopt safer sexual behaviors with partners who are HIV discordant or whose status they do not know. Specifically, HIV-positive men less often engage in insertive UAI with HIV-negative partners, and HIV-negative men less often have receptive UAI with HIV-positive partners. The significance of these observations is underscored by the strong association we observed between new HIV diagnosis and UAI with an HIV-infected partner or partner of unknown HIV status. These findings validate patients' reporting of partner HIV status as a risk factor for HIV and demonstrate the utility of integrating questions about sex partners into clinical risk assessments. The similar prevalences of new HIV diagnoses in men who denied all UAI (1.8%) and men who acknowledged UAI with HIV-negative partners only (1.7%) during the previous year—both prevalences much lower than for the potentially exposed group—suggest that restricting UAI to partners believed to be HIV-negative is protective, although a substantial risk of HIV persists.
The large differences in behavior we observed among HIV-negative MSM based on their partners' HIV status are consistent with several previous studies that showed higher rates of UAI among MSM in HIV-concordant partnerships than in discordant partnerships 19,26–29 and suggest that disclosure of HIV status results in the adoption of safer sexual behaviors. Conversely, a study of 206 HIV-positive MSM in an HIV clinic found that men were not more likely to engage in safe sex with partners to whom they disclosed their HIV status than with partners to whom they did not disclose their HIV status. 30 Although it is clear that disclosure does not always lead to safer behaviors, particularly between discordant men in a primary relationship, the preponderance of evidence indicates that MSM adopt safer behaviors in HIV-discordant partnerships. More research is needed on means to increase disclosure and to assess the impact of disclosure on sexual behavior.
Many HIV-positive MSM in our clinic (40%) reported UAI in the preceding year with a man of opposite or unknown HIV status. The persistence of high-risk sexual behavior 6,31–41 and the occurrence of high rates of STDs 4,42–53 among some persons infected with HIV have been recognized for at least 15 years. The frequency of such behaviors may be increasing. 4 Among HIV-infected MSM, we observed an association between methamphetamine use and UAI with discordant partners or partners of unknown HIV status. Methamphetamine use has previously been identified as a risk factor for HIV among injection drug–using MSM and non-injection drug–using MSM. 54–57 In our clinic, it also appears to be a risk factor for transmitting HIV to others.
Our study has several limitations. First, our findings may not be generalizable, especially to populations of MSM outside STD clinics. The utility of incorporating partner HIV status into standard risk assessments should be evaluated in MSM in other geographic areas and clinical settings. Second, we relied on patient self-report of HIV status and partner status to define patients as potential transmitters or as being potentially exposed to HIV. We believe that it is unlikely that the strong association we observed between newly testing HIV-positive and UAI with HIV-positive or status unknown partners is a consequence of patients' misrepresenting their prior testing experience. Given the social undesirability of acknowledging UAI with someone of opposite or unknown HIV status, however, it seems likely that our approach using face-to-face interviews may have underestimated the proportion of MSM who are potential transmitters or potentially exposed. Third, the risk assessment we used is fairly complex, involving separate questions for insertive and receptive anal intercourse by each category of partner HIV status. We believe the detail provided by this approach is useful in helping patients and counselors develop a risk reduction plan, but this belief has not been formally tested, and our approach may be too time-consuming for some clinics to use without additional resources. On the other hand, our findings suggest that simply asking about any UAI with a partner of discordant or unknown HIV status may be relatively sensitive and specific for identifying MSM at greatest risk for undiagnosed HIV infection and might easily be incorporated into standard HIV risk assessments. Finally, although we observed a strong association between new HIV diagnosis and UAI with a partner of discordant or unknown HIV status, we do not currently have enough data to assess whether uninfected persons who acknowledge this behavior actually have a higher rate of HIV acquisition, a finding that would demonstrate more definitively the need to target this group for intensified intervention. However, cohort studies of MSM have found that baseline sexual risk taking is associated with future sexual risk taking. 58,59
Among the most urgent questions in HIV prevention is how to reduce risk-taking behavior of both HIV-positive and HIV-negative MSM. We have demonstrated that incorporating partner HIV status into routine sexual histories obtained by clinicians from MSM in an STD clinic identifies potential HIV transmitters as well as those at highest risk for new HIV diagnosis. Public health programs and research based in STD clinics should incorporate partner HIV status into risk assessments for MSM and should evaluate prevention interventions directed toward those identified as being at greatest risk. Where practical considerations preclude detailed behavioral histories, we believe that at a minimum, all clinicians should routinely ask their HIV negative MSM patients a single question: “In the last year, have you had anal sex without a condom with anyone who was HIV-positive or whose HIV status you did not know?” HIV positive patients should be asked about UAI with partners who are HIV negative or of unknown HIV status. Obtaining a history of drug use, particularly of methamphetamine, also should be routine. Extending this research to heterosexual populations at high risk for HIV is an additional priority.
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