Gay, bisexual, and other men who have sex with men (collectively referred to as MSM) continue to be disproportionately affected by HIV in the United States. Although MSM represent approximately 2% of the US adult population,1 they accounted for 62% of all newly diagnosed HIV infections and 79% of newly diagnosed HIV infections among adolescent and adult males in 2011.2 Sexual risk behaviors account for most HIV infections in MSM, and receptive anal intercourse without condom use has the highest risk for HIV acquisition among them.3–5 Common HIV-related risk factors among MSM include multiple concurrent sex partners,6,7 condomless anal intercourse with unknown serostatus or presumed HIV-negative partners,8,9 use of alcohol or drugs before or during sex,10 and inconsistent or incorrect condom use.11
Reducing the number of new HIV infections among MSM is a public health priority, and the use of male latex condoms for the prevention of sexually acquired HIV infection is a critical component of prevention efforts in the United States12 and globally.13 Latex condoms provide a nearly impermeable barrier to HIV,14 and epidemiological studies of HIV-discordant heterosexual couples, in which one partner has HIV infection and one does not, indicate that correct and consistent condom use is highly effective in preventing HIV infection.15,16 Estimates of condom effectiveness have been reported in the literature but mainly among heterosexual HIV-discordant couples15 and in cohort studies of clinic patients with diagnosed sexually transmitted infections17,18 that sometimes included an undefined minority of MSM.19
An analysis of HIV seroconversion studies published from 1987 to 1992 found condoms to be 90%–95% effective when used consistently during penile–vaginal intercourse.20 A large randomized community prospective study of 17,264 sexually active men and women in rural Uganda found that consistent condom use during penile–vaginal intercourse reduced HIV incidence by 63% (95% confidence interval [CI]: 12% to 85%), whereas inconsistent condom use offered no protection.21 A Cochrane review and meta-analysis of 14 cohort studies found that consistent use of condoms accounted for an estimated 80% reduction in HIV seroconversion among heterosexuals with HIV-positive partners.15 In addition, recent studies show that consistent and correct use of condoms is highly effective in reducing the risk of acquiring other sexually transmitted infections among men and women.18
In contrast to studies of heterosexuals, a review published in 199722 yielded only 1 study that reported an estimate of the effectiveness of condom use during penile–anal intercourse among MSM. In a cohort of 2915 HIV-seronegative MSM from 4 centers of the Multicenter AIDS Cohort Study followed every 6 months for 24 months, the HIV seroconversion rate was significantly lower among men who reported using condoms with all of their sex partners compared with men who reported using condoms with none of their sex partners (0.7% vs. 2.4%, respectively).23 Based on these incidence estimates, condom effectiveness for “always use” versus “never use” is computed to be 70.8%. A recent meta-analysis by the World Health Organization of 5 observational studies assessing condom effectiveness among MSM in developing countries estimated a 64% reduction in HIV acquisition risk (95% CI: 32% to 80%).24
There is a critical need for studies to investigate condom effectiveness according to consistency of use during penile–anal intercourse among MSM. This article reports analyses to estimate condom effectiveness among MSM based on data from 2 large prospective HIV prevention trials that assessed condom use and HIV serostatus at standard intervals over multiple years. The article also compares the condom effectiveness estimate for MSM based on the current analyses to the published estimate of condom effectiveness (80%) from a meta-analysis of cohort studies of heterosexuals.15
We identified existing data sets from 2 HIV prevention trials that enrolled HIV-uninfected MSM in the United States, which collected both risk behavior data and HIV test results at standard intervals (every 6 months) and had at least 100 HIV seroconversions over the course of the trial. With data from the VAX 00425 and Project EXPLORE trials,8 in each data set, we modeled condom effectiveness in preventing HIV seroconversion among MSM engaging in receptive or insertive anal intercourse with at least 1 HIV-positive partner. Our analyses focused on estimating the effectiveness of condoms in reducing HIV incidence among MSM who reported that they always used condoms (ie, consistent users) compared both with those who reported they never used condoms and with those who reported sometimes using condoms. We estimated condom effectiveness in each data set separately and in both data sets combined.
The VAX 004 trial enrolled HIV-uninfected MSM from 57 US sites during 1998–1999 into a randomized placebo-controlled trial of a recombinant HIV-1 envelope glycoprotein subunit (rgp120) vaccine that proved ineffective at 36 months of follow-up.25 We excluded participants who reported injection drug use at any point before or during the trial, non-US participants, participants who were found to have HIV infection at baseline, and participants with no study visit after enrollment, as well as visit records during any interval during which participants reported having sex with women. Self-reported condom use was assessed by use of standard interviewer-administered questionnaires at baseline and every 6 months thereafter (see Table S1, Supplemental Digital Content, http://links.lww.com/QAI/A601). HIV-1 status was determined at each study visit by a standard HIV-1 enzyme-linked immunosorbent assay; enzyme immunoassay-positive tests underwent confirmatory immunoblot assay; and for those confirmed antibody positive at any visit, a stored serum specimen from the previous study visit was tested by a highly sensitive and specific nucleic acid-based amplification test. After applying the exclusion criteria, 4492 MSM with 23,567 visit records were eligible for analyses, of whom 315 (7.0%) acquired HIV infection. Among all men in the analyses, 2167 MSM (48% of the included sample) reported any anal sex with an HIV-positive partner at any time during the study, of whom 154 (7.1%) acquired HIV infection. Of men reporting any anal sex with an HIV-positive partner, 1343 (62%) reported any receptive anal sex with an HIV-positive partner, and 1930 (89%) reported any insertive anal sex with an HIV-positive partner (see Figure S1, Supplemental Digital Content, http://links.lww.com/QAI/A601).
Project EXPLORE enrolled HIV-uninfected MSM from 6 US cities during 1999–2001 into a randomized controlled behavioral intervention trial in which the active intervention arm did not significantly reduce HIV incidence compared with the control intervention arm.8 We excluded participants who reported injection drug use at any point before or during the trial, participants who were found to have HIV infection at baseline, participants with no study visit after enrollment, as well as visit records for any intervals during which participants reported having sex with women. At baseline and follow-up visits every 6 months, audio computer-assisted self-interviewing was used to collect sexual behaviors (see Table S1, Supplemental Digital Content, http://links.lww.com/QAI/A601). At each visit, blood samples were tested for HIV antibodies by enzyme-linked immunosorbent assay; if positive, specimens were retested in duplicate, and repeatedly reactive samples were confirmed by Western blot assay or immunofluorescence assay.
After applying the exclusion criteria, 3233 MSM with 18,884 visit records were eligible for analyses; of whom 195 (6.0%) acquired HIV infection. Among all men in the analyses, 1323 MSM (41% of the included sample) reported any anal sex with an HIV-positive partner at any time during the study, of whom 71 (5.4%) acquired HIV infection. Of men reporting any anal sex with an HIV-positive partner, 871 (66%) reported any receptive anal sex with an HIV-positive partner and 1095 (83%) reported any insertive anal sex with an HIV-positive partner (see Figure S2, Supplemental Digital Content, http://links.lww.com/QAI/A601).
In analyses that used the combined trial data sets, after exclusions above, we included 7725 MSM with 42,451 visits before selecting only those who reported sex with any HIV-positive partner at any study visit. There are 3490 MSM who reported sex with an HIV-positive partner during 9246 visits, and among these men, 225 acquired HIV infection (6.4%) (see Figure S3 Supplemental Digital Content, http://links.lww.com/QAI/A601).
We included MSM in both the active and control arms of the trials. We believe this is appropriate as (1) our analysis was designed to determine the effectiveness of self-reported condom use on HIV incidence regardless of which intervention was received and (2) in both trials, statistically significant differences in HIV incidence were not found when comparing the intervention and control arms. The VAX 004 and Project EXPLORE questionnaires included comparable variables to assess condom use by consistency (always, sometimes, and never) and by partner serostatus (see Table S1, Supplemental Digital Content, http://links.lww.com/QAI/A601).
All analyses were conducted using 3 analysis data sets: EXPLORE, VAX 004, and EXPLORE and VAX 004 combined. We compared the distribution of demographic characteristics for the EXPLORE and VAX 004 data sets using χ2 test statistics. The demographic factors common to both data sets are age (categorized as ≤25, 26–30, 31–35, and ≥36 years), race/ethnicity (categorized as non-Hispanic white, non-Hispanic black, Hispanic, Asian/Pacific Islander, other/unknown), education (categorized as <high school, high school, college, graduate school), and region (categorized as Northeast, Midwest, South, and West). We calculated the percentage of condom use during anal sex acts for each 6-month interval and the total number of HIV-positive partners by receptive, insertive, and the combined receptive and insertive anal sex categories for both the EXPLORE and VAX 004 data.
We computed the HIV incidence per 100 person-years (PY), where PY was calculated by summing over all intervals for all subjects in the condom risk group categories of never, sometimes, and always. In addition, we calculated the total number of anal sex acts per condom risk group category (always, sometimes, or never use) among men reporting an HIV-positive sex partner. The incidence and corresponding 95% CI were calculated using a Poisson regression model with the PY as the offset in the Poisson model. The risk per sex act and 95% CI were estimated using a logistic regression model. In addition, the condom effectiveness based on risk per sex act and 95% CI for “always” versus “never” condom use was calculated using a log-binomial model.
We estimated condom effectiveness using receptive anal sex only, insertive anal sex only, and combined receptive and anal sex. We categorized condom use consistency for each subject for each 6-month interval as either, “always”, “sometimes”, or “never” based on the percentage of time they used a condom during an anal insertive or receptive sex act. To be categorized as “always”/“never” condom use, the subject must have reported condom use during all or none of the anal sex acts (respectively) with the HIV-positive partner during the 6-month interval. Subjects were categorized as “sometimes” condom use if the proportion of time they used a condom during a 6-month interval was between 0 and 1. For each 6-month interval, a subject was coded as HIV-positive or HIV-negative based on serological test result at the visit marking the end of the previous study interval and analyzed using an interval censored time-to-event model. A complementary log–log model was used to model the interval censored time to HIV seroconversion. The hazard ratio was estimated for comparison of the different categories of condom use, and effectiveness was defined as 100 × (1 − hazard ratio). We estimated condom effectiveness using both univariable and multivariable models. The univariable models only included the condom consistency group and interval. The multivariable model additionally controlled for age, race/ethnicity, education, and region regardless of statistical significance in the univariable models. All analyses were conducted using SAS version 9.2, and all P values <0.05 were considered statistically significant.
A secondary analysis was conducted to compare the condom effectiveness estimates identified in this study for MSM during anal intercourse with HIV-positive partners to published condom effectiveness estimates based on 14 prospective studies for heterosexual men and women in HIV-discordant couples reported in the Cochrane review.15 The Cochrane review reported 2 estimates of condom effectiveness: one based on a meta-analysis of all studies reporting effectiveness results of “always” use versus “never” use, and a second based on a subset of studies with longer than average follow-up times. We compared our unadjusted estimate of condom effectiveness (ie, not adjusting for study factors of age, race/ethnicity, education, and region) to the 2 Cochrane estimates using a Poisson model with PY as the offset and study, condom use (“always”, “never”), and the interaction of study and condom use in both models.
The demographic characteristics of the combined trial populations indicated the majority of participants were aged 31 years or older at enrollment, non-Hispanic white, and reported having a college diploma or more advanced degree (Table 1). However, participants in Project EXPLORE were significantly more likely to be younger, non-white, report a higher education level, and reside in the Northeast or West than participants in the VAX 004 trial.
Per-Act Transmission Risk Findings
The risk of HIV infection per act of anal intercourse reported with an HIV-positive partner was significantly higher for never condom use than always condom use in both trials for reported receptive anal sex (EXPLORE: 0.0111 vs. 0.0015; P < 0.001; VAX 004: 0.0041 vs. 0.0022; P = 0.0032) and for any anal sex (receptive or insertive) (EXPLORE: 0.0035 vs. 0.0007; P < 0.0001; VAX 004: 0.0018 vs. 0.0010; P = 0.0043) (Table 2). The per-sex act risk of HIV infection was significantly higher for never condom use than for always condom use in Project EXPLORE participants during reported insertive anal sex (0.0027 vs. 0.0011; P = 0.025) but not for VAX 004 participants (0.0020 vs. 0.0013; P = 0.051).
Condom Effectiveness Estimate
In the multivariable analysis of data combined from the 2 trials, controlling for study, age, race/ethnicity, education, and region of residence, the effectiveness of condom use for men reporting anal sex with an HIV-positive male partner was estimated comparing self-reported “always use” to “never use.” Estimated condom effectiveness was 72.3% (95% CI: 60.7% to 80.5%) for receptive anal sex, 62.9% (95% CI: 46.3% to 74.3%) for insertive anal sex, and 70.5% (95% CI: 58.2% to 79.2%) for any receptive or insertive anal sex (Table 3). The estimated effectiveness for condom use during insertive anal sex was not statistically different from that for receptive anal sex (P = 0.17).
Self-reported “always use” to “sometimes use” was significantly protective in multivariable analyses in each trial separately and when combined for any anal sex reported with HIV-positive partners. Condom effectiveness comparing “sometimes use” and “never use” was not significantly protective in either trial or both combined for any anal sex reported. All estimates of condom effectiveness were lower in VAX 004 than in EXPLORE, but the pattern across sexual activity was the same (Table 3).
Although all analyses reported here included only US MSM, in a sensitivity analysis, when data from men at non-US sites in the VAX 004 trial were included, there was no statistically significant difference in estimated condom effectiveness for men reporting any receptive or insertive anal sex (data not shown).
Consistency of Condom Use
Table 4 presents the results of analyses of condom use consistency for reported partners of any HIV status (positive, negative, or unknown) by trial and anal sex act. Among MSM in the 2 trials combined with male partners of any HIV status, for at least one 6-month interval, 65.0% reported always condom use, 73.8% sometimes condom use, and 40.2% never condom use for receptive or insertive anal sex. Across all their study visits, 16.4% reported always use, 14.3% sometimes use, and 4.9% never use. These rates were similar for MSM in each of the 2 trials (Table 4).
As shown in Figure 1, for each 6-month study interval, the proportion of MSM reporting condom use during any anal sex with HIV-positive or unknown status partners was consistently higher than that reported with partners believed to be HIV-negative.
Comparison of Findings to Cochrane Review
Estimated condom effectiveness estimates for consistent use based on HIV incidence rates were reported in the Cochrane review15 as 82.9% (95% CI: 66.7% to 91.2%) for the entire set of included studies and 80.2% (95% CI: 56.3% to 91.0%) for the subset of studies reporting longer follow-up times (Note that the 95% CIs were not published but were calculated from the data provided in the Cochrane review). The adjusted (Table 3) estimated effectiveness of condom use among MSM with HIV-positive partners based on estimated HIV incidence in the combined EXPLORE and VAX 004 samples is 69.2% (95% CI: 58.0% to 80.3%). Our estimated effectiveness did not differ significantly from the Cochrane review estimate for all studies (estimated percentage difference is −13.75, 95% CI: 2.59 to 30.09, P = 0.10) or the subset of studies reporting longer follow-up times (estimated percentage difference is −11.00, 95% CI: 31.04 to 9.05, P = 0.27).
Given that the proportion of new HIV infections in the United States annually is greatest for MSM, it is important to have robust and accurate estimates of the effectiveness of condoms and other prevention methods that are specific to this population. This study was able to assess condom effectiveness among MSM who reported having HIV-positive partners in multiple sites in 2 large prospective cohorts.
The point estimate in our analysis of condom effectiveness when “always” used by MSM during anal sex with any HIV-positive male partners is 70%, modestly less than the 80% estimate for condoms when “always” used by heterosexual HIV-discordant couples. Although these point estimates do not differ by tests of statistical significance, it is more appropriate to use the MSM-specific point estimate of 70% effectiveness for discussions and models involving anal sex among MSM than to continue use of the heterosexual 80% effectiveness point estimate for MSM.
This study found that inconsistent (“sometimes”) condom use with HIV-positive male partners over months to years offers minimal or no protection, underscoring the importance of the inclusion of messaging by their HIV prevention providers, which supports the adoption and continuation of consistent condom use for MSM. In these analyses and in many previous epidemiologic studies, inconsistent condom use with partners of any HIV status is more frequently reported by MSM than consistent condom use.6,26 Although condom use is often measured over short time frames (eg, at last sex, in past 3 months), rates of “always” use fall significantly when measured over longer time frames.7,19 HIV prevention providers should inform MSM who are not using condoms consistently of the low protection offered by inconsistent use, and additional prevention options should be considered.
There are limitations in the data available that affect this analysis. Self-reports of condom use are not validated nor is self-report of partner HIV status. It is likely that some partners believed to have been HIV-negative may have unrecognized HIV infection. No data are available about the treatment status of sex partners reported to have HIV infection. The analysis therefore cannot account for HIV acquisition through sex with partners who had unrecognized HIV infection (ie, were reported as negative or unknown HIV status) or those whose partners had suppressed viral load. In addition, because most MSM engaged in multiple sexual behaviors, it is not possible to assess condom effectiveness among MSM who had only 1 type of sexual behavior (eg, oral sex but no anal sex, insertive anal sex but no oral or receptive anal sex). Nonetheless, we provide a robust estimate of 70% effectiveness of condoms for prevention of HIV acquisition among MSM reporting anal sex with HIV-positive male partners (with or without other sexual behaviors). This finding is consistent with the prior understanding that for all sexual exposures, among both MSM and heterosexuals, condoms offer substantial but partial protection against HIV acquisition when they are consistently used.
Our analysis also found that among MSM in the 2 trials, all of whom received sustained behavioral interventions, a low proportion (16.4%) reported “always” (consistent) condom use for all sexual events over a year or longer, regardless of partner HIV status. MSM rarely reported anal sex with only HIV-positive partners. However, the analysis found that the frequency of condom use is greater with partners reported to have HIV infection or unknown HIV status and lower with partners of negative HIV status. The substantial protective effectiveness of condoms cannot be fully realized without their consistent use over prolonged periods of sexual activity and potential HIV exposure.
Our findings of strong but partial effectiveness for consistent condom use, minimal effectiveness for inconsistent condom use, and low rates of consistent condom use over 1–2 years, even among persons receiving high quality risk-reduction counseling, may contribute to a better understanding of the persistent rates of HIV infection among MSM in the United States, despite current levels of condom use promotion and provision. A recent analysis of data from MSM who were interviewed in the 20 cities participating in the National HIV Behavioral Surveillance System found that reported anal sex without condoms any time during the previous 12 months increased from 45% in 2005, to 54% in 2008, and 57% in 2011 (χ2 test for trend, P < 0.001).27 From a public health perspective, these data suggest the need to further intensify efforts to educate HIV-uninfected MSM and improve their ability to accurately assess both their risk of HIV acquisition and the effectiveness of their current use of condoms (consistently or inconsistently) during anal sex. These data also suggest a need to provide access to additional highly effective HIV prevention tools and strategies, including more frequent HIV testing (including testing as couples) and daily oral antiretroviral preexposure prophylaxis when indicated.28 In addition, these findings may be useful to researchers modeling the impact and cost-effectiveness of behavioral interventions whose outcomes are measured by changes in reported condom use and to those modeling combinations of biomedical and condom-based behavioral prevention methods to reduce the rate of new HIV infections among MSM.
The authors thank the study teams and participants of the VAX 004 and EXPLORE trials.
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