Introduction
Some recent reports on HIV seroprevalence and self-reported sexual behaviors suggest that the epidemic of infection with HIV-1 may be waning among men who have sex with men (MSM). In a study of HIV seroprevalence among MSM attending clinics for sexually transmitted diseases (STD) in New York City, the HIV seroprevalence declined from 53 to 34% between 1988 and 1993, with the most dramatic decline among white MSM [1]. A brief self-administered questionnaire completed by 7650 MSM in New York City in 1998 found that the percentage of MSM using condoms during their first episode of anal intercourse increased from 10% in 1980 to 80% in 1993, and remained at this level to 1998. Although 39% reported having unprotected anal sex, only 11% were doing so with a partner of different or unknown HIV serostatus (T. Mayne, personal communication). In contrast, data from other cities indicate increases in unsafe sexual behavior. In San Francisco, a survey using a brief peer-administered questionnaire found that the percentage of MSM reporting unprotected anal sex increased between 1994 and 1997, with the largest increases among MSM 25 years of age and younger. Concurrently, the incidence of rectal gonorrhea reported by the local health department increased during the same time period, validating the self-reported sexual behavior [2]. During a period of reintroduction of syphilis in Seattle in 1997-1998, two-thirds of the cases were MSM [3]. Other recent studies from San Francisco and Vancouver report similar increases in unsafe behaviors [4,5].
The Young Men's Survey in New York City (YMS-NYC), as described in this paper, provides important contemporary data about the status of the HIV epidemic in a subpopulation of very young MSM in New York City, the city reporting the largest number of AIDS cases among MSM in the United States [6]. Few studies to date include young MSM under the age of 22 years [7-15]. For example, in two large recent surveys of MSM in New York City, less than 10% of the study population were under 22 years of age [1,7]. Furthermore, the study included a large proportion of minority young MSM, a group for which limited data are available [7-15].
Materials and methods
The YMS-NYC is part of a national survey conducted in seven metropolitan areas [16]. The survey was designed to estimate the prevalence of HIV antibody, markers of hepatitis B virus (HBV) infection and syphilis, and the frequency of risk behaviors among MSM aged 15-22 years who attend public venues such as bars, dance clubs, business establishments, social organizations, sex establishments and street locations. The survey was conducted in accordance with the national protocol [16].
Potential venues and their time periods of high attendance were identified through interviews with community leaders, service providers, venue owners and other community informants; a review of local gay publications and other marketing materials; and focus groups of young MSM. Enumerations of MSM were conducted at the venues during high-attendance 4 h time periods (sampling periods) to select venues for monthly sampling frames. Venues and their associated sampling periods (e.g. Friday evenings from 10.00 p.m. to 2.00 a.m.) were eligible for inclusion in monthly sampling frames if the enumerations produced a minimum of seven eligible men during a 4 h sampling period. This minimum was chosen to obtain the required sample size within a 12 month survey period. Sampling frames were updated monthly to include or remove venues and sampling periods.
Each month, a sample of 12 to 16 venues and their associated sampling periods was randomly selected. For each of these primary venues, two alternative venues were randomly selected with overlapping sampling periods. Sampling events were then conducted at each of the primary venues at the time of their randomly selected sampling periods. Alternative venues were used when the primary venue was closed or not attended by young MSM. Three non-random sampling events per month were allowed.
During each sampling event, staff counted all men who appeared to meet the study's age criterion and who entered a defined venue-specific intercept area (e.g. a section of the sidewalk in front of a dance club). These enumerated men were consecutively approached and screened for eligibility when recruitment staff were available. The approach and screening procedures were the same at all venue types. The eligibility criteria were 15-22 years of age and resident of one of the five boroughs of New York City or specified contiguous counties in Long Island, New York State and New Jersey. Young men who had previously participated in the survey were not eligible, as determined by directly asking all potential participants or by staff recognition of previous participants. Sexual orientation or behaviors were not included as eligibility criteria and were not ascertained in the initial approach.
Eligible and willing men were escorted to a mobile van equipped with three interview rooms. When all available interview rooms were occupied, potential participants were given an appointment for later during the sampling event or for another day. In the van, a trained interviewer/counsellor obtained informed consent, administered a standardized questionnaire, conducted HIV pre-test counselling, obtained a blood specimen, and provided referrals for social and medical services as needed. A US$50 reimbursement for time and effort was given. The survey and HIV antibody testing were anonymous; participant, interviews and specimens were identified by a survey identification number only.
The questionnaire collected data on demographics, venue attendance, lifetime sexual behavior with men and women, partner type and sexual behavior over the previous 6 months, history of STD, history of HIV antibody testing, and drug and alcohol use. An exchange partner was defined as a partner with whom the participant had sex to receive items such as food, shelter, transportation, drugs or money. Non-steady partners were defined as 'pick-ups', 'one-night stands' or casual partners with whom the participant had sex only one or two times, but were not exchange partners. Steady partners were defined as regular partners with whom the participant had sex three or more times, but were not exchange partners. Unprotected receptive anal, insertive anal and oral sex were defined as having that particular type of sex without using a condom every time.
Laboratory testing
Blood specimens were tested for HIV antibody by enzyme-linked immunosorbent assay (Sanofi Diagnostics Pasteur, Chaska, MN, USA). Sera that were reactive on first testing were retested in duplicate. Each sample that repeatedly tested positive by enzyme-linked immunosorbent assay was confirmed by Western blot assay (Bio-Rad, Hercules, CA, USA, or Epitope, Inc., Organon Teknika Corp., Durham, NC, USA).
Specimens were tested for hepatitis B surface antigen, antibody to hepatitis B surface antigen and antibody to hepatitis B core antigen (Abbott Laboratories, Abbott Park, IL, USA). Participants were considered 'immune by vaccination' by the presence of antibody to hepatitis B surface antigen only, 'immune by infection' by the presence of antibody to hepatitis B core antigen or hepatitis B surface antigen, or 'susceptible' by the lack of any markers of infection. Screening for syphilis was conducted using the rapid plasma reagin test (Wampole Laboratories, Division of Carter-Wallace, Inc., Cranbury NJ, USA). Positive samples were confirmed using the microhemagglutination assay for Treponema pallidum (Fujirebio Inc., Chuo-ku, Tokyo, Japan).
Statistical analysis
It is possible that the survey was more likely to contact men who frequently attend public venues. Therefore, an initial analysis was conducted to determine whether, within the MSM enrolled in this study, the frequency of attendance at public venues was associated with risk behaviors or HIV antibody status. For each venue type, an initial score was assigned on the basis of the frequency of attendance during 365 days in the year. For example, those men attending a type of venue every day were assigned a score of 365 for that venue type. Those attending a type of venue once a week were assigned a score of 52 for that venue type. The scores for each type of venue were summed to create an overall frequency of venue attendance score. Median scores were compared by HIV antibody status, and risk behaviors examined in this paper (lifetime history of an STD, having anal sex, using needles to inject drugs, having sex with a woman, and a recent history of unprotected anal and oral sex). No significant differences were found. Therefore, it is unlikely that, among the MSM enrolled, the data were biased by frequent venue attenders.
Associations between HIV antibody status, demographic characteristics and lifetime behaviors were examined using chi-square analyses and calculation of odds ratios. The variables included were: age, race/ethnicity, educational level, residence, living situation, sexual orientation, and lifetime history of an STD, having anal sex, running away from home, having forced sex, using needles to inject drugs, and having sex with a woman. Recent behaviors were not examined in relation to HIV antibody status because the study identified only prevalent cases of HIV infection with unknown dates of infection. Multivariate analysis of the association of HIV antibody status with selected covariates was conducted using logistic regression. The covariates included were those significantly associated with HIV antibody status by univariate analyses.
Results
Sampling events and street intercepts
Between December 1997 and September 1998, 115 sampling events were conducted at street locations (40), dance clubs (21), other businesses (16), bars (15), sex clubs (15) and social organizations (8). The 115 sampling events occurred disproportionately at street locations compared with the sampling frame. This occurred because 31.3% of the events were non-random, as allowed by the protocol, and these events were disproportionately street locations (20.3% for randomly selected events and 66.7% for non-random events). During these sampling events, 2521 men were approached and 2111 (83.7%) agreed to a brief interview to determine eligibility. Of 958 men who were determined to be eligible, 612 (63.9%) enrolled. Men who did not enrol were significantly more likely to be older (P = 0.001), black or Asian/Pacific islander (P = 0.001) and to have been approached at dance clubs (P = 0.001) than men who enrolled. The remaining analysis is based on the 541 enrolled men who reported ever having had oral or anal sex with a male partner (MSM) (88.4% of total enrolled).
Study sample of men who have sex with men
Almost half of the study sample (46.6%) was recruited at street locations, 17.0% at sex establishments, 12.0% at business establishments, 9.2% at social organizations, 8.7% at dance clubs and 6.5% at bars.
The characteristics of the 541 MSM are presented in Table 1. Over one-third of the sample was 15-18 years old, and a diverse population was enrolled with respect to race/ethnicity and area of residence. Two-thirds of the MSM (63.0%) considered themselves to be gay, and 28.5% considered themselves to be bisexual. A majority of the MSM lived with their parents/guardian or other relatives. Approximately 40% of the study sample reported ever having run away from home, and nearly one-third reported ever having been forced to have sex.
Risk behaviors
Almost all young MSM (91.9%) reported ever having had anal sex with another man in their life, 16.3% reported ever having had an STD, and 5.9%
reported ever having used needles to inject drugs not prescribed by a physician, including steroids and hormones (Table 1). Table 2 and Table 3 present additional lifetime and recent sexual risk behaviors reported by the men. Almost all (93.0%) had had a male partner in the previous 6 months. Of these men, 17.3% had had an exchange partner and 39.8% had had a male partner who was 30 years of age or older (Table 2).
Overall, almost one half (46.1%) of the men reported unprotected anal sex with a male partner in the previous 6 months, 35.4% reported unprotected receptive anal sex, and 30.8% unprotected insertive anal sex (Table 3). Most men reported having had unprotected oral sex. Although the percentage of men reporting unprotected sex with steady partners approached 50%, one quarter of men reported unprotected anal sex with exchange partners (Table 3).
Two-thirds of the men reported having had a female partner some time in their life, with 22.7% reporting having had a female partner in the previous 6 months (Table 2). Of those with female partners, 89.4% also had male partners in the previous 6 months. Almost half (45.5%) of the men reported unprotected vaginal sex, and 17.1% reported unprotected anal sex with their female partners (Table 3).
Serological results and association with demographics and risk behaviors
Of the 541 men enrolled, 529 (97.8%) were tested for HIV antibody, 534 (98.7%) were tested for markers of HBV infection and 536 (99.1%) were tested for syphilis. Testing was not completed for some participants if the counsellors determined during counselling that the participant was not psychologically ready to be tested, the participant refused testing or there was an unsuccessful venipuncture.
Among the 529 MSM tested for HIV antibody, 64 (12.1%) were positive. Of the 64 who tested positive, 36 (56.3%) reported having had a previous HIV antibody negative test. Of 35 who reported having previously tested negative and had a known last test date, 23 (65.7%) had tested negative within the year before their interview and 31 (88.6%) within the 2 years before their interview. Thirteen (20.3%) of the 64 who tested positive reported that they were seropositive by questionnaire. All self-reported positive results were confirmed by serological testing.
Among 534 MSM tested for markers of HBV infection, 64 (12.0%) were considered immune because of previous infection and 120 (22.5%) were immune by vaccination. A total of 350 (65.5%) had no markers and were thus considered susceptible. Only five men out of 536 tested were initially positive for syphilis by the rapid plasma reagin test and, of these, three were confirmed to be positive, resulting in a seroprevalence of 0.6%.
Table 4 presents the unadjusted and adjusted odds ratios for being HIV antibody positive by demographic and risk behavior variables found to be significantly associated with HIV antibody status. Being 19-22 years old, of mixed or black race/ethnicity, and ever having had an STD were significantly associated with HIV seropositivity. A lifetime history of anal sex had an elevated odds ratio, but it was not statistically significant. No other demographic characteristics or lifetime behaviors were associated with HIV antibody status (education, residence, living situation, sexual orientation, ever having run away from home, ever having had forced sex, ever having used needles, ever having had sex with a women). Risk behaviors or the type of partners in the previous 6 months were also not associated with HIV antibody status. Multiple logistic regression found that being older, of mixed race, black or ever having had an STD remained significantly associated with being HIV antibody positive.
Discussion
This study sample of young MSM who attended public venues in New York City were found to be at high risk of HIV infection, as illustrated by the high HIV seroprevalence and the large proportion engaging in unprotected sex. Furthermore, self-reported testing histories suggest that a large proportion of the infections were recently acquired. These findings are disturbing given the city-wide prevention campaigns targeting this population. Evidence from other cities support the finding that currently, young MSM are at high risk of HIV infection [2,3,14]. It is likely that young MSM have been at higher risk than older men throughout most of the epidemic, a reflection of the factors associated with being young, such as a lack of communication skills and a sense of invulnerability [8]. However, the current level of risk, as indicated by the percentage engaging in unprotected sex, is alarming. One new factor that may contribute to the recent high level of risk behaviors is the expanded availability of highly effective antiretroviral therapies. Important advances have been made in the treatment of HIV infection, with significant declines in HIV-related morbidity and mortality [17,18]. Extensive media coverage of the successes of new treatments and of the use of post-exposure prophylaxis may have reduced concerns about placing oneself at risk or, if infected, exposing others [19]. Further research is needed to determine the role of new treatments in relation to high-risk behaviors in this young generation of MSM.
The YMS-NYC findings support the need for the development and expansion of outreach and HIV prevention efforts for young MSM. The challenge for developing effective prevention programs is to integrate the knowledge about who is at risk, from studies such as YMS-NYC, with information on why people continue to put themselves at risk. Community-level interventions consisting of small groups in combination with peer outreach and publicity campaigns, or the use of popular opinion leaders have been demonstrated to reduce the proportion of MSM reporting unprotected sex [20,21]. Such programs need to be reviewed for their applicability to very young MSM, who may be difficult to reach. In addition, information needs to be included about new treatments for those already infected and emphasis needs to be placed on the fact that new treatments and post-exposure prophylaxis are not substitutes for safer sex.
The YMS-NYC also found a particularly high HIV seroprevalence among young minority MSM and MSM with a history of STD. These associations remained significant even after controlling for a history of anal sex and age, a factor known to have a direct association with HIV seroprevalence. Other studies in New York City have found samples of young MSM who are at substantial risk, although most of the studies were not contemporary, had small sample sizes, were convenience samples or lacked HIV serological data [15,22-24].
Outreach strategies need to continue and be expanded to young minority MSM, particularly young black MSM. A small-group, multiple session intervention demonstrated reductions in the frequency of unprotected sex among African-American MSM [25], although such an approach encountered problems with the recruitment of interested men and completion of the sessions [26]. The incorporation of HIV risk reduction programs into other health services, community organizations, and local faith institutions may assist in reaching a young minority population at very high risk.
In addition to identifying venues that attract a large proportion of minority MSM, it is important to target STD clinics and other primary care settings, where screening and treatment for STD can be combined with HIV prevention efforts. STD have been shown to be an important factor for HIV acquisition. In the YMS-NYC, a history of STD may be a surrogate measure for risk behaviors. STD can also enhance the risk of HIV acquisition by providing a vulnerable portal of entry for the virus, increasing the presence of lymphocytes due to inflammatory responses and increasing viral shedding [27-29].
The prevention of HBV infection is another area of substantial need in this population, as illustrated by the susceptibility of two-thirds of the men in this survey. A highly effective vaccine is available, and mechanisms to reach young MSM are needed. Interventions focused on preventing HBV infection provide an additional opportunity for engaging young MSM in HIV prevention efforts.
A large proportion of the young MSM in this survey also had sex with women, and much of this contact was unprotected. Previous research indicates that this subpopulation is unlikely to participate in the gay community, and is thus not likely to be reached by prevention programs occurring in that community [30]. Therefore, prevention efforts targeted towards MSM having sex with women present a significant prevention challenge. Furthermore, more research is needed to obtain a better understanding of the contextual variables associated with unprotected sex among men having sex with both men and women, so that effective prevention programs can be developed and implemented.
The YMS-NYC provided an important opportunity to assess the status of the HIV epidemic in a sample of young MSM frequenting public venues in New York City. The particular strengths of this study were its focus on a very young population of MSM, the collection of both serological and risk behavior data, the multi-stage sampling strategy, and the large sample size. The results of this study, however, provide limited opportunities for generalization because the study sample is not representative of all young MSM in New York City. The study sample recruited was mostly minority and the MSM enrolled were those who attended public venues and who chose to participate (64% of those eligible). Older, black and Asian/Pacific islanders were less likely to enrol. Nevertheless, these data identify a subgroup of MSM who are at high risk, and clearly points to the need for further research to understand their HIV risk and for targeting prevention and referral services to those at greatest risk of HIV infection.
Acknowledgements
The authors wish to thank the YMS-NYC staff (Christian Castro, Carmelo Figueroa, George Gates, Ricko Hernandez, Scott Ikeda, Yusef Junquera, Leniere Miley and Dwayne Williams) for their work and devotion in conducting this study, staff from YMS-Dallas (Kyle Funderburgh, Santiago Pedraza and Stewart Thomas) and YMS-Baltimore (Wil Edgar and Terry Precord), who helped in the conduct of YMS-NYC, the YMS Community Advisory Board for their advice and contributions, Gina Secura and Elvin Magee of the Centers for Disease Control and Prevention, and the study participants who gave their time and effort. This paper is dedicated to the memory of Carmelo Figueroa.
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