Xu, Fujie MD, PHD; Sternberg, Maya R. PHD; Markowitz, Lauri E. MD
Behavioral surveillance in the general population through random probability sampling can provide the denominator data of various groups at high risk for HIV infection.1 In the United States, male-to-male sexual contact remains the most important route of HIV transmission. Men who have sex with men (MSM) is the population most impacted by the HIV epidemic.2 Most recent surveillance estimates show that about 30,000 HIV infections occurred in MSM in the United States in 2006, representing 53% of all incident HIV infections in that year.3 Because of the high burden of HIV infection in MSM, it is important to estimate the prevalence of MSM behavior in the general population and monitor trends.4
The term “MSM” is now widely used, and can be a standardized measure allowing for comparisons across reports and surveillance systems and the analysis of trends. There are several population-based studies in the United States about the prevalence of MSM behavior, but they were often limited to large metropolitan areas where HIV-related risk behaviors are generally more prevalent.5–9 Recent national estimates of the prevalence of MSM behavior have been reported from the 2002 National Survey of Family Growth (NSFG), but the survey did not collect biologic specimens for assessment of disease burden.10
Many reports have described significant differences in HIV risk among subsets of MSM, including subgroups defined by race-ethnicity and homosexual or gay identity2,9,11–13—variations that are lost with a generic term like MSM. The understanding of social, demographic, and behavioral characteristics among MSM is often crucial for the design and evaluation of targeted interventions.14–17 Although race-ethnicity is routinely included in surveys and studies about MSM in the United States, fewer population-based surveys include sexual orientation as a demographic variable.6,9–12 There are concerns that the ubiquitous use of MSM can undermine the self-determined sexual identity of members of sexual-minority groups and obscure elements of sexual behaviors that are important for public health research and intervention.9,14
We analyzed data for men 18 to 59 years of age who participated in the National Health and Examination Surveys (NHANES) conducted in 2001 through 2006 in the United States. We compared the demographic and behavioral characteristics of MSM and non-MSM (men who reported only female sex partners), estimated the prevalence of HIV and herpes simplex virus type 2 (HSV-2) infections, and described differences by sexual orientation. We also estimated the prevalence and population sizes of MSM by 3 commonly used definitions: Men who reported (1) ever having had a same-sex partner, (2) having had a same sex partner in the past year, and (3) homosexual orientation.
Study Population and Survey Methods
The NHANES is a series of cross-sectional surveys to compile nationally representative statistics on the health of the population in the United States. Details of the survey methodology have been published previously.18 The most recent series is designed to run continuously with data released every 2 years. Participants are chosen according to a complex, stratified, multistage probability sampling design to select a nationally representative sample of civilian noninstitutionalized population in the United States and are interviewed and examined by medical professionals.
During NHANES, participants undergo health examinations in specially equipped mobile examination centers, where the questionnaire about sexual and drug use behaviors is administered in a private room using audio computer assisted self-interview (ACASI) in either English or Spanish. For each 2-year cycle during NHANES 2001–2006, about 6300 male participants of all ages were sampled for interview and examination; the response rate for examination was 75% to 80%.19
Testing for HIV and HSV-2 Infection
Blood samples from survey participants were collected during health examinations at the mobile examination centers. Serum specimens from participants aged 14 to 49 years were tested for antibodies to HIV and HSV-2. HIV antibodies were tested using HIV-1/HIV-2 Peptide EIA (Genetic Systems, Redmont, WA). All repeated positive specimens were confirmed by Western blot assay (Calypte Serum Western blot; Calypte Biomedical Corporation, Pleasanton, CA). In rare cases, participants who consented to the HIV test but did not have sufficient serum available for the serum antibody tests were tested for HIV antibody using urine (Calypte HIV-1 Peptide EIA, Calypte Biomedical Corporation); positive specimens were retested and confirmed by Western blot assay (Calypte Urine Western blot; Calypte Biomedical Corporation).20
Serum antibodies to HSV-2 were detected using a type-specific immunodot assay. Purified glycoprotein gG-2 of HSV-2 was used as the antigen in the assay. The performance of the immunodot assays is high with respect to sensitivity and ability to discriminate between herpes simplex virus type 1 and HSV-2.21,22 In NHANES 2001–2006, the same immunodot assays and the same laboratory were used as for previous NHANES.23
Definitions of MSM and Sexual Orientation
During NHANES 2001–2006, “sex” was defined as vaginal, oral, or anal sex. Survey participants aged 18 to 59 years were interviewed about the lifetime number of male and female sex partners and partners in the past 12 months. Only men who answered “yes” to the question “have you ever had sex?” were asked “In your lifetime, with how many men have you had sex?” Having ever had same-sex sex partners (MSM-Ever) was defined as reporting one or more lifetime male partners. Recent same-sex contact was similarly assessed (“In the past 12 months, with how many men have you had sex?”). MSM-Past Year was defined as reporting one or more male partners in the past 12 months, and is a subset of MSM-Ever. Sexual orientation was assessed by the question “Do you think of yourself as… heterosexual or straight (that is, sexually attracted only to women); homosexual or gay (that is, sexually attracted only to men); bisexual (that is, sexually attracted to men and women); something else; or you're not sure?” This question was added in the NHANES starting in the year of 2001.
For this article, the term MSM will only apply to behavior (having had sex with men, ever, or in the past year), while sexual orientation will refer to or be synonymous with self-identification. For instance, homosexual MSM-Ever will refer to men who reported having ever had sex with men and also self-identified as homosexual or gay.
SUDAAN software (Release 9.1, Research Triangle Institute, Cary, NC) was used for statistical analyses.24 All estimates were weighted to account for the selection probabilities and adjustment for nonresponse.25,26 We used medical examination weights provided by NCHS.27 Variance estimates were calculated using a Taylor series linearization that incorporated the complex sample design of the survey. An estimate is considered unreliable if the relative standard error was >30% of the estimate.26 Confidence intervals for the prevalence were calculated using a logit transformation with the standard error of the logit prevalence estimated using the Δ method. P-values for comparing MSM groups with non-MSM and among subgroups of MSM-Ever were based on a test for independence using an F-statistic derived from a Wald χ2 for categorical variables. Medians are computed through an estimate of the cumulative distribution function based on ungrouped data.
For this article, race-ethnicity was defined by self-report as non-Hispanic white, non-Hispanic black, Mexican American and “other”; the other category includes all participants who did not belong to the 3 main categories, such as those who reported “multiracial” and persons whose race-ethnicity was missing. Poverty level was defined by US Census Bureau, and is assigned by dividing total family income by the poverty threshold index, then adjusting for number of persons in the household at the year of interview (available at: http://www.census.gov/hhes/www/poverty/definitions.html).
Demographic and Behavioral Characteristics of MSM
Of all men aged 18 to 59 years in NHANES 2001–2006, 92.8% reported having ever had sex. MSM-Ever was reported by 5.2% (95% confidence interval (CI), 4.4–6.2) of sexually experienced men. Among MSM-Ever, 57% (95% CI, 44.9–68.0) reported one or more male sex partner in the past year (MSM-Past Year).
We compared demographic and behavioral characteristics of MSM-Ever and MSM-Past Year with those of men who reported only female partners (non-MSM) (Table 1). Among MSM-Ever, the mean age was 40.1 years and 76.2% were non-Hispanic whites (Table 1). MSM-Ever were significantly more likely to have higher education (P < 0.0001). MSM-Ever were more likely than non-MSM to have had first sex at age <15 years (31.9% vs. 17.3%, P = 0.0035). MSM-Ever were also more likely to have had 10 or more lifetime sex partners (73.6% vs. 40.8%), have 2 or more sex partners in the past 12 months (41.0% vs. 18.4%), and to have ever used cocaine (46.1% vs. 26.6%) (all P < 0.0001) (Table 1). The median number of lifetime sex partners (male and female) was 19.1 for MSM-Ever and 6.3 for Non-MSM (P = 0.0008) (Table 1).
As a subset of MSM-Ever, MSM-Past Year reflect the demographic characteristics of MSM-Ever in general (Table 1). However, among MSM-Past Year only 6.6% were currently married. In MSM-Past Year, 59.1% reported 2 or more sex partners in the past year, compared with 41.0% of MSM-Ever, suggesting that MSM-Past Year may have higher sexual risk in the recent past.
HIV and HSV-2 Infection in MSM
The prevalence of HIV was 0.2% (95% CI, 0.1–0.4) in non-MSM, 9.1% (95% CI, 4.8–16.4) in MSM-Ever, and 11.8% (95% CI, 6.0–21.9) in MSM-Past Year (Table 1). Because the number of persons with HIV infection was small, the HIV prevalence estimates all have wide confidence intervals and may be unreliable. The prevalence of HSV-2 was higher in MSM-Ever (18.4%) and in MSM-Past Year (19.6%) than in non-MSM (12.5%) but the differences were not statistically significant (Table 1).
Differences by Sexual Orientation AmongMSM-Ever
Of MSM-Ever, 44.5% self-identified as homosexual or gay, 19.2% as bisexual and 35.3% as heterosexual or straight (Table 2). The 3 subgroups of MSM-Ever by sexual orientation were similar in age and race/ethnicity, but differed by poverty and education level. The percent of MSM who were currently married or living with a partner varied by sexual orientation: no homosexual MSM-Ever was currently married, compared with 27% of bisexuals and 47.1% of heterosexuals (Table 2).
The median number of lifetime male partners was significantly different by sexual orientation (Table 2), and was highest among homosexuals (17.7) and lowest in heterosexuals (1.0) (P < 0.001). Among MSM-Ever who were self-identified as heterosexual, 62.4% reported only 1 male partner in lifetime (data not shown). More than three-quarter (76.8%) of homosexual MSM-Ever reported 10 or more lifetime male partners, compared with 37.5% of bisexuals and 3.2% of heterosexuals (P < 0.001). Among homosexual and bisexual MSM-Ever, over 40% reported 2 or more male partners in the past year, suggesting that these 2 groups can potentially be at high risk for HIV acquisition/transmission. In contrast, only 1.0% of heterosexuals reported 2 or more male partners in the past year (Table 2).
Heterosexual MSM-Ever reported the highest median number of female sex partners in lifetime, followed by bisexuals (Table 2). The weighted percent of homosexual MSM-Ever who had zero female sex partner was 46.6% (data not shown) and the median number of lifetime female sex partners was low (0.2, 95% CI, 0.0–0.9). In contrast, 44.8% of bisexuals and 67.0% of heterosexuals reported 10 or more lifetime female sex partners.
There were no significant differences in the number of total (male and female) lifetime sex partners by sexual orientation. Among the 3 subgroups of MSM-Ever, the median number of total lifetime sexual partners was lowest among heterosexuals (Table 2), but this median is still more than double that in non-MSM: 15.7 (95% CI, 10.5–21.2) versus 6.3 (95% CI, 5.8–7.0) (Table 1). Among homosexual and bisexual MSM-Ever, 46.9% and 57.7%, respectively, reported having had 2 or more total partners in the past year; among heterosexual MSM-Ever, this percentage was lower (25.9%) (Table 2).
Homosexual and bisexual MSM had higher burden of HIV infection: 16.5% (95% CI, 8.5–29.6) in homosexual MSM-Ever and 4.1% (95% CI, 1.2–13.3) in bisexual MSM-Ever (Table 2). In this survey, there were no HIV infections in heterosexual MSM-Ever. The prevalence of HSV-2 was not statistically different in the 3 MSM-Ever subgroups defined by sexual orientation (Table 2).
Prevalence and Population Size of MSM
We estimated the prevalence and population size of 3 groups of MSM in the United States: MSM-Ever, MSM Past Year, and homosexual orientation. The prevalence of MSM-Ever differed by age, highest in men aged 30 to 39 years (7.0%) and lowest in those 18 to 29 years (3.1%) (Table 3). Pairwise comparisons showed that the prevalence of MSM-Ever was significantly higher in non-Hispanic whites (5.4%) than in non-Hispanic blacks (3.6%, P < 0.05). The prevalence of MSM-Ever was higher in those with more than high school education compared with those with high school education or less (6.9% vs. 2.9%, P < 0.005). Similarly, the prevalence of MSM-Past Year and homosexual orientation differed by education level. Homosexual orientation also differed by race-ethnicity—non-Hispanic black men reported the lowest prevalence of homosexual orientation (1.1%) (Table 3).
Based on the January 2004 census data in the United States, we estimated the population size of the 3 MSM groups as the product of: (1) prevalence, (2) total population count for men aged 18 to 59 years, and (3) percent of men aged 18 to 59 who had had sex. The estimated population size of MSM-Ever was 4.0 million (95% CI, 3.3–4.7). The population size of MSM-Past Year was 2.2 million (95% CI, 1.6–3.0) and homosexual orientation was 1.8 million (95% CI, 1.1–2.6).
The NHANES are designed to provide nationally representative estimates by demographic groups. We described the demographic and behavioral characteristics of MSM-Ever and MSM-Past Year in a population-based sample and compared these characteristics with non-MSM. Consistent with prior research, MSM-Ever and MSM-Past Year reported having first sex at younger age and having had larger number of lifetime sex partners than non-MSM. Male-to-male sexual contact, either ever or in the recent past, is among important markers of high risk for HIV infection. Monitoring the prevalence and trend of MSM behavior (ever and in past year) in the general population can provide the essential data regarding the population size and characteristics of these high risk groups and their changes over time, and thus is important for the prevention and control of HIV infection.
Estimates of HIV prevalence from NHANES 1999 to 2002 have been reported and were found to be consistent with national estimates by the Centers for Disease Control and Prevention.28 The prevalence of HIV in men who ever had sex with men was 8.5% from NHANES 1999 to 2002,28 similar to the prevalence of 9.1% we found from NHANES 2001 to 2006. Due to the small number of HIV infections, the prevalence estimate from NHANES 2001 to 2006 is not precise. Despite this limitation, our analyses support previous reports that the MSM population is among the populations hardest hit by the HIV epidemic in the United States.29
The prevalence of HIV infection differed greatly by sexual orientation. Among MSM-Ever, HIV prevalence was highest among homosexual MSM-Ever and lowest among heterosexual MSM-Ever. The numbers of male partners in lifetime and in the past year, indicators of cumulative and recent risk for sexual acquisition of HIV infection, were highest among homosexual MSM-Ever. Among MSM-Ever, those self-identified as homosexual or bisexual were more likely to have multiple sex partners in the past year than heterosexuals, and therefore, were potentially at greater risk for recent HIV acquisition and transmission. Although not yet widely included as part of surveys or studies, sexual orientation can help further identify subgroups at the highest risk for HIV infection among MSM-Ever. At the same time, although the prevalence of HIV infection appears to be low in the subgroup of MSM self-identified as heterosexual or straight, these men still reported higher numbers of sex partners compared to non-MSM.
Our study, with participants drawn from the general population, supports previous reports that bisexual MSM is one of the most important bridge populations.30,31 The prevalence of HIV infection in bisexual MSM-Ever was more than 20 times higher than in non-MSM. Among bisexual MSM-Ever, 44.8% had 10 or more lifetime female sex partners, 27.0% were currently married, and 29.9% had 2 or more female sex partners in the past year. In addition, among MSM-Past Year, 6.6% were currently married, corresponding to about 150,000 couples in the United States based on the 2004 Census. Furthermore, 13.5% of MSM-Ever and 12.2% of MSM-Past Year were widowed, devoiced or separated. The female partners of these men are potentially at high risk for HIV infection. Despite the high rates of HIV infection among MSM who were self-identified as homosexual, the risk of HIV transmission to women is likely to be limited due to their low number of lifetime female partners.
We found that about 20% of MSM (Ever or Past Year) had HSV-2 infection. This finding is consistent with reports in the literature: A large multisite study and a study in Baltimore among MSM reported similar prevalence of HSV-2 (20.3% and 19.3%, respectively).32,33 However, the prevalence was somewhat higher (32.3%) in a study of MSM living in New York City.34 HSV-2 seroprevalence did not vary by sexual orientation. The lack of difference may be explained by the fact that the total number of sex partners (male and female) did not differ by sexual orientation, and that female partners can be an important source for HSV-2 infection; HSV-2 prevalence in sexually active women is high and similar to that among MSM.23,33
Data from population-based surveys have several limitations: First, the prevalence of MSM behavior is relatively low in the general population, resulting in small sample sizes; we had to combine data from multiple NHANES survey cycles for reliable analyses. Second, reporting bias is a concern and may have contributed to the observed differences in the prevalence of MSM behavior by age, race-ethnicity, and education level as the respondents' willingness to report socially-censured behaviors such as male-to-male sexual contact may vary by these characteristics. Although definitive estimation of the willingness to report is never possible, higher education level may be associated with increased willingness to report. Lower willingness to report may have, as least in part, contributed to the lower prevalence of MSM behavior and homosexual orientation reported by black men.35 ACASI was used in the NHANES survey in an effort to increase the willingness to report.4,36 Lastly, we did not control for type I error in our analyses and some statistical significance might have been due to chance alone.
Our analyses provide national estimates concerning the prevalence and population size of MSM groups defined by sexual behavior and sexual orientation. We found that 5.2%, or about 1 in every 20, sexually experienced men aged 18 to 59 ever had a male sex partner, 2.9% had a male-to-male sexual contact in the past year, and 2.3% reported homosexual or gay orientation. Previous research indicates that same-sex behavior and homosexual orientation are more prevalent in large cities. In a population-based survey of 18- to 59-year-old men living in the largest cities in the United States, Laumann et al found 10.2% of sexually active men reported having had male sex partners in the previous year and 9% identified as gay or bisexual.5 Among sexually active men living in New York City surveyed through residential telephone, 12% reported same-sex sexual behavior in the past year and 4% reported a gay identity.9 However, in NSFG 2002, 6.0% of sexually active men reported that they had had sex with another men at some time in their lives, 2.9% reported having sex with another men in the last 12 months, and 2.3% reported their sexual orientation as homosexual.10 These data are similar to our estimates from NHANES considering the sampling errors of the surveys. In NSFG 2002, questions related to HIV risk behaviors were administered by ACASI, as it was for NHANES.
This analysis provides some population-based estimates of behavioral and biomedical parameters that are important for the surveillance and prevention of HIV and other STDs. Population-based statistics about MSM behavior, sexual orientation and HIV and HSV-2 infection are an important part of the national estimates that describe the HIV epidemic in the United States, and are also important for the planning and evaluation of control efforts in high risk populations. Ongoing data collection through NHANES will provide updates in the future and can potentially allow for analyses of long-term trends.
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