Sexually Transmitted Diseases:
An Opportunity for Prevention: Prevalence, Incidence, and Sexual Risk for HIV Among Young Asian and Pacific Islander Men Who Have Sex With Men, San Francisco
Choi, Kyung-Hee PhD, MPH*; McFarland, Willi MD, PhD*†; Neilands, Torsten B. PhD*; Nguyen, Sean†; Louie, Brian†; Secura, Gina M.‡; Behel, Stephanie‡; Mackellar, Duncan PhD‡; Valleroy, Linda PhD‡
From the *University of California, San Francisco Center for AIDS Prevention Studies, San Francisco, California, †San Francisco Department of Public Health, San Francisco, California, ‡Centers for Disease Control and Prevention, Atlanta, Georgia
Correspondence: Kyung-Hee Choi, PhD, Center for AIDS Prevention Studies, University of California, San Francisco, 74 New Montgomery Street, Suite 600, San Francisco, CA 94105. Email: email@example.com.
Received for publication January 5, 2004, and accepted March 22, 2004.
Objectives: We investigated HIV prevalence and incidence and related risk factors among young Asian and Pacific Islander (API) men who have sex with men (MSM).
Design: We conducted a cross-sectional survey.
Methods: A venue-based sample of 496 young API MSM in San Francisco completed face-to-face questionnaires and received HIV counseling and testing.
Results: HIV prevalence was 2.6% and annualized HIV incidence was 1.8% per year. In multivariate analysis, being American-born, having 51+ lifetime sex partners, and having attended a “‘circuit party” (multiday large MSM gatherings) were associated with HIV infection. Forty-seven percent of the sample reported unprotected anal intercourse in the past 6 months.
Conclusions: The current levels of HIV prevalence, HIV incidence, and sexual risk behavior suggest an emerging HIV epidemic among young API MSM in San Francisco.
ALTHOUGH THE HIV EPIDEMIC has entered the third decade in the United States, AIDS is still not common among Asians and Pacific Islanders (APIs). Whereas Asians and Pacific Islanders (APIs) represent 4% of the U.S. population,1 they account for only 0.76% of all U.S. AIDS cases.2 This proportion of the API AIDS cases has remained unchanged since 1990 (0.62%).3
Because of the small number of reported AIDS cases in the U.S. API population, it is often believed that few APIs engage in risky behaviors.4 Available data do not support this assertion. Recent studies have shown that young API men who have sex with men (MSM) are as likely as or more likely than other MSM groups to engage in unsafe sex. For example, a survey of MSM aged 23 to 29 in Los Angeles found equivalent rates of unprotected insertive anal intercourse among APIs, Latinos, and blacks (38%, 39%, and 33%, respectively) and similar rates of unprotected receptive anal intercourse among APIs and blacks (29% vs. 24%).5 A 4-city study of MSM aged 17 to 25 found comparable rates of unprotected anal intercourse during the 6-month time period for APIs and whites (39% vs. 36%) but a higher rate for APIs relative to blacks (39% vs. 30%).6 A 13-city survey of MSM aged 15 to 25 showed similar patterns of unprotected anal intercourse in the past 3 months (28% APIs, 24% whites, 17% black).7
Existing data,5,6,8–12 however, show that estimated HIV prevalence in young API MSM ranges from as low as 2%11 to as high as 27%.8 Also, there are no clearcut patterns in HIV seropositivity when making comparisons across ethnic groups. The San Francisco Young Men’s Health Study, for example, found equivalent rates of HIV infection among API MSM and Latino MSM (27% vs. 25%).8 However, the same study showed that an HIV infection rate for APIs was higher relative to whites and lower relative to blacks (27% vs. 16% and 35%, respectively). The 7-city Young Men’s Survey, on the other hand, reported similar HIV infection rates among APIs and whites (3% and 3%, respectively), but a lower rate among APIs relative to Latinos and blacks (3%, 7%, and 14%, respectively).12 Because most studies of young MSM have included less than 60 APIs,5,6, 8–10 it has been difficult to assess the generalizability of research findings for the API population. Small sample sizes have also precluded characterization of risk factors for HIV infection in this ethnic group.
In addition, there is only 1 study that has estimated HIV incidence among young API MSM.13 The Young Men’s Survey reported the lowest annual HIV incidence for APIs (0.0%) compared with other ethnic groups (1.8% for Latinos, 2.4% for whites, and 4.0% for blacks). However, generalizing this study finding to the API MSM population is problematic. All but 1 city recruited 30 or fewer API men. Moreover, these cities are diverse in terms of the HIV epidemic and the concentration of the API population. For example, HIV incidence varied significantly by city ranging from 0.7% in Seattle and 1.2% in San Francisco to 3.3% in Dallas and 7.6% in New York. APIs represent 31% of the city population in San Francisco versus 3% in Dallas.1
To increase our understanding of the HIV epidemic among young API MSM, we conducted the first large survey of 566 API men aged between 18 and 29 years of age in San Francisco. We estimated HIV prevalence and incidence, and identified demographic and behavioral risk factors associated with HIV infection.
Materials and Methods
From January 2000 to September 2001, study participants were recruited using the venue-based, time/space sampling procedures developed by the Centers for Disease Control and Prevention (CDC) for their Young Men’s Survey.14 We first identified venues frequented by API MSM through individual interviews and focus groups with community informants who were knowledgeable about young API MSM such as members of the gay API community, public health officials, and HIV and social service providers. At identified venues, research teams counted and conducted eligibility interviews of men who appeared to be Asians or Pacific Islanders under 30 years of age. Eighteen- to 29-year-old male residents of the San Francisco Bay Area (ie, San Francisco, Alameda, Contra Costa, San Mateo, Santa Clara, and Marin counties) who self-identified as Asian or Pacific Islander were eligible to participate. Based on these data, we constructed monthly sampling frames of venues and associated days and time periods in which we might expect to find at least 7 API men who were eligible for the survey and might enroll in a given 4-hour time period. Throughout the study period, we added and deleted venues and day/time periods from the sampling frame if they did or did not meet the criterion of 7 eligible men in a 4-hour time period.
At the end of each month, 12 to 30 venues and day/time periods (eg, a bar on Friday night from 10 pm to 2 am) were randomly selected from an updated sampling frame and scheduled for sampling in the following month. During sampling events, potential participants were approached consecutively and screened for eligibility as they walked down a preselected stretch of sidewalk, waited in line, or entered a venue. Eligible men who chose to participate were escorted to a large recreational vehicle that contained phlebotomy and private rooms used for mobile testing and counseling. Inside the vehicle, study participants provided written informed consent, completed a standardized questionnaire administered by an interviewer, received HIV/sexually transmitted disease prevention counseling, had their blood drawn through venipuncture for HIV, hepatitis B, and syphilis testing, and gave their urine sample for gonorrhea and chlamydia testing. Participants received $50 in cash and were scheduled to return to the San Francisco Department of Public Health 2 weeks later to obtain posttest counseling and results.
We minimized the likelihood of enrolling the same individual more than once by asking all screened men whether they had already participated in our study. Previous participants were ineligible. In addition, we tested specimens suspected of duplicate enrollees who reported the same ethnicity and birth date using a human antibody fingerprinting method (Viral & Rickettsial Disease Laboratory, CA DHS, Richmond, CA).15 When auto-antibody profiles matched, we considered that specimens came from the same participant and only analyzed data from the first enrollment. The study protocol was approved by Institutional Review Boards at the Centers for Disease Control and Prevention and at the University of California, San Francisco.
The questionnaire collected information on sociodemographic characteristics, sexual behavior, and substance use. Respondents were asked about their ethnicity, age, education, sexual orientation (gay [homosexual], bisexual, straight [heterosexual], “none of the above,” or “don’t know”), birthplace (American- or foreign-born), and length of time in the United States (if they were born overseas). They were also asked how many male partners they had in their lifetime and in the past 6 months, whether they had engaged in unprotected anal intercourse with men in their lifetime and in the past 6 months, and whether they had ever been diagnosed with a sexually transmitted disease, had ever injected drugs, had ever attended a “circuit party” (a series of parties held as part of a special event for MSM), and had ever used “club drugs” (ie, methylenedioxymethamphetamine [ecstasy], methamphetamines [speed], γ-hydroxybutyrate [GHB], ketamine [special K], lysergic acid diethylamide [LSD]).16 In addition, they were asked whether they had previously been tested for HIV, and if they had, the results of their last test.
Serum samples were initially screened for HIV-1 antibodies by a standard sensitive enzyme immunoassay (EIA) (Vironostika HIV-1 Microelisa; Organon Teknika Corp., Durham, NC) and samples with a reactive EIA were confirmed as positive by immunofluorescent antibody (Fluorognost HIV-1 IFA; Waldheim Pharmazeutika Ges.m.b.H, Vienna, Austria). To identify samples that likely came from recent seroconverter, the sensitive/less sensitive EIA algorithm testing strategy known as STARHS (Serological Testing Algorithm for Recent HIV Seroconversion [STARHS]) was used.17,18 Confirmed positive specimens were tested with the Vironostika LS HIV-1 EIA, modified from the standard Vironostika HIV-1 EIA to be less sensitive by an increased specimen dilution and a decreased specimen incubation period. Standard optical densities (SOD) from the less sensitive assay were calculated. Subjects whose specimens tested nonreactive on the less sensitive EIA (median SOD <1.0) were considered likely to have seroconverted within the last 170 days.
Syphilis was detected by a nontreponemal antibody test (VDRL Slide test; Becton Dickinson Microbiology Systems, Sparks, MD) and confirmed by a treponemal antibody test (Serodia Treponema pallidum passive particle agglutination [TP-PA] test; Fujirebio Inc., Fairfield, NJ). Strand Displacement Amplification (BDProbeTec ET Chlamydia trachomatis and Neisseria gonorrhoeae Amplified DNA Assays; Becton Dickinson) was used to detect gonococcal and chlamydial DNA in urine specimens.
The prevalence, with 95% confidence intervals, of HIV, syphilis, gonorrhea, and chlamydia were computed for the entire sample. Crude HIV incidence was calculated from the less sensitive EIA results by dividing the number of persons with recent infection by the total number of persons with recent infection plus uninfected persons (ie, the “susceptible population”). The estimate was annualized as “percent per year” using the formula: crude incidence × ([365 days/170 days] × 100). Ninety-five percent confidence intervals for estimated HIV incidence were constructed using a Bonferroni procedure that assumes a Poisson distribution, an α of 0.025, and adjusts for variability around the 170-day less sensitive EIA window period (132-212 days).17,18
Guided by previous studies,5,6, 8,12, 19 we examined the following demographic and behavioral risk factors associated with HIV infection: ethnicity, age, education, sexual orientation, birthplace, lifetime number of male sex partners, having ever been diagnosed with a sexually transmitted disease, having ever injected drugs, having ever used club drugs, and having ever attended a circuit party. As a result of zero counts of HIV-positive cases and other predictors at some levels of the ethnicity variable, we collapsed the ethnicity variable into 2 categories: participants who self-identified as multiethnic versus participants who chose a single Asian/Pacific Islander ethnic group to avoid analysis problems arising from quasicomplete separation. Unadjusted odds ratios and 95% profile likelihood confidence intervals of the odds ratio for each predictor were calculated by logistic regression. Statistical significance of the predictors was evaluated by likelihood ratio tests. Potential confounders and predictors that were statistically significant at the 0.25 level or below in unadjusted analyses were considered for subsequent multivariate logistic regression models. The number of variables in these models was then reduced by a backward elimination procedure in which the least significant variable was dropped at each step until all variables remaining in the model met the 0.25 significance criterion or were important confounders. Overall fit of the final models after the backward elimination procedure was assessed with the Hosmer-Lemeshow goodness-of-fit test.
We approached 2393 API men during 224 sampling events and screened 2134 (89%) of these men for their eligibility. Of 909 eligible men, 566 (62%) agreed to participate in the study. Participation rates were not significantly different by age and ethnicity. Among the 566 enrollees, 496 reported at least 1 lifetime male sexual partner. The final sample of 496 young API MSM represented diverse API origins: 28% Filipino, 27% Chinese, 16% Vietnamese, 4% Japanese, 4% Thai, 3% Korean, 10% multiethnic, and 8% other Asian or Pacific Islander. The median age was 25 years. Fifty percent were college graduates. Most identified as gay (82%) or bisexual (13%). Seventy percent of participants were born overseas. A majority of foreign-born respondents were Chinese (30%), Filipino (22%), or Vietnamese (21%). The median time in the United States was 13 years (range, <1-28 years).
HIV Risk and Testing Behaviors
The median number of male lifetime sexual partners was 12 (range, 1-300). The median number of male sex partners in the past 6 months was 2 (range, 0-100). Forty-seven percent of the API MSM reported unprotected anal intercourse in the past 6 months (12% insertive only, 9% receptive only, and 26% both insertive and receptive). Seventeen percent of the API MSM reported ever having a sexually transmitted disease. Twenty percent of the API MSM reported having ever attended a circuit party. Sixty percent had used club drugs and 2% had injected drugs in their lifetime. Twenty-four percent of the API MSM had never been tested for HIV.
Prevalence and Incidence of HIV and Sexually Transmitted Diseases
Overall HIV prevalence was 2.6% (Table 1). The annual incidence of HIV was 1.8%. The prevalence of markers for syphilis, gonorrhea, and chlamydia was 0.6%, 0.4%, and 2.9%, respectively.
Factors Associated With HIV Infection
Table 2 presents point estimates and 95% confidence intervals for HIV seroprevalence by participant characteristics. Subgroups of API MSM with high HIV prevalence included men who reported a multiethnic background, 51 or more lifetime male partners, and having ever attended a circuit party. MSM who reported being Thai, having a nongay/bisexual identity, and ever injecting drugs also had high but very imprecise estimates of HIV prevalence (Table 2). Table 3 reports results of bivariate and multivariate logistic regression analyses. In the multivariate analysis, being American-born, having 51 or more lifetime sexual partners, and having attended MSM circuit parties were strongly associated with HIV infection. The Hosmer-Lemeshow test suggests an adequate fit of the final multivariate model (chi-squared  = 6.68, P = 0.35).
Unprotected Anal Intercourse and Knowledge of HIV Seropositivity
Of 13 participants who tested positive for HIV in our study, 5 (38%) knew that they were infected with the virus before being tested in the study, but 8 (62%) did not. Six of the 13 HIV-positive men engaged in unprotected anal intercourse in the past 7 months (46%; none insertive only, 3 receptive only [23%], and 3 both insertive and receptive [23%]). One of 5 men who knew about their HIV infection before being tested in the study engaged in unprotected anal intercourse in the past 6 months (20%; none insertive only and 2 receptive only [20%]), whereas 5 of 8 men who did not know about their infection before being tested in the study engaged in unprotected anal intercourse (63%; none insertive only, 1 receptive only [25%], and 3 both insertive and receptive [38%]).
In our sample of 18- to 29-year-old API MSM who attended venues frequented by MSM in San Francisco, 2.6% were infected with HIV. This estimate was similar to those reported for young API MSM by many previous HIV prevalence studies conducted in other cities.6,9–12,20 For example, the Young Men’s Survey found that HIV prevalence was 3.0% for both 15- to 22-year-old and 23- to 29-year-old API participants.12,20 By contrast, it was 10 times lower than that observed for 18- to 29-year-old API participants (27%) of the San Francisco Young Men’s Health Study.8 This difference could partly be because the Young Men’s Health Study enrolled only 26 APIs and was conducted almost 10 years earlier when San Francisco was thought to have higher background HIV prevalence in its general MSM community, which was estimated as high as 50% in the mid-1980s.21 Of note, the current estimated prevalence of HIV among MSM of all ages (not including MSM who inject drugs) in San Francisco is 27%.22
In our sample of API MSM aged 18 to 29, overall HIV incidence was 1.8%. This estimate was similar to the 2.2% estimated for all MSM in San Francisco.22 We also found that a large proportion of men had never tested, and many who were HIV-positive were unaware of their infection and engaged in unprotected anal intercourse. HIV service providers should recognize API men’s need for early diagnosis and referral for treatment and prevention services. Culturally sensitive and appropriate programs should be developed to increase access to testing among young API MSM because they could encounter barriers to seeking care such as shame and stigma associated with AIDS and homosexuality, language, economic constraints, and legal issues related to immigration status.23–25 In April 2003, the Centers for Disease Control and Prevention issued a new HIV prevention initiative recommending HIV testing as part of routine medical care and use of a rapid oral-fluid test, the OraQuick (OraSure Technologies, Inc., Bethlehem, PA), in nonmedical settings.26 This initiative might target young API MSM to reduce HIV incidence and further spread of the virus.
Circuit party attendance was a notably strong predictor of HIV seropositivity in this population. The odds of being infected with HIV was more than 6 times greater among respondents who had attended a circuit party compared with those who had not. Recent studies have reported high levels of unsafe sex and drug use among circuit party attendees, suggesting great potential for HIV transmission.27–29 Our study documented the association between circuit party attendance and HIV infection. This finding underscores the need for intensive prevention efforts targeting young API MSM who go to circuit parties. It has been suggested that such efforts could include educating men about their risk of substance use and related sexual risk-taking while attending circuit party events, distribution of prevention materials at a party, and changing peer norms promoting risk behaviors.27
In our study, API MSM born outside the United States were less likely to be infected with HIV compared with those born in the United States. This finding contradicts a recent study that showed no difference in HIV prevalence between American- and foreign-born public sexually transmitted disease clinic attendees of all ethnicities in Los Angeles, California.19 However, it is consistent with the gradient in AIDS prevalence observed from Asia to California.30 Comparison of AIDS cases reported through the year 2000 in Japan and San Francisco, for instance, revealed that the cumulative population rate of AIDS was the lowest among adults in Japan (16 per 100,000), followed by Japanese-born Japanese living in San Francisco (310 per 100,000) and American-born Japanese in San Francisco (841 per 100,000). Meanwhile, the cumulative rate of AIDS among all San Franciscans was 3433 per 100,000. Our finding could, in part, reflect the more extensive HIV epidemic afflicting MSM in the United States than those in Asia. In contrast to an estimated HIV prevalence of 27% in San Francisco,22 a recent study of MSM in China, for example, found that 3% of participants tested positive for HIV.31 A majority of foreign-born respondents in our sample emigrated from such countries that are now experiencing an emerging HIV epidemic in the MSM population. Because their likelihood of HIV acquisition could increase with a longer stay in the United States, special attention should be paid to their needs to maintain a lower prevalence in the immigrant group.
Our study found low levels of sexually transmitted diseases among young API MSM. However, more recent data suggest that rectal gonorrhea and early syphilis among API MSM of all ages have been on the rise from 1999 to 2002 in San Francisco.32 These data reported by McFarland and colleagues32 are consistent with other studies that have reported increasing rates of sexually transmitted diseases in the general MSM community in several U.S. cities, including San Francisco.33–36 The high prevalence of unprotected anal intercourse found in our sample suggests that the prevalence of sexually transmitted diseases might increase among young API MSM. Thus, to maintain low levels of sexually transmitted diseases, prevention campaigns should target these men to help reduce their sexual risk behaviors.
We acknowledge that sampling and selection bias might have affected our estimates of HIV infection and risk behaviors. We only sampled English-speaking API men who frequented MSM-identified venues; thus, study findings might not generalize to those who do not speak English or attend public venues. Nonetheless, few API intercepted by our staff only spoke Asian languages. Our staff had language competency in Mandarin, Cantonese, Vietnamese, and Tagalog. The 62% participation rate achieved in our study was comparable to those reported by other venue-based HIV prevalence studies.5,9,12 However, HIV-related risk behaviors between participants and refusals might have differed. Because we have no data to document this possible difference, it is difficult to determine whether our results are over- or underestimates. Nonetheless, this study was able to sample a large number of API MSM to provide a more precise estimate of HIV prevalence, identify correlates of HIV infection, and an estimate of HIV incidence for the first time. Future studies need to validate our results with a more representative sample of API MSM that includes both English- and non-English-speaking men.
Many studies of young MSM have called for early and intensified prevention efforts to curb the rapidly rising HIV epidemic in this population, particularly blacks and Latinos.7,12,13 Although our study documents relatively low HIV prevalence among young API MSM, these men’s prevention needs should not be ignored. Our data show a moderate level of HIV incidence as well as high rates of sexual risk behaviors and limited knowledge about HIV serostatus. These conditions suggest that API HIV prevalence could soon catch up with the majority of the MSM community. HIV would spread rapidly among API men if the number of infected individuals in their sexual networks rises and unsafe sexual practices persist. Educational programs promoting risk reduction strategies, including condom use and HIV testing, must continue to maintain low HIV prevalence in this population. Complacency around the current state of the epidemic within the API MSM community could result in a surge of HIV infections.
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