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Article

Commercial Sex Work and Risk of HIV Infection Among Young Drug-Injecting Men Who Have Sex With Men in San Francisco

Bacon, Oliver MD, MPH*; Lum, Paula MD, MPH†; Hahn, Judith PhD, MA‡; Evans, Jennifer MS*; Davidson, Peter BA‡; Moss, Andrew PhD§; Page-Shafer, Kimberly PhD, MPH*

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Author Information

From the *Center for AIDS Prevention Studies, Department of Medicine, University of California San Francisco, California; the † Positive Health Program, Department of Medicine, San Francisco General Hospital and University of California at San Francisco, California; ‡ EPI-CENTER, San Francisco General Hospital, University of California at San Francisco, California; and the § Department of Epidemiology and Biostatistics, University of California San Francisco, California

The authors acknowledge the tireless and dedicated assistance of Pam Axelson, Alya Briceno, John Day, Caycee Cullen, Sugar Edwards, Ro Giuliano, Gina Hobson, Gina Limon, Peter Morse, Kim Pierce, and Kyle Ranson. The authors also acknowledge the San Francisco Community Clinic Consortium for medical services provided through Street Outreach Services and thank all the young men and women who agreed to participate in the UFO Study.

Financial support for the UFO study was provided by the National Institute of Health/National Institute of Drug Abuse grant R01-DA-12803. Dr. Bacon was supported by NIMH grant T32 MH-19105 (Traineeships in AIDS Prevention Studies).

Oliver Bacon designed and performed the data analysis and wrote the manuscript; Paula Lum, Judith Hahn, and Andrew Moss conceived of the UFO study, acquiring the data and contributed to planning the data analysis; Jennifer Evans contributed to planning, performing, and reviewing the data analysis; Peter Davidson contributed to acquiring the data and planning the analysis; and Kimberly Page-Shafer conceived of the UFO study, acquiring the data, assisted with the data analysis and writing of the manuscript. All authors critically reviewed and contributed to the manuscript during its development.

We dedicate this paper to the memory of our colleague, Dr. Mike Pendo, who contributed so creatively to finding ways to reduce risk and prevent HIV among men in San Francisco.

The Committee on Human Subjects Research at the University of California, San Francisco reviewed and approved the study protocol.

Correspondence: Kimberly Page-Shafer, PhD, MPH, the Center for AIDS Prevention Studies, 50 Beale Street, Suite 1200, San Francisco, CA 94105. E-mail: kshafer@psg.ucsf.edu.

Received for publication April 8, 2005, and accepted September 2, 2005.

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Abstract

Objective: The objective of this study was to investigate the relationship between sex work and HIV infection among young injection drug-using men who have sex with men (MSM-IDU).

Study Design: This study was a cross-sectional analysis of behavioral and serologic data collected from 227 street-recruited MSM-IDU in San Francisco, California, between January 2000 and November 2001.

Results: Sixty-eight percent of participants reported being paid by another man for sex. HIV prevalence was 12% (95% confidence interval, 8–16%); 42% of seropositive participants were unaware of their infection. HIV was independently associated with higher number of paying male partners and history of gonorrhea and inversely associated with number of female partners, education, and syringe-sharing. Consistent condom use overall was 41%, but varied significantly by type of partner.

Conclusions: Among MSM-IDU in San Francisco, sex work with men is strongly associated with HIV infection and the prevalence of condom use is low. HIV prevention among MSM-IDU must be tailored to address the excess risk associated with sex work.

THE HIV EPIDEMIC IN SAN FRANCISCO began and continues to be centered in the large population of men who have sex with men (MSM). Injection drug-using men who have sex with men (MSM-IDU) have the highest risk for HIV infection in that city, with an estimated annual incidence of 4.6% in the year 2000, up from 2.0% in 1997.1 By comparison, incidence rates are estimated at 0.6% among IDUs and 1.7% among noninjecting MSM.1 Several studies have noted that HIV infection among IDUs in San Francisco is largely attributable to sexual risk, more so even than injection risk.2,3 A study of street-recruited IDUs, sampled cross-sectionally over 10 years in San Francisco, found strong associations between sex with men and HIV seroconversion among male IDUs and between commercial sex work and seroconversion among female IDUs without a significant contribution from IDU behaviors.2 We have previously found that among young (<30 years) street-recruited IDUs in San Francisco, prevalent HIV infection was concentrated in males who reported sex with men and who were recruited from a neighborhood (the Polk Street area) frequented by male sex workers and street hustlers.3 Elsewhere, Rietmeijer et al4 showed an independent association between nongay-identified MSM, injection drug use, and sex work, or “hustling,” in MSM in Long Beach and Denver. In that study, hustling was associated a higher number of partners, more frequent anal sex with men and women, and less frequent condom use during anal sex with occasional male partners. Both hustlers and drug-injecting MSM reported less consistent condom use with female partners than did other MSM.4 Subpopulations who exhibit overlapping high risk for HIV such as MSM-IDU, sex workers, and nongay-identified men who have sex with men may pose unique challenges for HIV prevention as a result of economic disincentive and nongay-identification.5 In this article, we assess HIV-associated risk and protective behavior (consistent condom use) in a group of young MSM-IDU who also reported a history of sex with men (MSM-IDU) and specifically investigate the hypothesis that risk for HIV infection is independently associated with sex work in this population.

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Materials and Methods

Study Population

We studied 227 males who reported both IDU and sex with men and who were screened for participation in a longitudinal cohort study of young IDU in San Francisco: the UFO-3 Study. The UFO-3 Study cohort is the third in a series of studies of young (<30 years) IDU (UFO-1 studied HIV, hepatitis C virus [HCV], and hepatitis B virus [HBV] infections3,6–8; UFO-2 studied hepatitis B immunization strategies.9 Like in previous studies (UFO-1, 1997–1999), this study focused on young (<30 years), English-speaking IDU for HIV, HCV, and HBV infections using methods described in detail previously.3 In brief, participants in the current study were recruited by peer outreach workers in various high-risk neighborhoods in San Francisco. They were then screened for eligibility and enrolled at one of three study sites located in the Haight, Mission, and Tenderloin areas between January 2000 and November 2001. At baseline, of 846 eligible individuals, 584 (69%) were male, 227 of whom were classified as MSM (acknowledged ever having had receptive or insertive oral or anal intercourse with another man) and are included in this analysis. Participation was anonymous, but participants were recognized with a unique identifier to screen out repeaters; all were paid $20 both at enrollment and on return for test results. The Committee on Human Subjects Research at the University of California, San Francisco, reviewed and approved the study protocol.

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Data Collection

After informed consent, trained interviewers administered a 30- to 45-minute structured questionnaire eliciting information on: demographics; mobility; medical history, including diagnosed sexually transmitted infections (STI) and previous HIV and hepatitis testing; incarceration; past and present injection and noninjection drug use history; and sexual behaviors, including partners, practices, condom use, and sex work, which was defined as ever having received money or drugs in exchange for sex. Participants were asked about both lifetime and current (past 3 months) exposures. All participants received pretest counseling from trained, certified HIV test counselors before venipuncture for serologies.

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Services and Referrals

All participants screened for the study who were either unsure of their vaccination history or stated that they had not been vaccinated were offered hepatitis A virus and HBV vaccination for free. HIV-positive participants who reported no current engagement with care were offered assistance with access. Study staff assisted with follow up to referral services, making appointments, as well as accompanying participants, if desired, to their first provider visit. Drug treatment referrals were also provided to those participants who expressed an interest; intermittently, direct intake was available, allowing highly facilitated referrals, particularly to the outpatient methadone clinic at San Francisco General Hospital. Some special programs were offered such as influenza vaccine during seasonal periods. More generally, outreach workers provided other forms of support such as assistance in replacing lost or stolen identification and accessing social and welfare services. In addition, a nurse practitioner with physician backup was available during specific evenings at the principal study site to assist participants with general medical needs.

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Serologies

Antibody to HIV (anti-HIV) was detected using an enzyme-linked immunoassay (EIA) (Abbott Laboratories, Abbott Park, IL); repeatedly reactive EIAs were confirmed by Western blot. Antibodies to HBV core antigen (anti-HBc) and surface antigen (anti-HBs) were detected using an EIA (Abbott Laboratories). HBV surface antigen (HBsAg) was detected using microparticle EIA (Abbott Laboratories). Antibody to HCV (anti-HCV) was detected using a second-generation EIA (Ortho Diagnostics Systems, Raritan, NJ).

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Statistical Analyses

Point prevalences, odds ratios (ORs), and 95% confidence intervals (CIs) were calculated. Bivariate associations were analyzed using the chi-squared test of association and Fisher exact test for small cell sizes. To examine associations between continuous variables whose values were collected in categorical fashion, the midpoint of each categorical stratum was used (for instance, if participants responded that the number of sexual partners was 5–10, then 7.5 was the estimated number of partners used in analyses). Unconditional multiple logistic regression analysis was used to identify correlates independently associated with HIV infection. Multivariate models were constructed to include variables significant in bivariate analyses, a priori hypotheses, and potential confounders such as age. All analyses were conducted using STATA version 7.0 (Stata Corp., College Station, TX).

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Results

Twenty-seven of 227 participants tested HIV-positive (12%; 95% CI, 8–16%); 47% and 49% had evidence of HCV and HBV infections, respectively (anti-HCV- and anti-HBc-positive). All but one of the 27 HIV-positive men reported previous HIV testing. Although 15 of 26 (58%) knew their HIV status, eight (31%) believed themselves to be HIV-uninfected, and three (12%) did not know their prior test results. Of the 15 who knew of their HIV infection, 11 (73%) had ever received medical care for their HIV disease, and five (33%) were receiving care at the time of the interview.

Sociodemographic characteristics and associations with HIV infection are shown in Table 1. Median age of participants was 23; 80% of participants were white; 88% had been incarcerated at least once; 40% reported unstable housing in the 3 months before interview; and 53% reported selling sex or drugs or panhandling as a main source of income. HIV prevalence decreased significantly with increasing levels of education, but was not associated with age, race, incarceration history, or housing (Table 1).

Table 1
Table 1
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Lifetime Sexual and Drug-Use Exposures

Participants had a median of eight male (interquartile range [IQR] 4–38) and 18 female (IQR 4–38) lifetime sex partners. Two thirds of participants (68%) had engaged in sex work with men, with a median lifetime number of eight paying male partners (IQR 4–38). Over one fourth (28%) reported having been previously diagnosed with an STI by a medical professional. Median number of years of IDU was 5 (IQR 2–7); polysubstance use was common: 78% reported injecting heroin in the previous 3 months, 69% reported injecting methamphetamine, and 50% reported injecting both. The majority (85%) had ever exchanged needles, and 75% procured all (34%) or most (41%) of their needles from exchange services. Table 2 shows selected sexual and drug-use exposures and associations with HIV infection. The odds of HIV infection increased significantly with lifetime number of paying male sex partners: men who reported 11 to 100 such partners compared with none (0) were more likely to have HIV infection (20% vs. 8%; OR, 2.88; 95% CI, 1.03–8.06). The odds of HIV were higher in men who reported male sex partners exclusively compared with men who reported sex with both male and female partners (43% vs. 9%; OR, 7.79; 95% CI, 2.75–22.01) and among those who reported being previously diagnosed with gonorrhea (44% vs. 10%; OR, 7.35; 95% CI, 2.36–22.86) or endocarditis (43% vs. 11%; OR, 6.07; 95% CI, 1.25–29.5). Men who reported higher numbers of female sex partners were significantly less likely to be HIV-infected as were those who reported having ever shared injection equipment (Table 2). No associations were found between HIV infection and recent needle- or equipment-sharing (data not shown).

Table 2
Table 2
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Recent Sexual Behaviors

Seventy-eight percent (N = 177) of MSM-IDU reported at least one anal or vaginal intercourse partner in the 3 months before the interview (recent sexual activity). Of these, 44 (25%), 63 (36%), and 69 (39%) reported sex with men only, women only, or both men and women, respectively. Sixty-six (40%) had only casual partners, 55 (34%) had a steady partner only, and 43 (26%) had both casual and steady partners. Table 3 shows factors, including knowledge of HIV status and types of sexual partnerships and their associations with consistent condom use (defined as using a condom during all episodes of anal or vaginal intercourse with all partners), among those who had recent sexual activity. Less than half (41%) of this group reported consistent condom use; no associations were found between actual or perceived HIV status, but significant differences were noted by partner type. The proportion of men reporting consistent condom use with recent sexual partners was significantly higher among those who reported sex with men exclusively or with men and women (26 of 44 [59%] and 33 of 69 [48%], respectively) compared with those who reported sex with women only (14 of 63 [22%]), among those who reported having casual partners only (38 of 66 [58%]) compared with men who reported only steady partners (13 of 55 [24%]) or steady and casual partners (11 of 43 [26%]), and among those who reported having engaged in sex work in the past 3 months (37 of 73 [51%]) compared with those who did not (16 of 54 [30%]). The proportion of men reporting consistent condom use did not vary with age, education, STI history, use of any particular drug, or route of administration (data not shown).

Table 3
Table 3
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Independent Correlates of HIV Infection

Table 4 shows variables independently associated with HIV infection among MSM-IDU in multivariate analyses. Variables positively associated with HIV infection included number of lifetime paying sexual partners, history of gonorrhea, and having been diagnosed with endocarditis. Number of female sexual partners, years of education, and having ever shared injection equipment were inversely associated with HIV infection. Analyses showed that the number of lifetime paying male partners and having exclusively male sexual partners were highly collinear (or at least on the same causal pathway). Because we sought to examine, a priori, the association between transactional sex and excess risk of HIV in this population, the final model includes the variable describing number of paying male sex partners.

Table 4
Table 4
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Discussion

It is significant that in this population of young MSM, sampled based on a history of IDU, HIV infection is associated primarily with sexual risk factors. The odds of HIV infection were significantly higher (over sixfold) among those who reported 11 or more paying male partners in their lifetime compared with those who reported none. Although male sex work and street hustling have been present in San Francisco for years, particularly in certain neighborhoods,10 little work has been done to assess how these activities contribute to or sustain the HIV epidemic there. Our analysis was undertaken specifically, in part, to quantify the level of excess risk between sex work and HIV infection with the understanding that this group of men is generally much riskier than MSM not engaging in commercial sex work. Sex work, not previously shown to be independently associated with HIV to our knowledge in San Francisco, may have emerged in the present analysis as a result of an “unmasking” effect,11 as the prevalence of other high-risk exposures such as needle-sharing has declined.12 The population of young street-based IDU from which this sample is drawn includes many involved in the illegal street economy (drug sales, theft, panhandling) and survival sex, that is, sexual intercourse in exchange for money for living expenses or drug purchases or for drugs themselves.13,14 Evidence of high-risk sexual partnering is apparent by the high odds of HIV infection in association with gonorrhea in multivariate analyses and with herpes infection in bivariate examination. Paid sex may also be associated with risk not measured in this study. For instance, paying partners may originate from higher risk groups, including older men, who are more likely to be HIV-infected.15 If men with the highest number of partners are more dependent on income from sex work, they may also be less likely to insist on condom use with their clients and more likely to engage in paid unprotected receptive anal intercourse (i.e., “barebacking”16). It is important to note that although significant excess risk for HIV was associated with paying partners in this sample, the level of risk among all participants, regardless of sex work, was quite high.

A very high proportion of participants (59%) did not report consistent condom use during recent anal intercourse. This is substantially higher than reported (39%) in a sample of gay and bisexual IDU in San Francisco by Bluthenthal et al,12 who reported significant declines in unprotected sex among gay and bisexual IDU over a 12-year period. Although reported condom use among men in our study with paying partners (51%) was considerably higher than that reported by men who did not engage in sex work (30%), taken as a whole, this low rate of consistent condom use provides insufficient protection against HIV infection. The high point prevalence of sexual risk reported by men in this study reflects the limitations of both targeting and sustaining behavioral prevention efforts among very high-risk men in San Francisco. Given the high prevalence of HIV in this city and the associations observed between sex work with men and HIV infection, significant measures are needed to increase condom acceptability and promotion, and further attention is urgently needed to address intersecting risk factors in this population. We note that associations between condom use behaviors and risk for HIV infection in this sample cohort should be interpreted cautiously; participants were asked about recent condom use, whereas HIV infection may be remote in many of those infected. Indeed, many of the significant associations with HIV infection addressed lifetime exposures.

Recent injection risk behaviors were not associated with HIV infection; however, an inverse association was found between any lifetime history of sharing needles and prevalent HIV infection. This association is unlikely to reflect a reduced risk of HIV associated with needle-sharing, a known risk factor for HIV acquisition. It may reflect lower current perceived risk-taking among those who knew or thought themselves to be HIV-infected and may therefore have been less likely to report ever sharing in the past. There is some evidence for this: a lower proportion of participants (eight of 15 [53%]) who, on the basis of prior testing, knew they were HIV-positive reported ever sharing equipment than those who reported being HIV-negative (126 of 167 [75%]), although this trend was not quite significant (P = 0.06). Another hypothesis, injection practice serosorting, cannot be assessed because no data were collected regarding participants’ perception or knowledge of injecting partners’ HIV status. Although partner-sorting behaviors are a hypothesized strategy for risk HIV and STD risk reduction,17–19 injection-related serosorting has not been documented. Indeed, other studies of MSM-IDU have found no differences in injection risk or sexual risk concurrent with participants’ HIV status,5,20 and likelihood of HIV serostatus disclosure is low among high-risk MSM21 and MSM who use drugs.22

Methamphetamine use, widely recognized as increasing HIV transmission and risk behavior among MSM in San Francisco,23–27 was highly prevalent among our participants: nearly all (93%) of the sample had injected methamphetamine in their lifetime, and 69% had done so within the prior 3 months. However, no associations were detected between methamphetamine use and risk behavior (inconsistent condom use) or HIV infection, likely as a result of the almost ubiquitous prevalence of methamphetamine exposure.

We have previously reported on the lack of association between HIV infection and sex with female partners among male IDU.3 Because our data are cross-sectional and also do not capture participants’ beliefs or knowledge about the HIV serostatus of their partners, we cannot draw conclusions about the directionality of this association. The men in our study who reported having female sex partners in the prior 3 months were least likely to report consistent condom use, possibly reflecting either an accurate assumption regarding their own HIV status or a decreased concern about risk of acquiring HIV infection from, or transmitting HIV infection to, their female partners. This warrants at least some concern that “bridging” could be occurring between sexually active bisexual or MSM and heterosexual populations, as has been debated in previous work.28–31

The inverse relationship between level of education and HIV risk in developed countries has been observed in many other studies.32–34 Level of education is often interpreted as a marker for socioeconomic status (SES), and lower levels of education and income have been associated with a higher prevalence of various health risk behaviors. It is possible that education is a marker for underreported risk such as more risky injection practices or unmeasured exposures such as decreased self-efficacy, perceived control, or social capital. In our study, the inverse relationship between educational level and HIV risk was robust enough to persist in a population that was young and almost universally of low SES.

This study has a number of limitations inherent to cross-sectional, observational studies. First, the population was recruited and sampled using convenience methods in various areas of San Francisco known to be frequented by IDU, making it difficult to generalize these findings to MSM-IDU populations in other settings. Second, as a result of the cross-sectional nature of the data, temporality cannot be inferred. The consistency of associations between sex exposures and HIV infection are nevertheless instructive regarding key risk for HIV in this population. Third, exposures of sensitive or illegal nature may be underreported, resulting in a conservative bias. This effect, coupled with power constraints associated with small sample size, raises the possibility that associations were not detected when in fact they might have existed (such as the relationship between number of paying male partners and consistent condom use). The small sample size also makes it difficult to detect associations between particular drug classes or routes of ingestion in a sample with widespread polysubstance use. Finally, some analyses and their interpretation were hampered by a lack of detail, including whether participants used condoms correctly, condom breakage, and, as noted, perception and knowledge of sexual (or injecting) partners’ HIV status. Future collection of these types of data may be especially useful in assessing both risky and potentially protective behaviors in groups with multiple risk exposures, potentially leading to new prevention strategies.

The remarkably consistent relationship between HIV infection and numerous sexual risk variables suggests that sexual behavior is a principal target for prevention efforts in this unique population. Among MSM-IDU, excess risk for HIV can be linked contextually (socially, situationally, and biologically) to high-risk sex and drug dependence, interlinked hazards which, combined with the continued high prevalence of HIV, continue to pose the biggest challenge to HIV prevention in San Francisco.5 Sex work poses particular challenges for prevention efforts, because it may offer powerful economic disincentives to condom use. MSM-IDU who are, for lack of a better term, “gay for pay” and have both male and female sex partners, as did many of the participants in this study, may not identify with most prevention campaigns that target men who self-identify as exclusively gay. This may explain why almost half (43%) of the men who tested HIV-positive in this study were unaware of their serostatus. Collectively, the observations in this study reinforce the urgent need for targeted HIV prevention. Current prevention strategies aimed at MSM-IDU use traditional behavioral interventions such as voluntary counseling and testing, education, and condom promotion at HIV testing locations, needle exchanges, and neighborhood venues. Without an effective vaccine, however, it is crucial to try new prevention interventions that do not rely on condom use alone in this vulnerable population with limited opportunity for negotiation during sex. Two such approaches have been proposed, including rectal microbicides and daily, preexposure chemoprophylaxis using antiretroviral medications with low potential for toxicity.35,36 It will be important to include MSM-IDU in any clinical trials of these potential prevention strategies.

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