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Homophobia as a Barrier to HIV Prevention Service Access for Young Men Who Have Sex With Men To the Editors: Men who have sex with men (MSM) bear a disproportionate HIV burden across low- and middle-income countries, and there has been a reemergence of HIV among MSM in high-income regions.1–3 Despite this excess burden, it is estimated that only 1.2% of all HIV prevention funding is targeted toward MSM.4 Globally, HIV prevention services only reach an estimated 10% of MSM, demonstrating that coverage of HIV services for MSM is not commensurate with need.5,6 Among MSM, young men who have sex with men (YMSM) face a unique set of challenges that make them particularly vulnerable to HIV infection and poorer HIVrelated health outcomes.7 YMSM account for a large proportion of incident and newly diagnosed HIV cases in many parts of the world.8–10 Increased HIV risk among YMSM has been connected with a myriad of risk factors, including disparities in access to health services and structural factors like homophobia (ie, sexual stigma,11 defined as the “shared belief system through which homosexuality is denigrated, discredited, and constructed as invalid relative to heterosexuality11,12(p1)”), which have been associated with increased HIV risk behaviors and decreased rates of HIV testing among MSM.13–22 Despite their heightened vulnerability, there is a paucity of research examining the social and structural determinants of accessibility of HIV prevention services among YMSM, especially outside the United States. Moreover, programmatic Supported by a grant from the Bill and Melinda Gates Foundation (Grant Number: OPP52767). The funder did not play any role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the preparation, review, or approval of the article. The authors have no conflicts of interest to disclose.

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data concerning MSM are rarely disaggregated by age, and data on youth are seldom broken out by sexual orientation. Finally, there is an extremely limited amount of data regarding the effects of structural factors on access to evidencebased interventions among YMSM, underscoring a major gap in public health research. We characterized disparities in access to HIV prevention services and structural factors among YMSM relative to older MSM. We also assessed the association between social and structural factors and access to HIV services among YMSM. We conducted a secondary analysis on data from a larger cross-sectional study of MSM and their health providers (n = 5066) on access to HIV services, implemented by the Global Forum on MSM & HIV. The methodology of this study has been previously described.23 In brief, from June to August 2010, participants completed an anonymous online survey administered in Chinese, English, French, Russian, and Spanish. The survey measured 12 psychometric constructs, including scales previously validated on homophobia and internalized homophobia (ie, internalized sexual stigma or internalized homonegativity, broadly defined as the process in which MSM internalize society’s negative attitudes about homosexuality) and an 18-item measure on access to recommended HIV prevention services (eg, condoms, lubricants, and HIV testing).11,24–31 The items in the homophobia measure have Likert scales ranging from 1 to 4; low to high responses correspond with strong disagreement to strong agreement with statements on perceived homophobia. The items in the internalized homophobia measure also have responses ranging from 1 to 4; low to high responses correspond with “never” to “often” endorsing statements that reflect internalized homophobia. The items in the accessibility measures have responses ranging from 1 to 5; low to high responses correspond with low to high accessibility of different HIV services (Table 1). Male participants who reported having sex with men and provided complete data on the exposures and outcomes of interest were included in this study. This subset did not differ from the overall sample with respect to

Letters to the Editor

age, education, income, and region (data not shown). The x2 and Wilcoxon rank sum tests were used to evaluate differences between YMSM and older MSM. Among YMSM, multivariable linear regression using a stepwise (backward elimination) procedure was used to identify correlates of access to HIV prevention services while controlling for HIV status. The final model used did not show evidence of departure from linearity in qnorm plots. This study was approved by Research Triangle Institute International’s Internal Review Board. Among the 2981 MSM included and eligible, 47% (n = 1402) were YMSM. YMSM respondents were from Asia (73%), Latin America (9%), Australasia (7%), North America (6%), Europe (3%), and Africa (2%). The median age among YMSM was 25 (interquartile range, 22–28). Self-reported HIV prevalence among YMSM was 14%. The majority of YMSM self-identified as gay (86%) and had 2 or more sexual partners in the past year (67%). Over a third (34%) had never been tested for HIV, 30% reported unstable housing, and 3% were homeless. Results revealed that significantly fewer YMSM reported “easy access” to 17 out of the 18 HIV prevention services measured when compared with older MSM (Table 1). For example, compared with older MSM, YMSM reported lower access to HIV testing [36% vs. 52% (P , 0.001)], condoms [35% vs. 46% (P , 0.001)], and lubricants [21% vs. 33% (P , 0.001)]. Furthermore, YMSM had a significantly lower overall mean score for access to HIV prevention services compared with older MSM [3.1 vs. 3.6 (P , 0.001)]. In addition, we found that a greater percentage of YMSM, relative to older MSM, perceived a high degree of social discrimination based on sexual orientation in their country of residence. A greater proportion of YMSM reported that, in the country where they reside, MSM are not treated like everyone else [95% vs. 93% (P = 0.02)], most people have a poor perception of MSM [68% vs. 63% (P = 0.001)], and most people think that MSM are dangerous [65% vs. 48% (P , 0.001)]. YMSM had significantly higher mean homophobia scores than older MSM [2.5 vs. 2.3 (P , www.jaids.com |

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TABLE 1. Disparities in Access to HIV Prevention Strategies, Homophobia, and Internalized Homophobia Between YMSM and Older MSM YMSM (n = 1402) Access to HIV prevention services (range, 1–5; lowest to highest access; Cronbach alpha = 0.96) Composite score, mean (SD) Measure items (dichotomized): The following is “easily accessible in my community” STI testing HIV counseling HIV testing Condoms STI treatment Antiretroviral therapy† Media campaigns to reduce HIV HIV education materials Mental health services Sex education Lubricants HIV interventions that reduce risk behaviors Free or low-cost medical care Laws and policies to ensure access to HIV prevention services Substance abuse treatment programs Health facilities for MSM Media campaigns to reduce homophobia Needle exchange programs Homophobia (range, 1–4; lowest to highest homophobia; Cronbach alpha = 0.81) Composite score, mean (SD) Measure items (dichotomized): “Strongly/Somewhat Agree” with the following: “In the country I live in .” Gay men/MSM are not treated like everyone else in my country Most people think poorly of gay men/MSM Most people think that gay men/MSM are dangerous Most employers will not hire gay men/MSM Most people think that gay men/MSM cannot be trusted Gay men/MSM are not actively involved in HIV/AIDS policy and program development Most people think that MSM are not as intelligent as the average person Internalized homophobia (range, 1–4; lowest to highest internalized homophobia; Cronbach alpha = 0.84) Composite score, mean (SD) Measure items (dichotomized): “Often/Sometimes” endorse the following: I wish I weren’t gay/bisexual/MSM I think it is best to avoid personal/social involvement with other gay/bisexual/MSM I would accept the chance to be completely heterosexual Being gay/bisexual/MSM is a negative feature of who I am I try to stop being attracted to men I would like to get professional help to change my sexual orientation to straight I do not feel connected with gay/bisexual/MSM

Older MSM (n = 1579)

n

%

n

%

P*

3.1

1

3.6

1

,0.001

559 533 497 488 457 33 398 398 322 308 285 285 292 279 270 162 139 124

40 38 36 35 33 32 29 29 23 22 21 21 21 20 20 12 10 9

962 899 799 717 868 170 558 607 475 386 511 570 519 526 424 325 216 296

62 58 52 46 56 59 36 40 31 25 33 37 34 34 28 21 14 19

,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 0.064 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 0.001 ,0.001

2.5

1

2.3

1

,0.001

1331 951 894 802 647 648 260

95 68 65 57 47 46 19

1461 973 746 835 614 626 286

93 63 48 53 39 40 19

0.02 0.001 ,0.001 0.02 ,0.001 0.001 0.78

1.9

1

1.6

1

,0.001

557 497 463 357 327 289 273

40 36 33 26 23 21 20

452 453 366 301 237 162 173

29 29 24 19 10 10 11

,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001

*The x2 test for dichotomized items, Wilcoxon rank sum test for composite scores. Items in each measure were dichotomized as follows: homophobia items as Strongly/Somewhat agree vs. otherwise, internalized homophobia items as Often/Sometimes vs. otherwise, and access to HIV prevention services as “easily accessible” vs. otherwise. Item responses within each measure were averaged to generate a composite score for homophobia, internalized homophobia, and access to HIV prevention services and Cronbach alphas were calculated to evaluate internal inconsistency. †Among HIV-positive participants (n = 393).

0.001)]. Moreover, we found that a larger proportion of YMSM more frequently endorsed statements that reflect internalized homophobia, relative to older

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MSM. For example, it was more common for YMSM to wish they were not a sexual minority [40% vs. 29% (P , 0.001)], express desire to get profes-

sional help to change their sexual orientation [21% vs. 10% (P , 0.001)], and believe that being a sexual minority is a negative aspect of their identity [26% Ó 2013 Lippincott Williams & Wilkins

J Acquir Immune Defic Syndr  Volume 63, Number 5, August 15, 2013

vs. 19% (P , 0.001)]. The overall mean score for internalized homophobia was significantly higher overall among YMSM compared with older MSM [1.9 vs. 1.6 (P , 0.001)]. Multivariate analyses showed that both homophobia and internalized homophobia were independently and negatively associated with access to HIV prevention among YMSM, controlling for HIV status, relationship status, education, and housing. Increased homophobia was associated with a mean decline of 0.38 points (95% confidence interval: 0.30 to 0.47) in the score for access to HIV prevention services. Increased internalized homophobia was associated with an average decline of 0.27 points (95% confidence interval: 0.17 to 0.37) in the score for access to HIV prevention services among YMSM. In this large online sample, our data suggest that YMSM may be at increased risk for HIV compared with older MSM, due to significant disparities in access to services and social determinants of health. YMSM have considerably lower access to HIV interventions that have been proven effective to prevent HIV infection and transmission. Additionally, YMSM reported higher levels of homophobia and internalized homophobia, which are associated with high-risk sexual behaviors.13,15–17,19–22 Importantly, YMSM who exhibited the greatest levels of homophobia and internalized homophobia had the most compromised access to HIV prevention services, suggesting that higher levels of homophobia adversely impact access to tools that are effective in reducing new HIV infections and forward transmission. This finding is consistent with prior studies that have shown an inverse relationship between higher homophobia and access to HIV services.14,18,32 The combination of these deleterious social factors and the lack of access to services may further exacerbate heightened vulnerability of YMSM to HIV. This study has several limitations. Our study uses a convenience sample and may be subject to selection bias. Although our findings are consistent with other MSM surveys from Asia and Europe, generalizability to all MSM is limited. Moreover, similar to other observational studies, there may be other unmeasured confounders (eg, depression, gender roles) that we did not account for, which may be Ó 2013 Lippincott Williams & Wilkins

associated with both our exposures of interest and access to HIV services. In light of the global shifts in funding investments to key populations most affected by HIV (eg, the Global Fund’s emphasis on sexual orientation and gender identity in their investment strategy), the importance of parallel efforts to reduce barriers to accessing HIV-related services can hardly be overstated. Targeted efforts to alleviate this inequity in access to evidence-based HIV prevention interventions for YMSM are urgently needed to successfully curb the HIV epidemic in this population.26–31 For example, communitybased social marketing campaigns aimed at YMSM social networks and peeradministered network-based health education strategies have shown promise in expanding HIV testing, treatment, and knowledge among YMSM.33,34 The few evidence-based interventions that are specific to YMSM are far from adequate, and scaling-up existing HIV interventions alone will likely be insufficient, as social factors like homophobia impede uptake of HIV prevention services, especially among YMSM.7 Disparities in HIV incidence and access to HIV prevention services among YMSM will likely persist unless prevention services are tailored to the specific needs of YMSM, strategies promoting resilience are supported, and efforts to reduce barriers to access are developed and funded. As we strive to eradicate HIV, structural interventions addressing homophobia and discrimination—including policies decriminalizing homosexuality—should be implemented and prioritized to ensure that YMSM have an equal opportunity for an AIDSfree generation. Glenn-Milo Santos*† Jack Beck‡ Patrick A. Wilson§ Pato Hebert‡ Keletso Makofane‡ Thomas Pyun‡ Tri Do† Sonya Arreolak George Ayala‡ *HIV Prevention Section, San Francisco Department of Public Health, San Francisco, CA †Department of Epidemiology and Biostatistics, School of Medicine,

Letters to the Editor University of California San Francisco, San Francisco, CA ‡The Global Forum on MSM & HIV (MSMGF), Oakland, CA §Department of Sociomedical Sciences, Mailman School of Public Health, Columbia University, New York, NY kUrban Health Program, RTI International, San Francisco, CA

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ERRATA Higher CNS Penetration–Effectiveness of Long-Term Combination Antiretroviral Therapy Is Associated with Better HIV-1 Viral Suppression in Cerebrospinal Fluid: Erratum In the article by Cusini et al, appearing in JAIDS: Journal of Acquired Immune Deficiency Syndromes, Vol. 62, No. 1, pp. 28-35 entitled “Higher CNS Penetration-Effectiveness of Long-term Combination Antiretroviral Therapy Is Associated With Better HIV-1 Viral Suppression in Cerebrospinal Fluid”, there are some errors in Tables 4 and 5. In Table 4, wrong CPE score of patient 1 should be 1 / 7 not 1 / 6 and in Table 5 the median CPE rank 2010 of the treatment regimens with a detectable viral load in CSF should be 6 with a range of 6-7 not with a range of 6-8. The repeated statistical analysis with the corrected score of 7 in patient 1 yield a new odds ratio of 0.37 per unit higher (95% CI: 0.22-0.61) instead of 0.38 (95% CI: 0.17 to 0.87) and a P-value of 0.032 instead of 0.022 maintaining significance (last line of table 5). Therefore, the authors confirm their statement that in our series analysing 87 CSF the patients taking a treatment regimen with a higher CPE rank had a better suppression of HIV-1 in CSF. In the absence of formal PK data on drug elimination in CSF, the extrapolation of the trough levels (Cmin) were based on mean terminal t1/2 in plasma which represented the only surrogate available under the assumption of an instantaneous equilibrium between plasma and CSF. The plasma elimination t1/2 considered were all established in population pharmacokinetic models developed on the basis of a systematic review of published literature. The reported values have thus to be considered as an order of magnitude, rather than as precise values and the authors advocate for further evaluation of the PK behavior of ART in CSF. The corrected tables are shown below. REFERENCE

Cusini A, Vernazza P, Yerly S, et al. Higher CNS penetration-effectiveness of long-term combination antiretroviral therapy is associated with better HIV-1 viral suppression in cerebrospinal fluid. J Acquir Immune Defic Syndr. 2013;62:28–35.

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Homophobia as a barrier to HIV prevention service access for young men who have sex with men.

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