Anal Sex Role Segregation and Versatility Among Men Who Have Sex With Men: EXPLORE Study : JAIDS Journal of Acquired Immune Deficiency Syndromes

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Brief Report: Epidemiology and Prevention

Anal Sex Role Segregation and Versatility Among Men Who Have Sex With Men

EXPLORE Study

Tieu, Hong-Van MD, MS*,†; Li, Xin MS, PhD; Donnell, Deborah PhD; Vittinghoff, Eric PhD§; Buchbinder, Susan MD; Parente, Zachary G. BA*; Koblin, Beryl PhD*

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JAIDS Journal of Acquired Immune Deficiency Syndromes 64(1):p 121-125, September 1, 2013. | DOI: 10.1097/QAI.0b013e318299cede
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Abstract

Anal sex role patterns and correlates during unprotected anal sex were examined longitudinally among HIV-negative men who have sex with men. Nearly 9.6% were exclusively receptive, 16.7% exclusively insertive, and 63.0% versatile. Versatility was more likely with primary and HIV-negative/unknown status partners and among younger men and substance users but less likely among Blacks and with higher number of partners. Exclusively receptive role was more likely with HIV-negative/unknown status partners and among younger men and substance users but less likely with higher number of partners. Examining anal sex role patterns helps understand the factors that drive the epidemic among men who have sex with men.

INTRODUCTION

The United States HIV epidemic has had a devastating impact on men who have sex with men (MSM), with half of new HIV infections occurring in this risk group.1,2 Among MSM, unprotected anal sex (UAS) is common and poses high acquisition risk, especially to the receptive partner.3–11

Anal sex role preference is an important component of sexual identity among MSM, differs across cultures,12–16 and mostly corresponds to sexual positioning.14 The prevalence of versatile sexual position in UAS, with men assuming both insertive and receptive roles, varies considerably across sociocultural contexts, may affect HIV transmission dynamics,17,18 and may have implications for male circumcision for HIV prevention among MSM. Analysis of anal sex role patterns among MSM in the United States, particularly longitudinal descriptions, has been limited. In this report, we used longitudinal data from HIV-negative MSM in the EXPLORE Study to classify UAS episodes during 6-month periods as exclusively receptive, exclusively insertive, or versatile and identified correlates of these behavioral patterns.

METHODS

The EXPLORE Study recruited MSM in 6 cities between 1999 and 2001.19,20 Men were eligible if they were HIV negative, 16 years or older, and reported having anal sex with ≥1 men in the past year. The participants underwent behavioral risk assessment using audio-computer–assisted self-interviewing technology every 6 months, along with HIV antibody testing. A total of 4295 HIV-negative men were enrolled, with average follow-up of 3.25 years. Follow-up for men who seroconverted ended at the seroconversion study visit. The study did not detect a significant difference in HIV seroincidence between the behavioral intervention and control groups but found lower rates of UAS in the intervention group during follow-up compared with control group.19

Data from the baseline and semiannual visits over 30 months were used for this analysis. At every visit, participants self-reported, using audio-computer–assisted self-interviewing, number of sex acts in the previous 6 months by partner HIV status and anal sex role (insertive vs. receptive), both with and without a condom. The analysis focused on UAS acts, rather than protected anal sex, since we were interested in HIV acquisition and transmission risk conferred by UAS. We first classified the UAS acts reported by each participant across all study visits as exclusively receptive, exclusively insertive, or versatile.

Next, in the primary analysis, we applied this classification to all UAS acts reported at each visit by partner HIV serostatus. Thus, each participant contributed up to 3 outcomes at each included participant-visit (ie, UAS role with HIV-positive, negative, and unknown status partners). Multinomial logistic regression was used to estimate the independent associations of covariates with these repeated measures, contrasting exclusively receptive and versatile with exclusively insertive, the least risky behavioral pattern. Robust standard errors were used to account for within-subject correlation of the repeated outcomes. Participant-visits with missing covariate information were excluded. We assessed the effects of baseline and time-dependent covariates for the previous 6 months. The multinomial models were implemented in Stata Version 12.0 (Stata Corp, College Station, TX).

RESULTS

Baseline Sociodemographic and Risk Behavior Characteristics

Baseline characteristics of the men in EXPLORE have been described previously.19 Mean age was 34 years (SD, 9.4). A majority (73%) were white, 15% Hispanic, and 7% black, and 64% had at least a college degree. Although 40% had an annual household income of <$30,000, 76% were fully employed. Eleven percent reported heavy alcohol use in the 6 months before baseline. Non-injection drug use was reported by 65%. The median number of male sex partners was 7 (interquartile range, 3–18), with 42% reporting ≥10. UAS was reported by 69%, receptive UAS by 48%, and insertive UAS by 55%. Receptive UAS with an HIV-positive or unknown status partner was reported by 28%.

UAS Roles

A majority of the men (63.0%) reported versatile positioning during UAS across all visits, with a median of 7.5 UAS acts per 6-month interval. Among the 17% of participants who were exclusively insertive during UAS, there was a median of 1.0 UAS act per interval; among the 9.6% who were exclusively receptive during UAS, there was a median of 0.8 UAS act per interval. Nearly 11% of the men reported no UAS acts across all visits.

Nearly 70% of the visits (13,552 of 19,416 visits) reported UAS and were included in the analysis. Table 1 shows the distribution of participant-visits contributing to the multivariate analysis of role preferences in UAS. Far fewer visits reported UAS with HIV-positive (1980) and unknown status (5924) than with HIV-negative partners (9001). For visits with UAS, 19.9% of visits were classified as exclusively receptive, 31.2% exclusively insertive, and 48.9% versatile. With HIV-positive partners, 53.5% of included participant-visits were classified as exclusively insertive in UAS. In contrast, with HIV-negative partners, 53.2% were classified as versatile. With unknown status partners, the most prevalent role was exclusively insertive (45.8%).

T1-17
TABLE 1:
Unprotected Anal Sex Role Stratified by HIV Status of Male Sex Partner

Correlates of Anal Sex Role

In multivariate multinomial models (Table 2), partner HIV status was strongly associated with exclusively receptive compared with exclusively insertive periods: 51% more likely with unknown status and 2.3 times more likely with HIV-negative vs. HIV-positive partners. Being exclusively receptive compared with exclusively insertive during UAS was more likely among those reporting amyl nitrate use and less likely among older men, men reporting ≥10 partners, and men reporting Chlamydia infection. Versatility compared with exclusively insertive was also strongly associated with partner HIV status: 34% more likely to report versatility with unknown status and 3.5 times more likely with HIV-negative vs. HIV-positive partners. Men were less likely to be versatile compared with exclusively insertive if they were older, black, and had multiple partners, but more likely to be versatile if they reported having a primary partner and used amyl nitrates, amphetamines, or hallucinogens.

T2-17
TABLE 2:
Correlates of Sexual Role Preference in Unprotected Anal Sex, Multivariate Multinomial Models

DISCUSSION

In one of the few prospective studies to follow a large cohort of MSM over a long period, almost two thirds of men reported both insertive and receptive positions during UAS over 30 months, with only a small proportion remaining exclusively insertive or exclusively receptive. Of participant-visits where UAS was reported, half were classified as versatile.

The prevalence of versatility may have implications for the future of the HIV epidemic. In a cross-sectional study of MSM in San Francisco, 14% were exclusively receptive in the previous 6 months, 30% exclusively insertive, and 55% versatile, very close to our classification of participant-visits during UAS.14 However, when all anal sex acts (both unprotected and protected) were taken into account, we found that a very high proportion (83.6%) had versatility of role (data not shown). Similarly, among MSM in Australia, 83% reported versatility over the previous 12 months, whereas 9% were exclusively insertive and 8% exclusively receptive.21 Several modeling studies proposed that greater role versatility could promote HIV transmission22–25 because versatile men at high infection risk through receptive UAS are likely to transmit HIV through insertive UAS.17,21 A modeling study based in Peru suggested that HIV prevalence in a context in which all men were versatile would stabilize at a level approximately 20% points higher than if only 30% were versatile.17

UAS role patterns may have implications for male circumcision among MSM. Although circumcision has been shown to reduce HIV acquisition among heterosexual men,26–28 data on its effect among MSM are conflicting. A meta-analysis of observational studies failed to show any significant difference in HIV infection between circumcised and uncircumcised MSM.29 Similarly, a Cochrane review did not show any significant effect of male circumcision on HIV acquisition among MSM. However, in the same review, circumcision was found to significantly reduce HIV acquisition by 73% among circumcised MSM who reported exclusively or predominantly insertive anal sex roles.30 Given that male circumcision is likely to be effective in preventing HIV infection only among MSM who are mainly insertive,30,31 our finding that merely 16.7% were exclusively insertive during UAS over 30 months suggests that promoting male circumcision may be of limited value as an HIV prevention strategy for MSM in the United States.

We found that partner HIV status was important in anal sex role, as has been reported by others, with higher risk receptive and versatile roles reported with unknown status and HIV-negative partners.32–35 Versatility was the most common pattern with HIV-negative partners, whereas exclusively insertive behavior during UAS predominated with HIV-positive partners.

Higher prevalence of versatility, relative to exclusively insertive sex, among MSM with primary partners likely reflects better knowledge of partner HIV serostatus. Higher risk role patterns were consistently common with HIV-negative or unknown status partners than HIV infected, suggesting a practice of seropositioning, a type of seroadaptive behavior36–38 already reported as associated with decreased risk of HIV in EXPLORE.39,40 This demonstrated behavioral adaptation to lower risk behaviors based on the knowledge of partners' HIV status highlights the importance of accurate knowledge of HIV status from regular HIV testing in MSM in the United States.

Versatile compared with exclusively insertive roles during UAS were less common among blacks than whites. This finding may reflect the influence of sociocultural constructs of masculinity, sexual identity, and gender role.41,42 In a qualitative study of young black MSM, respondents perceived themselves, and the insertive sex role, as masculine and most expressed a preference for masculine partners to retain their own sense of masculinity and/or maintain their heterosexual identity.42 Similarly, in a cross-sectional sample of MSM, 63% of 24 black respondents preferred being insertive, as compared with 39% of whites; in recent anal intercourse episodes, 54% of black MSM were exclusively insertive.14 These findings are consistent with the conclusion reached by Millett et al43,44 that risk behaviors, in particular UAS, do not explain black/white disparities in HIV incidence.

We found that exclusively receptive and versatile men tended to be younger. A plausible explanation is that in partnerships between men of different ages, the older partner is likely to have higher socioeconomic status and more sexual experience, and the younger to feel disempowered—differences that are then sometimes expressed in traditional sex roles.42 Our finding that exclusively receptive men during UAS tended to be younger might be contributing to the rising HIV incidence in young MSM in the United States.2

Substance use has been clearly found to be associated with unprotected anal intercourse among MSM using global and event-level data.45–50 In our analysis, global use of amyl nitrates during the previous 6 months was associated with higher probability of both exclusively receptive and versatile roles during UAS, whereas global use of amphetamines and hallucinogens during the previous 6 months was associated with versatile roles. However, such an association was not found when examining situational drug and alcohol use in conjunction with UAS. Although substance use may be contributing to UAS risk, these data do not support that substance use in conjunction with UAS has a role in anal sex role decisions.

There are limitations to our study. The differential change in sexual behaviors between intervention and control arms and intensity of risk reduction counseling may limit the generalizability of our results to the general MSM population. Sexual risk behaviors were self-reported, thus subject to recall and social desirability bias, although the latter should have been limited by audio-computer–assisted self-interviewing. Because we focused on UAS episodes only and condom use might not have been accurately reported, misclassification bias might have occurred. Our classification of behaviors as exclusively insertive, exclusively receptive, or versatile may obscure differences between “typical” versatility and behavioral patterns that are predominantly, but not exclusively, insertive or receptive. Last, EXPLORE followed men between 1999 and 2004, and behavioral patterns and their correlates may have changed in the ensuing 10 years.

CONCLUSIONS

The high rate of versatility during UAS may have implications on the future of the HIV epidemic among MSM in the United States, as several modeling studies have suggested the high impact that versatile behaviors have on HIV transmission dynamics. Only a minority of EXPLORE participants were exclusively insertive during UAS, suggesting that promoting male circumcision may have a limited role as an HIV prevention strategy for MSM in the United States. This study provides insight into the prevalence of role segregation and versatility during UAS among MSM in the United States and correlates of these behavioral patterns over time and emphasizes the significance of examining anal sex role patterns in understanding factors driving the HIV epidemic among MSM.

REFERENCES

1. Hall HI, Song R, Rhodes P, et al.. Estimation of HIV incidence in the United States. JAMA. 2008;300:520–529.
2. Prejean J, Song R, Hernandez A, et al.. Estimated HIV incidence in the United States, 2006–2009. PLoS One. 2011;6:e17502.
3. Koblin BA, Torian LV, Guilin V, et al.. High prevalence of HIV infection among young men who have sex with men in New York City. AIDS. 2000;14:1793–1800.
4. Ruiz J, Facer M, Sun RK. Risk factors for human immunodeficiency virus infection and unprotected anal intercourse among young men who have sex with men. Sex Transm Dis. 1998;25:100–107.
5. Buchbinder SP, Douglas JM Jr, McKirnan DJ, et al.. Feasibility of human immunodeficiency virus vaccine trials in homosexual men in the United States: risk behavior, seroincidence, and willingness to participate. J Infect Dis. 1996;174:954–961.
6. Kingsley LA, Detels R, Kaslow R, et al.. Risk factors for seroconversion to human immunodeficiency virus among male homosexuals. Results from the Multicenter AIDS Cohort Study. Lancet. 1987;1:345–349.
7. Vittinghoff E, Douglas J, Judson F, et al.. Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am J Epidemiol. 1999;150:306–311.
8. Koblin BA, Taylor PE, Avrett S, et al.. The feasibility of HIV-1 vaccine efficacy trials among gay/bisexual men in New York City: Project ACHIEVE. AIDS Community Health Initiative Enroute to the Vaccine Effort. AIDS. 1996;10:1555–1561.
9. Dean L, Meyer I. HIV prevalence and sexual behavior in a cohort of New York City gay men (aged 18–24). J Acquir Immune Defic Syndr Hum Retrovirol. 1995;8:208–211.
10. Osmond DH, Pollack LM, Paul JP, et al.. Changes in prevalence of HIV infection and sexual risk behavior in men who have sex with men in San Francisco: 1997–2002. Am J Public Health. 2007;97:1677–1683.
11. Seage GR III, Mayer KH, Lenderking WR, et al.. HIV and hepatitis B infection and risk behavior in young gay and bisexual men. Public Health Rep. 1997;112:158–167.
12. Hernandez M, Uribe P, Gortmaker S, et al.. Sexual behavior and status for human immunodeficiency virus type 1 among homosexual and bisexual males in Mexico City. Am J Epidemiol. 1992;135:883–894.
13. Carrier JM. "Sex-role preference" as an explanatory variable in homosexual behavior. Arch Sex Behav. 1977;6:53–65.
14. Wei C, Raymond HF. Preference for and maintenance of anal sex roles among men who have sex with men: sociodemographic and behavioral correlates. Arch Sex Behav. 2011;40:829–834.
15. Wegesin DJ, Meyer-Bahlburg HF. Top/bottom self-label, anal sex practices, sex practices, HIV risk and gender role identity in gay men in New York City. J Psychol Human Sex. 2000;12:43–62.
16. Han CS. A qualitative exploration of the relationship between racism and unsafe sex among Asian Pacific Islander gay men. Arch Sex Behav. 2008;37:827–837.
17. Goodreau SM, Peinado J, Goicochea P, et al.. Role versatility among men who have sex with men in urban Peru. J Sex Res. 2007;44:233–239.
18. Goodreau SM, Carnegie NB, Vittinghoff E, et al.. What drives the US and Peruvian HIV epidemics in men who have sex with men (MSM)? PLoS One. 2012;7:e50522.
19. Koblin B, Chesney M, Coates T. Effects of a behavioural intervention to reduce acquisition of HIV infection among men who have sex with men: the EXPLORE randomised controlled study. Lancet. 2004;364:41–50.
20. Koblin BA, Husnik MJ, Colfax G, et al.. Risk factors for HIV infection among men who have sex with men. AIDS. 2006;20:731–739.
21. Lyons A, Pitts M, Smith G, et al.. Versatility and HIV vulnerability: investigating the proportion of Australian gay men having both insertive and receptive anal intercourse. J Sex Med. 2011;8:2164–2171.
22. Wiley JA, Herschkorn SJ. Homosexual role separation and AIDS epidemics: insights from elementary models. J Sex Res. 1989;26:434–449.
23. Van Druten H, Van Griensven F, Hendriks J. Homosexual role segregation: implications for analyzing and modeling the spread of HIV. J Sex Res. 1992;29:477–499.
24. Trichopoulos D, Sparos L, Petridou E. Homosexual role separation and spread of AIDS. Lancet. 1988;2:965–966.
25. Goodreau SM, Goicochea LP, Sanchez J. Sexual role and transmission of HIV type 1 among men who have sex with men, in Peru. J Infect Dis. 2005;191(suppl 1):S147–S158.
26. Gray RH, Kigozi G, Serwadda D, et al.. Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet. 2007;369:657–666.
27. Bailey RC, Moses S, Parker CB, et al.. Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet. 2007;369:643–656.
28. Auvert B, Taljaard D, Lagarde E, et al.. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 Trial. PLoS Med. 2005;2:e298.
29. Millett GA, Flores SA, Marks G, et al.. Circumcision status and risk of HIV and sexually transmitted infections among men who have sex with men: a meta-analysis. JAMA. 2008;300:1674–1684.
30. Wiysonge CS, Kongnyuy EJ, Shey M, et al.. Male circumcision for prevention of homosexual acquisition of HIV in men. Cochrane Database Syst Rev. 2011;6:CD007496.
31. Sanchez J, Sal Y, Rosas VG, Hughes JP, et al.. Male circumcision and risk of HIV acquisition among MSM. AIDS. 2011;25:519–523.
32. Suarez TP, Kelly JA, Pinkerton SD, et al.. Influence of a partner's HIV serostatus, use of highly active antiretroviral therapy, and viral load on perceptions of sexual risk behavior in a community sample of men who have sex with men. J Acquir Immune Defic Syndr. 2001;28:471–477.
33. Crawford JM, Rodden P, Kippax S, et al.. Negotiated safety and other agreements between men in relationships: risk practice redefined. Int J STD AIDS. 2001;12:164–170.
34. Xia Q, Molitor F, Osmond DH, et al.. Knowledge of sexual partner's HIV serostatus and serosorting practices in a California population-based sample of men who have sex with men. AIDS. 2006;20:2081–2089.
35. Van de Ven P, Kippax S, Crawford J, et al.. In a minority of gay men, sexual risk practice indicates strategic positioning for perceived risk reduction rather than unbridled sex. AIDS Care. 2002;14:471–480.
36. Snowden JM, Raymond HF, McFarland W. Prevalence of seroadaptive behaviours of men who have sex with men, San Francisco, 2004. Sex Transm Infect. 2009;85:469–476.
37. Parsons JT, Schrimshaw EW, Wolitski R, et al.. Sexual harm reduction practices of HIV-seropositive gay and bisexual men: serosorting, strategic positioning, and withdrawal before ejaculation. AIDS. 2005;19:S13–S25.
38. McFarland W, Chen YH, Raymond HF, et al.. HIV seroadaptation among individuals, within sexual dyads, and by sexual episodes, men who have sex with men, San Francisco, 2008. AIDS Care. 2011;23:261–268.
39. Philip SS, Yu X, Donnell D, et al.. Serosorting is associated with a decreased risk of HIV seroconversion in the EXPLORE Study Cohort. PLoS One. 2010;9:pii:e12662.
40. Vallabhaneni S, Li X, Vittinghoff E, et al.. Seroadaptive practices: association with HIV acquisition among HIV-negative men who have sex with men. PLoS One. 2012;7:e45718.
41. Williams JK, Wyatt GE, Resell J, et al.. Psychosocial issues among gay- and non-gay-identifying HIV-seropositive African American and Latino MSM. Cultur Divers Ethnic Minor Psychol. 2004;10:268–286.
42. Fields EL, Bogart LM, Smith KC, et al.. HIV risk and perceptions of masculinity among young black men who have sex with men. J Adolesc Health. 2012;50:296–303.
43. Millett GA, Peterson JL, Wolitski RJ, et al.. Greater risk for HIV infection of black men who have sex with men: a critical literature review. Am J Public Health. 2006;96:1007–1019.
44. Millett GA, Flores SA, Peterson JL, et al.. Explaining disparities in HIV infection among black and white men who have sex with men: a meta-analysis of HIV risk behaviors. AIDS. 2007;21:2083–2091.
45. Van Tieu H, Koblin BA. HIV, alcohol, and noninjection drug use. Curr Opin HIV AIDS. 2009;4:314–318.
46. Colfax G, Guzman R. Club drugs and HIV infection: a review. Clin Infect Dis. 2006;42:1463–1469.
47. Plankey MW, Ostrow DG, Stall R, et al.. The relationship between methamphetamine and popper use and risk of HIV seroconversion in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr. 2007;45:85–92.
48. Carey JW, Mejia R, Bingham T, et al.. Drug use, high-risk sex behaviors, and increased risk for recent HIV infection among men who have sex with men in Chicago and Los Angeles. AIDS Behav. 2009;13:1084–1096.
49. Koblin BA, Murrill C, Camacho M, et al.. Amphetamine use and sexual risk among men who have sex with men: results from the National HIV Behavioral Surveillance study—New York City. Subst Use Misuse. 2007;42:1613–1628.
50. Mansergh G, Shouse RL, Marks G, et al.. Methamphetamine and sildenafil (Viagra) use are linked to unprotected receptive and insertive anal sex, respectively, in a sample of men who have sex with men. Sex Transm Infect. 2006;82:131–134.
Keywords:

role segregation; versatility; anal sex role; men who have sex with men; HIV

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