Skip to main content
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2016 Dec 1.
Published in final edited form as: AIDS Behav. 2015 Dec;19(12):2270–2279. doi: 10.1007/s10461-015-1067-1

Gender Expression and Risk of HIV Infection among Black South African Men Who Have Sex with Men

Theodorus G M Sandfort 1, Tim Lane 2, Curtis Dolezal 1, Vasu Reddy 3
PMCID: PMC4605836  NIHMSID: NIHMS677672  PMID: 25869555

Abstract

To explore demographic, behavioral and psychosocial risk factors for HIV infection in South African MSM we recruited 480 MSM (aged 18 and 44 years) using respondent-driven sampling. Data were collected through individual computer-assisted face-to-face interviews. Participants were tested for HIV. RDS-adjusted HIV prevalence is 30.1% (unadjusted 35.6%). Few participants had ever engaged in both receptive and insertive anal sex; sex with women was frequently reported. Independent demographic and behavioral correlates of HIV infection include age, education, number of male sexual partners, ever having been forced to have sex, and ever having engaged in transactional sex; engagement in sex with women was a protective factor. Psychosocial risk factors independently associated with HIV infection were feminine identification, internalized homophobia, and hazardous drinking. Our findings confirm what has been found in other studies, but also suggest that the dynamics and context of sexual transmission among MSM in South Africa differ from those among MSM in Western countries.

Keywords: South Africa, MSM, HIV prevalence, risk factors, femininity

INTRODUCTION

In the past decade several studies have demonstrated a high prevalence of HIV among MSM in sub-Saharan Africa, providing convincing evidence that even in generalized epidemics, MSM are at elevated risk, with studies reporting a prevalence of up to 50% (118). Beyrer and colleagues (19), in a review of the global epidemiology of HIV infection among MSM, concluded that with an estimated prevalence of 18% in sub-Saharan MSM, the level is substantially higher than that in the general population adult men; they estimated these odds to be 3.8 (20).

Risk factors for HIV infection in sub-Saharan MSM, primarily of demographic and behavioral nature, have been identified as well. Studies have shown that older MSM are more likely to be infected than younger MSM (8, 10, 11, 15, 17, 18, 21, 22), although incidence seems higher among younger MSM (7). HIV infection also seems to be associated with indicators of social vulnerability, including lower levels of education (9, 10), being unemployed (5), and low income (11). Behavioral risk factors for HIV infection in sub-Saharan MSM include having engaged in receptive anal intercourse (6, 8, 9, 11), number of sexual partners (15, 16), having been paid for sex (12, 16, 18, 21) (while having paid for sex seems to be a protective factor (9)), and having experienced violence (5, 17, 22).

One of the few psychosocial factors that have been shown to be associated with HIV infection among sub-Saharan MSM is self-identification as gay (4, 8, 16, 17, 22). Ross and colleagues reported, for instance, that MSM who identified as gay or homosexual had an over three times higher odds [Adjusted Odds Ratio (AOR) 3.06; 95% Confidence Interval (CI) 1.01 to 9.31] of being HIV infected compared to MSM who did identify as bisexual or in another way.

The aim of the present study is to assess HIV prevalence in a community of South African MSM and to explore whether there are psychosocial risk factors of HIV infection in addition to gay identity and independent of demographic and behavioral risk factors. Explored together, these risk factors may enhance our understanding of how HIV is transmitted in this population and inform policy and program priorities. Same-sex sexuality was illegal in South Africa until the end of apartheid; the 1996 Constitution includes explicit prohibition of discrimination based on sexual orientation (23, 24). However, same-sex sexuality remains highly stigmatized, as in other sub-Saharan countries, being among the countries with the lowest level of social acceptance worldwide (25). In addition, gender seems to be a significant factor in the expression of same-sex sexuality, much more so than in developed countries. Display of feminine behaviors and participation in traditionally feminine occupations appears more prominent in the Black gay population in South Africa compared to gay populations in the Western world (2630).

METHODS

Study population

Participants were recruited using respondent-driven sampling (RDS) (31, 32), a strategy chosen because of the hidden nature of homosexuality in South Africa and the importance of fostering a strong sense of confidentiality and safety in potential participants. Eligibility criteria for study participation included age older than 18; having engaged in oral, anal, or masturbatory sex with another man in the prior 12 months; living, working, or socializing in the Tshwane metropolitan area; fluency in English, Sepedi (Northern Sotho), or isiZulu; and willingness to take an HIV rapid test. Consistent with RDS methodology, seeds, 20 in total, distributed between three and five coupons to eligible men from their social networks. Once these men enrolled in the study and completed study procedures, staff provided them with recruitment coupons for further distribution, and so on. Aside from meeting all study eligibility criteria, the seeds were Black and were purposively selected. Based on suggestions in current theoretical literature describing procedures for increasing the probability of long and diverse recruitment chains (3133), we developed a priori a matrix of demographic characteristics (e.g. age, sexual orientation/gender identity, geographic residence) and identified individuals already known to us through previous field work as being able to recruit from large networks (i.e. “sociometric stars”). This approach to identifying and selecting seeds has been described in several studies where RDS has been successfully implemented (22, 34). All study participants received vouchers to be redeemed at a supermarket as primary incentive for their own participation, as well as secondary incentives for each successful referral to the study. All participants were linked using their coupon identification numbers.

Study procedures and measures

All participants completed a 90-minute interviewer-administered computer-assisted personal interview. All interviews were conducted in a safe private space by choice of the participant either in the office of the Human Sciences Research Council in the Center of Pretoria or in one of the townships, e.g., in a community health center. Research staff involved in screening, interviewing, HIV testing, and instruction for participant recruitment were trained in a three-day session.

The survey addressed demographic characteristics (age, education, housing quality (35), financial problems (36, 37)) and behavioral attributes, including engagement in receptive and insertive anal sex, sex with women, and group sex; having received money or other incentives in return for sex (transactional sex); having experienced sexual abuse as a child; and number of male partners. For the current analyses we used lifetime indicators to increase the chances of identifying risk factors that most likely have preceded the infection. Not having information about when infection took place, we considered recent indicators, such as number of partners in the past year, less appropriate.

Sexual attraction was assessed with the question “Do you currently feel more sexually attracted to men or to women?” and a 5-point response scale (1=“Only to women”; 5=“Only to men”). Sexual identification was assessed with the question “What word would you use to describe your sexuality? Would you call yourself gay, bisexual, or straight, or would you use another word?” Self-perceived femininity was assessed with a 6-item scale with 3 items assessing level of masculinity and femininity each (38); Cronbach alpha in this study was .947. Sexual identity confusion and internalized homophobia were assessed with subscales adapted from the Lesbian, Gay, and Bisexual Identity Scale (LGBIS) (39, 40); sexual identity confusion was assessed with a 4-item scale (e.g., “I am not totally sure what my sexual orientation is”) and internalized homophobia was assessed with a 7-item scale (e.g., “I wish I were only sexually attracted to women”); Cronbach alpha was .892 and .849, respectively. Secrecy about one’s sexual orientation was assessed with an 8-item scale based on (41); Cronbach alpha = .960). Hazardous drinking was assessed with the 10-item Alcohol Use Disorders Identification Test (AUDIT)(4246), e.g., “How often during the last year have you had a feeling of guilt or remorse after drinking?” The AUDIT has a theoretical range of 0–40, and a dichotomous score was calculated using the recommended criterion of 8 or higher to indicate hazardous drinking. Drug problems were assessed with 9 items from the Drug Abuse Screening Test (45), e.g., “Are you always able to stop using drugs when you want to?” A dichotomous variable was calculated to indicate a “yes” response to at least one of the 9 drug problem questions.

Following completion of the survey, participants met with a staff nurse for rapid HIV testing. Participants were given the option to learn their HIV status, either immediately or up to 6 weeks after the test. HIV blood testing was conducted following a serial algorithm in accordance with South African national guidelines (47). All participants were screened by licensed nurses using two licensed rapid test kits (EZ Trust HIV 1 & 2, CS Innovation; First Response, Premier Medical Corporation). Non-reactive samples were interpreted as negative. Samples that were reactive on both tests were confirmed as positive. There were no indeterminate results.

Ethical considerations

All study procedures were approved by the New York State Psychiatric Institute Institutional Review Board in the US and the Human Sciences Research Council Research Ethics Committee in South Africa. Participants provided separate written informed consent for the survey and HIV testing components of the study. Study staff provided referrals for further HIV testing and counseling, mental health, or primary care as indicated. All individuals who tested HIV-positive were referred for specialized HIV follow-up care.

Data analysis

Since RDS was the recruitment method used for this sample, all data were adjusted prior to analyses using a RDS II estimator (33, 48). This approach gives greater weight to those with a small personal network size (PNS), since those men presumably would be less likely to be recruited into the study. Weights were calculated as the inverse of the participant’s PNS. This value was then multiplied by the sample size (N) and then divided by the sum of weights (Σw). The following weighting formula reflects the original sample size of 480: (1 / PNS) * (N / Σw). Note that when data are weighted, the Ns produced in different analyses are often slightly discrepant; therefore, Ns may not always add up to 480.

HIV prevalence rates and 95% confidence intervals were calculated for various subsamples and chi-square tests were used to compare HIV prevalence rates among these subsamples. Logistic regressions were run to determine what factors were associated with HIV status. Initially bivariate models were tested with each independent variable (IV) included in the regression individually. Then a backward step-wise regression was used to identify which of the multiple factors within the various domains would be most strongly associated with HIV status. In this approach, the regression model begins with all IVs all in one regression model. It then repeatedly removes the least significant variable and re-runs the model until all the variables in the model are significantly associated with the dependent variable. In this case a backward stepwise approach is strongly indicated because it reduces degrees of freedom by removing unrelated or highly correlated variables and unlike the forward stepwise approach it allows the model to take predictor variable interactions into account.

RESULTS

In total 480 eligible participants were recruited in 18 waves between August 2011 and January 2013. The mean age in the sample was 24.5 years (Standard Deviation 5.3); 52.2% had some post-secondary education; 69.9% identified as gay or transgender; 44.3% had ever had sex with a woman (see Table 1).

Table 1.

Characteristics of men who have sex with men (MSM) and HIV infection in Tshwane, South Africa (RDS-adjusted).

Total
N (%)
HIV prevalence
% (95% CI)
Education
    Secondary or lower 229 (47.8) 37.6 (31.5 – 44.0) ***
    Post secondary 250 (52.2) 23.2 (18.4 – 28.8)
Regular income
    No 312 (64.9) 26.6 (22.0 – 31.8) *
    Yes 169 (35.1) 37.7 (29.8 – 44.2)
Sexually abused as child
    No 429 (89.4) 29.1 (25.0 – 33.6)
    Yes 51 (10.6) 39.2 (27.0 – 52.9)
Anal sex (ever)a
    Receptive only 170 (35.4) 43.5 (36.3 – 51.1) ***
    Insertive only 142 (29.7) 12.7 (08.1 – 19.2)
    Receptive and insertive 165 (34.3) 35.7 (24.4 – 38.3)
Ever sex with a woman
    No 267 (55.7) 42.7 (36.9 – 48.7) ***
    Yes 212 (44.3) 14.2 (10.1 – 19.5)
Ever group sex
    No 392 (81.7) 28.6 (24.3 – 33.2)
    Yes 88 (18.3) 37.5 (28.1 – 48.0)
Ever forced sex by man
    No 417 (87.1) 24.2 (20.4 – 28.6) ***
    Yes 62 (12.9) 69.4 (57.0 – 79.5)
Ever transactional sex
    No 369 (76.9) 23.8 (19.8 – 28.5) ***
    Yes 111 (23.1) 50.5 (41.3 – 59.6)
Sexual attraction
    Only attracted to men 317 (66.0) 37.2 (32.1 – 42.7) ***
    Also attracted to women 163 (34.0) 16.0 (11.1 – 22.4)
Sexual identification
    Gay or transgender 332 (69.6) 38.0 (32.9 – 43.3) ***
    Bisexual, straight or other 145 (30.4) 13.1 (08.5 – 19.6)
Hazardous drinking
    No 267 (55.6) 24.7 (19.9 – 30.2) **
    Yes 213 (44.4) 37.1 (30.9 – 43.8)
Drug problems
    No 427 (88.8) 30.2 (26.0 – 34.7)
    Yes 54 (11.2) 29.6 (19.1 – 42.9)
*

p ≤ .05;

**

p ≤ .01;

***

p ≤ .001.

CI, confidence interval.

a

Three men had engaged in neither insertive nor receptive anal intercourse.

We estimate that 30.1% of Black MSM in the Tshwane metro are HIV infected. MSM who have ever tested for HIV are more likely to test HIV positive in this study than men who have never tested [79.2% versus 67.3%; OR: 1.83, 95% CI: 1.15–2.90]. Among men who have ever tested for HIV, those who had tested one year ago or longer are more likely to be HIV positive than men who had tested within the past year (OR 2.36, 95% CI 1.49–3.94). Among MSM who tested HIV positive, nearly half (48.3%) thought that it was unlikely or very unlikely that they were HIV-infected.

Correlates of HIV infection

In RDS-adjusted bivariate analyses, HIV infection is associated with all included demographic variables. HIV-positive MSM are more likely to be older, have a lower level of education, have regular income from work, live in housing of poorer quality, and have financial problems (see Tables 1 and 2).

Table 2.

Risk factors for HIV infection among men who have sex with men (MSM) in Tshwane, South Africa (RDS-adjusted).

HIV
negative
Mean/%
HIV
positive
Mean/%
Unadjusted
OR (95% CI)
Adjusted
OR (95% CI)a
Sociodemographic
Age (years) 23.7 26.3 1.09 (1.05, 1.13) *** 1.15 (1.10, 1.22) ***
Education (post secondary) 57.4% 40.3% 0.50 (0.34, 0.75) *** 0.58 (0.35, 0.96) *
Regular income 31.8% 42.8% 1.61 (1.08, 2.41) *
Housing quality 4.04 3.60 0.73 (0.62, 0.87) ***
Money problems 2.62 2.88 1.28 (1.05, 1.56) *
Behavioral
Sexually abused as child 9.2% 13.8% 1.54 (0.84, 2.81)
Only receptive anal sex (ever) 28.7% 51.7% 2.63 (1.76, 3.94) ***
Only insertive anal sex (ever) 37.1% 12.6% 0.24 (0.14, 0.42) ***
Number of male partners, lifetimeb 0.83 1.26 7.03 (4.32, 11.42) *** 2.09 (1.12, 3.87) *
Ever sex with a woman 45.3% 20.8% 0.23 (0.14, 0.35) *** 0.43 (0.23, 0.83) *
Ever group sex 16.7% 22.8% 1.48 (0.91, 2.40) 0.43 (0.20, 0.93) *
Ever forced sex by man 5.7% 29.7% 7.00 (3.91, 12.54) *** 3.11 (1.43, 6.79) **
Ever transactional sex 16.4% 38.9% 3.27 (2.10, 5.09) *** 2.17 (1.15, 4.10) *
Psychosocial
Sexual attraction only to men 59.2% 81.9% 3.09 (1.92, 4.97) ***
Identification as gay/transgender 62.2% 86.9% 4.06 (2.39, 6.92) ***
Femininity 2.69 3.49 2.21 (1.78, 2.74) *** 1.50 (1.11, 2.04) **
Sexual identity confusion 2.12 1.85 0.45 (0.31, 0.64) ***
Internalized homophobia 2.23 1.88 0.25 (0.16, 0.37) *** 0.40 (0.22, 0.71) **
Secrecy about orientation 2.38 1.66 0.40 (0.31, 0.51) ***
Hazardous drinking 40.0% 54.5% 1.98 (1.21, 2.67) ** 1.81 (1.06, 3.07) *
Drug problems 11.3% 11.0% 0.98 (0.53, 1.83)

OR = odds ratio; 95% CI = 95% confidence interval.

*

p ≤ .05;

**

p ≤ .01;

***

p ≤ .001.

a

Variables in the multivariate model are the variables that remained after backward stepwise procedures.

b

Log-transformed.

In terms of sexual behavior, men who have engaged in anal sex exclusively as the insertive partner have lower odds of being HIV infected compared to men who either only have practiced receptive anal sex exclusively, or both receptive and insertive anal sex. The more male sexual partners men report (lifetime, log transformed), the more likely it is that they are HIV infected. Men who ever had sex with a woman are less likely to be infected compared to men who never had sex with a woman. Men who ever have been forced by a man to have sex, and men who ever engaged in transactional sex, are more likely to be HIV positive. Having been sexually abused as a child and ever having engaged in group sex are not associated with HIV infection.

In bivariate logistic regressions, HIV infection is also associated with most of the psychosocial variables included in the analyses. Men who report exclusive sexual attraction to men (versus predominant attraction toward men, or any attraction toward women), identification as gay or transgender (versus straight or bisexual), and perception of oneself as relatively more feminine are more likely to be HIV-infected. Men who experience more confusion about their sexual identity and more internalized homophobia, and who are more secretive about their sexual orientation, are less likely to be HIV infected. Men with alcohol use problems are more likely to be infected. Having drug use problems is not associated with HIV infection.

Multivariate analyses

In the multivariate backward stepwise logistic regression analysis, age and education continue to be associated with HIV infection (Table 2). Behavioral characteristics independently associated with greater odds of HIV infection are number of male sexual partners (lifetime, log transformed), ever having had sex with a woman, ever having been forced by a man to have sex, and ever having engaged in transactional sex. Men who report more lifetime male sex partners, ever had been forced by a man to have sex, and ever engaged in transactional sex are more likely to be infected. Men who ever engaged in sex with a woman or in group sex are less likely to be HIV infected.

Psychosocial characteristics independently associated with HIV infection are femininity, internalized homophobia, and hazardous drinking. Men who see themselves as feminine, experience less internalized homophobia, and engage in hazardous drinking are more likely to be infected.

DISCUSSION

Our study documents a prevalence of HIV of 30.1% among Black MSM living in Tshwane. This is at the higher end of the prevalence range of other studies conducted among MSM in South Africa (4, 8, 11, 17, 22). Differences in HIV prevalence between studies—ranging from 13.2% (11) to 28.3% (22) for RDS-adjusted estimates and from 10.4% (4) to 49.5% (8) for unadjusted estimates—are likely to reflect differences in provincial HIV prevalence levels (49) in addition to difference in sampling methods, sample characteristics, moment when studies were conducted, and whether or not estimates were RDS-adjusted. The prevalence reported in this study is higher than what is reported for the population in general in Gauteng province and comparable to the prevalence among young women observed in antenatal care clinics (50). That men who tested HIV positive in this study are less likely to have been tested in the past year compared to men who test negative might suggest an avoidance of HIV testing due to an awareness of increased risk of infection. It could also be that for some men there was no reason to get tested in the past year because they had tested positive before; however, while 145 men tested HIV positive in the study, only 29 men said that it was very likely that they were positive of whom 16 actually tested negative.

Our results show a clear association between HIV and underexplored psychosocial factors that are specific to emerging African gay communities. In particular, the gender nonconforming subset of the MSM population has significantly higher odds of HIV infection as measured through feminine gender identification. Conversely, sexual identity confusion, i.e. men’s uncertainty about their same-sex desires, also correlates with decreased risk of HIV infection, as does internalized homophobia and secrecy about sexual identity or behavior. These factors appear to operate quite differently from what has been observed in US MSM populations. In contrast to the US literature, which has demonstrated internalized homophobia to be positively associated with sexual risk behavior and HIV infection (5156), our findings suggest internalized homophobia to have a protective effect against HIV infection. We attribute this to the comparatively larger proportion of non-gay identifying MSM, who are gender conforming and more likely to exclusively adopt the insertive role in anal sex, experience greater sexual identity confusion, and therefore are less open about their same-sex desires or practices; because of their sexual role, their infection risk is lower than that of the gay-identifying feminine men who are more likely to engage in receptive anal intercourse, and be more open about their sexuality (8, 57, 58); preliminary analyses seem to support this interpretation (59).

Regarding demographic and behavioral risk factors of HIV infection our findings confirm those of other studies and offer some additional insights. Demographic factors suggest that social vulnerability, including low education, poor housing and no regular income, are risk factors for HIV infection in this population (5, 911), as it has been found in the South African population in general (49). Most behavioral variables are bivariately associated with HIV infection in the expected direction. As in other studies, lifetime number of male partners is associated with greater likelihood of being infected (15, 16), as is engagement in receptive anal intercourse (6, 8, 9, 11). Transactional sex and forced sex by men (life time) turn out to substantially increase men’s risk for HIV infection, independent of other factors (5, 12, 1618, 21).

Two counterintuitive findings need further explanation: having engaged in insertive anal sex and ever having had sex with women resulted in lower odds of HIV infection. These findings can only be understood by taking into account specific characteristics of this population. Among African MSM populations, the proportion of men who also have sex with women is much higher than what usually is observed in samples of MSM populations in the US. Furthermore, these men are much more likely to only engage in insertive anal sex when they have sex with men. However, MSM who do not have sex with women are much more likely to engage exclusively in receptive anal intercourse (6, 6062). Given the higher efficiency of HIV transmission for receptive anal sex (63), insertive sex and sex with women are likely to be “protective” factors in the population of African MSM (8, 11, 57).

Another surprising finding is that experiences of child sexual abuse are not associated with HIV infection, while this has been identified among Western gay men as an important determinant of sexual risk behavior (64) as well as HIV infection (65). As far as we know, none of the studies that identified risk factors for HIV infection in African MSM has established childhood sexual abuse as a risk factor, potentially indicating that the effect of this abuse is overshadowed by other factors or is culturally specific.

All psychosocial variables included in the study, except for drug use problems, are bivariately associated with HIV infection. The observed association between hazardous drinking and HIV infection has been noted in other studies (66), and could reflect either that those engaging in excessive alcohol consumption are more likely to engage in risky sexual interactions; or that problem drinking is a coping behavior among HIV-positive MSM (67). However, because of what is known about alcohol consumption patterns among black South African MSM (68), it is more likely that hazardous drinking has an enduring character and is associated with a way of living that also includes risky sexual practices. Both behaviors should be seen in the context of strong societal rejection of same-sex sexuality that might promote risky sexual practices as well as hazardous alcohol consumption.

Multivariate modeling of demographic and behavioral risk factors shows results that are remarkably consistent with other scholarship from the region. However, our analysis includes psychosocial factors which independently contribute to the risk of HIV infection. Furthermore, while other studies (4, 8, 11, 6971) have shown the higher risk among gay-identified MSM in Africa but also in the US and the Caribbean, our analysis shows the importance of gender non-conformity which may intersect with gay identification to produce unique risks (72).

Our findings suggest two other conclusions about HIV transmission among MSM in South Africa. Bivariate results suggest that those MSM most affected by HIV are not actually driving the epidemic among South African MSM. Given the smaller likelihood of transmission from a receptive to an insertive partner than vice versa (63), those MSM most affected are rather likely endpoints in high-transmission networks centered on men who have sex with both men and women (MSMW) and who are exclusively insertive with other men. These MSMW potentially allow for bi-directional transmission to both women and receptive MSM.

The observed relative exclusivity of receptive and insertive sexual roles (lifetime), also observed in Latin American MSM (73, 74), suggests that HIV prevalence could potentially be much higher among South African MSM if role versatility were more prevalent. Modeling studies have shown that HIV spreads more rapidly if MSM engage in both receptive and insertive anal sex (7578). With over a third of the men only having engaged in either receptive or insertive anal sex during their life, our study found a sexual role exclusivity that is substantially greater than what studies among Western MSM show. Studies among Western MSM populations demonstrate that many MSM have a preference for insertive or receptive anal sex (or for both roles), and that preference cross-sectionally corresponds with actual practice (79). Behaviorally and over a longer time period these MSM are, however, more likely to engage in both roles. For instance, 63% of the 4295 MSM from 6 major US-cities had a versatile behavior pattern over a 30-month period (80). Other studies report similar or even bigger proportions of MSM who engage in both receptive and insertive anal sex (57, 8185). Our ethnographic research suggests that versatility may be becoming more prevalent among MSM in South Africa, as local MSM communities, through increased exposure, adopt sexual practices and identities informed by the ideologies of global gay-identified communities, particularly those of the North American, Western European, and Australian gay communities whose sexualities are currently most in vogue in emerging gay community contexts. This development, also observed in other non-Western cultures (86), would imply a critical moment for HIV prevention to prevent a sudden rise in infections.

Our findings have several practical implications. First and foremost, our findings make clear that MSM as a category comprise diverse expressions in terms of self-identification, gender identification, and sexual role patterns. This diversity has implications for how these different groups can be reached and should be addressed. Because of their visibility, the more feminine men who identify as gay are probably the easiest to reach, although in accessing services they might encounter specific stigma related to their gender-nonconforming behavior. The men who do not identify as gay can probably best be reached through their gay-identifying sexual partners or by mainstreaming prevention and including attention for transmission through anal sex and sex between men in prevention efforts targeting the general population. Because the engagement in sex varies, men need different skills to protect themselves; while feminine men need the competence to negotiate that their insertive partners use condoms, the men who are more likely to have the insertive role need to be convinced of the need to protect themselves, but more importantly, their receptive partner. These negotiations are of course complicated by other factors, such as the relative scarcity of insertive partners, and lack of resources and resulting transactional sex. Interventions focusing on the promotion of HIV testing seem particularly relevant for MSM who identify as gay and feminine.

While our study focused on comparisons between men, it should be stressed that their behaviors occur in a social context in which acceptance of same-sex sexuality is extremely low compared to Western contexts. As others have argued and demonstrated, this context contributes to risky sexual practices as well as a lack of adequate policy responses (8789), indicating the relevance of interventions that include structural components (9092).

The cross-sectional design of the study limits the ability to make causal inferences. Other limitations are related to the assumptions of the RDS methodology; it is possible that not all subgroups of MSM are proportionally represented. In addition, to recruit the required sample size we had to use a larger than optimal number of seeds. Due to transportation challenges in a low-resource environment, the recruitment period was long. Furthermore, there is a potential selection bias towards those who sought HIV testing in a competent care environment. It is possible that sensitive behaviors were underreported (e.g., transactional sex, receptive sex) or over-reported (e.g., exclusively insertive sex). Although we assessed assumed likelihood of being HIV positive, we did not identify men who knew they were HIV positive; linkage to and retention in care, and medication adherence were also not assessed. Finally, it could be that there are unmeasured co-founders that were not taken into account in the multivariate models.

CONCLUSIONS

This study confirms the high prevalence of HIV among South African MSM. The identified risk factors for HIV infection confirm findings from other studies but also reflect the distinctiveness of this population of South African MSM, with sex role exclusivity being relatively frequent and feminine self-identification being relatively common. The dynamics and context of sexual transmission among MSM in South Africa seem to differ from those among MSM in Western countries.

ACKNOWLEDGMENTS

We thank OUT Well-being, the communities that partnered with us in conducting this research, and the study participants for their contributions. We also thank study staff at all participating institutions for their work and dedication, in particular Kate Collier, MPH, and William Tsang.

Supported by grants from the National Institute of Mental Health (R01-MH083557; PI: Theodorus Sandfort, PhD, and P30 MH43520; PI: Robert Remien, PhD).

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health.

Footnotes

The authors have no conflict of interest to disclose.

REFERENCES

  • 1.Vuylsteke B, Semde G, Sika L, Crucitti T, Ettiegne Traore V, Buve A, et al. High prevalence of HIV and sexually transmitted infections among male sex workers in Abidjan, Cote d'Ivoire: need for services tailored to their needs. Sex Transm Infect. 2012;88(4):288–293. doi: 10.1136/sextrans-2011-050276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Baral S, Sifakis F, Cleghorn F, Beyrer C. Elevated risk for HIV infection among men who have sex with men in low- and middle-income countries 2000–2006: a systematic review. PLoS Med. 2007;4(12):e339. doi: 10.1371/journal.pmed.0040339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Wade AS, Larmarange J, Diop AK, Diop O, Gueye K, Marra A, et al. Reduction in risk-taking behaviors among MSM in Senegal between 2004 and 2007 and prevalence of HIV and other STIs. ELIHoS Project, ANRS 12139. AIDS Care. 2010;22(4):409–414. doi: 10.1080/09540120903253973. [DOI] [PubMed] [Google Scholar]
  • 4.Burrell E, Mark D, Grant R, Wood R, Bekker LG. Sexual risk behaviours and HIV-1 prevalence among urban men who have sex with men in Cape Town, South Africa. Sex Health. 2010;7(2):149–153. doi: 10.1071/SH09090. [DOI] [PubMed] [Google Scholar]
  • 5.Baral S, Burrell E, Scheibe A, Brown B, Beyrer C, Bekker LG. HIV risk and associations of HIV infection among men who have sex with men in peri-urban Cape Town, South Africa. BMC Public Health. 2011:11. doi: 10.1186/1471-2458-11-766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Sanders EJ, Graham SM, Okuku HS, van der Elst EM, Muhaari A, Davies A, et al. HIV-1 infection in high risk men who have sex with men in Mombasa, Kenya. AIDS. 2007;21(18):2513–2520. doi: 10.1097/QAD.0b013e3282f2704a. [DOI] [PubMed] [Google Scholar]
  • 7.Sanders EJ, Okuku HS, Smith AD, Mwangome M, Wahome E, Fegan G, et al. High HIV-1 incidence, correlates of HIV-1 acquisition, and high viral loads following seroconversion among men who have sex with men in Coastal Kenya. AIDS. 2012;27:437–446. doi: 10.1097/QAD.0b013e32835b0f81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Rispel LC, Metcalf CA, Cloete A, Reddy V, Lombard C. HIV prevalence and risk practices among men who have sex with men in two South African cities. J Acquir Immune Defic Syndr. 2011;57(1):69–76. doi: 10.1097/QAI.0b013e318211b40a. [DOI] [PubMed] [Google Scholar]
  • 9.Price MA, Rida W, Mwangome M, Mutua G, Middelkoop K, Roux S, et al. Identifying at-risk populations in Kenya and South Africa: HIV incidence in cohorts of men who report sex with men, sex workers, and youth. J Acquir Immune Defic Syndr. 2012;59(2):185–193. doi: 10.1097/QAI.0b013e31823d8693. [DOI] [PubMed] [Google Scholar]
  • 10.Merrigan M, Azeez A, Afolabi B, Chabikuli ON, Onyekwena O, Eluwa G, et al. HIV prevalence and risk behaviours among men having sex with men in Nigeria. Sex Transm Infect. 2011;87(1):65–70. doi: 10.1136/sti.2008.034991. [DOI] [PubMed] [Google Scholar]
  • 11.Lane T, Raymond HF, Dladla S, Rasethe J, Struthers H, McFarland W, et al. High HIV prevalence among men who have sex with men in Soweto, South Africa: results from the Soweto Men's Study. AIDS Behav. 2011;15(3):626–634. doi: 10.1007/s10461-009-9598-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Dahoma M, Johnston LG, Holman A, Miller LA, Mussa M, Othman A, et al. HIV and related risk behavior among men who have sex with men in Zanzibar, Tanzania: results of a behavioral surveillance survey. AIDS Behav. 2011;15(1):186–192. doi: 10.1007/s10461-009-9646-7. [DOI] [PubMed] [Google Scholar]
  • 13.Smith AD, Tapsoba P, Peshu N, Sanders EJ, Jaffe HW. Men who have sex with men and HIV/AIDS in sub-Saharan Africa. Lancet. 2009;374(9687):416–422. doi: 10.1016/S0140-6736(09)61118-1. [DOI] [PubMed] [Google Scholar]
  • 14.van Griensven F. Men who have sex with men and their HIV epidemics in Africa. AIDS. 2007;21(10):1361–1362. doi: 10.1097/QAD.0b013e328017f868. [DOI] [PubMed] [Google Scholar]
  • 15.Wade AS, Kane CT, Diallo PAN, Diop AK, Gueye K, Mboup S, et al. HIV infection and sexually transmitted infections among men who have sex with men in Senegal. AIDS. 2005;19(18):2133–2140. doi: 10.1097/01.aids.0000194128.97640.07. [DOI] [PubMed] [Google Scholar]
  • 16.Ross MW, Nyoni J, Ahaneku HO, Mbwambo J, McClelland RS, McCurdy SA. High HIV seroprevalence, rectal STIs and risky sexual behaviour in men who have sex with men in Dar es Salaam and Tanga, Tanzania. BMJ open. 2014;4(8):e006175. doi: 10.1136/bmjopen-2014-006175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Lane T, Osmand T, Marr A, Shade SB, Dunkle K, Sandfort T, et al. The Mpumalanga Men's Study (MPMS): Results of a baseline biological and behavioral HIV surveillance survey in two MSM communities in South Africa. PLoS ONE. 2014;9(11):e111063. doi: 10.1371/journal.pone.0111063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Vu L, Adebajo S, Tun W, Sheehy M, Karlyn A, Njab J, et al. High HIV prevalence among men who have sex with men in Nigeria: implications for combination prevention. J Acquir Immune Defic Syndr. 2013;63(2):221–227. doi: 10.1097/QAI.0b013e31828a3e60. [DOI] [PubMed] [Google Scholar]
  • 19.Beyrer C, Baral SD, van Griensven F, Goodreau SM, Chariyalertsak S, Wirtz AL, et al. Global epidemiology of HIV infection in men who have sex with men. Lancet. 2012;380(9839):367–3677. doi: 10.1016/S0140-6736(12)60821-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Beyrer C, Baral SD, Walker D, Wirtz AL, Johns B, Sifakis F. The expanding epidemics of HIV Type 1 among men who have sex with men in low- and middle-income countries: diversity and consistency. Epidemiol Rev. 2010;32(1):137–151. doi: 10.1093/epirev/mxq011. [DOI] [PubMed] [Google Scholar]
  • 21.Baral S, Trapence G, Motimedi F, Umar E, Iipinge S, Dausab F, et al. HIV prevalence, risks for HIV infection, and human rights among men who have sex with men (MSM) in Malawi, Namibia, and Botswana. PLoS One. 2009;4(3):e4997. doi: 10.1371/journal.pone.0004997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Cock J. Engendering gay and lesbian rights: The equality clause in the South African constitution. Women Stud Int Forum. 2003;26(1):35–45. [Google Scholar]
  • 23.Hoad N, Martin K, Reid G, editors. Sex & Politics in South Africa. Cape Town: Double Storey; 2005. [Google Scholar]
  • 24.Reid G. The canary of the Constitution: same-sex equality in the public sphere. Soc Dynamics. 2010;36(1):38–51. [Google Scholar]
  • 25.Murray SO, Roscoe W, editors. Boy-wives and Female Husbands. Studies of African Homosexuality. New York: St. Martin's Press; 1998. [Google Scholar]
  • 26.Rabie F, Lesch E. 'I am like a woman': constructions of sexuality among gay men in a low-income South African community. Cult Health Sex. 2009;11(7):717–729. doi: 10.1080/13691050902890344. [DOI] [PubMed] [Google Scholar]
  • 27.Reid G. 'A man is a man completely and a wife is a wife completely': Gender classification and performance amongst 'ladies' and 'gents' in Ermelo, Mpumalanga. In: Reid G, Walker L, editors. Men Behaving Differently South African Men Since 1994. Cape Town: Double Storey; 2005. pp. 205–229. [Google Scholar]
  • 28.Swarr AL. Moffies, artists, and queens: race and the production of South African gay male drag. J Homosexual. 2004;46(3–4):73–89. doi: 10.1300/J082v46n03_05. [DOI] [PubMed] [Google Scholar]
  • 29.Reid G. How to Be a Real Gay: Gay Identities in Small-town South Africa. Scottsville, South Africa: University of KwaZulu-Natal Press; 2013. [Google Scholar]
  • 30.Heckathorn DD. Respondent-driven sampling: A new approach to the study of hidden populations. Soc Probl. 1997;44(2):174–199. [Google Scholar]
  • 31.Heckathorn DD, Semaan S, Broadhead RS, Hughes JJ. Extensions of respondent-driven sampling: a new approach to the study of injection drug users aged 18–25. AIDS Behav. 2002;6(1):55–67. [Google Scholar]
  • 32.Salganik MJ, Heckathorn DD. Sampling and estimation in hidden populations using respondent driven sampling. Sociol Methodol. 2004;34(1):193–240. [Google Scholar]
  • 33.Abdul-Quader AS, Heckathorn DD, McKnight C, Bramson H, Nemeth C, Sabin K, et al. Effectiveness of respondent-driven sampling for recruiting drug users in New York City: findings from a pilot study. J Urban Health. 2006;83(3):459–476. doi: 10.1007/s11524-006-9052-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Lane T, Osmand T, Marr A, Shade SB, Dunkle K, Sandfort T, et al. The Mpumalanga Men's Study (MPMS): Results of a baseline biological and behavioral HIV surveillance survey in two MSM communities in South Africa. PLoS ONE. 2014;9(9):e111063. doi: 10.1371/journal.pone.0111063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Dunkle KL, Jewkes RK, Brown HC, Gray GE, McIntryre JA, Harlow SD. Transactional sex among women in Soweto, South Africa: Prevalence, risk factors and association with HIV infection. Soc Sci Med. 2004;59(8):1581–1592. doi: 10.1016/j.socscimed.2004.02.003. [DOI] [PubMed] [Google Scholar]
  • 36.Díaz RM, Ayala G, Bein E. Sexual risk as an outcome of social oppression: Data from a probability sample of Latino gay men in three U.S. cities. Cultur Divers Ethnic Minor Psychol. 2004;10:255–267. doi: 10.1037/1099-9809.10.3.255. [DOI] [PubMed] [Google Scholar]
  • 37.Díaz RM, Ayala G, Bein E, Henne J, Marin BV. The impact of homophobia, poverty, and racism on the mental health of gay and bisexual Latino men: Findings from 3 US cities. Am J Public Health. 2001;91:927–932. doi: 10.2105/ajph.91.6.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Storms MD. Sex-role identity and its relationships to sex-role attributes and sex-role stereotypes. J Pers Soc Psychol. 1979;37(10):1779–1789. [Google Scholar]
  • 39.Mohr JJ, Fassinger RE. Measuring dimensions of lesbian and gay male experience. Meas Eval Couns Dev. 2000;33:66–90. [Google Scholar]
  • 40.Mohr JJ, Fassinger RE. Sexual orientation identity and romantic relationship quality in same-sex couples. Pers Soc Psychol B. 2006;32(8):1085–1099. doi: 10.1177/0146167206288281. [DOI] [PubMed] [Google Scholar]
  • 41.Day NE, Schoenrade P. Staying in the closet versus coming out: Relationships between communication about sexual orientation and work attitudes. Pers Psychol. 1997;50(1):147–163. [Google Scholar]
  • 42.Barry KL, Fleming MF. The Alcohol Use Disorders Identification Test (AUDIT) and the SMAST-13: Predictive validity in a rural primary care sample. lcohol Alcoholism. 1993;28(1):33–42. [PubMed] [Google Scholar]
  • 43.Bradley KA, McDonell MB, Kivlahan DR, Diehr P, Fihn SD. The AUDIT alcohol consumption questions: Reliability, validity and responsiveness to change in older male primary care patients. Alcohol Clin Exp Res. 1998;22(8):1842–1849. doi: 10.1111/j.1530-0277.1998.tb03991.x. [DOI] [PubMed] [Google Scholar]
  • 44.Gache P, Michaud P, Landry U, Accietto C, Arfaoui S, Wenger O, et al. The Alcohol Use Disorders Identification Test (AUDIT) as a screening tool for excessive drinking in primary care: reliability and validity of a French version. Alcohol Clin Exp Res. 2005;29(11):2001–2007. doi: 10.1097/01.alc.0000187034.58955.64. [DOI] [PubMed] [Google Scholar]
  • 45.Maisto SA, Carey MP, Carey KB, Gordon CM, Gleason JR. Use of the AUDIT and the DAST-10 to identify alcohol and drug use disorders among adults with a severe and persistent mental illness. Psychol Assessment. 2000;12(2):186–192. doi: 10.1037//1040-3590.12.2.186. [DOI] [PubMed] [Google Scholar]
  • 46.Saunders JB, Aasland OG, Babor TF, de la Fuente JR, Grant M. Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO collaborative project on early detection of persons with harmful alcohol consumption--II. Addiction. 1993;88(6):791–804. doi: 10.1111/j.1360-0443.1993.tb02093.x. [DOI] [PubMed] [Google Scholar]
  • 47.Department of Health. National HIV Counselling and Testing (HCT) Policy Guidelines. Pretoria: National Department of Health; 2010. [Google Scholar]
  • 48.Volz E, Heckathorn DD. Probability based estimation theory for respondent driven sampling. J Off Stat. 2008;24(1):79–97. [Google Scholar]
  • 49.Shisana O, Rehle T, Simbayi LC, Zuma K, Jooste S, Pillay-van-Wijk V, et al. South African national HIV prevalence, incidence, behaviour and communication survey, 2008. A turning tide among teenagers? Cape Town: HSRC Press; 2009. [Google Scholar]
  • 50.National Department of Health. The 2012 National Antenatal Sentinel HIV & Herpes Simplex Type-2 Prevalence Survey in South Africa. Pretoria: National Department of Health; 2013. [Google Scholar]
  • 51.Hatzenbuehler ML, Nolen-Hoeksema S, Erickson SJ. Minority stress predictors of HIV risk behavior, substance use, and depressive symptoms: results from a prospective study of bereaved gay men. Health Psychol. 2008;27(4):455–462. doi: 10.1037/0278-6133.27.4.455. [DOI] [PubMed] [Google Scholar]
  • 52.Shoptaw S, Weiss RE, Munjas B, Hucks-Ortiz C, Young SD, Larkins S, et al. Homonegativity, substance use, sexual risk behaviors, and HIV status in poor and ethnic men who have sex with men in Los Angeles. J Urban Health. 2009;(86 Suppl 1):77–92. doi: 10.1007/s11524-009-9372-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Meyer IH, Dean L. Internalized homophobia, intimacy, and sexual behavior among gay and bisexual men. In: Herek GM, editor. Stigma and Sexual Orientation. Thousand Oaks, CA: Sage; 1998. pp. 160–186. [Google Scholar]
  • 54.Newcomb ME, Mustanski B. Moderators of the relationship between internalized homophobia and risky sexual behavior in men who have sex with men: a meta-analysis. Arch Sex Behav. 2009;40(1):189–199. doi: 10.1007/s10508-009-9573-8. [DOI] [PubMed] [Google Scholar]
  • 55.Jeffries WL, Marks G, Lauby J, Murrill CS, Millett GA. Homophobia is associated with sexual behavior that increases risk of acquiring and transmitting HIV infection among Black men who have sex with men. AIDS Behav. 2013;17(4):1442–1453. doi: 10.1007/s10461-012-0189-y. [DOI] [PubMed] [Google Scholar]
  • 56.Ross MW, Berg RC, Schmidt AJ, Hospers HJ, Breveglieri M, Furegato M, et al. Internalised homonegativity predicts HIV-associated risk behavior in European men who have sex with men in a 38-country cross-sectional study: some public health implications of homophobia. BMJ open. 2013;3(2) doi: 10.1136/bmjopen-2012-001928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Hart TA, Wolitski RJ, Purcell DW, Gomez C, Halkitis P. Sexual behavior among HIV-positive men who have sex with men: What's in a label? J Sex Res. 2003;40(2):179–188. doi: 10.1080/00224490309552179. [DOI] [PubMed] [Google Scholar]
  • 58.Vu L, Tun W, Sheehy M, Nel D. Levels and correlates of internalized homophobia among men who have sex with men in Pretoria, South Africa. AIDS Behav. 2012;16(3):717–723. doi: 10.1007/s10461-011-9948-4. [DOI] [PubMed] [Google Scholar]
  • 59.Sandfort TGM. Gender and sexual orientation in South African MSM; Quantitative findings; Paper presented at the LGBT Seminar; February 17, 2015; New York. [Google Scholar]
  • 60.Beyrer C, Trapence G, Motimedi F, Umar E, Iipinge S, Dausab F, et al. Bisexual concurrency, bisexual partnerships, and HIV among Southern African men who have sex with men. Sex Transm Infect. 2010;86(4):323–327. doi: 10.1136/sti.2009.040162. [DOI] [PubMed] [Google Scholar]
  • 61.Caceres CF, Konda KA, Salazar X, Leon SR, Klausner JD, Lescano AG, et al. New populations at high risk of HIV/STIs in low-income, urban coastal Peru. AIDS Behav. 2008;12(4):544–551. doi: 10.1007/s10461-007-9348-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Konda KA, Lescano AG, Leontsini E, Fernandez P, Klausner JD, Coates TJ, et al. High rates of sex with men among high-risk, heterosexually-identified men in low-income, coastal Peru. AIDS Behav. 2008;12(3):483–491. doi: 10.1007/s10461-007-9221-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Baggaley RF, White RG, Boily M-CC. HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention. Int J Epidemiol. 2010;39(4):1048–1063. doi: 10.1093/ije/dyq057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Koenig LJ, Doll LS, O'Leary AE, Pequegnat WE. From child sexual abuse to adult sexual risk: Trauma, revictimization, and intervention. Washington, DC: American Psychological Association; 2004. [Google Scholar]
  • 65.Mimiaga MJ, Noonan E, Donnell D, Safren SA, Koenen KC, Gortmaker S, et al. Childhood sexual abuse is highly associated with HIV risk-taking behavior and infection among MSM in the EXPLORE Study. J Acquir Immune Defic Syndr. 2009;51(3):340–348. doi: 10.1097/QAI.0b013e3181a24b38. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Koblin BA, Husnik MJ, Colfax G, Huang Y, Madison M, Mayer K, et al. Risk factors for HIV infection among men who have sex with men. AIDS. 2006;20(5):731–739. doi: 10.1097/01.aids.0000216374.61442.55. [DOI] [PubMed] [Google Scholar]
  • 67.Daniels J, Maleke K, Lane T, Struthers H, McIntyre J, Coates T. MSM ‘Taking alcohol’ in rural and township settings in South Africa: A pilot study using PhotoVoice to elucidate the relationship between unhealthy alcohol consumption and HIV risk behavior. 20th International AIDS Conference; July 20–25; Melbourne, Australia. 2014. [Google Scholar]
  • 68.Lane T, Shade SB, McIntyre J, Morin SF. Alcohol and sexual risk behavior among men who have sex with men in South African township communities. AIDS Behav. 2008;12(4 Suppl):S78–S85. doi: 10.1007/s10461-008-9389-x. [DOI] [PubMed] [Google Scholar]
  • 69.Tabet SR, de Moya EA, Holmes KK, Krone MR, de Quinones MR, de Lister MB, et al. Sexual behaviors and risk factors for HIV infection among men who have sex with men in the Dominican Republic. AIDS. 1996;10(2):201–206. doi: 10.1097/00002030-199602000-00011. [DOI] [PubMed] [Google Scholar]
  • 70.Maulsby C, Sifakis F, German D, Flynn CP, Holtgrave D. Partner characteristics and undiagnosed HIV seropositivity among men who have sex with men only (MSMO) and men who have sex with men and women (MSMW) in Baltimore. AIDS Behav. 2012;16(3):543–553. doi: 10.1007/s10461-011-0046-4. [DOI] [PubMed] [Google Scholar]
  • 71.Sandfort TGM, Nel J, Rich E, Reddy V, Yi H. HIV testing and self-reported HIV status in South African men who have sex with men: results from a community-based survey. Sex Transm Infect. 2008;84(6):425–429. doi: 10.1136/sti.2008.031500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Logie CH, Newman PA, Chakrapani V, Shunmugam M. Adapting the minority stress model: Associations between gender non-conformity stigma, HIV-related stigma and depression among men who have sex with men in South India. Soc Sci Med. 2012;74(8):1261–1268. doi: 10.1016/j.socscimed.2012.01.008. [DOI] [PubMed] [Google Scholar]
  • 73.Peinado J, Goodreau SM, Goicochea P, Vergara J, Ojeda N, Casapia M, et al. Role versatility among men who have sex with men in urban Peru. J Sex Res. 2007;44(3):233–239. doi: 10.1080/00224490701443676. [DOI] [PubMed] [Google Scholar]
  • 74.Jeffries WL. A comparative analysis of homosexual behaviors, sex role preferences, and anal sex proclivities in Latino and non-Latino men. Arch Sex Behav. 2009;38(5):765–778. doi: 10.1007/s10508-007-9254-4. [DOI] [PubMed] [Google Scholar]
  • 75.Goodreau SM, Golden MR. Biological and demographic causes of high HIV and sexually transmitted disease prevalence in men who have sex with men. Sex Transm Infect. 2007;83(6):458–462. doi: 10.1136/sti.2007.025627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Van Druten H, Van Griensven F, Hendriks J. Homosexual role separation - Implications for analyzing and modeling the spread of HIV. J Sex Res. 1992;29(4):477–499. [Google Scholar]
  • 77.Wiley JA, Herschkorn SJ. Homosexual role separation and Aids epidemics - Insights from elementary models. J Sex Res. 1989;26(4):434–449. [Google Scholar]
  • 78.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(Supplement 1):S147–S158. doi: 10.1086/425268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Moskowitz DA, Rieger G, Roloff ME. Tops, bottoms and versatiles. Sex Relation Ther. 2008;23(3):191–202. [Google Scholar]
  • 80.Tieu HV, Li X, Donnell D, Vittinghoff E, Buchbinder S, Parente ZG, et al. Anal sex role segregation and versatility among men who have sex with men: EXPLORE Study. J Acquir Immune Defic Syndr. 2013;64(1):121–125. doi: 10.1097/QAI.0b013e318299cede. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Lyons A, Pitts M, Grierson J. Versatility and HIV vulnerability: patterns of insertive and receptive anal sex in a national sample of older Australian gay men. AIDS Behav. 2013:1–8. doi: 10.1007/s10461-012-0332-9. [DOI] [PubMed] [Google Scholar]
  • 82.Lyons A, Pitts M, Smith G, Grierson J, Smith A, McNally S, 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(8):2164–2171. doi: 10.1111/j.1743-6109.2010.02197.x. [DOI] [PubMed] [Google Scholar]
  • 83.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(4):829–834. doi: 10.1007/s10508-010-9623-2. [DOI] [PubMed] [Google Scholar]
  • 84.Wegesin DJ, Meyer-Bahlburg HF. Top/bottom self-label, anal sex practices, HIV risk and gender role identity in gay men in New York City. J Psychol Hum Sexuality. 2000;12(3):43–62. [Google Scholar]
  • 85.Pachankis JE, Buttenwieser IG, Bernstein LB, Bayles DO. A longitudinal, mixed methods study of sexual position identity, behavior, and fantasies among young sexual minority men. Arch Sex Behav. 2013;42(7):1241–1253. doi: 10.1007/s10508-013-0090-4. [DOI] [PubMed] [Google Scholar]
  • 86.de Lind van Wijngaarden JW. Being both and acting 'man': exploring patterns of masculinisation among young same-sex-attracted men in Thailand. Cult Health Sex. 2014:1–13. doi: 10.1080/13691058.2014.939595. [DOI] [PubMed] [Google Scholar]
  • 87.Parker RG, Easton D, Klein CH. Structural barriers and facilitators in HIV prevention: A review of international research. AIDS. 2000;14(Suppl 1):S22–S32. doi: 10.1097/00002030-200006001-00004. [DOI] [PubMed] [Google Scholar]
  • 88.Chakrapani V, Newman PA, Shunmugam M, McLuckie A, Melwin F. Structural violence against Kothi-identified men who have sex with men in Chennai, India: a qualitative investigation. AIDS Educ Prev. 2007;19(4):346–364. doi: 10.1521/aeap.2007.19.4.346. [DOI] [PubMed] [Google Scholar]
  • 89.Baral S, Logie CH, Grosso A, Wirtz AL, Beyrer C. Modified social ecological model: a tool to guide the assessment of the risks and risk contexts of HIV epidemics. BMC Public Health. 2013:13. doi: 10.1186/1471-2458-13-482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Cahill S, Valadez R, Ibarrola S. Community-based HIV prevention interventions that combat anti-gay stigma for men who have sex with men and for transgender women. J Public Health Pol. 2013;34(1):69–81. doi: 10.1057/jphp.2012.59. [DOI] [PubMed] [Google Scholar]
  • 91.Mayer KH, Wheeler DP, Bekker LG, Grinsztejn B, Remien RH, Sandfort TGM, et al. Overcoming Biological, Behavioral, and Structural Vulnerabilities: New Directions in Research to Decrease HIV Transmission in Men Who Have Sex With Men. J Acquir Immune Defic Syndr. 2013;63:S161–S167. doi: 10.1097/QAI.0b013e318298700e. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Sullivan PS, Carballo-Dieguez A, Coates T, Goodreau SM, McGowan I, Sanders EJ, et al. Successes and challenges of HIV prevention in men who have sex with men. Lancet. 2012;380(9839):388–399. doi: 10.1016/S0140-6736(12)60955-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

RESOURCES