Association between sexual role and HIV status among Peruvian men who have sex with men seeking an HIV test: a cross-sectional analysis

Abstract

In Latin America, sexual role, sexual identity and sexual practices are intricately related; the roles activo, pasivo and moderno often encompass sexual identity and sexual practices. We aimed to understand the association between sexual role and HIV status in Peruvian men who have sex with men. HIV-testing services at Epicentro Salud, a Peruvian gay men’s health centre, were paired with clinic data on demographics and sexual behaviour. Bidirectional stepwise logistic regression was conducted to determine associations between sexual role and HIV status. Of 366 clients who underwent HIV testing, 86 (23.5%) tested positive. There was a strong association between sexual role (‘activo’ or typically insertive, ‘pasivo’ or typically receptive, ‘moderno’ or typically versatile) and a positive HIV test (p = 0.002). Compared to clients with an activo role, those who reported a pasivo (OR = 6.14) and moderno (OR = 6.26) role were more likely to test positive for HIV. Sexual role was associated with sexual identity (gay, straight and bisexual) and gender of partners in the past six months. Self-reported pasivo and moderno sexual roles were strongly associated with a positive HIV test result. Further research should examine differences in sexual practices between sexual role groups.

Keywords

Peru sexual identity sexual role men homosexual men who have sex with men MSM HIV AIDS receptive anal sex insertive anal sex

Introduction

There were an estimated 76,000 people living with Human Immunodeficiency Virus (HIV) in Peru in 2012.^1,2 The Peruvian HIV epidemic is concentrated among men who have sex with men (MSM) and transgender women (TGW), with 56% of new infections occurring within these populations.³ Compared to the general population HIV prevalence of 0.40% among adults 15–49, in MSM it is estimated to be between 11–23%.^1,2,4–6

When considering HIV transmission among MSM, researchers often distinguish between the level of risk experienced by practicing insertive versus receptive anal sex.⁷ It is well documented, for example, that condomless receptive anal intercourse (AI) carries the highest risk for HIV infection compared to condomless insertive anal intercourse.^8,9 But sexual practices do not occur in a social vacuum, and for this reason it is becoming increasingly common in HIV prevention literature from Latin America to distinguish between sexual identity (homosexual, bisexual, heterosexual and transgender), sexual role (activo, pasivo and moderno) and sexual practices (insertive and/or receptive anal intercourse).¹⁰ Although sexual identity, role and practices refer to distinct aspects, they are intricately related to one another and may overlap; the roles activo, pasivo and moderno often encompass one’s personal identity as well as a sexual act. The ‘activo’ or insertive partner in AI is typically perceived as a dominant role ‘aligned with masculine heterosexuality’, while, being ‘pasivo’, often associated with a feminine identity, is the receptive partner in AI. ‘Moderno’ men engage in both receptive and insertive AI, and this role has been described as a ‘masculine reconceptualization of gay identity’.¹⁰ These identities often reach beyond the act of sex itself to define the way men view themselves, and it is not uncommon for activo men to self-identify as heterosexual and have female partners and covertly pursue sex with men, while pasivo men may more readily self-identify as gay.^10–12

An association between sexual role and HIV among Peruvian MSM has been documented¹⁰; nonetheless, this finding is not universal. For example, among three studies of Mexican MSM, only one found the highest HIV prevalence in receptive MSM, while the remaining two found versatile MSM to have the highest prevalence.^13–16 A study of MSM in India found that receptive MSM had the highest risk for HIV compared to insertive MSM (OR = 5.8) while versatile MSM had lower odds (OR = 4.9).¹⁷ An analysis of 2655 MSM across six Peruvian cities found receptive MSM had the highest HIV prevalence (16.6%) followed by versatile (12.9%) then insertive (6.5%).¹⁸ In a more recent study of Peruvian MSM, versatile men experienced the highest prevalence of HIV.¹⁰

In recent years, several models have been employed to examine the effect of role versatility on the HIV epidemic. Goodreau et al. note that role-versatile sexual networks may contribute to the high HIV prevalence in Peru.¹³ Much of this would be dependent on mixing patterns between the sexual role groups, however, and whether MSM tend to adhere to assortative (like with like) or disassortative (like with unlike) mixing; for example, if versatile MSM are more likely to choose partners who are also versatile identified, or partners who are insertive/receptive.¹³

We aimed to analyse the association between sexual role, sexual identity and sexual practices with HIV status in a community-based sample of MSM.

Materials and methods

We conducted a retrospective analysis of anonymised, existing clinic data from MSM that had received an HIV test during 2012–2013 at Epicentro Salud, a community-based sexually transmitted infection (STI) clinic for MSM/TGW. Rapid HIV testing was performed using the Alere Determine HIV-1/2 Combo Ag/Ab (ALERE Healthcare, S.L.U) test and confirmed by indirect immunofluorescence assay. A physician-administered health behaviours intake form collected information on demographics; self-described sexual identity (gay, bisexual and straight); how clients identify themselves with regard to their sexual role (activo, pasivo, versatile, other); sexual behaviours (number of sex partners and type of sexual behaviours including condom use during the previous three months); partner type (casual, stable, or paid/paying partners; partner’s gender); reported STI symptoms and recreational drug use during sex.

The analysis was restricted to biological males who were first-time HIV testers at the centre, provided data on their sexual role on the health behaviours intake form, and were identified as MSM or MSMW (MSM and women) because they (a) self-identified as gay or bisexual, (b) reported having sex with men in the last six months or (c) reported their most recent sex partner was male. We excluded men who were participating in the various HIV-related research studies underway at the clinic. TGW were not included in this analysis.

Clients were asked two separate questions: (1) what is their overall sexual role (i.e. how they generally identified themselves: activo, pasivo, or moderno) and (2) what was their sexual position with their most recent partner (male partner, activo/insertive position ‘I inserted my penis into my partner’s anus’; male partner, pasivo/receptive position ‘My partner inserted his penis into my anus’; male partner, versatile position ‘We both inserted our penises into each other’s anus’; female partner, vaginal sex).

To assess the association between sexual role and HIV status, a multivariate, bidirectional stepwise logistic regression analysis was performed in Stata version 12.1 (Stata Corp, College Station, TX). This method was chosen because there were two main outcomes of interest and of other potentially associated or confounding variables collected by the survey. Backward elimination was performed on a model including the two main exposures described above (overall sexual role and sexual position with the most recent partner), age, and four variables that yielded significant associations with a positive HIV test (p < 0.05 from a likelihood ratio test [LRT]) during the univariate analysis. Because sexual role and sexual practices are alike, but do not overlap completely, both variables were assessed as main exposures in the same model. Forward selection methods were then utilised by adding remaining variables from the survey to the model one at a time, and testing the models using an LRT. Variables which were not significantly associated with a positive HIV test (p < 0.05), but which changed the coefficient values of sexual role by more than 10%, were kept in the model as potential confounders. Variables which were neither associated with the outcome, nor altered the effect measures of sexual role were discarded.

Association between sexual role and the additional variables in the model was analysed using contingency tables and Chi square test or Fisher’s exact test, as required.

The study was approved by the London School of Hygiene and Tropical Medicine Ethics Committee, and deemed exempt from review by the local human ethics committee in Lima, Peru since it used pre-existing, unidentifiable clinic data.

Results

A total of 366 MSM were included in this dataset with a median age of 26 (range 16–62 years) (Table 1). Of the 97 patients who provided their highest level of schooling, 70.1% (68 patients) had a university level of education. About half (203 or 55.5%) reported their primary visit reason as a general check-up screening, with the second most common reason reported as ‘risky sexual conduct’ (86 patients or 23.5%). Eighty-six (23.5%) tested positive for HIV, and 289 clients (79.0%) self-identified as gay, with 74 identifying as bisexual (20.2%) and three clients (0.8%) as straight. The majority of clients reported a moderno sexual role (196 or 53.6%) followed by an activo role (101 or 27.6%) and then pasivo (69 or 18.9%) (Table 1).

Table 1.

Distribution of HIV cases by variable; crude and adjusted odd ratios for an HIV-positive test result.

Variable	Number of subjects, N (%)	HIV positive, N (%)	OR (95% CI)	AOR^a (95%CI)
Age in years
16–19	28 (7.7)	3 (10.7)	Ref	Ref
20–29	214 (58.5)	58 (27.1)	3.09 (0.90–10.65)	2.96 (0.71–12.33)
30–39	71 (19.4)	14 (19.7)	2.05 (0.53–7.76)	2.04 (0.42–10.02)
40–49	42 (11.5)	10 (23.8)	2.60 (0.64–10.47)	2.83 (0.51–15.63)
50+	11 (3.0)	1 (9.1)	0.83 (0.08–8.99)	0.27 (0.02–5.11)
Occupation^b
Employed/employee	206 (56.3)	59 (28.6)	Ref	Ref
Independently employed	37 (10.1)	7 (18.9)	0.58 (0.24–1.39)	0.54 (0.19–1.51)
Student	111 (30.3)	15 (13.5)	0.39 (0.21–0.73)	0.28 (0.13–0.58)
Unemployed	12 (3.3)	5 (41.7)	1.78 (0.54–5.83)	2.82 (0.70–11.36)
Sexual identity
Gay	289 (79.0)	67 (23.2)	Ref	Ref
Bisexual	74 (20.2)	18 (24.3)	1.07 (0.59–1.93)	0.82 (0.28–2.44)
Straight	3 (0.8)	1 (33.3)	1.65 (0.15–18.55)	9.51 (0.38–237.24)
Overall sexual role^b
Activo	101 (27.6)	8 (7.9)	Ref	Ref
Pasivo	69 (18.9)	21 (30.4)	5.09 (2.09–12.33)	6.14 (1.62–23.23)
Moderno	196 (53.6)	57 (29.1)	4.77 (2.17–10.45)	6.26 (2.17–18.00)
Sexual role with most recent partner
Partner was male – activo/insertive	153 (41.8)	23 (15.0)	Ref	Ref
Partner was male – pasivo/receptive	126 (34.4)	39 (31.0)	2.53 (1.42–4.54)	1.65 (0.70–3.90)
Partner was male – moderno/versatile	76 (20.8)	23 (30.3)	2.45 (1.27–4.75)	1.47 (0.64–3.37)
Partner was female – vaginal	11 (3.0)	1 (9.1)	0.56 (0.07–4.62)	0.07 (0.004–1.41)
Partner in last condomless sexual encounter^b
Does not apply	115 (31.4)	19 (16.5)	Ref	Ref
Casual partner	106 (29.0)	22 (20.8)	1.32 (0.67–2.61)	0.94 (0.42–2.12)
Stable partner	145 (39.6)	45 (31.0)	2.27 (1.24–4.16)	3.88 (1.73–8.70)
Self-reported genital warts in last six months^b
No	326 (89.1)	70 (21.5)	Ref	Ref
Yes	40 (10.9)	16 (40.0)	2.44 (1.23–4.84)	2.82 (1.21–6.61)
Gender of sex partners in last six months
Only men	315 (86.1)	72 (22.9)	Ref	Ref
Men and women	48 (13.1)	13 (27.1)	1.25 (0.62–2.50)	3.44 (0.90–13.16)
Does not apply (No sex in last six months)	3 (0.8)	1 (33.3)	1.69 (0.15–18.87)	0.77 (0.04–16.87)
Who was last sexual partner^b
Stable partner	198 (54.1)	47 (23.7)	Ref	Ref
Casual partner	166 (45.4)	38 (22.9)	1.07 (0.68–1.69)	2.12 (1.03–4.37)
I paid for/was paid for sex	2 (0.6)	1 (50.0)	1.25 (0.13–12.23)	32.11 (1.25–825.00)
At least one sex partner had STI in last three months
No	282 (77.1)	65 (23.1)	Ref	Ref
Yes	38 (10.4)	6 (15.8)	0.63 (0.25–1.56)	0.64 (0.23–1.83)
Does not remember/does not apply	46 (12.6)	15 (32.6)	1.62 (0.82–3.17)	1.54 (0.68–3.48)

AOR adjusted for all variables in the final model.

p < 0.05 from likelihood ratio test.

Multivariate analysis

The final model was based on 366 clients, and included the variables: overall sexual role (activo, pasivo, moderno); sexual position with most recent partner (male partner, insertive position; male partner, receptive position; male partner, versatile position; female partner, vaginal sex); occupation; partner in most recent sexual relationship without a condom (casual, stable, sex worker, other/not applicable); self-reported genital warts in the previous six months; age; sexual identity (gay, straight, bisexual); gender of sex partners in the previous six months (male/female); partner type during last sex (casual, stable, participant paid/was paid for sex); and whether a sexual partner was thought to have an STI in the previous three months. Sexual role with most recent partner, occupation, sexual identity, gender of partners in the previous six months and whether a sexual partner was thought to have an STI in the previous three months each impacted the effect measure of sexual role by 10% or more, and were included in the model as potential confounders.

Sexual role and HIV

In the univariate analysis, clients’ overall sexual role was strongly associated with a positive HIV test (p < 0.0001), as was sexual role with their most recent partner (p = 0.003). In the multivariable analysis, there was strong evidence (p = 0.002) against the null hypothesis of no association between overall sexual role and HIV after controlling for other variables. Compared to the baseline of those who report an activo role, those who reported a pasivo (OR = 6.14, 95% CI = 1.62–22.33) or moderno role (OR = 6.26, 95% CI = 2.17–18.00) were significantly more likely to have a positive HIV test result (Table 1).

Although sexual role with most recent sexual partner was found to be significant in the univariate analysis (p = 0.003), during the multivariate analysis, the LRT was consistent with a weak association when controlled for other variables (p = 0.08).

Sexual role and self-reported partnerships

Overall sexual role was independently associated with the variables sexual position with most recent partner (p < 0.0001), sexual identity (p < 0.0001) and gender of partners in the previous six months (p < 0.0001) using a Fisher’s exact test (Table 2).

Table 2.

Contingency table for association with self-reported sexual role.

	Sexual role
	Activo (%)	Pasivo (%)	Moderno (%)	p
Type of sex partners in the past six months^a
Only men	73 (73.0)	66 (97.1)	176 (90.3)	< 0.0001
Men and women	27 (27.0)	2 (2.9)	19 (9.7)	< 0.0001
Sexual identity^a
Gay	66 (65.3)	63 (91.3%)	160 (81.6)	< 0.0001
Bisexual	33 (32.7)	5 (7.3%)	36 (18.4)
Straight	2 (2.0)	1 (1.5%)	0 (0.0)
Sexual role with most recent partner^a
Partner was male – activo/insertive	92 (91.1)	2 (2.9)	59 (30.1)	< 0.0001
Partner was male – pasivo/receptive	1 (1.0)	66 (95.7)	59 (30.1)
Partner was male – moderno/versatile	1 (1.0)	0 (0.0)	75 (38.3)
Partner was female – vaginal	7 (6.9)	1 (1.5)	3 (1.5)
Was condom used with last sexual partner^a
Yes	67 (66.3)	35 (50.7)	125 (63.8)	0.143
No	33 (32.7)	34 (49.3)	70 (35.7)
Do not remember	1 (1.0)	0 (0.0)	1 (0.5)

p value from a Fisher’s exact test.

In general, activo men were the most likely to report partnerships with women and a bisexual or straight identity, as expected. Moderno men were less likely to report female partnerships than activo men, but more likely than pasivo men to do so. For example, 9.7% of moderno MSM reported having sex with men and women in the previous six months, compared to 27.0% of activo men, and only 2.9% of pasivo men. Likewise, 18.4% of moderno men reported a bisexual identity, compared to 7.3% of pasivo men and 32.7% of activo men (Table 2).

For activo and pasivo MSM, the position reported with their most recent male sexual partner was generally concordant with the overall role with which they identified; 91.1% of activo-identified MSM reported an insertive position with their most recent male partner, and 95.7% of pasivo men reported a receptive role with their most recent partner (Table 2). When asked about their most recent partner, 30.1%, of moderno MSM reported an insertive position, 30.1% reported a receptive position, and 38.3% reported having both receptive and insertive sex with their most recent partner. Activo men were most likely to report that their most recent partner was female (6.9% of activo men), compared to 1.5% among pasivo and moderno men (Table 2).

Sexual role and self-reported STIs

Clients were asked to self-report STI symptoms experienced over the past six months, as well as knowledge of their partners’ STI status. 10.9% of clients self-reported that they had experienced genital warts within the past six months, and 10.4% reported that they thought at least one of their partners had an STI in the past three months. While genital warts were significantly associated with a positive HIV test (p = 0.004), evidence was consistent with no association between genital warts and clients’ overall sexual role (p = 0.451). Knowledge of whether a sexual partner had an STI in the past three months was neither associated with sexual role (p = 0.321) nor HIV (p = 0.319); however, this variable affected the OR for the association between sexual role and HIV by more than 10%.

Discussion

Findings

The HIV prevalence in this sample of clients presenting to a community centre in Lima Peru (23.5%) was high compared to most studies of HIV prevalence in similar populations, which typically range between 11–23%.^1,2,4–6 Sexual role was strongly associated with a positive HIV test, sexual position with most recent partner, sexual identity and gender of partners in the previous six months.

MSM reporting an overall sexual role as moderno had the highest odds of a positive HIV test when adjusted for other variables, followed by pasivo and then activo MSM. Although moderno MSM in our sample had the highest AOR for HIV, they were closely followed by pasivo MSM (Table 1). The finding that moderno and pasivo MSM are at the highest risk of HIV infection is consistent with data from others studies in Peru and worldwide. While insertive MSM are typically found to have lower HIV prevalence compared to receptive and versatile MSM, whether receptive or versatile MSM experience the highest odds varies from study to study.¹³ Further information (such as number of sexual partners) would be useful to understand if these odds are truly similar, or if there are behavioural differences between activo and moderno MSM that account for this apparent similarity.

While activo and pasivo MSM reported role-concordant practices with their most recent male partner, moderno MSM were nearly as likely to report an exclusively insertive or receptive role within their most recent partnership as a versatile role. Qualitative work conducted among Peruvian MSM indicates that versatile men often rely on cultural cues regarding their partners’ identity to determine what role to take within that particular partnership, taking a receptive role if their partner is perceived to be a very masculine activo man, or a receptive role if their partner is perceived to be more effeminate.¹⁰ An overall versatile role was the most commonly reported in our sample and is consistent with Goodreau’s 2007 study, which found that 56% of MSM in Lima identified as versatile, as well as noting the possibility that self-reported versatile identification may be increasing but true increase in versatile behaviour remains unclear.¹⁸

Moderno men were less likely to report female partnerships and bisexual identity than activo men but more likely to do so than receptive men. As moderno MSM experienced the highest odds of HIV in our sample when adjusted for other factors, it is worth considering that moderno MSM who also have sex with women may act as a bridging population for HIV from the gay community to women in Peru. While we found no evidence in the published literature indicating the spread of HIV from moderno MSM to women, one study found that 35% of moderno men reported having a female partner in the past three months, and questioned whether activo men (with a lower risk for HIV, but who are more likely to have female partners) or moderno men (with an intermediate risk for HIV, but fewer reported female partners) posed greater risk of acting as a bridging population to women. Goodreau et al. noted that insertive only MSM had higher number of female partnerships, potentially exposing more women to HIV than versatile men, even though they had a lower prevalence.¹⁸

The finding that moderno MSM had the highest odds of an HIV-positive test also has implications with regard to the spread of HIV among MSM. If moderno men were to become infected during receptive sex, and then engage in insertive sex with an uninfected partner, this could facilitate spread of the virus. Goodreau et al.’s model explored this possibility, noting that mixing patterns between sexual role groups have an important impact on the epidemic. Unfortunately, no data were collected in our sample on the perceived identity of sexual partners, which would have allowed us to determine whether the moderno MSM were likely to adhere to assortative or disassortative mixing.

Limitations

This was a non-random sample of visitors to Epicentro Salud who primarily self-identified as gay. We aimed to analyse only unique, first time visitors; however, it is possible that some men were repeat testers. Further, since men went to the clinic specifically for HIV testing, they might have done so out of concern of an HIV exposure, thereby inflating the HIV prevalence. Although the clinic intake form included a question on the number of sexual partners in the past three months, there was insufficient data to include the variable in our analysis. Finally, as a cross-sectional study, it is impossible to establish causality for these findings.

Conclusions

We found that overall sexual role was strongly associated with the outcome of an HIV-positive test. MSM reporting a moderno role experienced the highest odds ratio of HIV, followed closely by MSM who were pasivo. Sexual role was strongly associated with sexual identity and gender of sexual partners in the previous six months. Future research in Peru should further explore mixing patterns between activo, pasivo and moderno MSM as well as partnerships between moderno MSM and women.

Footnotes

Acknowledgements

The authors would like to acknowledge the staff of Epicentro Salud for their work in treating patients as well as collecting and entering data for analysis. Special thanks to Dr. Italo Sanchez.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

References

UNAIDS. Peru country fact sheet, www.unaids.org/en/regionscountries/countries/peru/ (2013, accessed 2 July 2015).

Silva-Santisteban

Raymond

Salazar

. Understanding the HIV/AIDS epidemic in transgender women of Lima, Peru: results from a sero-epidemiologic study using respondent driven sampling. AIDS Behav 2012; 16: 872–881.

Peru launches campaign to increase HIV testing among men [press release]. UNAIDS, 30 November 2012.

Vagenas P, Ludford KT, Gonzales P, Peinado J, Cabezas C, Gonzales F, et al. Being unaware of being HIV-infected is associated with alcohol use disorders and high-risk sexual behaviors among men who have sex with men in Peru. AIDS Behav 2013.

MINSA [Peruvian Ministry of Health]. Informe nacional sobre los progresos realizados en el país [National report on progress made in the country]. Available at: http://www.unaids.org/en/dataanalysis/knowyourresponse/countryprogressreports/2012countries/ce_PE_Narrative_Report.pdf (accessed 15 August 15 2014).

Galea J. Personal communication, 2013.

Armbruster

Roy

Kapur

. Sex role segregation and mixing among men who have sex with men: implications for biomedical HIV prevention interventions. PloS One 2013; 8: e70043–e70043.

CDC. HIV among gay and bisexual men Atlanta, GA: Centers for Disease Control and Prevention (CDC); [updated 1 July 2013, 1 September 2013], http://www.cdc.gov/hiv/risk/gender/msm/facts/index.html (2013, accessed 2 July 2015).

Vittinghoff

Douglas

Judson

. Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am J Epidemiol 1999; 150: 306–311.

10.

Clark

Salvatierra

Segura

. Moderno love: sexual role-based identities and HIV/STI prevention among men who have sex with men in Lima, Peru. AIDS Behav 2013; 17: 1313–1328.

11.

Konda

Lescano

Celentano

. In Peru, reporting male sex partners imparts significant Risk of incident HIV/sexually transmitted infection: all men engaging in same-sex behavior need prevention services. Sex Transm Dis 2013; 40: 569–574.

12.

Blas

Alva

Carcamo

. Effect of an online video-based intervention to increase HIV testing in men who have sex with men in Peru. PloS One 2010; 5: e10448–e10448.

13.

Goodreau

Goicochea

Sanchez

. 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.

14.

Carrier

. Sexual behavior and spread of AIDS in Mexico. Med Anthropol 1989; 10: 129–142.

15.

Izazola-Licea

Valdespino-Gomez

Gortmaker

. HIV-1 seropositivity and behavioral and sociological risks among homosexual and bisexual men in six Mexican cities. J Acquir Immune Defic Syndr 1991; 4: 614–622.

16.

Hernandez

Uribe

Gortmaker

. 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.

17.

Hemmige

Snyder

Liao

. Sex position, marital status, and HIV risk among Indian men who have sex with men: clues to optimizing prevention approaches. AIDS Patient Care STDs 2011; 25: 725–734.

18.

Goodreau

Peinado

Goicochea

. Role versatility among men who have sex with men in urban Peru. J Sex Res 2007; 44: 233–239.