Abstract
Objectives:
While men who have sex with men (MSM) are disproportionately affected by Peru’s overlapping HIV and STI epidemics, there is little data on how partnership- and network-level factors affect STI transmission in Peru. We explored partnership- and network-level factors associated with gonorrhoea/chlamydia (GC/CT) and/or syphilis infection among MSM in Peru.
Methods:
We present results of a cross-sectional secondary analysis of MSM (n=898) tested for syphilis, GC/CT infection as part of the screening process for two STI control trials in Lima, Peru. Participants completed questionnaires on demographics, sexual identity and role, characteristics of their three most recent sexual partners (partner sexual orientation, gender, role, partnership type, partner-specific sexual acts) and 30-day sexual network characteristics (number of sexual partners, partnership types, frequency of anal/vaginal intercourse). Participants were tested for syphilis and urethral, rectal, and oropharyngeal GC/CT. Differences in network characteristics were analysed with chi-square and Kruskal-Wallis tests.
Results:
Approximately 38.9% of participants had a new STI diagnosis (syphilis [RPR≥16]: 10.6%; GC/CT: 22.9%; syphilis-GC/CT co-infection: 5.4%). Condomless anal intercourse (CAI) was not significantly associated with an STI diagnosis. Gay-identified participants with exclusively homosexual networks had a higher prevalence of STIs (47.4%) than gay-identified MSM with only heterosexual/ bisexual partners (34.6%, p=0.04), despite reporting fewer sexual partners (any partners: 2, 1–4 vs. 3, 2–6; p=0.001; casual partners: 1, 0–3 vs. 2, 1–4; p=0.001) and more stable partnerships (1, 0–1 vs. 0, 0–1; p=0.003) in the last month.
Conclusions:
Network size and number of casual sexual partners were associated with GC/CT infection among MSM in Peru. Despite reporting fewer sexual risk behaviours (smaller network size, more stable partnerships, less CAI), MSM with homosexual-only sexual networks had a higher prevalence of GC/CT and syphilis. These findings suggest network composition among MSM in Peru plays an important role in risk for STI acquisition.
Keywords: Sexual Networks, Latin America, Men
INTRODUCTION:
Men who have sex with men (MSM) and transgender women (TW) are disproportionately affected by Peru’s overlapping HIV and STI epidemics.1 Among MSM, studies have demonstrated a prevalence of urethral Neisseria gonorrhoea and/or Chlamydia trachomatis (GC/CT) infection of 1.5–5.5% and syphilis infection of 7.4–10.5%, compared to the general population of men in Peru where the prevalence is 0.1% for GC, 4.2% for CT, and 0.5% for syphilis.2–5 Previous studies have highlighted the importance of sexual networks in determining HIV/STI risk by demonstrating differences in disease transmission among Peruvian MSM according to sexual identity, sexual role, partnership status, and sexual network location.6–10 However, current HIV/STI prevention efforts in Peru do not adequately address network patterns of disease transmission and have not had a significant impact on the HIV epidemic among MSM.2,11,12 Gaining a better understanding of the interaction between individual- and partnership-level risk factors with sexual network patterns, and addressing how these factors drive STI transmission, is a crucial step towards development of tailored HIV prevention interventions in Latin America.
Previous research on sexual networks has demonstrated that individuals within a network may share both direct and indirect linkages with their sexual partners, establishing overlapping contexts for sexual risk behaviour and disease transmission.13 While increased frequency of sexual risk behaviour (e.g., condomless anal intercourse) is considered one of the primary drivers of HIV transmission, research suggests that sexual network characteristics, such as density, composition, structure, and epidemiologic characteristics within the network, may be equally important.14–16 As risk behaviours and HIV/STI infection cluster within specific sexual networks, increased network size and partner concurrency are associated with an individual’s higher likelihood of HIV and STI acquisition.13,15,17 Importantly, while sexual network characteristics may increase risks for HIV/STI transmission, they can also be exploited for the benefit of public health by retracing pathways of transmission for the delivery of prevention interventions.
In Peru, previous analysis surrounding partnership and sexual network characteristics has primarily focused on HIV transmission. Role versatility, frequency of condomless anal intercourse, and partnership type have been found to be important determinants of HIV transmission among Peruvian MSM, with stable partnerships estimated to account for one third of new HIV infections.18–20 Sexual network analysis of HIV positive pregnant women in Peru found that likelihood of HIV acquisition was more highly associated with sexual network characteristics and risk behaviours of their male partners than individual-level behaviours of the women themselves.21 Despite the importance of sexual network characteristics for HIV/STI-associated risk behaviours and transmission, there is currently little data on the impact of partnership- and network-level factors on STI transmission among Peruvian MSM. To aid in the development of network-level prevention strategies in Latin America, we compare partnership- and network-level factors associated with GC/CT and/or syphilis infection among MSM in Peru and explore how variations in sexual network patterns may be associated with STI-specific differences in acquisition risk.
METHODS
Participants and Recruitment
We conducted a secondary analysis of data collected during the screening process for two trials of expedited partner therapy for MSM with GC and/or CT infection.22,23 Research staff recruited participants at STI clinics and venues frequented by MSM in Lima and Callao, Peru between August 2012 and June 2014. Enrolment was limited to individuals who: 1) were at least 18 years old, 2) assigned male sex at birth, and 3) reported oral and/or anal sex with a male or TW partner in the preceding year.
Study Procedures
All participants completed a computer-assisted self-interview behavioural survey, which assessed both participant- and partnership-level variables. Respondent variables included age, education, sexual orientation/gender identity (heterosexual, bisexual, homosexual, transgender) and role (activo [insertive], pasivo [receptive], moderno [versatile]), position during intercourse, condom use, and total number of sexual partners within last month. Questions specific to the three most recent sexual contacts included partner-specific sexual acts (anal, vaginal, oral intercourse), partner sexual orientation/gender identity and role, partnership type (stable, casual, anonymous, sex worker, sex work client), position during intercourse (insertive, receptive, both), and condom use.
Participants underwent physical examination for signs of symptomatic urethritis or proctitis, as well as primary or secondary syphilis. Urine samples as well as rectal and pharyngeal swabs were collected and tested for GC/CT infection with nucleic acid amplification testing (NAAT) using the Gen-Probe Aptima II assay (Hologic, San Diego, CA, USA) at the U.S. Naval Medical Research Unit-6 (NAMRU-6) Bacteriology Laboratory in Callao. Only participants with NAAT results from all three anatomic sites were included in this analysis. TW participants were excluded from this analysis due to the small number of TW enrolled (n=19). Blood was collected for syphilis testing by rapid plasma reagin (RPR) assay (RPRnosticon, Biomérieux, Marcy l’Etoile, France) with microhaemagglutination for Treponema pallidum (MHA-TP) confirmation (MHA-TP, Organon Teknika, Durham, NC, USA). Serial dilution of RPR titres for positive results was performed at the Asociación Civil Impacta Salud y Educación laboratory in Lima. For the purpose of this analysis, RPR titres ≥ 16 were considered consistent with current syphilis infection. HIV testing was offered, but not required as a condition of enrolment.22 Participants were compensated 15 Nuevos soles (approximately US$5.00) and provided with five condoms and sachets of lubricant for their participation.
Participants with clinically symptomatic urethritis or proctitis were treated with ceftriaxone 250mg intramuscular injection and azithromycin 1g orally at the screening visit, according to CDC Guidelines.24 All participants were provided with results of NAAT testing within two weeks and treated with ceftriaxone and azithromycin (for asymptomatic GC) or azithromycin alone (for asymptomatic CT infection). Participants with syphilis were treated according to the stage of their infection following physician review of previous RPR titres and treatment history.
Consent/Permissions
Written informed consent was obtained from all participants prior to enrolment. The study protocol was reviewed and approved by the Office of Human Research Participant Protection (OHRPP) at the University of California, Los Angeles (IRB 11–003095), the Comite Institucional de Bioética at Asociación Civil Impacta Salud y Educación (Certificate 0053–2012-CE), and NAMRU-6 (Protocol HRPP NAMRU6.2012.0033). The complete study from which this secondary analysis is derived was registered on clinicaltrials.gov ().
Data Analysis
Bivariate analyses, with chi-square and Fisher’s exact tests when appropriate, were used to estimate the association of participant characteristics and sexual behaviours with four groups of participants based on the type(s) of infection diagnosed during screening procedures: 1) no syphilis or GC/CT infection (referred to as STI-negative), 2) syphilis infection, 3) GC/CT infection (Urethral, Rectal, and/or Pharyngeal), and 4) syphilis-GC/CT co-infection. Sexual networks were assessed by enumerating the number of sexual partners, number of partners of different types (e.g., stable, casual, anonymous, commercial), and number of different partners with whom anal and/or vaginal intercourse was performed within last 30 days. Characteristics of the three most recent sexual partnerships were also obtained, as described above. Kruskal-Wallis tests were used to measure differences in the distribution of non-parametric numeric variables between groups based on type(s) of infection. We performed an additional sub-analysis exploring network characteristics according to partner sexual orientation (all partners reported heterosexual/bisexual versus all partners reported homosexual), stratified by participant sexual orientation (heterosexual/bisexual or homosexual). Participants who did not report all partnerships as heterosexual/bisexual or homosexual (e.g., reported females or both bisexual and homosexual partners) were excluded from this sub-analysis. All analyses were conducted using Stata 12.0 (StataCorp, College Town, TX). Complete case analysis was performed for variables with missing data; less than 5% of data were missing for any single variable.
RESULTS
Sample Characteristics
We evaluated 898 MSM (median age 27 years) between 2012 and 2014. Participants most commonly reported their sexual orientation as homosexual (68.0%, 574/844) and moderno sexual role (49.4%, 423/857). The median number of reported sexual partners was 2 (IQR: 1, 4) and median number of episodes of condomless receptive anal intercourse was 1 (0, 1) in the last month. More than half of the sample (61.1%, 549/898) was STI negative. Among MSM diagnosed with an STI, 27.2% (95/349) were diagnosed with syphilis, 59.0% (206/349) were diagnosed with GC/CT, and 13.8% (48/349) were diagnosed with syphilis-GC/CT co-infection. Within the GC/CT subgroup, 8.7% (22/254) of diagnoses were urethral GC/CT only, 20.9% (53/254) were pharyngeal GC/CT only, 41.3% (105/254) were rectal GC/CT only, and 29.1% (74/254) were GC/CT in multiple anatomic sites.
Characteristics and Sexual Risk Behaviours by Type of STI Diagnosed
STI-negative participants were more likely to identify their sexual role as activo (25.4%, 133/523) when compared with MSM with syphilis (11.0%, 10/91), GC/CT (14.9%, 29/195), or syphilis-GC/CT co-infection (20.8%, 10/48; p<0.01). STI-negative participants reported fewer episodes of any receptive anal intercourse in the last month (median, IQR: 1, 0–2) than MSM with syphilis (1.5, 1–12.5), GC/CT (2, 1–4) or syphilis-GC/CT co-infection (1.5, 0–3; p<0.01).
Sexual partnership and respondent characteristics according to STI diagnosis are reported in Table 1. MSM with only GC/CT infection were younger (median age, IQR: 25.5, 22–30; p<0.01), more likely to identify their sexual role as pasivo (32.8%, 64/195; p<0.01), and reported greater numbers of MSM/TW partners (median, IQR: 3, 2–5; p<0.01) than participants in all other groups. MSM with syphilis-GC/CT co-infection reported greater median numbers of casual partners (2, 0–2) than participants with no infection (1, 0–2) or syphilis only (1, 0–2; p<0.01).
Table 1:
Respondent and sexual partnership characteristics within the last 30 days associated with STI diagnosis among MSM in Lima, Peru (N=917)
| No STI (n=549) |
Syphilis Only (n=95) |
GC/CT Only (n=206) |
Syphilis & GC/CT (n=48) |
p | |
|---|---|---|---|---|---|
| Age (n=895) | 28 (24, 34) | 28 (23, 34) | 25.5 (22, 30) | 26 (22, 29) | <0.001 |
| Education (n=895) | |||||
| Less than high school | 50 (9.1) | 10 (10.5) | 31 (15.1) | 2 (4.3) | |
| Completed high school | 131 (24.0) | 24 (25.3) | 45 (21.8) | 14 (29.8) | 0.216 |
| Higher education | 366 (66.9) | 61 (64.2) | 130 (63.1) | 31 (66.0) | |
| Sexual Orientation (n=844) | |||||
| Heterosexual/Bisexual | 175 (34.1) | 19 (20.2) | 60 (31.3) | 16 (36.4) | 0.059 |
| Homosexual | 339 (65.9) | 75 (79.8) | 132 (68.7) | 28 (63.6) | |
| Sexual Role (n=857) | |||||
| Activo (insertive) | 133 (25.4) | 10 (11.0) | 29 (14.9) | 10 (20.8) | |
| Pasivo (receptive) | 155 (29.6) | 23 (25.3) | 64 (32.8) | 10 (20.8) | 0.001 |
| Moderno (versatile) | 235 (44.9) | 58 (63.7) | 102 (52.3) | 28 (58.3) | |
| Sexual Partners (all genders) (n=868) | 2 (1, 3) | 2 (1, 4) | 3 (2, 5) | 3 (2, 3) | <0.001 |
| MSM/TW Partners | |||||
| MSM/TW Sexual Partners (n=749) | 2 (1, 4) | 2 (1, 5) | 3 (2, 5) | 2 (2, 3) | <0.001 |
| MSM/TW Partnership Type | |||||
| Stable (n=707) | 0 (0, 1) | 0 (0, 1) | 0 (0, 1) | 0 (0, 1) | 0.947 |
| Casual (n=709) | 1 (0, 2) | 1 (0, 2) | 2 (0, 3) | 2 (0, 2) | 0.001 |
| Anonymous (n=704) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0.670 |
| Commercial (n=698) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0.117 |
| Anal insertive intercourse (n=373) | 1 (0, 2) | 1 (1, 3) | 1 (0, 3) | 0.5 (0, 1) | 0.475 |
| Anal condomless insertive (n=247) | 1 (0, 1) | 0 (0, 2) | 1 (0, 2) | 1 (1, 1) | 0.189 |
| Anal receptive intercourse (n=372) | 1 (0, 2) | 1.5 (1, 12.5) | 2 (1, 4) | 1.5 (0, 3) | 0.008 |
| Anal condomless receptive (n=261) | 1 (0, 1) | 0 (0, 4) | 1 (0, 2) | 1 (1, 1) | 0.810 |
| Female Partners** | |||||
| Female Sexual Partners (n=743) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0.335 |
| Female Partnership Type | |||||
| Stable (n=56) | 0 (0, 1) | 0 (0, 0) | 0 (0, 1) | 0 (0, 0) | 0.375 |
| Casual (n=53) | 1 (0, 2) | 1 (1, 1) | 0 (0, 1) | 1 (0, 2) | 0.527 |
| Anonymous (n=53) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0.5 (0, 1) | 0.716 |
| Commercial (n=52) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0 (0, 0) | 0.931 |
| Vaginal intercourse (n=58) | 1 (1, 3) | 1 (1, 1) | 0 (0, 1) | 0 (0, 0) | 0.051 |
| Vaginal condomless intercourse (n=46) | 1 (0.5, 2.5) | - | 0 (0, 1) | - | 0.071 |
| Anal intercourse (n=58) | 0 (0, 2) | - | 0 (0, 0) | 0 (0, 0) | 0.136 |
| Anal condomless intercourse (n=29) | 1.5 (1, 2) | - | 0 (0, 1) | - | 0.049 |
Results are presented as either Median (IQR) or n (%)
Genetically female at birth
Note: Bold indicates statistical significance
Stratification by Participant and Partner Sexual Orientation
Sexual partnership and respondent characteristics, stratified by both respondent and partner sexual identity, are reported in Table 2. Homosexual participants who reported only homosexual partners were more likely to have obtained an education beyond high school (77.7%, 205/266; p<0.01) and to report more stable partners in the last month (median, IQR: 1, 0–1; p<0.01) than homosexual-identified MSM with only heterosexual/bisexual partners (52.3%, 56/107 & 0, 0–1, respectively). Homosexual-identified MSM with homosexual partners were also less likely to describe their sexual role as pasivo (19.3%, 51/266) than homosexual participants with only heterosexual/bisexual partners (66.0%, 70/107; p<0.01).
Table 2:
Participant and sexual partnership characteristics within the last 30 days based on both respondent and partner sexual identity among MSM in Lima, Peru (N=492)
| Heterosexual and Bisexual Respondents | Homosexual Respondents | |||||||
|---|---|---|---|---|---|---|---|---|
| Characteristics/Variables | n | Hetero/Bi Partnersa (n=56) |
Homosexual Partnersb (n=63) |
p | n | Hetero/Bi Partnersa (n=107) |
Homosexual Partnersb (n=266) |
p |
| Sexually Transmitted Infection | 119 | 373 | ||||||
| No Infection | 31 (55.4) | 38 (60.3) | 0.839 | 70 (65.4) | 140 (52.6) | 0.04 | ||
| Syphilis Only | 6 (10.7) | 6 (9.5) | 10 (9.3) | 42 (15.8) | ||||
| GC/CT Only | 15 (26.8) | 13 (20.6) | 25 (23.4) | 65 (24.4) | ||||
| Syphilis-GC/CT Co-Infection | 4 (7.1) | 6 (9.5) | 2 (1.9) | 19 (7.2) | ||||
| Age | 119 | 26 (22, 31) | 28 (24, 33) | 0.136 | 372 | 29 (26, 36) | 27 (23, 34) | 0.005 |
| Education | 119 | 371 | ||||||
| Less than high school | 7 (12.5) | 4 (6.4) | 0.508 | 15 (14.0) | 13 (4.9) | <0.001 | ||
| Completed high school | 13 (23.2) | 15 (23.8) | 36 (33.6) | 46 (17.4) | ||||
| Higher education | 36 (64.3) | 44 (69.8) | 56 (52.3) | 205 (77.7) | ||||
| Sexual Role | 114 | 365 | ||||||
| Activo (insertive) | 15 (27.3) | 29 (49.2) | 0.001 | 1 (0.9) | 43 (16.6) | <0.001 | ||
| Pasivo (receptive) | 15 (27.3) | 2 (3.4) | 70 (66.0) | 51 (19.3) | ||||
| Moderno (versatile) | 25 (45.4) | 28 (47.5) | 35 (33.0) | 166 (64.1) | ||||
| Sexual Partners (all genders) | 116 | 2 (1, 3) | 2 (1, 4) | 0.956 | 359 | 3 (2, 6) | 2 (1, 4) | 0.001 |
| MSM/TW Partners | ||||||||
| MSM/TW Sexual Partners | 108 | 2 (1, 3) | 2 (1, 4) | 0.456 | 317 | 3 (2, 6) | 2 (1, 4) | 0.001 |
| MSM/TW Partnership Type | ||||||||
| Stable | 103 | 1 (0, 1) | 1 (0, 1) | 0.830 | 305 | 0 (0, 1) | 1 (0, 1) | 0.003 |
| Casual | 104 | 1 (0, 2) | 1 (0, 2) | 0.711 | 304 | 2 (1, 4) | 1 (0, 3) | 0.001 |
| Anonymous | 103 | 0 (0, 0) | 0 (0, 0) | 0.613 | 304 | 0 (0, 0) | 0 (0, 0) | 0.692 |
| Commercial | 102 | 0 (0, 0) | 0 (0, 0) | 0.567 | 299 | 0 (0, 0) | 0 (0, 0) | 0.162 |
| Anal insertive intercourse | 50 | 1 (0, 2) | 1 (1, 3) | 0.286 | 145 | 0 (0, 1) | 1 (1, 3) | 0.001 |
| Anal condomless insertive | 38 | 1 (0, 2) | 1 (0, 1) | 0.745 | 94 | 1 (1, 3) | 1 (0, 1) | 0.022 |
| Anal receptive intercourse | 50 | 1 (0, 2) | 0 (0, 1) | 0.014 | 146 | 3 (1, 5) | 1 (0, 2) | <0.001 |
| Anal condomless receptive | 26 | 1 (1, 2) | 1 (0, 2) | 0.389 | 115 | 1 (0, 2) | 1 (0, 1) | 0.275 |
| Female Partnersc | ||||||||
| Female Sexual Partners | 107 | 0 (0, 0) | 0 (0, 0) | 0.448 | 313 | 0 (0, 0) | 0 (0, 0) | 0.908 |
| Female partnership type | ||||||||
| Stable | 8 | 0 (0, 1) | 1 (0, 1) | 0.693 | 4 | 1 (0, 1) | 0 (0, 0) | 0.439 |
| Casual | 7 | 0 (0, 2) | 2 (2, 2) | 0.248 | 3 | 1 (0, 1) | 2 (2, 2) | 0.221 |
| Anonymous | 7 | 0 (0, 1) | 0 (0, 0) | 0.617 | 3 | 0 (0, 0) | 0 (0, 0) | 1 |
| Commercial | 7 | 0 (0, 0) | 0 (0, 0) | 1 | 2 | 0 (0, 0) | 0 (0, 0) | 1 |
| Vaginal intercourse | 8 | 1 (1, 2) | 1 (0, 1) | 0.182 | 8 | 0 (0, 1) | 0 (0, 0) | 0.564 |
| Vaginal condomless intercourse | 8 | 1 (0, 2) | 1 (0, 1) | 0.505 | 6 | 0 (0, 1) | 0 (0, 0) | 0.513 |
| Anal intercourse | 8 | 0 (0, 2) | 1 (0, 1) | 1 | 8 | 0 (0, 1) | 0 (0, 0) | 0.564 |
| Anal condomless intercourse | 3 | 3 (2, 4) | 1 (1, 1) | 0.221 | 6 | 0 (0, 1) | 0 (0, 0) | 0.513 |
Results are presented as either Median (IQR) or n (%). Only participants who reported exclusively heterosexual/bisexual partners or exclusively homosexual partners are included in this sub-analysis
Reported sexual identity of three last sexual partners as only heterosexual/bisexual
Reported sexual identity of three last sexual partners as only homosexual
Genetically female at birth
Note: Bold indicates statistical significance
These variations in sexual role, partnership, and network contexts translated into differences in STI prevalence as homosexual participants with only homosexual partners had a higher prevalence of STIs (47.4%, 126/266) than homosexual MSM with only heterosexual/bisexual partners (34.6%, 37/107; p=0.04), despite reporting fewer sexual partners (2, 1–4 vs 3, 2–6; p=0.001), fewer casual partners (1, 0–3 vs 2, 1–4; p=0.003), and fewer episodes of any receptive anal intercourse (1, 0–2 vs 3, 1–5; p<0.001) in the last month. Homosexual-identified participants with exclusively homosexual networks were significantly more likely to be diagnosed with syphilis (22.9%, 61/266 vs 11.2%, 12/107; p<0.01). They also had a higher prevalence of GC/CT infection (31.6%, 84/266 vs 25.2%, 27/107), though not statistically significant (p=0.26).
Among MSM who identified as heterosexual/bisexual, those who reported only heterosexual/bisexual partners were more likely to report their sexual role as pasivo than those with only homosexual partners (27.3%, 15/56 vs 3.4%, 2/63; p<0.01). Consistent with this finding, heterosexual/bisexual MSM with exclusively heterosexual/bisexual partners also reported more episodes of receptive anal intercourse in the last month (median, IQR: 1, 0–2 vs 0, 0–1; p=0.01). Quantitative, though statistically non-significant, differences in patterns of STI transmission were also observed as heterosexual/bisexual MSM with non-gay male partners had a higher prevalence of GC/CT (33.9%, 19/56 vs 30.2%, 19/63) but a lower frequency of syphilis infection (17.8%, 10/56 vs 30.2%, 12/63) compared to heterosexual/bisexual MSM with exclusively homosexual partners.
DISCUSSION
To the best of our knowledge, our study is the first to evaluate associations between different STI pathogens and MSM sexual network characteristics in Latin America, adding to the limited data available regarding the influence of network characteristics on STI prevalence in these high-risk populations. While previous research has demonstrated that the STI epidemic is concentrated within certain MSM sub-populations, there is limited data exploring the partner-level factors that define STI transmission within these high-risk sexual networks.18–20 Our data highlight the heterogeneity of the STI epidemic among Peruvian MSM, and demonstrate how unique individual risk behaviours, partnership dynamics, and network structures can differentiate patterns of disease transmission and STI risk between individuals in these high-risk communities.
Participants diagnosed with GC/CT tended to be younger, have a higher incidence of receptive anal intercourse, report a pasivo sexual role, be more likely to have casual partnerships, and report a greater number of sexual partners than those diagnosed with syphilis or no STI. While it is not surprising that a higher incidence of GC/CT was associated with increased risk behaviour, it is interesting that condomless anal intercourse was not significantly associated with any STI diagnosis. Consistent with prior research, this finding suggests that sexual network size, prevalence of disease in the network, and characteristics of partnerships constituting the network may better predict STI risk than frequency of condomless intercourse.13,17 While our results support previous studies showing that network size is associated with STI prevalence, our findings also add nuance to this assumption by suggesting that network size may be more important for the transmission of certain STIs compared to others (e.g., GC/CT versus syphilis in our sample).
To illustrate this point, participants diagnosed with syphilis tended to be older, report a moderno sexual role, have fewer casual partners, and report fewer sexual partners overall than those diagnosed with GC/CT. As respondents diagnosed with syphilis had smaller sexual network size and fewer casual partnerships than those with GC/CT, our findings suggest that a higher prevalence of syphilis within one’s sexual network may lead to an increased risk of transmission, independent of individual risk behaviours within that network. As prior research has estimated that only half of MSM diagnosed with syphilis complete treatment, coupled with findings that as many as 56% of syphilis diagnoses are due to re-infection, our findings suggest that ongoing syphilis transmission through core networks with high baseline prevalence of infection are inadequately managed by current guidelines for STI treatment and prevention in Peru.25–27 Given the known risks of HIV transmission with syphilis co-infection, our findings demonstrate the need for resources to be directed toward identifying and screening these core networks.27
Participants with only urethral GC/CT were less likely to have a secondary education, more likely to self-identify as heterosexual/bisexual, report an activo sexual role, and participate in condomless insertive anal intercourse. These findings are consistent with previous research in Peru describing the activo sexual role as a representation of the masculine, dominant partner often associated with heterosexual orientation.7 As prior studies have suggested that only 14.3–42.1% of MSM with GC/CT urethritis in this population are symptomatic, and that heterosexually-identified MSM with an activo sexual role are considered (by both themselves and their partners) to have lower risk for HIV/STI transmission, these men represent a substantial risk for STI transmission to both their male and female partners.4,9 These findings highlight the need for targeted health promotion messages and increased screening for urethral GC/CT among heterosexual/bisexual-identified MSM to reduce risks for HIV/STI acquisition in their networks.
Participants identified as homosexual and reported only homosexual partners were more educated, had fewer sexual partners, had more stable partnerships, and were less likely to engage in condomless insertive anal intercourse than gay-identified MSM with non-gay identified sexual partners. However, despite reporting a lower frequency of sexual risk behaviour than gay-identified MSM with heterosexual/bisexual partners, these men had a higher prevalence of STIs. As the HIV/STI epidemic in Peru is concentrated within the MSM/TW population, these findings support the idea that the prevalence of STIs within a network is a primary determinant of STI transmission for partnerships within the network, consistent with prior research indicating that HIV and syphilis transmission are associated with all-male sexual networks.3,17,28 These findings suggest the need for tailored public health messages and network-based interventions targeted to specific high risk MSM sub-populations, rather than blanket efforts directed to an undifferentiated “MSM community”. Specific strategies could include partner-based efforts for the dissemination of HIV/STI treatment and prevention resources, as well as social network-based systems for diffusion of new education approaches and prevention technologies.22,29,30
Some limitations of our study need to be considered when interpreting the data. First, there is an inherent bias in a secondary analysis of self-reported data from a cross-sectional study. As the recruitment site is known in the community for HIV/STI research, findings may reflect a higher risk population, which may limit the generalizability to the MSM population as a whole. However, this allowed us to focus on MSM subpopulations that are high-risk for future HIV/STI infection and/or transmission, a priority for public health efforts. Additionally, as our data was limited to the three most recent sexual partners, we may be not have captured all of the intricacies of these high-risk sexual networks. This limitation was mitigated somewhat by including information on the total number of partners during the last thirty days. By restricting data to the three most recent sexual partners, we were able to limit recall bias and increase accuracy of the solicited partnership characteristics. Finally, our study was limited to respondent-reported data and did not include information from the partners themselves, limiting the ability to evaluate possible linkages within networks. Obtaining more detailed descriptions of sexual networks in this population will be an important objective for future research.
Our findings highlight the nuances and complexities of the STI epidemic among Peruvian MSM, as MSM sub-populations appear to exhibit different individual- and partnership-level factors contributing to STI transmission within their network. While certain high-risk behaviours do confer a higher risk for STI transmission, such as an increased number of casual sex partners, individual risky sexual behaviours are not the only drivers of the STI epidemic in Peru and may not be the most important determinants of STI risk. Despite participating in less risky sexual behaviours (e.g. less condomless anal intercourse, more stable partnerships, smaller network size), patterns of GC/CT and syphilis infection appeared to be concentrated within homosexual-only MSM sexual networks in our sample, suggesting that the subgroups comprising one’s sexual network (e.g., heterosexual/bisexual vs homosexual vs TW vs cis-gender women) and prevalence of STIs within those subgroups play a critical role in an individual’s risk for STI acquisition. These findings highlight the need for targeted health promotion messages tailored to particular MSM sub-populations to address the specific risk factors driving the STI epidemic within those sub-populations (e.g., increased condom use and STI screening among heterosexually-identified MSM, and increased efforts toward partner notification and expedited partner therapy among homosexually-identified MSM). However, it is important to note that transmission dynamics are complex and influenced by sexual network structure, partner-level sexual interactions, individual behavioural decision-making processes, and population-level patterns of HIV/STI prevalence. Additional research is needed to gain a deeper understanding of how individual behaviour, partnership dynamics, and sexual network structures influence HIV and STI transmission among MSM in Latin America.
KEY MESSAGES:
Prevalence of STIs of subgroups that comprise one’s sexual network plays an important role in an individual’s risk for STI acquisition
Sexual network data can provide crucial information in understanding risks for STI transmission that may be missed at the individual- or partnership-level
Understanding sexual network characteristics can be a powerful tool in developing targeted public health interventions
ACKNOWLEDEGEMENTS
The authors would like to thank the staff at Asociación Civil Impacta Salud y Educación for their help in completing this study and Silvia Montano with NAMRU-6 for processing the GC/CT samples. We would also like to thank the participants of this study for sharing their lives with us. Research funding was provided by NIH grants R25 MH087222, K23 MH084611, and R21 MH092232 to JLC, K23 AI110532 to JEL.
REFERENCES:
- 1.UNAIDS. 2016 Peru Country Fact Sheet, 2016. [Google Scholar]
- 2.Clark JL, Lescano AG, Konda KA, et al. Syndromic management and STI control in urban Peru. PLoS ONE 2009;4:e7201.doi: 10.1371/journal.pone.0007201 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Perez-Brumer AG, Konda KA, Salvatierra HJ, et al. Prevalence of HIV, STIs, and risk behaviors in a cross-sectional community- and clinic-based sample of men who have sex with men (MSM) in Lima, Peru. PLoS ONE 2013;8:e59072.doi: 10.1371/journal.pone.0059072 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Passaro RC, Segura ER, Perez-Brumer AG, et al. Body parts matter: social, behavioral, and biological considerations for urethral, pharyngeal, and rectal gonorrhea and chlamydia screening among MSM in Lima, Peru. Sex Transm DisPublished Online First: 20 February 2018. doi: 10.1097/OLQ.0000000000000816 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Cárcamo CP, Campos PE, García PJ, et al. Prevalences of sexually transmitted infections in young adults and female sex workers in Peru: a national population-based survey. Lancet Infect Dis 2012;12:765–73.doi: 10.1016/S1473-3099(12)70144-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Clark JL, Konda KA, Segura ER, et al. Risk factors for the spread of HIV and other sexually transmitted infections among men who have sex with men infected with HIV in Lima, Peru. Sex Transm Infect 2008;84:449–54.doi: 10.1136/sti.2008.031310 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Clark J, Salvatierra J, Segura E, et al. Moderno love: sexual role-based identities and HIV/STI prevention among men who have sex with men in Lima, Peru. AIDS Behav 2012;17:1313–28.doi: 10.1007/s10461-012-0210-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Clark JL, Perez-Brumer A, Salazar X. “Manejar la situacion”: partner notification, partner management, and conceptual frameworks for HIV/STI control among MSM in Peru. AIDS Behav 2015;19:2245–54.doi: 10.1007/s10461-015-1049-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Blair CS, Segura ER, Perez-Brumer AG, et al. Sexual orientation, gender identity and perceived source of infection among men who have sex with men (MSM) and transgender women (TW) recently diagnosed with HIV and/or STI in Lima, Peru. AIDS Behav 2016;20:2178–85.doi: 10.1007/s10461-015-1276-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Verre M, Peinado J, Segura E, et al. Socialization patterns and their associations with unprotected anal intercourse, HIV, and syphilis among high-risk men who have sex with men and transgender women in Peru. AIDS Behav 2014;18:2030–9.doi: 10.1007/s10461-014-0787-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Lee SW, Deiss RG, Segura ER, et al. A cross-sectional study of low HIV testing frequency and high-risk behaviour among men who have sex with men and transgender women in Lima, Peru. BMC Public Health 2015;15:408.doi: 10.1186/s12889-015-1730-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Sanchez J, Lama JR, Kusunoki L, et al. HIV-1, sexually transmitted infections, and sexual behavior trends among men who have sex with men in Lima, Peru. J Acquir Immune Defic Syndr 2007;44:578–85.doi: 10.1097/QAI.0b013e318033ff82 [DOI] [PubMed] [Google Scholar]
- 13.Amirkhanian YA. Social networks, sexual networks and HIV risk in men who have sex with men. Curr HIV/AIDS Rep 2014;11:81–92.doi: 10.1007/s11904-013-0194-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Smith AMA, Grierson J, Wain D, et al. Associations between the sexual behaviour of men who have sex with men and the structure and composition of their social networks. Sex Transm Infect 2004;80:455–58.doi: 10.1136/sti.2004.010355 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Rothenberg R, Baldwin J, Trotter R, et al. The risk environment for HIV transmission: results from the Atlanta and Flagstaff network studies. J Urban Health 2001;78:419–32.doi: 10.1093/jurban/78.3.419 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Amirkhanian YA, Kelly JA, Kirsanova AV, et al. HIV risk behaviour patterns, predictors, and sexually transmitted disease prevalence in the social networks of young men who have sex with men in St Petersburg, Russia. Int J STD AIDS 2006;17(1):50–6.doi: 10.1258/095646206775220504 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Birkett M, Kuhns LM, Latkin C, et al. The sexual networks of racially diverse young men who have sex with men. Arch Sex Behav 2015;44:1787–97.doi: 10.1007/s10508-015-0485-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.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:S147–58.doi: 10.1086/425268 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.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.doi: 10.1371/journal.pone.0050522 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Goodreau SM, Carnegie NB, Vittinghoff E, et al. Can male circumcision have an impact on the HIV epidemic in men who have sex with men? PLoS ONE 2014;9:e102960.doi: 10.1371/journal.pone.0102960 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Johnson KM, Alarcón J, Watts DM, et al. Sexual networks of pregnant women with and without HIV infection. AIDS 2003;17:605–12.doi: 10.1097/01.aids.0000050785.28043.b9 [DOI] [PubMed] [Google Scholar]
- 22.Clark JL, Segura ER, Oldenburg CE, et al. Expedited partner therapy (EPT) increases the frequency of partner notification among MSM in Lima, Peru: a pilot randomized controlled trial. BMC Med 2017;15:94.doi: 10.1186/s12916-017-0858-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Clark JL, Segura ER, Oldenburg CE, et al. Traditional and web-based technologies to improve partner notification following syphilis diagnosis among men who have sex with men in Lima, Peru: pilot randomized controlled trial. J Med Internet Res 2018;20:e232.doi: 10.2196/jmir.9821 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Workowski KA, Bolan GA. Sexually transmitted diseases treatment guidelines, 2015. MMWR Morb Mortal Wkly Rep 2015;64:1–137.25590678 [Google Scholar]
- 25.Tang EC, Segura ER, Clark JL, et al. The syphilis care cascade: tracking the course of care after screening positive among men and transgender women who have sex with men in Lima, Peru. BMJ Open 2015;5:e008552.doi: 10.1136/bmjopen-2015-008552 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Park H, Konda KA, Roberts CP, et al. Risk factors associated with incident syphilis in a cohort of high-risk men in Peru. PLoS ONE 2016;11:e0162156.doi: 10.1371/journal.pone.0162156 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Solomon MM, Mayer KH, Glidden DV, et al. Syphilis predicts HIV incidence among men and transgender women who have sex with men in a preexposure prophylaxis trial. Clin Infect Dis 2014;59:1020–26.doi: 10.1093/cid/ciu450 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Castillo R, Konda KA, Leon SR, et al. HIV and sexually transmitted infection incidence and associated risk factors among high-risk MSM and male-to-female transgender women in Lima, Peru. J Acquir Immune Defic Syndr 2015;69:567–75.doi: 10.1097/QAI.0000000000000667 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Clark JL, Perez-Brumer AG, Segura ER, et al. Anticipated notification of sexual partners following STD diagnosis among men who have sex with men and transgender women in Lima, Peru: a mixed methods analysis. PLoS ONE 2016;11(9):e0163905.doi: 10.1371/journal.pone.01639055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Braun HM, Segura ER, Lake JE, et al. Individual and partnership factors associated with anticipated versus actual partner notification following STI diagnosis among men who have sex with men and/or with transgender women in Lima, Peru. Sex Transm InfectPublished Online First: 30 November 2017.doi: 10.1136/sextrans-2017-053292 [DOI] [PMC free article] [PubMed] [Google Scholar]