Skip to main content

Factors associated with testing for HIV and other sexually transmitted infections in men who have sex with men and transgender women in Bangkok, Thailand

Abstract

Background

Routine screening for HIV and other sexually transmitted infections (STIs) facilitates early diagnosis and treatment, thereby preventing morbidity and onward transmission. We estimated the prevalence of prior HIV/STI testing among men who have sex with men (MSM) and transgender women (TGW) in Bangkok, Thailand, and identified factors associated with prior testing.

Methods

Cross-sectional analyses were performed using data collected at enrollment into an HIV incidence cohort. From April to October 2017, MSM and TGW were enrolled if they were aged 18–35 years, reported anal intercourse with a male or TGW partner, and reported behavioral vulnerability to HIV. Participants answered questions about demographics, sexual behaviors, and lifetime HIV/STI testing history. Multivariable robust Poisson regression was used to estimate risk ratios (RRs) and 95% confidence intervals (CIs) for factors potentially associated with prior testing.

Results

Among 1,014 participants, 348 (34.3%) were TGW and the median age was 21.6 (interquartile range 20.0-24.8) years. Prior testing for HIV was reported by 421 (41.5%) and for other STIs by 268 (26.4%). HIV testing was more common among participants aged ≥ 22 years (RR 1.37 [95% CI 1.13–1.67]), with college education as compared to secondary or less (RR 1.37 [95% CI 1.08–1.72]), and who met male sexual partners online (RR 1.52 [95% CI 1.24–1.85]), but lower among participants attracted to both men and women as compared to men only (RR 0.64 [95% CI 0.51–0.81]) and who met male sexual partners in bars (RR 0.83 [95% CI 0.72–0.97]). Similar associations were observed with prior testing for other STIs, including increased testing among participants with college education (RR 1.52 [95% CI 1.11–2.09]) and who met male sexual partners online (RR 1.73 [95% CI 1.30–2.31]), but lower among participants attracted to both men and women (RR 0.70 [95% CI 0.51–0.96]) and who met male sexual partners in bars (RR 0.67 [95% CI 0.54–0.83]).

Conclusions

Despite behavioral vulnerability, prior testing for HIV and other STIs was uncommon. Online engagement strategies may be effectively reaching Thai MSM and TGW who meet sexual partners online, but new interventions are needed to encourage testing among younger, less educated, and bisexual MSM and TGW.

Introduction

The Joint United Nations Programme on HIV/AIDS (UNAIDS) has set a target for zero new HIV infections by 2030 as part of its Sustainable Development Goals. Routine testing of vulnerable individuals is crucial to curbing the spread of human immunodeficiency virus (HIV) and other sexually transmitted infections (STIs). Early diagnosis of persons living with HIV (PLWH) facilitates rapid initiation of antiretroviral therapy to reduce HIV-related morbidity [1,2,3] and prevent onward HIV transmission [4,5,6]. HIV transmission can also be reduced by the early diagnosis and treatment of concurrent bacterial STIs [7, 8]. Amongst people with and without HIV, detecting and treating bacterial STIs can prevent the development of long-term sequelae such as pelvic inflammatory disease, proctitis, and their potentially devastating complications [9, 10]. Testing services for HIV and other STIs can be co-located to efficiently reach vulnerable populations [11,12,13] and can be leveraged to link vulnerable individuals to biologic and behavioral prevention programs [14,15,16].

Access to routine testing is particularly important for sexual and gender minority populations such as men who have sex with men (MSM) and transgender women (TGW), who are disproportionately affected by HIV and other STIs [17, 18]. These two groups are often conflated [19, 20], but it is increasingly recognized that individuals who were assigned male sex at birth and identify as men (cisgender men) exhibit different sexual behaviors and other characteristics from individuals who were assigned male sex at birth and identify as women (transgender women), even when both engage in sex with men [21, 22]. Guidelines in the United States and Europe recommend annual testing of sexually active cisgender men and TGW who have sex with men for HIV and other STIs with consideration for more frequent testing [23, 24]. Additionally, in the United States, testing every three months is recommended for those who are prescribed HIV pre-exposure prophylaxis (PrEP) [25] and in Thailand such testing is recommended every six months [26]. Despite such recommendations, HIV diagnosis is often delayed until relatively late in the disease course [27,28,29,30,31,32] and many asymptomatic bacterial STIs go undiagnosed in routine care [32,33,34,35,36], particularly in resource-limited settings. Prior evidence from settings other than Thailand suggests that HIV testing is more common among people with higher education, HIV-related knowledge, and self-recognition of HIV risk [37,38,39,40].

Thailand has been a global leader in research on the prevention and treatment of HIV [41,42,43,44] and was one of the first Southeast Asian countries to recommend PrEP for MSM who are behaviorally vulnerable to HIV [45]. Despite this, PrEP uptake has been low [46, 47]. While HIV incidence among MSM in Bangkok appears to be declining, data suggest increasing HIV diagnoses among TGW since 2014 [48]. MSM and TGW in Bangkok also have a high burden of predominantly asymptomatic chlamydia and gonorrhea infections that would go undetected without routine testing [49, 50]. We estimated the prevalence of self-reported prior testing for HIV and other STIs among MSM and TGW in Bangkok, Thailand. We identified factors associated with prior testing for HIV and other STIs in order to inform the design of targeted interventions to increase testing uptake.

Methods

Study population

Cross-sectional analyses were performed using data collected at enrollment into an HIV incidence cohort. From April through October 2017, participants were enrolled at two sites in Bangkok, Thailand, as previously described [51]. Bangkok is a city with highly visible sexual and gender minority populations who, despite an outward appearance of acceptance by the community, still face stigma and discrimination that create barriers to healthcare engagement [52]. Recruitment activities at the Royal Thai Army Clinical Research Centre site included social media advertisements for free HIV testing and direct outreach to bars, saunas, and other entertainment venues. Recruitment activities at the Vaccine Trial Centre at Mahidol University included community engagement via health campaigns and festivals as well as referrals from community-based organizations. Both sites conducted recruitment activities at universities and encouraged peer referrals. Eligible participants were cisgender men or TGW, aged 18–35 years, who reported anal intercourse with a male or TGW partner and one or more of the following criteria in the six months prior to enrollment: (1) engaging in condomless anal intercourse with a male or TGW partner living with HIV or with unknown HIV status; (2) having three or more sexual partners; (3) exchanging sex for money, goods, or drugs; or (4) being diagnosed with a new STI such as syphilis, gonorrhea, chlamydia, or herpes. These criteria were selected based on prior studies showing higher HIV and STI incidence in people from this age group and with these sexual behaviors [53,54,55]. Participants were excluded if they were living with HIV or had previously received an investigational HIV vaccine candidate. Participants received risk reduction counseling and underwent testing for HIV and syphilis at three, six, 12, and 18 months after enrollment. Participants who were diagnosed with HIV were referred to a hospital clinic accessible via the national health care benefit; study staff provided counseling to facilitate engagement in care and antiretroviral treatment initiation.

All participants provided written informed consent in either Thai or English. The study was approved by institutional review boards at Walter Reed Army Institute of Research, Silver Spring, MD, USA; Faculty of Tropical Medicine at Mahidol University, Bangkok, Thailand; and the Royal Thai Army, Bangkok, Thailand.

Data collection

Data for these cross-sectional analyses were collected at the screening visit for the prospective HIV incidence cohort study, which included a computer-assisted self-interview (CASI) questionnaire that collected detailed information regarding participant demographics, sexual behaviors, and STI history. The CASI approach reduced the potential for errors in transcribing participant responses, ensured consistent administration of the questionnaire, and allowed for programming of skip patterns and logic checks to optimize data validity. Data collected on case report forms were compiled into a password-protected electronic database and underwent 100% verification against source documents for key variables (demographics, eligibility, HIV test results, syphilis test results, and end of study disposition) by a trained clinical study monitor.

The outcome variables of interest for these analyses were (1) prior lifetime history of HIV testing and (2) prior lifetime history of testing for other STIs. Prior testing history was assessed by the questions “Have you ever been tested for HIV?” and “Have you ever been tested for sexually transmitted infections, or STIs? (STIs can include syphilis, gonorrhea, chlamydia, herpes.)” If yes, participants were asked whether they had ever been diagnosed with an STI by a doctor or clinic. If so, they were asked whether they had specifically ever been diagnosed with syphilis, gonorrhea, chlamydia, and/or herpes and when they had most recently received an STI diagnosis with answer choices of within three months, within six months, within one year, or more than one year prior.

Independent variables evaluated in these analyses included age, gender identity, sexual attraction, education level, income, and venues for meeting male sexual partners (bars, saunas, online). These variables were assessed by self-report via the CASI questionnaire. Gender was categorized using a validated two-step method that included asking participants which sex they were assigned at birth (male or female) and how they described their current gender identity (male, female, transgender woman, or transgender man) [56, 57]. If a participant responded with both sex assigned at birth and current identity as male, the participant was characterized as a cisgender MSM. If a participant responded with sex assigned at birth as male and gender identity as either female or TGW, the participant was categorized as a TGW. For these cross-sectional analyses of data collected at the screening visit for a longitudinal study, fluidity of gender during longitudinal follow-up was not considered.

Statistical analyses

All enrolled participants who answered both questions about prior testing were included in these analyses. Comparisons between groups of interest were made using the Chi-squared test for categorical variables or Student’s t-test for continuous variables. In separate analyses for prior HIV testing and prior STI testing, unadjusted and adjusted robust Poisson regression models were used to estimate risk ratios (RRs) and 95% confidence intervals (CIs) for pre-specified factors potentially associated with any lifetime history of testing [58]. All pre-specified factors were included in the adjusted multivariable models, regardless of significance in unadjusted modeling. Analyses were performed using Stata 15.1 (StataCorp LP, College Station, TX).

Results

Characteristics of the study population

A total of 1,014 enrolled participants answered both questions about prior testing and were included in these analyses. These participants had a median age of 21.6 (interquartile range [IQR] 20.0–24.8) years. The study population included 657 (64.8%) cisgender men, 348 (34.3%) TGW, and 9 (0.9%) participants with other/unknown gender identity. Sexual attraction mostly or only to men was reported by 790 (77.9%) participants, both men and women by 197 (19.4%), and women only by 27 (2.7%). Participants reported a median of 5 (IQR 3–8) male or TGW sexual partners in the six months prior to enrollment. Any lifetime history of prior testing for HIV was reported by 421 (41.5%) and for other STIs by 268 (26.4%; Table 1).

Table 1 Study population characteristics, overall and by lifetime history of testing for hiv or other sexually transmitted infections

Prior STI diagnoses

Among the 268 participants who reported any lifetime history of testing for STIs other than HIV, a prior positive test result was self-reported by 57 (21.3%). Specifically, a prior diagnosis of syphilis was reported by 20 previously-tested participants (7.5%), chlamydia by 17 (6.3%), gonorrhea 15 (5.6%), and herpes by 6 (2.2%). Among the 57 participants with a prior STI diagnosis, 12 (21.0%) reported a prior positive STI test result but none of the specific STIs solicited, 34 (59.6%) reported just one of the specific STI diagnoses, 10 (17.5%) reported two different STI diagnoses, and one (1.8%) reported a history of all four solicited STIs (Fig. 1). Among these 57 participants, 12 (21.0%) stated that their most recent STI was within the preceding three months, 13 (22.8%) in the preceding 3–6 months, 14 (24.6%) in the preceding 6–12 months, and 18 (31.6%) more than one year prior to enrollment.

Fig. 1
figure 1

Of 268 participants who reported previously being tested for a sexually transmitted infection, 57 (21.3%) reported that they had been diagnosed with a sexually transmitted infection by a doctor or clinic. These participants were asked to specify whether they had been diagnosed with any or all of the following: syphilis, gonorrhea, chlamydia, and/or herpes. Twelve participants reported a history of sexually transmitted infection but did not indicate any of the solicited diagnoses

Factors associated with any lifetime history of HIV or STI Testing

After adjusting for potentially confounding factors, HIV testing uptake was higher among participants aged ≥ 22 years as compared to < 22 years (RR 1.37 [95% CI 1.13–1.67]), with college education as compared to secondary or less (RR 1.37 [95% CI 1.08–1.72]), and who met male sexual partners online (RR 1.52 [95% CI 1.24–1.85]), but lower among participants attracted to both men and women as compared to men only (RR 0.64 [95% CI 0.51–0.81]) and who met male sexual partners in bars (RR 0.83 [95% CI 0.72–0.97]; Table 2). Gender identity, income, and meeting male sexual partners at saunas were not associated with prior testing for HIV in the multivariable model. Similar associations were observed with prior testing for other STIs, including increased testing among participants with college education (RR 1.52 [95% CI 1.11–2.09]) and who met male sexual partners online (RR 1.73 [95% CI 1.30–2.31]), but lower testing among participants attracted to both men and women (RR 0.70 [95% CI 0.51–0.96]) and who met male sexual partners in bars (RR 0.67 [95% CI 0.54–0.83]). Age, gender identity, income, and meeting male sexual partners at saunas were not associated with prior testing for other STIs.

Table 2 Factors associated with testing for HIV and other sexually transmitted infections testing among cisgender men and transgender women who have sex with men in Bangkok, Thailand (n = 1014)

Discussion

Despite recruitment based on behavioral vulnerability to HIV, prior testing for HIV was observed in fewer than half of participants in our study. This is similar to what has been reported in several prior studies of Thai MSM and TGW [59,60,61]. Prior testing for other STIs was even less common in our study, despite a high number of cases detected among the minority of participants who had been previously tested. MSM and TGW in Bangkok have experienced recent surges or outbreaks of STIs such as syphilis [62] and hepatitis C [63]. Early diagnosis and treatment of such infections is critical to interrupting chains of transmission.

We found that participants who met their male sexual partners online were more likely to have been tested for both HIV and other STIs. One prior study that recruited MSM in Bangkok who used mobile applications to find sexual partners found higher testing uptake than was observed in our overall study population, with about two-thirds reporting prior testing for HIV and three-quarters reporting prior testing for other STIs [64]. In Thailand and much of Southeast Asia, smartphones and high-speed internet are frequently used to socialize and find sexual partners [64,65,66]. These digital platforms can be leveraged to connect vulnerable populations to HIV and STI testing services. For example, online sex-seeking platforms could be used for targeted marketing and promotions to incentivize HIV and STI testing [67]. Motivational interviewing is a goal-oriented counseling technique that can potentially be delivered over the phone [68] and has been used to successfully promote HIV testing among MSM in Hong Kong [69]. HIV self-testing with online supervision may be appropriate for young MSM who seek sexual partners online but are disinterested in venue-based testing [70]. Many of these types of interventions are already being deployed in Bangkok and their success probably contributes to the increased testing uptake observed amongst participants in our study who met sexual partners online.

Conversely, we identified gaps in testing uptake among participants who met sexual partners outside of online settings, particularly those who met male sexual partners at bars. Decentralization of HIV and STI testing services may increase accessibility of these services to people who are not currently seeking testing in traditional healthcare settings or being reached by targeted online interventions. For example, lay providers can be successfully trained to provide rapid diagnostic testing for HIV [71] and community-based organizations can be leveraged to deliver HIV and STI prevention packages to venues frequented by behaviorally vulnerable MSM and TGW [47]. When designing public health interventions to increase HIV and STI testing, providing a combination of options that range from predominantly online engagement to predominantly in-person may best address the needs and preferences of diverse populations in need of testing [72]. Strategies for successful linkage to care after HIV or STI diagnosis outside of traditional healthcare settings will need to be carefully considered [73].

We found that prior testing for HIV and other STIs was most common among participants who reported sexual attraction exclusively to men, revealing a potential gap in accessibility of testing to individuals with other sexual preferences. It is important to note that all participants in this study, regardless of sexual attraction, reported sex with male or TGW partners. Bisexual or heterosexual individuals who engage in same-sex sexual practices may feel particularly marginalized or stigmatized and be less likely to access MSM-focused venues for HIV or STI testing [74,75,76]. Healthcare providers and organizations must recognize the diversity of sexual preferences represented amongst MSM and TGW populations in order to create welcoming spaces and differentiated methods for delivering testing services to sexual and gender minority populations that may otherwise be overlooked.

Knowledge about HIV and other STIs influences risk perception and subsequent testing uptake [77]. This may at least partly explain the relationship between higher education and increased testing in our study. Prior studies have shown that discordance between self-perceived and actual risk may be a barrier to uptake of testing services by Thai MSM and TGW [78] as well as MSM travelers to Thailand [79]. In one study of MSM attending saunas in Bangkok, younger participants were more likely than older ones to demonstrate sexual behaviors associated with HIV risk but had a false perception of low HIV risk [80]. Interventions to increase knowledge about HIV and other STIs, delivered in early academic settings and outside of academic settings, may help to improve testing uptake.

It should be noted that most of the data for these analyses were assessed by self-report and could be susceptible to both recall and social desirability biases; use of CASI for data collection should have reduced the latter. Data were collected cross-sectionally at enrollment into a study that included routine HIV and syphilis screening, so analyses were based primarily on historic experiences and temporal associations could not be evaluated. The study was conducted at two sites in Bangkok with experience engaging sexual and gender minority populations, so findings may not be generalizable to other settings. Recruitment activities that focused on bars, saunas, and online networking platforms may have enriched the study population for participants who met sexual partners via these venues.

Conclusions

We observed substantial room for improvement in testing uptake for HIV and other STIs among MSM and TGW in Bangkok, Thailand. Differentiated models of service delivery that leverage online and offline opportunities for engagement will be needed to reach diverse, marginalized populations that are behaviorally vulnerable to HIV and other STIs.

Data availability

The Henry M. Jackson Foundation for the Advancement of Military Medicine (HJF) and the Water Reed Army Institute of Research (WRAIR) are committed to safeguarding the privacy of research participants. Distribution of data will require compliance with all applicable regulatory and ethical processes, including establishment and approval of an appropriate data-sharing agreement. To request a minimal data set, please contact the data coordinating and analysis center at PubRequest@hivresearch.org and indicate the RV348B study along with the name of the manuscript.

Abbreviations

AIDS:

Acquired immune deficiency syndrome

AR:

Army Regulation

CASI:

Computer-assisted self-interview

CFR:

Code of Federal Regulations

CI:

Confidence intervals

HIV:

Human immunodeficiency virus

MSM:

Men who have sex with men

PrEP:

Pre-exposure prophylaxis

RR:

Risk ratio

STIs:

Sexually transmitted infections

TGW:

Transgender women

UNAIDS:

Joint United Nations Programme on HIV/AIDS

U.S.:

United States

References

  1. TEMPRANO ANRS Study Group, Danel C, Moh R, Gabillard D, Badje A, Le Carrou J, et al. A trial of early antiretrovirals and isoniazid preventive therapy in Africa. N Engl J Med. 2015;373(9):808–22.

    Article  CAS  Google Scholar 

  2. INSIGHT START Study Group, Lundgren JD, Babiker AG, Gordin F, Emery S, Grund B, et al. Initiation of antiretroviral therapy in early asymptomatic HIV Infection. N Engl J Med. 2015;373(9):795–807.

    Article  CAS  Google Scholar 

  3. Grinsztejn B, Hosseinipour MC, Ribaudo HJ, Swindells S, Eron J, Chen YQ, et al. Effects of early versus delayed initiation of antiretroviral treatment on clinical outcomes of HIV-1 infection: results from the phase 3 HPTN 052 randomised controlled trial. Lancet Infect Dis. 2014;14(4):281–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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):388–99.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, et al. Antiretroviral therapy for the prevention of HIV-1 Transmission. N Engl J Med. 2016;375(9):830–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kroon E, Phanuphak N, Shattock AJ, Fletcher JLK, Pinyakorn S, Chomchey N, et al. Acute HIV infection detection and immediate treatment estimated to reduce transmission by 89% among men who have sex with men in Bangkok. J Int AIDS Soc. 2017;20(1):21708.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol. 2004;2(1):33–42.

    Article  CAS  PubMed  Google Scholar 

  8. King CC, Ellington SR, Kourtis AP. The role of co-infections in mother-to-child transmission of HIV. Curr HIV Res. 2013;11(1):10–23.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Wynn A, Bristow CC, Cristillo AD, Murphy SM, van Broek N, Muzny C, et al. Sexually transmitted infections in pregnancy and reproductive health: Proceedings of the STAR Sexually Transmitted Infection Clinical Trial Group Programmatic Meeting. Sex Transm Dis. 2020;47(1):5–11.

    Article  PubMed  Google Scholar 

  10. Davies B, Turner KM, Leung S, Yu BN, Frolund M, Benfield T, et al. Comparison of the population excess fraction of Chlamydia trachomatis infection on pelvic inflammatory disease at 12-months in the presence and absence of chlamydia testing and treatment: systematic review and retrospective cohort analysis. PLoS ONE. 2017;12(2):e0171551.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Plax K, Garbutt J, Kaushik GN. HIV and sexually transmitted infection testing among high-risk youths: supporting positive opportunities with teens (SPOT) youth center. Am J Public Health. 2015;105(7):1394–8.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Nowak RG, Ndembi N, Dauda W, Jibrin P, Bentzen SM, Nnaji CH, et al. Implementation of and early outcomes from anal cancer screening at a community-engaged health care facility providing care to nigerian men who have sex with men. J Glob Oncol. 2019;5:1–11.

    PubMed  Google Scholar 

  13. Kayode BO, Mitchell A, Ndembi N, Kokogho A, Ramadhani HO, Adebajo S, et al. Retention of a cohort of men who have sex with men and transgender women at risk for and living with HIV in Abuja and Lagos, Nigeria: a longitudinal analysis. J Int AIDS Soc. 2020;23(Suppl 6):e25592.

    PubMed  PubMed Central  Google Scholar 

  14. Baggaley R, Dalal S, Johnson C, Macdonald V, Mameletzis I, Rodolph M, et al. Beyond the 90-90-90: refocusing HIV prevention as part of the global HIV response. J Int AIDS Soc. 2016;19(1):21348.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jones MU, Ramadhani HO, Adebajo S, Gaydos CA, Kokogho A, Baral SD, et al. Seizing opportunities for intervention: Changing HIV-related knowledge among men who have sex with men and transgender women attending trusted community centers in Nigeria. PLoS ONE. 2020;15(3):e0229533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Crowell TA, Baral SD, Schwartz S, Nowak RG, Kokogho A, Adebajo S, et al. Time to change the paradigm: limited condom and lubricant use among Nigerian men who have sex with men and transgender women despite availability and counseling. Ann Epidemiol. 2019;31:11–9.

    Article  PubMed  Google Scholar 

  17. Stenger MR, Baral S, Stahlman S, Wohlfeiler D, Barton JE, Peterman T. As through a glass, darkly: the future of sexually transmissible infections among gay, bisexual and other men who have sex with men. Sex Health. 2017;14(1):18–27.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Poteat T, Scheim A, Xavier J, Reisner S, Baral S. Global Epidemiology of HIV Infection and Related Syndemics Affecting Transgender People. J Acquir Immune Defic Syndr. 2016;72(Suppl 3):210–9.

    Google Scholar 

  19. Poteat TC, van der Merwe LLA, Sevelius J, Keatley J. Inclusion as illusion: erasing transgender women in research with MSM. J Int AIDS Soc. 2021;24(1):e25661.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Perez-Brumer AG, Oldenburg CE, Reisner SL, Clark JL, Parker RG. Towards ‘reflexive epidemiology’: Conflation of cisgender male and transgender women sex workers and implications for global understandings of HIV prevalence. Glob Public Health. 2016;11(7–8):849–65.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Poteat T, Ackerman B, Diouf D, Ceesay N, Mothopeng T, Odette KZ, et al. HIV prevalence and behavioral and psychosocial factors among transgender women and cisgender men who have sex with men in 8 African countries: A cross-sectional analysis. PLoS Med. 2017;14(11):e1002422.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Poteat TC, Celentano DD, Mayer KH, Beyrer C, Mimiaga MJ, Friedman RK, et al. Depression, sexual behavior, and HIV treatment outcomes among transgender women, cisgender women and men who have sex with men living with HIV in Brazil and Thailand: a short report. AIDS Care. 2020;32(3):310–5.

    Article  PubMed  Google Scholar 

  23. European Centre for Disease Prevention and Control. HIV and STI prevention among men who have sex with men. Stockholm: ECDC; 2015.

  24. DiNenno EA, Prejean J, Irwin K, Delaney KP, Bowles K, Martin T, et al. Recommendations for HIV Screening of Gay, Bisexual, and Other Men Who Have Sex with Men - United States, 2017. MMWR Morb Mortal Wkly Rep. 2017;66(31):830–2.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Centers for Disease Control. US Public Health Service. Preexposure prophylaxis for the prevention of HIV infection in the United States—2017 Update: a clinical practice guideline. https://www.cdc.gov/hiv/pdf/risk/prep/cdc-hiv-prep-guidelines-2017.pdf. Accessed 4 Jun 2020.

  26. Bureau of AIDS, TB, and STIs, Department of Disease Control, Ministry of Public Health, Thailand. Thailand National Guidelines on HIV/AIDS Treatment and Prevention 2017 Bangkok, Thailand: Ministry of Public Health; 2017. http://www.thaiaidssociety.org/images/PDF/hiv_thai_guideline_2560.pdf.

  27. Brown AE, Attawell K, Hales D, Rice BD, Pharris A, Supervie V, et al. Monitoring the HIV continuum of care in key populations across Europe and Central Asia. HIV Med. 2018;67:311.

    Google Scholar 

  28. Hu X, Liang B, Zhou C, Jiang J, Huang J, Ning C, et al. HIV late presentation and advanced HIV disease among patients with newly diagnosed HIV/AIDS in Southwestern China: a large-scale cross-sectional study. AIDS Res Ther. 2019;16(1):6.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Wojcik-Cichy K, Jablonowska O, Piekarska A, Jablonowska E. The high incidence of late presenters for HIV/AIDS infection in the Lodz province, Poland in the years 2009–2016: we are still far from the UNAIDS 90% target. AIDS Care. 2018;30(12):1538–41.

    Article  PubMed  Google Scholar 

  30. Esber AL, Coakley P, Ake JA, Bahemana E, Adamu Y, Kiweewa F, et al. Decreasing time to antiretroviral therapy initiation after HIV diagnosis in a clinic-based observational cohort study in four African countries. J Int AIDS Soc. 2020;23(2):e25446.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gamarel KE, Nelson KM, Stephenson R, Santiago Rivera OJ, Chiaramonte D, Miller RL, et al. Anticipated HIV Stigma and Delays in Regular HIV Testing Behaviors Among Sexually-Active Young Gay, Bisexual, and Other Men Who Have Sex with Men and Transgender Women. AIDS Behav. 2018;22(2):522–30.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Bristow CC, Espinosa da Silva C, Vera AH, Gonzalez-Fagoaga JE, Rangel G, Pines HA. Prevalence of bacterial sexually transmitted infections and coinfection with HIV among men who have sex with men and transgender women in Tijuana, Mexico. Int J STD AIDS. 2021;32(8):751–7.

    Article  CAS  PubMed  Google Scholar 

  33. Keshinro B, Crowell TA, Nowak RG, Adebajo S, Peel S, Gaydos CA, et al. High prevalence of HIV, chlamydia and gonorrhoea among men who have sex with men and transgender women attending trusted community centres in Abuja and Lagos, Nigeria. J Int AIDS Soc. 2016;19(1):21270.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Twahirwa Rwema JO, Lyons CE, Herbst S, Liestman B, Nyombayire J, Ketende S, et al. HIV infection and engagement in HIV care cascade among men who have sex with men and transgender women in Kigali, Rwanda: a cross-sectional study. J Int AIDS Soc. 2020;23(Suppl 6):e25604.

    PubMed  PubMed Central  Google Scholar 

  35. Jones J, Sanchez TH, Dominguez K, Bekker LG, Phaswana-Mafuya N, Baral SD, et al. Sexually transmitted infection screening, prevalence and incidence among South African men and transgender women who have sex with men enrolled in a combination HIV prevention cohort study: the Sibanye Methods for Prevention Packages Programme (MP3) project. J Int AIDS Soc. 2020;23(Suppl 6):e25594.

    PubMed  PubMed Central  Google Scholar 

  36. Van Gerwen OT, Jani A, Long DM, Austin EL, Musgrove K, Muzny CA. Prevalence of sexually transmitted infections and human immunodeficiency virus in transgender persons: a systematic review. Transgend Health. 2020;5(2):90–103.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ntsepe Y, Simbayi LC, Shisana O, Rehle T, Mabaso M, Ncitakalo N, et al. Perceptions about the acceptability and prevalence of HIV testing and factors influencing them in different communities in South Africa. SAHARA J. 2014;11:138–47.

    Article  PubMed  Google Scholar 

  38. Ye R, Liu C, Tan S, Li J, Simoni JM, Turner D, et al. Factors associated with past HIV testing among men who have sex with men attending university in China: a cross-sectional study. Sex Health. 2021;18(1):58–63.

    Article  PubMed  Google Scholar 

  39. Tunnage J, Yates A, Nwoga C, Sing’oei V, Owuoth J, Polyak CS, et al. Hepatitis and tuberculosis testing are much less common than HIV testing among adults in Kisumu, Kenya: results from a cross-sectional assessment. BMC Public Health. 2021;21(1):1143.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Crowell TA, Qian H, Tiemann C, Lehmann C, Boesecke C, Stoehr A, et al. Factors associated with testing for HIV and hepatitis C among behaviorally vulnerable men in Germany: a cross-sectional analysis upon enrollment into an observational cohort. AIDS Res Ther. 2021;18(1):52.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Muccini C, Crowell TA, Kroon E, Sacdalan C, Ramautarsing R, Seekaew P, et al. Leveraging early HIV diagnosis and treatment in Thailand to conduct HIV cure research. AIDS Res Ther. 2019;16(1):25.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Phanuphak N, Ramautarsing R, Chinbunchorn T, Janamnuaysook R, Pengnonyang S, Termvanich K, et al. Implementing a status-neutral approach to HIV in the Asia-Pacific. Curr HIV/AIDS Rep. 2020;17(5):422–30.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Thisyakorn U. Elimination of mother-to-child transmission of HIV: lessons learned from success in Thailand. Paediatr Int Child Health. 2017;37(2):99–108.

    Article  PubMed  Google Scholar 

  44. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med. 2009;361(23):2209–20.

    Article  CAS  PubMed  Google Scholar 

  45. Colby D, Srithanaviboonchai K, Vanichseni S, Ongwandee S, Phanuphak N, Martin M, et al. HIV pre-exposure prophylaxis and health and community systems in the Global South: Thailand case study. J Int AIDS Soc. 2015;18(4 Suppl 3):19953.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Jose JED, Sakboonyarat B, Mungthin M, Nelson KE, Rangsin R. Rising prevalence of HIV infection and associated risk factors among young Thai Men in 2018. Sci Rep. 2021;11(1):7796.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ramautarsing RA, Meksena R, Sungsing T, Chinbunchorn T, Sangprasert T, Fungfoosri O, et al. Evaluation of a pre-exposure prophylaxis programme for men who have sex with men and transgender women in Thailand: learning through the HIV prevention cascade lens. J Int AIDS Soc. 2020;23(Suppl 3):e25540.

    PubMed  PubMed Central  Google Scholar 

  48. van Griensven F, de Lind van Wijngaarden JW, Eustaquio PC, Wignall S, Azwa I, Veronese V, et al. The continuing HIV epidemic among men who have sex with men and transgender women in the ASEAN region: implications for HIV policy and service programming. Sex Health. 2021;18(1):21–30.

    Article  PubMed  Google Scholar 

  49. Hiransuthikul A, Janamnuaysook R, Sungsing T, Jantarapakde J, Trachunthong D, Mills S, et al. High burden of chlamydia and gonorrhoea in pharyngeal, rectal and urethral sites among Thai transgender women: implications for anatomical site selection for the screening of STI. Sex Transm Infect. 2019;95(7):534–9.

    Article  PubMed  Google Scholar 

  50. Hiransuthikul A, Pattanachaiwit S, Teeratakulpisarn N, Chamnan P, Pathipvanich P, Thongpaen S, et al. High subsequent and recurrent sexually transmitted infection prevalence among newly diagnosed HIV-positive Thai men who have sex with men and transgender women in the Test and Treat cohort. Int J STD AIDS. 2019;30(2):140–6.

    Article  PubMed  Google Scholar 

  51. Wansom T, Muangnoicharoen S, Nitayaphan S, Kitsiripornchai S, Crowell T, Francisco L, et al. Risk Factors for HIV Seroconversion in a High Incidence Cohort of Men Who Have Sex with Men and Transgender Women in Bangkok, Thailand. EClinicalMedicine. 2021;38:101033.

    Article  PubMed  PubMed Central  Google Scholar 

  52. United Nations Development Programme, United States Agency for International Development. Being LGBT in Asia: Thailand Country Report. Bangkok: United States Agency for International Development; 2014.

    Google Scholar 

  53. Werner RN, Gaskins M, Nast A, Dressler C. Incidence of sexually transmitted infections in men who have sex with men and who are at substantial risk of HIV infection - A meta-analysis of data from trials and observational studies of HIV pre-exposure prophylaxis. PLoS ONE. 2018;13(12):e0208107.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Zhang W, Xu JJ, Zou H, Zhang J, Wang N, Shang H. HIV incidence and associated risk factors in men who have sex with men in Mainland China: an updated systematic review and meta-analysis. Sex Health. 2016;89:67.

    Google Scholar 

  55. Malekinejad M, Barker EK, Merai R, Lyles CM, Bernstein KT, Sipe TA, et al. Risk of HIV Acquisition Among Men Who Have Sex With Men Infected With Bacterial Sexually Transmitted Infections: A Systematic Review and Meta-Analysis. Sex Transm Dis. 2021;48(10):e138–48.

    Article  Google Scholar 

  56. Lagos D, Compton D. Evaluating the use of a two-step gender identity measure in the 2018 general social survey. Demography. 2021;58(2):763–72.

    Article  PubMed  Google Scholar 

  57. Reisner SL, Conron KJ, Tardiff LA, Jarvi S, Gordon AR, Austin SB. Monitoring the health of transgender and other gender minority populations: validity of natal sex and gender identity survey items in a U.S. national cohort of young adults. BMC Public Health. 2014;14:1224.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004;159(7):702–6.

    Article  PubMed  Google Scholar 

  59. Wimonsate W, Naorat S, Varangrat A, Phanuphak P, Kanggarnrua K, McNicholl J, et al. Factors associated with HIV testing history and returning for HIV test results among men who have sex with men in Thailand. AIDS Behav. 2011;15(4):693–701.

    Article  PubMed  Google Scholar 

  60. Vutthikraivit P, Lertnimitr B, Chalardsakul P, Imjaijitt W, Piyaraj P. Prevalence of HIV testing and associated factors among young men who have sex with men (MSM) in Bangkok, Thailand. J Med Assoc Thai. 2014;97(Suppl 2):207–14.

    Google Scholar 

  61. Seekaew P, Pengnonyang S, Jantarapakde J, Sungsing T, Rodbumrung P, Trachunthong D, et al. Characteristics and HIV epidemiologic profiles of men who have sex with men and transgender women in key population-led test and treat cohorts in Thailand. PLoS ONE. 2018;13(8):e0203294.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Holtz TH, Wimonsate W, Mock PA, Pattanasin S, Chonwattana W, Thienkrua W, et al. Why we need pre-exposure prophylaxis: incident HIV and syphilis among men, and transgender women, who have sex with men, Bangkok, Thailand, 2005–2015. Int J STD AIDS. 2019;30(5):430–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Wansom T, Pinyakorn S, Kolsteeg CJ, Kroon E, Sacdalan CP, Chomchey N, et al. Brief Report: Group Sex and Methamphetamine Use Fuel an Explosive Epidemic of Hepatitis C Among HIV-Infected Men Who Have Sex With Men in Bangkok, Thailand. J Acquir Immune Defic Syndr. 2020;84(4):331–5.

    Article  PubMed  Google Scholar 

  64. Weiss KM, Jonas KJ, Guadamuz TE. Playing and Never Testing: Human Immunodeficiency Virus and Sexually Transmitted Infection Testing Among App-Using MSM in Southeast Asia. Sex Transm Dis. 2017;44(7):406–11.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Lim SH, Guadamuz TE, Wei C, Chan R, Koe S. Factors associated with unprotected receptive anal intercourse with internal ejaculation among men who have sex with men in a large Internet sample from Asia. AIDS Behav. 2012;16(7):1979–87.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Wei C, Lim SH, Guadamuz TE, Koe S. Virtual versus physical spaces: which facilitates greater HIV risk taking among men who have sex with men in East and South-East Asia? AIDS Behav. 2014;18(8):1428–35.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Anand T, Nitpolprasert C, Ananworanich J, Pakam C, Nonenoy S, Jantarapakde J, et al. Innovative strategies using communications technologies to engage gay men and other men who have sex with men into early HIV testing and treatment in Thailand. J Virus Erad. 2015;1(2):111–5.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Berg RC, Ross MW, Tikkanen R. The effectiveness of MI4MSM: how useful is motivational interviewing as an HIV risk prevention program for men who have sex with men? A systematic review AIDS Educ Prev. 2011;23(6):533–49.

    Article  PubMed  Google Scholar 

  69. Chan PS, Chidgey A, Lau J, Ip M, Lau JTF, Wang Z. Effectiveness of a Novel HIV Self-Testing Service with Online Real-Time Counseling Support (HIVST-Online) in Increasing HIV Testing Rate and Repeated HIV Testing among Men Who Have Sex with Men in Hong Kong: Results of a Pilot Implementation Project. Int J Environ Res Public Health. 2021;18(2):20.

    Article  Google Scholar 

  70. Samoh N, Peerawaranun P, Jonas KJ, Lim SH, Wickersham JA, Guadamuz TE. Willingness to Use HIV Self-Testing With Online Supervision Among App-Using Young Men Who Have Sex With Men in Bangkok. Sex Transm Dis. 2021;48(3):e41–4.

    Article  Google Scholar 

  71. Wongkanya R, Pankam T, Wolf S, Pattanachaiwit S, Jantarapakde J, Pengnongyang S, et al. HIV rapid diagnostic testing by lay providers in a key population-led health service programme in Thailand. J Virus Erad. 2018;4(1):12–5.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Phanuphak N, Anand T, Jantarapakde J, Nitpolprasert C, Himmad K, Sungsing T, et al. What would you choose: Online or Offline or Mixed services? Feasibility of online HIV counselling and testing among Thai men who have sex with men and transgender women and factors associated with service uptake. J Int AIDS Soc. 2018;21(Suppl 5):e25118.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Phanuphak N, Jantarapakde J, Himmad L, Sungsing T, Meksena R, Phomthong S, et al. Linkages to HIV confirmatory testing and antiretroviral therapy after online, supervised, HIV self-testing among Thai men who have sex with men and transgender women. J Int AIDS Soc. 2020;23(1):e25448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Lemke R, Weber M. That man behind the curtain: investigating the sexual online dating behavior of men who have sex with men but hide their same-sex sexual attraction in offline surroundings. J Homosex. 2017;64(11):1561–82.

    Article  PubMed  Google Scholar 

  75. Koo FK, Chow EP, Gao L, Fu X, Jing J, Chen L, et al. Socio-cultural influences on the transmission of HIV among gay men in rural China. Cult Health Sex. 2014;56:934.

    Google Scholar 

  76. Schrimshaw EW, Downing MJ Jr, Siegel K. Sexual venue selection and strategies for concealment of same-sex behavior among non-disclosing men who have sex with men and women. J Homosex. 2013;60(1):120–45.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Lin Y, Li C, Wang L, Jiao K, Ma W. The mediated effect of HIV risk perception in the relationship between peer education and HIV testing uptake among three key populations in China. AIDS Res Ther. 2021;18(1):8.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Seekaew P, Pengnonyang S, Jantarapakde J, Meksena R, Sungsing T, Lujintanon S, et al. Discordance between self-perceived and actual risk of HIV infection among men who have sex with men and transgender women in Thailand: a cross-sectional assessment. J Int AIDS Soc. 2019;22(12):e25430.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Wang Z, Fang Y, Yaemim N, Jonas KJ, Chidgey A, Ip M, et al. Factors Predicting Uptake of Sexually Transmitted Infections Testing among Men Who Have Sex with Men Who Are “Pre-Exposure Prophylaxis Tourists”-An Observational Prospective Cohort Study. Int J Environ Res Public Health. 2021;18:7.

    Google Scholar 

  80. Khawcharoenporn T, Mongkolkaewsub S, Naijitra C, Khonphiern W, Apisarnthanarak A, Phanuphak N. HIV risk, risk perception and uptake of HIV testing and counseling among youth men who have sex with men attending a gay sauna. AIDS Res Ther. 2019;16(1):13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The RV348B Study Group is deeply grateful to all study participants for their dedication to this study and to the Community Advisory Boards for their helpful input. The RV348B Study Group includes, from the Armed Forces Research Institute of Medical Sciences: Tanyaporn Wansom, Kirsten Smith, Siriwat Akapirat, Suchai Kitsiripornchai, Rapee Trichavaroj, Pornchanok Panjapornsuk, Vatcharain Assawadarachai, Nantana Tantibul, Bessara Nuntapinit, Phiromrat Rakyat, Anant Phramtong, Saowanit Getchalarat, Nampueng Churikanont, Nongluck Sangnoi; from the Faculty of Tropical Medicine, Mahidol University: Punnee Pitisuttithum, Sant Muangnoicharoen, Jittima Dhitavat, Arom Pitisuthitham, Benjaluck Phonrat, Yupa Sabmee, Nonthiya Chaisrisiri, Chalandakorn Ruengprasertkit, Jutarat Wattanakitwichai, Anchalee Yamklin; from the Royal Thai Army Clinical Research Centre: LTG Sorachai Nitayaphan, MG Narongrid Sirisopana, Prapaporn Savaraj, Wanlaya Lapwech, Siriluck Teerachia; from the Walter Reed Army Institute of Research: COL. Robert J. O’Connell, Sandhya Vasan, Merlin Robb, Trevor A. Crowell; from the U.S. Army Medical Materiel Development Activity: Elizabeth E. Heger, Paileen Mongelli, Brianna Whitworth, Dixion Rwakasyaguri; and from Emmes: Peter Dawson.

Prior presentation

This work has not been previously presented.

Disclaimer

The views expressed are those of the authors and should not be construed to represent the positions of the U.S. Army, the Department of Defense, or the Henry M. Jackson Foundation for the Advancement of Military Medicine. The investigators have adhered to the policies for protection of human subjects as prescribed in AR 70–25.

Funding

This study was supported by the U.S. Military HIV Research Program under cooperative agreements between the U.S. Army and the Henry M. Jackson Foundation for the Advancement of Military Medicine (W81XWH-11-2-0174, W81XWH-07-2-0067), with support from the Division of AIDS at the U.S. National Institute of Allergy and Infectious Diseases and the U.S. Army Medical Materiel Development Activity (Y1-AI-2642-12, Y1-AI-2642-16).

Author information

Authors and Affiliations

Authors

Consortia

Contributions

TAC contributed to study design and implementation, conceptualized these analyses, conducted the analyses, and authored the first draft of the manuscript. SN, NS, SK, and PP contributed to study design and implementation, oversaw the collection of clinical data, and assisted with interpretation of the data. TW conceptualized the study, contributed to study design and implementation, and assisted with the interpretation of results. LF, QL, ND, and PD provided data management and analytic support. RJO and SV conceptualized the study, contributed to the design of these analyses, assisted in the interpretation of results, and provided general oversight of the study and these analyses. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Trevor A. Crowell.

Ethics declarations

Ethics approval and consent to participate

All participants provided written informed consent in either Thai or English prior to any study procedures. The study was reviewed and approved by the institutional review boards at Walter Reed Army Institute of Research, Faculty of Tropical Medicine at Mahidol University, and the Royal Thai Army. The investigators adhered to the policies regarding the protection of human subjects as prescribed by Code of Federal Regulations (CFR) Title 45, Volume 1, Part 46; Title 32, Chap. 1, Part 219; and Title 21, Chap. 1, Part 50 (Protection of Human Subjects) and Army Regulation 70–25.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crowell, T.A., Nitayaphan, S., Sirisopana, N. et al. Factors associated with testing for HIV and other sexually transmitted infections in men who have sex with men and transgender women in Bangkok, Thailand. AIDS Res Ther 19, 25 (2022). https://doi.org/10.1186/s12981-022-00449-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12981-022-00449-0

Keywords