Introduction

The Joint United Nations Program on HIV/AIDS (UNAIDS) estimates that 25% of people infected with HIV globally did not know their HIV status in 2018 [1]. Nearly half (47%) of new HIV infections globally occur among key populations and their sexual partners, including men who have sex with men (MSM) [2]. Globally, the risk of HIV acquisition was 28 times higher among MSM than heterosexual men in 2017 [1, 3]. In Uganda, HIV prevalence among MSM is 13.2% compared to 5.9% in the general population and key populations including MSM account for more than a third of new HIV infections [3–6].

HIV testing is the entry point to HIV care; increasing testing coverage is a key step to reaching the first UNAIDS 90-90-90 target, i.e., 90% of people living with HIV knowing their HIV status. However, testing uptake is still low among MSM despite efforts to scale up prevention services for key populations (KP) in Uganda [5–8]. A recent bio-behavioral survey of Ugandan MSM found that 35% had never tested for HIV [6]. HIV self-testing (HIVST), in which an individual performs and interprets his/her own HIV test [8–13], is an acceptable and innovative approach that could increase knowledge of HIV sero-status among MSM, and is recommended by the World Health Organization and Uganda Ministry of Health [3,14–22]. In addition, HIVST is convenient since individuals can test at any time, in private, without having to present to a clinic during fixed working hours. In Uganda, healthcare stigma, discrimination, homophobic violence and criminalization are significant barriers to uptake of facility-based HIV testing among MSM [4, 6, 8, 23]. Scaling up access to HIVST could increase testing coverage among MSM with low access to facility-based services [3, 6]. Studies in other settings have demonstrated that 82–100% of MSM who test positive after HIVST seek additional testing and more than 80% were linked to treatment [11, 24]. However, few studies have evaluated uptake of HIVST among MSM in sub-Saharan Africa [22, 24]

Novel, effective strategies are urgently needed to increase coverage of HIV testing services among MSM, and promote linkage to prevention, care and treatment services. Peer distribution of HIVST kits in MSM networks may increase access to HIV testing in Uganda where 33% of MSM had never tested for HIV in 2012 [8, 9, 12, 25]. In a recent pilot intervention at the AIDS Support Organization (TASO) secondary distribution of referral coupons by MSM peers increased uptake of facility-based HIV testing [26]. Of 200 coupons distributed, 150 MSM (75%) presented at the facility for HIV testing, and >80% were frequent testers [27], suggesting that use of peer strategies could increase MSM uptake of HIV testing and other prevention services.

This study aimed to evaluate the preliminary effectiveness of peer distribution of HIVST oral fluid self-test kits to MSM networks in identifying undiagnosed HIV infection compared with standard-of-care (SOC) approaches.

Methods

Results

Population characteristics

A total of 297 participants were included in the analysis of which 150 (51%) were accrued using the peer HIVST distribution strategy. Of these, seven participants did not use HIVST. The median age of the remaining 143 participants was 25 years (interquartile range [IQR], [22–28] with a median number of eight sexual partners in the prior year (IQR 4–19) (Table 1). Most (58%) had received primary education, while 18% had no formal education. Before receiving their HIVST kit, the majority (82%) of participants received individual pre-HIV counselling and demonstration of HIVST use before accepting the kit and their testing history elicited. One third (32%) had never tested. Of those with history of HIV testing, 91% had tested for HIV only once in their lifetime. Most of the intervention participants (64%) did not know their sexual partner(s) HIV status.

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Table 1. Demographic characteristics.

https://doi.org/10.1371/journal.pone.0227741.t001

Peer-distributed HIVST uptake.

Peers distributed a total of 150 HIVST kits. The majority (95%) of the participants completed HIVST; 71 in TASO Masaka and 72 in Entebbe (S1 Fig). Nearly all (94%) received post-test HIV counselling from peers who distributed the kits or from peers at the TASO health facility. Most (61%) participants tested alone while 39% tested with the support and presence of the peer. Of the participants tested, the majority (85%) trusted the HIVST results. Overall, eight participants tested HIV positive 2/71 (2.8%) from Masaka and 6/72 (8.3%) from Entebbe), and all eight disclosed their HIV test results to the peers. All were linked to care by peers, re-tested to confirm their HIV status and initiated on ART. A total of 147 MSM in the TASO testing program were tested using SOC approaches yielding 4 (2.7%) undiagnosed infections between January and March 2018. In contrast, the peer HIVST kit distribution strategy reached 143 MSM and identified 8 participants with undiagnosed HIV infection during the 3 months of follow-up (5.6% vs 2.7%; P = 0.02, by the Fisher exact test).

Discussion

Our study found that one-in-three MSM in Uganda had never tested for HIV. Peer HIVST distribution identified twice as many undiagnosed HIV infections as SOC testing approaches. In this pilot study, that included 297 MSM, peer distributed HIVST reached significantly more never testers or MSM who had not tested in the previous six months. All participants who tested positive were linked for confirmatory testing and HIV care through appointment. Participants who did not turn up for appointments were followed up by peers, accompanied to the HIV care centre for a confirmatory test, and started on ART.

To our knowledge, this is one of the first studies in sub-Saharan Africa to evaluate secondary distribution of HIVST by MSM peers to their social and sexual networks. Our findings suggest that distributing HIVST kits through peer networks is feasible, acceptable and could be an effective strategy to increase uptake of HIV testing and linkage to care in a marginalized and stigmatized population with low testing coverage [8–15]. Our results are in agreement with prior studies done among heterosexual fishing communities in Uganda, and MSM in the United Kingdom and United States, in which peer distribution of HIVST had high uptake and acceptability and successfully identified undiagnosed HIV infections [13,18, 30, 31]. Identifying new HIV infections is an important first step to optimizing the treatment and care cascade for people infected with HIV, particularly for African MSM who are disproportionately affected by the HIV epidemic. The ability of the peer HIVST distribution strategy to reach MSM never-testers or infrequent testers suggests that it could increase testing coverage by accessing MSM who have never tested or tested once in life time and help attain the first UNAIDS 90 target—90% of HIV-infected MSM knowing their status.

Our findings support growing evidence that peer-based strategies are effective in increasing HIV testing among high-risk populations including MSM [13, 18]. A recent study compared respondent driven sampling to conventional outreach-based HIV testing strategies and found that peer-based chain recruitment was more efficient than conventional testing and counseling at identifying HIV infections among MSM [30]. However, prior studies that assessed peer-based testing strategies typically required testers to present at a clinic or research site for an HIV test, and thus only partially address the social and structural barriers that minority MSM encounter when seeking an HIV test. Community-based HIV self-testing delivered by members of a target community or social group could be more effective in reaching those who may not seek testing in high-stigma contexts [20, 32]. This approach builds on prior experiences of peer-driven distribution of HIV prevention tools and referral coupons for HIV testing in key populations, e.g., coupon distribution among MSM in Uganda [8–12].

The strengths of our study include leveraging peer social and sexual networks to increase HIV testing coverage through secondary distribution of HIVST. While we were unable to determine if peer recruiters and those that tested were in the same sexual networks, closed or interconnected sexual networks might help explain high HIV prevalence among MSM in this setting. A limitation of our study was that we report non-randomized comparisons which should be interpreted with caution. Few MSM tested positive so we may be overstating the yield of our peer-delivered intervention. Nevertheless, other studies support the effectiveness of peer-delivered combination prevention. Our results may not be generalizable to all MSM, because our sample was largely comprised of younger MSM. However, these findings contribute to the evidence base for African MSM, an understudied population. Information on education and HIV testing history was not collected during routine TASO program activities and there was considerable missing data. Nevertheless, missing data did not affect ascertainment of the primary outcome. Finally, we did not debrief peers to ascertain their experiences with HIVST distribution or assess whether they would distribute HIVST kits in the future, which could inform future program implementation. The time period for HIVST kits distribution was different from the standard of care moonlight and hotspot approaches, and it is possible that temporal trends confounded study outcomes.

Conclusion

We found that distributing HIVST kits through MSM peer-networks was feasible, acceptable and effective and could increase uptake of HIV testing and reduce undiagnosed infections among MSM in Uganda. Future implementation research should determine the cost-effectiveness of this strategy in finding and linking persons with undiagnosed infections to HIV care.

Supporting information

Acknowledgments

We are very grateful to The AIDS Support Organization (TASO) leadership of Masaka and Entebbe for allowing us to conduct this pilot study within their MSM dedicated care program. We are indebted to the TASO Program Director, Dr. Kenneth Mugisha and the Executive Director of TASO, Dr. Bernard Michael Etukoit for administratively supporting this study and to the participants for taking part in the study.