Awareness, willingness to use, and history of HIV PrEP use among gay, bisexual, and other men who have sex with men in Nigeria

Background Nigerian gay, bisexual, and other men who have sex with men (GBMSM) are disproportionately affected by HIV, with an estimated prevalence of between 11–35%. Pre-exposure prophylaxis (PrEP) has the potential to significantly decrease incident HIV infections among Nigerian GBMSM. Understanding the relationship between socio-demographic, sexual risk behavior, and psychosocial factors with PrEP awareness, willingness to use, and history of use among this group is pivotal to maximizing PrEP uptake. Methods Between March and June 2019, 419 participants completed an interviewer-administered survey assessing PrEP awareness, willingness to use, and history of use; socio-demographics; sexual risk behavior; and psychosocial factors. Bivariate and multivariable logistic regression were used to examine factors associated with PrEP awareness, willingness to use, and history of use. Results 53.6% were aware of PrEP; 80.1% were willing to use PrEP; and 29.7% had previously used PrEP. In multivariable analysis, factors associated with an increased odds of PrEP awareness include residing in Abuja [adjusted odds ratio (aOR) 5.02; 95% confidence interval (CI): 2.13 to 11.83] and Lagos (aOR 12.30; 95% CI: 4.92 to 30.67) vs. residing in Plateau, living with HIV (aOR 2.56; 95% CI: 1.54 to 4.72), using location-based apps for seeking sexual partners (aOR 4.06; 95% CI: 2.28 to 7.24), having health insurance (aOR 2.31; 95% CI: 1.08 to 4.40), history of suicidal thoughts (aOR 2.05; 95% CI: 1.02 to 4.10), and history of PrEP use (aOR 45.5; 95% CI: 5.60 to 370.04). Decreasing clinically significant depressive symptoms was associated with lower willingness to use PrEP (aOR 0.96; 95% CI: 0.92 to 0.99). Lastly, factors associated with increased odds of having a history of PrEP use were those reporting 6 or more insertive anal sex acts in the last 30 days compared to those with none (aOR 5.76; 95% CI: 1.58 to 20.98) and being aware of PrEP (aOR 29.6; 95% CI: 3.78 to 231.84). Discussion Nearly half of the Nigerian GBMSM in this study had no prior awareness of PrEP, but after being informed about its potential benefits, the majority were willing to use it. However, PrEP uptake among Nigerian GBMSM remains low. Findings suggest that educational messages are necessary to ensure appropriate PrEP scale-up, especially tailored towards Nigerian GBMSM.


Introduction
Nigeria has the fourth largest human immunodeficiency virus (HIV) epidemic in the world, with a prevalence of 1.4% among the general adult population and an estimated 1.9 million people living with HIV [1]. Nigerian gay, bisexual and other men who have sex with men (GBMSM) bear a disproportionately higher burden of HIV, with an estimated prevalence of 11-35% [2]. Oral pre-exposure prophylaxis (PrEP) is a biomedical prevention approach that significantly reduces HIV acquisition when taken daily [3][4][5]. Given its' efficacy, PrEP has the potential to significantly decrease new HIV infections among Nigeria GBMSM. In 2013, a consultation of community leaders, implementers, and academics from17 African countries gathered to assess HIV prevention priorities for GBMSM and identified oral PrEP as a major biomedical prevention strategy [6]. Currently, PrEP is not widely available in Nigeria, however there are two ongoing implementation and demonstration projects with an estimated 400-600 individuals currently taking PrEP [7].
Gaining an in-depth understanding of awareness of and acceptability of PrEP among Nigerian GBMSM is crucial for preparing for PrEP uptake, once it becomes more widely available. To date, only a few studies have investigated PrEP awareness, acceptability, and current use among African GBMSM. A recently published study of 459 HIV-negative Kenyan GBMSM found that 64.3% had awareness of PrEP and 44.9% were willing to use PrEP in the future [8].
Another study of 137 GBMSM in Ghana found low awareness but high acceptability of PrEP [9]. These studies provide preliminary evidence of PrEP being acceptable by African GBMSM.
To date, there are no known published studies that have explored the relationship between socio-demographic, sexual risk behavior, and psychosocial factors with PrEP awareness, willingness to use PrEP, and history of PrEP use for HIV prevention among Nigerian GBMSM. The goal of the current study is to examine these relationships among a community-recruited sample of GBMSM in four diverse regions of Nigeria. Understanding these relationships will be helpful for designing successful intervention programs to increase PrEP uptake among this marginalized group.

Participants and procedures
Between March and June 2019, 413 GBMSM enrolled in the study and completed a quantitative assessment. Inclusion criteria were: 1) 18 years of age or older; 2) currently residing in one of four Nigerian states (Abuja, Lagos, Delta or Plateau); 3) cis-gender male; and 4) having sex with another male.
Participants were recruited through community-based organizations (CBOs) in each of the four states and via snowball sampling. Outreach workers and peer educators at the respective CBOs shared information about the study with the target population during programming events (e.g., HIV testing and counseling, health education, advocacy events, etc.) and provided study contact information to individuals who were interested. Eligible participants were then asked to provide study information to their peer networks.
Study activities took place in private offices within our partner CBOs. The study was approved by the institutional review boards at Brown University and the Nigerian Institute of Medical Research. Informed verbal consent was obtained from each participant prior to enrolling them in study. Each participant completed an interviewer administered behavioral survey. Participants were compensated 4,000 Naira (10 US dollars) for their participation.
participants were asked: "Have you ever taken PrEP to prevent HIV?" (yes/no). We excluded participants who self-reported living with HIV and those currently residing in Delta or Plateau state, where PrEP is currently unavailable.

Data analysis
We assessed the distribution (percentages and means) of all variables by PrEP awareness, willingness to use, and history of use. Chi-square global tests of independence were used to assess independent association between variables. Bivariate logistic regression was conducted to assess the association between socio-demographic, sexual risk behavior, and psychosocial factors and the three PrEP-related outcomes (PrEP awareness, willingness to use PrEP, and history of PrEP use). It was determined that a sample size of 400 GBMSM (100 recruited in each of the four states) would provide 80% power to detect a 30% or greater difference in PrEP awareness between the four States sampled at a two sided .05 significance level. Variables significant at the p<0.05 level in the bivariate models were retained in each of the three multivariable models assessing these outcomes. Data were analyzed using SAS version 9.4 (Cary, NC).

Results
As seen in Table 1, Participants ranged in age from 18 to 60 years (mean = 29.2, SD = 5.8), with 59.4% identifying as bisexual, and 62.3% were single. More than a third (37.7%) of the sample was living with HIV and 32.1% had an STI diagnosis in the last year. Almost half (48.8%) had a primary care provider but only 15.6% had health insurance. The depression scores ranged from 0 to 60 with a mean score of 10.0 (SD = 11.5); 23.7% of participants had a score of 16 or higher, indicating moderate to severe depression. 18.9% of participants were indicated for hazardous drinking and history of drug use were prevalent: marijuana (42.2%), tramadol (15.2%), rophynol (15.1%), codeine (24.1%), poppers (8.6%), cocaine (7.1%). More than half the sample (53.6%) were aware of PrEP, 80.1% were willing to use PrEP, and 29.7% had a history of PrEP use.

PrEP awareness
In multivariable analysis (

Willingness to use PrEP
In multivariable analysis (Table 2), decreasing clinically significant depressive symptoms was associated with lower willingness to use PrEP (aOR 0.96; 95% CI: 0.92 to 0.99).

History of PrEP use
In the multivariable model (Table 2), factors associated with increased odds of having a history of PrEP use were those reporting 6 or more insertive anal sex acts in the last 30 days compared to those with none (aOR 5.76; 95% CI: 1.58 to 20.98) and being aware of PrEP (aOR 29.6; 95% CI: 3.78 to 231.84).

Discussion
This is the first quantitative study that we are aware of to explore PrEP awareness, willingness to use PrEP, and history of PrEP use among GBMSM in Nigeria and West Africa. Nearly half (46.4%) of the Nigerian GBMSM in this study had no prior awareness of PrEP, but after being informed about its potential benefits, the majority (80.1%) were willing to use it. Furthermore, PrEP uptake among Nigerian GBMSM remains low (29.7%). Our findings align with a recent review article that found relatively low PrEP awareness (16.9-44.3%) but higher willingness to use PrEP (53.3-74.8%) among GBMSM in low and middle income countries [13]. We found that residing Lagos and Abuja was significantly associated with PrEP awareness compared to residing in Plateau. This finding is likely explained by the recent availability of PrEP among GBMSM in these two states. Additionally, we found that people living with HIV had higher PrEP awareness compared to those who reported being HIV uninfected. Since recruitment occurred through CBOs, some of which provide HIV testing and counseling, and antiretroviral therapy, it is possible that people living with HIV may have been counselled on the efficacy of PrEP to decrease HIV transmission among serodiscordant sexual partnerships [14]. We found that individuals who had used location-based apps for seeking sexual partners had increased odds of being PrEP aware, compared to those who reported non-use. This finding support recommendation for using geosocial networking apps (e.g., Grindr, Badoo, etc) as potentially effective medium for dissemination of PrEP messaging as rollout expands in Nigeria, especially given thar more than half of the sample (53.4%) reported using these apps and these apps have been previously associated with greater number of sexual partners, condomless anal sex, and increased incidence of HIV and other sexually transmitted infections [15,16]. This is especially relevant in Nigeria where homosexuality is criminalized and limited safe spaces exist for GBMSM, with many resorting to these apps to meet other GBMSM for a friendship, relationship, and/or sex.
GBMSM with clinically significant depressive symptoms had a decreased odds of willingness to use PrEP. This finding highlights how mental health issues might affect interest in PrEP uptake, which is particularly important as psychosocial health problems has been associated with increased risk for HIV infection among GBMSM [17][18][19]. A recently published study found that experiencing 4 or more psychosocial health problems (i.e. depressive symptoms, post-traumatic stress disorder, alcohol dependence, tobacco use, and hard-drug use)compared to experience none or one psychosocial health problem-was significantly associated with increasing number of male sexual partners among Nigerian GBMSM [20]. Previous research has highlighted the need to screen for mental health problems among GBMSM PrEP users, as it may lead to suboptimal PrEP adherence [21] and overall health [22].
We found that having 6 or more insertive anal sex partners in the last 30 days and being aware of PrEP were significantly associated with history of PrEP use. This finding may provide evidence that the current ongoing demonstration trial of PrEP in Nigeria is capturing those who are at most risk and PrEP awareness translating to PrEP uptake. This finding highlights the need for a PrEP awareness campaign, on various platforms, that provides easily understood, evidence-based information about PrEP. This campaign will help increase health literacy both around PrEP specifically and more generally on various other topics related to sexual health Information about effectiveness, costs, and common side effects should be provided. The campaign should include testimonials trusted GBMSM community members, to add credibility and relatability of the health campaign. Also, key stakeholders such as GBMSM community opinion leaders, CBOs, and geosocial networking apps are major channels for dissemination of information about PrEP to Nigerian GBMSM. Intentional engagement of these groups, at every step, is pivotal to increasing PrEP knowledge among Nigerian GBMSM, which would facilitate PrEP uptake and adherence.
These findings should be examined in the context of some study limitations The cross-sectional design limits our ability to draw causal inferences from our findings. In addition, participants were mainly recruited through GBMSM community-based organizations and GBMSM social networks, thus findings may not be generalizable to GBMSM who do not seek services at these CBOS or are outside of these social networks. In addition, many of the measures relied on participant recall/self-report (e.g., HIV status); future studies should use more objective measurements when possible.
Despite these limitations, this is among the first known quantitative analyses of PrEP awareness/acceptability among Nigerian GBMSM. Additionally, this is the first study to sample GBMSM from four distinct regions of the country, which provided for a diverse sample of varied experiences.

Conclusions
Taken together, we found that nearly half of the Nigerian GBMSM in this study had no prior awareness of PrEP, but after being informed about its potential benefits, the majority were willing to use it. Furthermore, PrEP uptake among Nigerian GBMSM remains low. Findings suggest that educational messages are necessary to ensure appropriate PrEP scale-up, especially tailored towards Nigerian GBMSM.