Men who have sex with men (MSM) in Rwanda are disproportionately affected by HIV and
recognized by the Ministry of Health (MOH) to be a key population for HIV prevention
(MOH, 2018). Although national estimates of HIV prevalence among MSM do not exist,
studies conducted in Rwanda have reported HIV prevalence two to three times higher
among MSM compared with the general population of men (Murenzi et al., 2020; Ntale
et al., 2019). In Africa, MSM account for 6%–17% of new HIV infections annually (Bigna
& Nansseu, 2019). Among MSM in other East African countries, prevalence of HIV is
even higher, ranging from 14% in Uganda to 30% in Tanzania (Kambutse et al., 2019;
Karuga et al., 2016), underscoring the need for additional HIV prevention options
in East Africa.
Pre-exposure prophylaxis (PrEP), the use of anti-retroviral drugs to prevent HIV infection
in persons without HIV (World Health Organization, 2015), is now considered a first-line
HIV prevention option worldwide. PrEP reduces the risk of HIV infection by up to 99%
in a variety of populations, including MSM (Center for Disease Control and Prevention,
2020). Recent demonstration projects in the United States and Australia have found
no HIV seroconversions among MSM adherent to PrEP (Desai et al., 2017; Zablotska et
al., 2019). However, use of PrEP in sub-Saharan African (SSA) countries is low, mostly
due to limited availability associated with cost, despite the fact that most new HIV
infections globally occurinthisregion(Kambutseetal.,2019).Althoughseveral SSA countries,
including Kenya and South Africa, have begun implementing PrEP, with a focus on key
populations such as MSM, access to PrEP is not yet widely available in much of SSA,
including Rwanda (AVAC, 2020).
Awareness of and willingness to use PrEP seems to vary by diverse demographic characteristics
such as geography, age, and place of residence and is important to understand given
its implications for eventual adoption of PrEP (Strauss et al., 2017). In their study
in the United States, Ransome et al. (2019) identified that involvement with community
groups of gay, bisexual, and other MSM (as opposed to no involvement) was associated
with a higher likelihood of awareness of PrEP among MSM. In Ghana, a qualitative study
among MSM identified a low level of PrEP awareness (Ogunbajo et al., 2020). However,
after receiving information about PrEP, acceptability of PrEP was high and was related
to believing that PrEP was protective against HIV and had minimal side effects in
this study (Ogunbajo et al., 2020). In a study conducted in Kenya with MSM, PrEP awareness,
defined as having heard of PrEP, was 64.3% (Ogunbajo et al., 2019). In this Kenyan
study, regular condom use and membership in MSM organizations were associated with
PrEP awareness. However, willingness to use PrEP was low (44.9%) and family exclusion
was among the variables associated with acceptability of PrEP use (Ogunbajo et al.,
2019).
In Rwanda, national guidelines for HIV prevention have identified MSM as a key population
that could benefit from PrEP (MOH, 2018), although there has not yet been widespread
roll-out. The extent to which Rwandan MSM are aware of PrEP and/or find it acceptable
is unknown. To guide policy and PrEP scale-up and roll-out, further information is
needed. The aim of this study was to explore the awareness of PrEP among a sample
of Rwandan MSM, their willingness to use PrEP, and formulation preferences to inform
current and future implementation efforts.
Methods
Study Design
This was a descriptive cross-sectional survey of PrEP knowledge, and attitudes nested
within a longitudinal cohort study evaluating incidence and prevalence of human papillomavirus
and HIV among Rwandan MSM. This substudy uses survey data from the second study visit,
occurring 6 months after enrollment among participants who had tested negative for
HIV at the baseline visit. The 6-month follow-up visit data collection occurred between
September 2016 and February 2017. This study was approved by the Institutional Boards
of Rwanda National Ethic Committee (No. 910/RNEC/2016, No.100/RNEC/2020), and Albert
Einstein College of Medicine (2014–410, Reference: 066359) Institutional Review Board.
Study Settings
The study took place in Kigali City, the capital of and largest city in Rwanda, which
has an HIV prevalence of 4.4% among men (National Institute of Statistics, 2015).
Although same-sex behaviors are not criminalized in Rwanda (Adedimeji et al., 2019),
MSM, and the broader lesbian, gay, bisexual, transgender, and intersex (LGBTI) communities,
are highly stigmatized and socially isolated, with low access to sexual health information
or culturally sensitive health services (Adedimeji et al., 2019). Kigali has a large
concentration of MSM (Adedimeji et al., 2019), and has many MSM and LGBTI community
organizations that address human rights issues with varying capacities and provide
limited social and health support to these communities.
Study Population
Inclusion criteria for the parent longitudinal study were (a) self-identified men,
(b) had any type of sexual acts with another man in the past 6 months before enrollment
to the study (sexual acts in this context were defined as “any nature of sexual activities
that include manual, oral, insertive/receptive anal sex or oral-anal contact” (Adedimeji
et al., 2019), (c) age 18 years or older, (d) lived and maintained their social activities
in Kigali in the past 6 months before enrollment to the study, (e) not known to be
living with HIV, and (f) signed an informed consent form at enrollment.
The parent cohort had 350 participants, including 300 participants whose HIV status
was unknown. Participants in the parent cohort were recruited from community-based
MSM organizations and via snow-ball sampling. For the snow-ball sampling, a two-part
invitation for manda study information brochure were distributed to first recruited
participants who were then asked to recruit at least one additional study participant
from their sexual networks, community organizations, friends, or acquaintances known
to be MSM. An additional 50 participants known to be living with HIV were recruited
from health centers considered friendly and caring for key populations living with
HIV, including MSM. This recruitment procedure for the cohort has been previously
described and published (Adedimeji et al., 2019; Murenzi et al., 2020). For this study,
we used data from 283 participants who were not living with HIV at baseline and returned
for the second study visit (N = 225).
During the second study visit appointment, participants were required to undergo an
identification check and confirm their documented informed consent and HIV status
at baseline. Once this information was confirmed, participants were then asked to
complete the Audio-Computer Assisted Survey-Interview (ACASI) questions about PrEP.
To ensure confidentiality of the study participants, we scheduled appointments with
at least a 30- to 60-min interval between participants. The survey was administered
in Kinyarwanda, the main language spoken in Rwanda. To overcome literacy barriers,
participants could get help from a research assistant if they had difficulty reading,
or if they had difficulties listening to the the ACASI script or in using the ACASI
software. Participants received 8,000 Rwandan francs (∼USD $10) as an incentive after
completing the study assessment.
Measures
The processes for developing the research instruments followed an iterative process.
First, the instruments were adapted in English from a prior survey of PrEP awareness
among MSM (Gupta et al., 2017) and finalized after thorough review and input from
the research team with expertise in HIV, PrEP, and MSM health research in Rwanda to
ensure face and content validity. Second, the finalized English instrument was then
translated into Kinyarwanda, the language widely spoken in Rwanda, by a native Kinyarwanda
speaker also fluent in English. The third step was the back translation of the Kinyarwanda
instrument to English by a different native Kinyarwanda speaker who was fluent in
English. Next, we compared both the original and the translated versions, and any
discrepancies were resolved by an independent team of English and Kinyarwanda speakers.
Finally, the instrument was piloted with four MSM community members and refined further
to ensure comprehension and clarity, before being programmed into tablet computers
using the ACASI.
PrEP-related questions were preceded by this brief description: “These questions ask
you about PrEP—which stands for pre-exposure prophylaxis (also sometimes called Tenvir,
Truvada, or Tenofovir-Emtricitabine), which is a pill taken once a day that people
without HIV can take to reduce their risk of getting HIV before having any sex. It
involves a healthy person who does not have HIV taking a pill to prevent being infected
with HIV. For people who take the pill every day, studies have shown that it reduced
their risk of getting HIV by 95–99%.” We then assessed two outcomes: (a) Awareness
of PrEP (“Before today, have you ever heard of PrEP [Pre-Exposure Prophylaxis]?”)
and (b) Willingness to use PrEP (“Would you be willing to take anti-HIV medicines
[PrEP] to lower your chances of getting HIV?”), and categorized the responses (Yes,
No, Don’t know, or I prefer not to answer). Finally, we asked about preferred PrEP
formulations (e.g., pill, injection) or dosing strategies (daily or on-demand).
Predictor variables assessed for these outcomes included sociodemographic information
such as age, education level, current living arrangement, and sexual behavior practices,
including sexual behavior disclosure, number of male sex partners in the past 6 months,
number of vaginal or anal sex partners, and insertive/receptive anal sex acts with
a man and condom use in the past 6 months.
Data Analysis
Demographic and sexual behavior characteristics were analyzed as categorical or categorized
variables. Continuous variables were categorized as follows: age (<23, 23–25, 26–28,
or ≥29 years), number of male partners in the past 6 months (none, one, two to four,
or five and above), and number of female vaginal or male anal sex partners in the
past 6 months (none or ≥1). Outcome variables (Awareness of PrEP and Willingness to
Use PrEP) were dichotomized as Yes versus No, Don’t know, or I prefer not to answer.
Percentages were calculated for each variable and then compared for each outcome using
Fisher exact tests, whereas Cochran-Armitage trend tests compared categorized continuous
variables between groups. Logistic regression was used to identify associations between
demographic and sexual behavior characteristics with each of the outcomes, and an
odds ratio (OR) and 95% confidence interval (CI) were used to present these associations.
All analyses were performed with SAS statistical software (9.4; SAS Institute, Cary,
NC). p Values less than .05 were considered statistically significant.
Results
Sociodemographic and Sexual Behavior Characteristics of Study Participants
Among the 225 participants, the mean age was 26.7 years (median age = 26 years; interquartile
range was 23–29 years), of which 67 (30%) were 23 years old or younger. Ninety participants
(41%) lived alone, 80 (37%) reported having had between two and four male sexual partners
in the past 6 months, 111 (51%) reported having insertive anal sex with a man in the
past 6 months, and 80 (36%) reported having receptive anal sex with a man in the past
6 months. Please refer to Table 1.
Pre-Exposure Prophylaxis Awareness
Of the 225 participants, 104 (48%) reported awareness of PrEP (Table 2). The odds
of awareness of PrEP were almost twice as high (OR 1.86, 95% CI [1.05–3.30]) for those
having receptive anal sex with inconsistent condom use compared with those who did
not have receptive anal sex and less likely for those who reported living with other
(e.g., family or friends; OR 0.35, 95% CI [0.16–0.76]) compared with those living
with male or female partners.
Willingness to Take Pre-Exposure Prophylaxis
Of the 225 participants, 181 (83%) reported that they were willing to take PrEP (Table
2). However, the likelihood of being willing to use PrEP was almost half as low among
those who reported insertive anal sex acts and inconsistent condom use than those
who did not have insertive anal sex (OR 0.45, 95% CI [0.21–0.97]).
Preferred Pre-Exposure
Prophylaxis Formulations
Table 3 shows that of the 181 participants who were willing to take PrEP, 39% (n =
70/181) preferred PrEP in the form of a daily pill; 12% (n = 21/181) preferred taking
once-daily PrEP Monday and Friday, and another pill after intercourse; 9% (n = 17/181)
preferred PrEP on demand (2 pills taken 2–24 hr before intercourse followed by 1 pill
24 hr after the first dose, and the last pill 48 hr after the first dose for a total
of 4 doses over 48 hr). To receive PrEP as an injection, 22% (n = 39/181) preferred
an injection every 2–3 months, whereas 16% (n = 29/181) preferred an injection once
a month; 3% of study participants (n = 5/181) did not prefer any of these options.
Discussion
This is the first study of PrEP awareness and acceptability among Rwandan MSM, a marginalized
and key population at high risk for HIV. Within this community-recruited sample, we
found a relatively high awareness of PrEP (48% had heard of PrEP), and a very high
willingness to use this prevention strategy (83% were willing to use PrEP).
The relatively high awareness of PrEP among Rwandan MSM, despite the lack of formal
or planned outreach efforts of any kind for this population, may be due in part to
the manner in which participants in this study were recruited. Participants were identified
through MSM community associations, where they are likely to access or be connected
to sources of information to promote their health and well-being. For example, individuals
who were part of LGBTI associations may be better networked with other MSM, know how
or where to access online health information for MSM, and then also share new information
with other association members (Ogunbajo et al., 2019). A recent qualitative study
nested from the same cohort of this study found that peer-to-peer knowledge or advice
sharing, and online sources were important avenues to access information (Adedimeji
et al., 2019). In the New Orleans metropolitan area (United States), another study
found that participation or membership in gay community groups were associated with
increased PrEP awareness among MSM (Ransome et al., 2019). These findings reinforce
the critical role that community organizations and networks can have in promoting
PrEP uptake among MSM, as well as their role in raising a wareness of other health
issues among MSM.
A study in Kenya reported varying levels of awareness of PrEP and found that condom
use among men who have anal sex with other men was significantly associated with knowledge
of PrEP (Ogunbajo et al., 2019). Similarly, our study found that sometimes using condoms
with anal receptive sex was associated with awareness of PrEP, whereas other studies
elsewhere were inconclusive regarding predictors of awareness (Yi et al., 2017). There
were likely other important characteristics that were not measured, that may be associated
with awareness, such as an individual’s degree of connection to an MSM or LGBTI organization.
It is likely that such membership enhances access to health-related knowledge and
influences behaviors (Ransome et al., 2019). Additionally, other sources for information
about PrEP are likely to become important in Rwanda and may influence uptake among
MSM. The critical role of nurses, who already provide education and counseling at
health centers when individuals present for HIV testing or care, could be instrumental
in helping to promote PrEP awareness and uptake (Nelson et al., 2019). However, for
this to happen, nurses and other health care providers must create LGBTQ-friendly
and safe spaces (National LGBT Health Education Center, n.d.). It will be important
to study such social network factors in the future to better inform PrEP implementation
efforts.
A majority of participants (83%) were willing to use PrEP, similar to other studies
that have assessed willingness to use PrEP among MSM in SSA (Karuga et al., 2016;
Ogunbajo et al., 2019), which suggests potentially high uptake once PrEP is made available
and accessible in SSA. However, studies about PrEP acceptability from other low- and
middle-income countries have shown variability of PrEP acceptability (Lim et al.,
2017; Ogunbajo et al., 2020; Torres et al., 2019). These differences in the acceptability
of PrEP in low- and middle-income settings may reflect differences in the availability
of or access to online PrEP information in various languages, sociocultural differences
(e.g., attitudes toward allopathic drugs), sampling differences, and the manner in
which questions about the acceptability of PrEP were asked or data collected.
Our study found that willingness to use PrEP was negatively associated with insertive
anal sex acts and inconsistent condom use. This finding is consistent with other studies
in which high willingness to use PrEP was negatively associated with belief barriers
(e.g., sexual partners may expect sex without a condom; Torres et al., 2019). As PrEP
is being rolled out in Rwanda and elsewhere, future research should examine the actual
uptake of PrEP, and the factors associated with the use of PrEP in various contexts
to inform the ongoing scale-up and monitoring of any emerging disparities in the uptake
of PrEP, particularly in low- and middle-income countries for which limited data exist.
The most commonly preferred formulation for PrEP was a daily, oral preparation; however,
there was a range of preferences for different dosing strategies and formulations,
which is consistent with another study showing heterogeneity in preferences for PrEP
formations and dosing across diverse settings and populations (Wang et al., 2018).
Preferences for PrEP will be important to consider in implementing programs that include
different dosing strategies for MSM (e.g., daily or on-demand). It will also be important
to design PrEP implementation programs that are able to incorporate new formulations
as they become available.
Study Limitations
This study had some limitations, and findings should be interpreted within this context.
First, our study only included MSM from Kigali City, and the results may not be generalizable
to MSM living in other areas of Rwanda. Next, participants may have been influenced
by the HIV prevention questionnaires from the baseline visit and through involvement
with community and LGBTQ organizations, which provide information about approaches
to HIV prevention. In this study, the description of PrEP provided to participants
did not address the potential side effects of PrEP, which could influence the level
of willingness to take PrEP. However, most other studies of PrEP awareness have also
assessed PrEP acceptability in a similar fashion without mentioning side effects.
Finally, despite piloting and refinement of survey items in Kinyarwanda and the use
of ACASI, the concept of PrEP may still not have been understood by all participants.
Future surveys assessing new concepts could consider inclusion of visual images (e.g.,
an image of a person taking a pill orally) to help ensure comprehension.
Conclusion
In one of the first studies exploring PrEP for HIV prevention among Rwandan MSM, we
found a moderate level of awareness and a high willingness to use it. Because PrEP
is not yet currently widely available to MSM in Rwanda, other evidence-based prevention
programs and interventions must be promoted until funding is available to increase
access to PrEP. Further, research is needed to identify optimal approaches of improving
the sexual health of MSM and preventing HIV acquisition through outreach and linkage
to places where MSM can access respectful, nondiscriminatory care, including nursing
models of care to extend PrEP use once available.