HIV prevention efforts and resources have recently shifted toward universal coverage of HIV treatment as a strategy to ultimately decrease HIV incidence through sustained viral suppression among those living with HIV . Universal ‘treatment as prevention’ is a population-level strategy in which people living with HIV who have undetectable viral loads do not risk onward HIV transmission, known as undetectable = untransmittable (U = U). At the individual-level, the data supporting U = U have been consistently powerful, though ‘treatment as prevention’ at a population level has not shown similar impacts . Achieving sustained viral suppression is dependent on earlier steps in the HIV treatment cascade including HIV diagnosis, initiation of antiretroviral therapy (ART), and sustained treatment adherence. Among people living with HIV globally, only approximately two-thirds are receiving ART, with only half of those people on treatment being supported effectively to achieve viral suppression . Treatment adherence and sustained viral suppression requires consistent access to quality health care, which is a challenge particularly for key populations such as sexual and gender minorities (SGMs) as well as sex workers. Key populations bear a disproportionate burden of HIV, and disproportionately represent those who have limited access to the HIV treatment cascade. Understanding the heterogeneity of risks and barriers to services among populations, especially among key populations, may provide insight into strategies to effectively leverage treatment as prevention at the population level .
Stigma has been identified as a driver of the HIV pandemic, and a barrier to HIV prevention, diagnosis, and sustained treatment, especially among key populations. Stigma is a social process in which an individual or group is labeled based on a characteristic or perceived characteristic which appears to differ from social norms; and then linked to a stereotype or negative association, leading to adverse experiences, and limited opportunities and wellbeing [4,5]. Stigma experienced by individuals is often a reflection of society's limited understanding, tolerance, and acceptance of certain identities, behaviors, or health status – whether actual or perceived. Stigma attribution is often challenging, as identities may be dynamic and overlapping. Intersectional stigma is the potentially compounded effect of stigmas among individuals with multiple identities which may be devalued and stigmatized by some in society [6,7]. Within the context of HIV and key populations, stigmas may be the manifestation of fear of HIV as a health condition, as well as the perception of HIV risk associated with behaviors or identities [7–9].
Stigmas may be perceived, anticipated, and enacted; all of which have been linked to HIV risks among key populations through limiting engagement in HIV prevention, care, and treatment services across settings [10–21]. The elimination of stigma remains one of the three core UNAIDS pillars to achieve zero new HIV infections by 2030 . Consequentially, the WHO and UNAIDS have recommended increasing efforts to reduce stigma affecting key populations as critical to an effective HIV response [23,24]. However, relatively few interventions aiming to reduce stigma among people living with HIV and key populations have been taken to scale or evaluated . A systematic review highlighted that there has been limited study of stigma interventions globally, with only a small proportion in West and Central Africa, and limited evaluation of HIV outcomes among the intended beneficiaries of the stigma mitigation programs .
Senegal is a country in West Africa which has a concentrated HIV epidemic. The estimated prevalence of HIV among all adults of reproductive age is 0.4% with an HIV incidence of 0.10 per 1000 in 2018 . Similar to many European and North American settings, the burden of HIV is concentrated among key populations, with an estimated prevalence of HIV of 6.6% among sex workers and 27.6% among MSM . Senegal recently adopted a policy of universal treatment for HIV; however, achieving sustained viral suppression among those living with HIV may depend on effectively addressing stigmas among key populations to improve uptake and access to quality care.
Our study team led the implementation of the integrated stigma mitigation intervention among a longitudinal cohort of key populations in Senegal between 2015 and 2017 . The preliminary results observed a decrease in perceived healthcare stigmas among SGM, and a decrease in perceived and enacted healthcare stigma among female sex workers after 6 months . However, the results of this previous study did not evaluate differences in reductions by HIV status. Recognizing that understanding the intersectionality of stigmas is vital in informing an effective response to HIV, this study aims to characterize the relationship between stigma and HIV prevention and treatment through an intersectional lens. This current analysis utilizes 24 months of follow-up of the cohort participating in an integrated stigma mitigation intervention to measure HIV incidence among those at risk for HIV and viral suppression among those living with HIV; assess longitudinal differences in healthcare and intersecting stigma outcomes between those living with and at risk for HIV; and assess the relationship between viral suppression and stigma among key populations in Senegal.
Study setting and population
Individuals enrolled into a 24-month longitudinal cohort. The cohort took place in three urban centers in Senegal: Dakar, Mbour, and Thies; from September 2015 to August 2017. Two distinct cohorts were formed: the sex worker cohort designated for female sex workers; and the SGM cohort designated for cisgender MSM and transgender persons who have sex with men. Recruitment for the cohorts occurred through a combination of respondent driven sampling (RDS) and purposive sampling. Individuals who were recruited through RDS were invited to enroll in the cohort and complementary recruitment through community organizations via purposive sampling were leveraged to enroll additional individuals. For the sex worker cohort, individuals were eligible if they reported to be 18 years or older, assigned the female sex at birth, and having been engaged in sex work as a primary source of income during the year prior to enrollment. For the SGM cohort, individuals were eligible if they reported to be 18 years or older, reported to be assigned male sex at birth, and reported anal sex with another man in the year prior to enrollment. The SGM cohort was referred to as the MSM cohort in the previous analyses . In an effort to more accurately represent the heterogeneity of sex identity within this study population, it is now referred to as the SGM cohort. Participants in the cohort were administered sociobehavioral questionnaires and biological HIV testing at baseline and approximately every 4 months.
The implementation and assessment of the integrated stigma mitigation intervention was the primary purpose of the study. The integrated stigma mitigation intervention implemented over the course of the study period has been previously described . Briefly, the intervention components assessed in this analysis includes a community intervention targeting perceived and anticipated stigma, and a clinical intervention targeting enacted stigma in the healthcare setting. Participants in the cohort were provided the opportunity to engage in a community intervention which used a peer-based approach to deliver modules on HIV prevention and transmission; human rights; stigma and discrimination; reproductive health; and living with HIV. The clinical intervention consisted of training health workers to improve the clinical and social competency of the providers in addressing the needs of female sex workers, and SGMs.
The Johns Hopkins School of Public Health Institutional Review Board and the National Research Ethics Committee in Senegal provided approval.
Demographic characteristics are self-reported and treated as fixed variables. Sexual orientation and sex identity were only collected for the SGM cohort. Legal registration status of sex workers was only collected for participants in the sex worker cohort.
Interviewer administered sociobehavioral questionnaires were conducted at each study visit in French or Wolof. Stigma measures are time varying and reported as stigma within the 3-month period before each study visit. Stigma measures are defined in Supplementary Table 1, http://links.lww.com/QAD/B798. Anticipated healthcare stigma was measured as avoided seeking services due to key population status. Perceived healthcare stigma was defined as feeling afraid to seek healthcare services, or feeling mistreated in health centers due to key population status [28,29]. Enacted healthcare stigma was defined as having heard a healthcare provider make discriminatory remarks relating to key population status. Perceived family stigma is defined as feeling excluded from family activities or feeling that family members have made discriminatory remarks or gossiped because of key population status. Perceived friend stigma was defined as having felt rejected by friends because of key population status.
HIV status was determined through biological testing at each study visit. HIV testing was conducted using serial rapid testing in line with Senegalese national guidelines including determine HIV Ag/Ab HIV 1/2 and then and confirmatory testing with Biospot ImmunoComb II for those who tested positive. Plasma viral load was obtained for all participants living with HIV at each study visit. In this study, viral suppression was defined as a viral load less than or equal to 1000 viral RNA copies per milliliter. Seroconversion was measured cumulatively over 24 months among those who tested negative for HIV at visit 1. For those living with HIV, treatment adherence indicators were self-reported and defined as currently on ART.
Demographic characteristics were assessed as crude proportions among individuals enrolled in the longitudinal cohort.
Cohort-specific HIV incidence rates were calculated using discrete time to event survival analysis among participants not living with HIV at baseline. Individual person time was determined based on time to HIV diagnosis or time to censoring due to loss to follow-up.
Differences in reported healthcare stigma, social stigma, ART use, and viral suppression between longitudinal waves were assessed using a nonparametric test for trend across ordered groups . Baseline assessments only included individuals enrolled in the cohort and did not include other participants evaluated only through the RDS study.
Multivariable logistic regression (MLR) models with generalized estimating equations (GEE) were used to estimate the odds of each type of stigma over time by HIV status, aiming to assess differences in stigma by HIV status. MLR models with GEE was used to assess longitudinal difference in self-reported ART adherence and viral suppression over time separately. MLR models with GEE was used to assess the association between viral suppression and stigma. All models for the SGMs cohort adjusted for age, education, and sexual identity. All models for the female sex worker cohort adjusted for age, education, and sexual work registration status.
All analyses were conducted using STATA V.15.1 (STATA Corp, College Station, Texas, USA) statistical package.
Demographic characteristics are described in Table 1. Within the SGM cohort, 115 participated in Dakar, 49 in Mbour, and 19 in Thies. The average age of SGM cohort was 23 years with an interquartile range (IQR) of 21–26 and 13.7% (25/183) had no formal education. Overall, 87.9% (161/183) were single, never married, or divorced, and 5.5% (10/183) were in a stable relationship. The sexual orientation of SGMs included 57.4% (105/183) gay or homosexual, 38.8% (71/183) bisexual, and 3.8% (7/183) heterosexual. Overall, 57.4% (161/183) identified as male, 28.9% (51/183) identified as female, and 4.4% (7/183) identified as other. Overall, 16.4% (30/183) were unemployed.
Among the female sex worker cohort, 124 participated in Dakar, 48 in Mbour, and 20 in Thies. The average age was 38.5 years (IQR: 30–45). Overall, 88.5% (170/192) were single, never married, or divorced, and 1.6% (10/183) were in a stable relationship. Among sex workers, 69.3% (133/192) were not registered as sex workers, and 30.7% (59/191) were registered. Overall, 52.6% (101/192) had no employment other than sex work.
A total of 183 SGMs and 192 female sex workers participated in the longitudinal cohort. Participation by visit is reported in Supplementary Table 2, http://links.lww.com/QAD/B798.
HIV status at baseline and incidence over 24 months
Among SGMs 39.9% (73/183) were living with HIV at baseline including 38.2% (47/123) of cisgender men and 44.8% (26/58) gender minorities (Table 2). Among the SGM cohort 8/108 seroconverted over the 24 months of follow-up with an incidence of 3.21 [95% confidence interval (CI): 1.61–6.43] per 100 person-years.
Among female sex workers 36.6% (68/168) were living with HIV at baseline including 35.7% (20/56) of registered sex workers and 36.9% (48/130) of unregistered sex workers. Among sex workers 4/118 seroconverted over the 24 months of follow-up with an incidence of 1.32 (95% CI: 0.50–3.52) per 100 person-years.
Longitudinal stigma outcomes and intersectional stigmas
Crude numbers and proportions of stigma across study visits are reported in Supplementary Table 3, http://links.lww.com/QAD/B798. Among SGM perceived healthcare stigma (P < 0.001), anticipated healthcare stigma (P < 0.001), and perceived friend stigma (P = 0.047) reduced over follow-up (Table 3). SGM living with HIV had an increased odds of experiencing perceived healthcare stigma [adjusted odds ratio (aOR): 3.51; 95% CI: 1.75, 7.06] and anticipated stigma (aOR: 2.85; 95% CI: 1.06, 7.67) over the six study visits. Among sex workers perceived healthcare stigma (P = 0.043) and perceived friend stigma (P = 0.006) reduced over follow-up and did not differ by HIV status.
Antiretroviral therapy and viral suppression over 24 months
Crude numbers and proportions of self-reported ART adherence and viral suppression by study visit are reported in Supplementary Table 3, http://links.lww.com/QAD/B798. Self-reported as currently taking ART did not change over the follow-up period for SGMs (P = 0.383) or sex workers (P = 0.822) (Table 4). Viral suppression increased over the six visits for the SGM cohort (P = 0.028) and did not differ by gender. Viral suppression did not change over follow-up among sex workers (P = 0.357). Registered sex workers had decreased odds of viral suppression (aOR: 0.33; 95% CI: 0.14, 0.82) compared with nonregistered.
Viral suppression changes associated with stigma exposure
Among SGMs viral suppression was positively associated with perceived healthcare stigma (aOR: 2.87; 95% CI: 1.39, 5.55) and negatively associated with enacted healthcare stigma (aOR: 0.42; 95% CI: 0.18, 0.99) (Table 5). Among female sex workers viral suppression was positively associated with anticipated healthcare stigma (aOR: 4.02; 95% CI: 1.25, 12.94).
The study observed a reduction in anticipated and perceived stigmas; however, limited impact on reducing enacted stigma in healthcare settings. Among observed anticipated and perceived stigmas, stigma reduction varied by HIV status, suggested the impact of intersectional stigmas. Encouragingly, HIV incidence was lower than previous noninterventional cohorts among key populations in Senegal and viral suppression among SGMs living with HIV improved over the period of the intervention. Taken together, these data suggest the utility of integrating stigma mitigation interventions into HIV prevention, treatment, and care programs as a strategy to optimize sustained HIV-related outcomes among key populations.
Perceived stigma in the healthcare setting decreased over 24 months among both the SGM and sex worker cohorts, highlighting maintained resiliency among cohort participants despite no reduction in enacted stigma in the healthcare setting . The clinical component of the integrated stigma mitigation intervention provided training for healthcare providers on nonstigmatizing and adapted service delivery for key populations. However, enacted stigma was measured through participant-reported experiences with any healthcare provider, regardless of the healthcare provider's engagement in the clinical intervention. This suggests that even if some individual clinicians are trained and potentially improve their service delivery, key populations face continued risk of stigma by healthcare providers within the broader healthcare system who have not received adequate training. Other stigma reduction interventions addressing healthcare providers have evaluated changes in knowledge or attitudes among the healthcare workers themselves, but with few measuring changes in stigma among those receiving care [31–37]. These results suggest that training of individual healthcare providers is necessary, but not sufficient in addressing structural level stigmas in the healthcare setting. These data further suggest the importance of considering how stigma interventions are being evaluated to assess actual impact thorough care provision instead of only change in knowledge among providers. Moreover, these data suggest the potential utility of structural stigma mitigation interventions widely implemented across the healthcare system to ensure all healthcare providers receive training on the specific health needs of key populations.
Anticipated and perceived stigmas reduced over the 24 months; however, there were differential burdens of stigmas by HIV status. SGMs living with HIV had an increased odds of reporting anticipated and perceived stigmas over the follow-up period when compared with those who were not living with HIV. Even in the context of stigmas affecting key populations, the higher burden of stigma reported among those living with HIV suggests intersectionality of stigmas, and a potential compounded effect of layered or intersectional stigmas [38–40]. Given high levels of intersectional stigmas observed here, stigma reduction interventions should be integrated into HIV programs to address the specific needs of SGMs living with HIV and potentially improve uptake of services.
HIV incidence among participants in this cohort was relatively low compared with previous noninterventional longitudinal cohorts in Senegal, suggesting a potential benefit of integrated stigma mitigation interventions in HIV prevention . Among participants living with HIV, no statistically significant change was observed in self-reported treatment adherence. However, reported ART adherence among participants in the cohort was higher than previous estimates among key populations in Senegal, with both populations reporting above the UNAIDS goal of 90% on treatment at visit 1 in this study . A recent study estimated that among key populations living with HIV in Senegal, approximately half of female sex workers and one in 10 SGMs were aware of their HIV-positive status, suggesting that treatment adherence at visit 1 is higher in this cohort than among the broader communities of key populations in Senegal . Despite no change in reported treatment, viral suppression improved among SGMs during the study period, suggesting potential improved adherence to treatment.
Viral suppression for SGMs in this study increased over the study period, highlighting improved biological outcomes among cohort participants. However, a large increase between the first and second visits was observed, followed by a slight decrease in proportions with each subsequent visit. A sensitively analysis from visit 2 to visit 6 confirmed this decrease in viral suppression (P = 0.091). This may be due to slowed uptake of services or treatment adherence after the second visit, or a reduced efficacy of the treatment in sustaining viral suppression after the first months of treatment. This trend may also represent the emergence of primary HIV drug resistance among SGMs in the cohort. Primary resistance mutations were observed among SGMs at baseline of this study . Concurrently, the prevalence of primary and secondary drug resistance has increased over time in sub-Saharan Africa with increased use of ART which could ultimately compromise the effectiveness of HIV treatment . Given the role of stigma in limiting retention in ART programs, SGMs may be particularly vulnerable to developing HIV resistance. Alternatively, reductions observed may represent differential loss to follow-up, and the overall high loss of follow-up within the cohort. Moving forward with effective treatment may require evaluating current first-line regimens or considering resistance testing to guide therapeutic choices for SGMs living with HIV in Senegal.
Viral suppression was positively associated with perceived healthcare stigma among SGMs. This may represent the increased interactions with healthcare providers among those who were adherent to ART and suggests the potential resilience in mitigating the impact of the stigma on viral suppression. However, enacted stigma among was negatively associated with viral suppression highlighting the potential harms of enacted stigma on treatment outcomes. These finding suggest that for universal treatment as prevention to effectively eliminate new infections, enacted stigma in the healthcare setting is a key area for improvement to effectively address the HIV epidemic.
There are several limitations that should be considered in this study. Some implementation challenges have been previously described . This study leveraged RDS recruitment with the aim of enrolling a more diverse study population than through nonreferral-based recruitment. However, those who enrolled into the cohort are those who volunteered to participate and may differ from those who did not agree to enroll. Therefore, this study is subject to immigrative selection bias and the cohort is not a representative sample of the RDS population or the target population. Survival analysis assumes random censoring, or those that are lost to follow-up are represented by those who remain in the study. This assumption may not hold if outcomes among those lost to follow-up were different from those who remained in the study. In addition, levels of participation in study visits varied across follow-up. Therefore, individuals missing from study visits may be underrepresented in these results, creating a selection bias. Lastly, the ability to attribute reduction in stigma measures to the intervention alone remains limited, as participants may be influenced by general engagement in the study and observation instead of solely the stigma mitigation intervention.
The current study observed decreases in stigmas and improved HIV outcomes among key populations in Senegal. However, there were differential outcomes between key populations living with HIV and at risk for HIV, suggesting intersectional stigmas and increased barriers among those with multiple stigmatized identities. Given the decreases in certain forms of stigma and not others, understanding the mechanisms by which intersecting stigmas act to increase HIV acquisition and transmission risks may provide additional insights into strategies to optimize stigma mitigation interventions, and treatment as prevention programs among key populations. These data highlight the need to consider specific strategies to address multiple intersecting stigmas to effectively improve HIV-related prevention and treatment outcomes among key populations with diverse identities.
The authors would like to thank the study participants and study partners for making this study possible. Funding HIV Prevention 2.0 (HP2): Achieving an AIDS-Free Generation in Senegal is supported by the US Agency for International Development (USAID) under Cooperative Agreement No. AID-OAA-A-13-00089. Article development was supported by National Institutes of Mental Health under grant R01MH110358, Validation of Stigma Metrics for Marginalized Men; and a 2019–2020 T32 NRSA Predoctoral Training Fellowship in HIV Epidemiology and Prevention Sciences (2T32AI102623-06) within the Johns Hopkins University Center for Public Health and Human Rights.
Study conception: S.B., F.M.D., D.D., C.N., S.M., C.T.-K., N.L.-D., D.C. Study design: S.B., F.M.D., D.D., C.T.-K., N.L.-D., D.C., N.T. Protocol development: B.L., G.T., K.C., C.E.L., S.K., N.L.-D., S.B., F.M.D. Study activities and follow-up: G.T., K.C., B.L., S.K., C.E.L., S.B., F.M.D., D.D., I.B. Conceptual development of the analysis and article: C.E.L., S.B., O.O. Article development: C.E.L., S.B., O.O. Data analysis: O.O., C.E.L., S.K. Article review and contributions: all authors.
Conflicts of interest
There are no conflicts of interest.
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