Abstract
Objectives:
The current study aims to assess longitudinal differences in stigma and HIV outcomes among key populations at risk for and living with HIV.
Design:
Key populations enrolled into two parallel prospective cohorts; one for female sex workers and one for sexual and gender minorities (SGMs). Participants were recruited from three urban areas in Senegal; were followed for 24 months; and had the option to participate in an integrated stigma mitigation intervention.
Methods:
Participants included individuals both at risk for and living with HIV. Sociobehavioral questionnaires and biological HIV testing were administered every 3-4 months. Longitudinal analyses used nonparametric Chi-squared test for trends and multivariable logistic regression with generalized estimating equations.
Results:
183 SGM and 192 sex workers were enrolled. Among SGM participants, 39.9% were living with HIV at baseline and incidence over 24 months was 3.21/100 person-years. Among sex workers, 36.6% were living with HIV at baseline and incidence was 1.32/100 person-years. Among SGM, perceived healthcare stigma (P < 0.001), anticipated healthcare stigma (P < 0.001), and perceived friend stigma (P = 0.047) reduced, but differed by HIV status for perceived [adjusted odds ratio (aOR): 3.51; 95% confidence interval (CI): 1.75, 7.06] and anticipated healthcare stigmas (aOR: 2.85; 95% CI: 1.06-7.67). Among sex workers perceived healthcare stigma (P = 0.043) and perceived friend stigma (P = 0.006) reduced. Viral suppression increased among SGM (P = 0.028) and was associated with perceived (aOR: 2.87; 95% CI: 1.39-5.55) and enacted healthcare stigma (aOR: 0.42; 95% CI: 0.18-0.99).
Conclusions:
Overall, there were decreases in stigmas observed but clear differences in stigma patterns by HIV status. These data highlight the need to consider specific strategies to address multiple intersecting stigmas as a means of improving HIV-related prevention and treatment outcomes among key populations with diverse identities.
Keywords: Stigma, HIV, Sex Workers, Sexual and Gender Minorities, Senegal
Introduction
HIV prevention efforts and resources have recently shifted towards universal coverage of HIV treatment as a strategy to ultimately decrease HIV incidence through sustained viral suppression among those living with HIV[1]. 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[2]. 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[3]. Treatment adherence and sustained viral suppression requires consistent access to quality healthcare, 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[2].
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 [22]. Consequentially, the World Health Organization 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[25]. 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[26].
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[27]. 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 men who have sex with men (MSM)[27]. 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[28]. The preliminary results observed a decrease in perceived healthcare stigmas among sexual and gender minorities, and a decrease in perceived and enacted healthcare stigma among female sex workers after 6 months[28]. 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.
Methods
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: 1) the sex worker cohort designated for female sex workers; and 2) the sexual and gender minority 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 sexual and gender minority 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 sexual and gender minority cohort was referred to as the MSM cohort in the previous analyses[28]. In an effort to more accurately represent the heterogeneity of gender identity within this study population, it is now referred to as the sexual and gender minority cohort. Participants in the cohort were administered socio-behavioral 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[28]. 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.
Measures
Demographic characteristics are self-reported and treated as fixed variables. Sexual orientation and gender identity were only collected for the sexual and gender minority cohort. Legal registration status of sex workers was only collected for participants in the sex worker cohort.
Interviewer administered socio-behavioral 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. 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[29, 30]. 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 ½ 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.
Statistical Analyses
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[31]. 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 SGM cohort adjusted for age, education, and gender identity. All models for the female sex worker cohort adjusted for age, education, and sex work registration status.
All analyses were conducted using STATA V.15.1(STATACorp, College Station, TX) statistical package.
Results
Demographic Characteristics
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.
Table 1:
Demographic Characteristics of Longitudinal Cohort Participants
| Characteristics | Sexual and Gender Minorities (183) | Female sex workers (192) | ||
|---|---|---|---|---|
| N | % | n/N | % | |
| City | ||||
| Dakar | 115/183 | 62.8 | 124/192 | 64.6 |
| Mbour | 49/183 | 26.8 | 48/192 | 25.0 |
| Thies | 19/183 | 10.4 | 20/192 | 10.4 |
| Age | ||||
| Mean (IQR) | 23 (21-26) | 38.5 (30-45) | ||
| 18-24 | 109/183 | 59.6 | 22/192 | 11.5 |
| 25-30 | 57/183 | 31.2 | 31/192 | 16.2 |
| 31+ | 17/183 | 9.3 | 319/192 | 72.4 |
| Education | ||||
| No formal education | 25/183 | 13.7 | 70/192 | 36.5 |
| Some/Completed Primary education | 39/183 | 21.3 | 44/192 | 22.9 |
| Some/Completed secondary education | 89/183 | 48.6 | 72/192 | 37.5 |
| Greater than secondary | 30/183 | 16.4 | 6/192 | 3.1 |
| Marital Status | ||||
| Single/Never Married/Divorced | 161/183 | 87.9 | 170/192 | 88.5 |
| Stable Relationship | 10/183 | 5.5 | 3/192 | 1.6 |
| Widow/widower | 12/183 | 6.6 | 19/192 | 9.9 |
| Sexual orientation | ||||
| Gay or homosexual | 105/183 | 57.4 | - | - |
| Bisexual | 71/183 | 38.8 | - | - |
| Heterosexual | 7/183 | 3.8 | - | - |
| Gender | ||||
| Cisgender men | 123/183 | 67.7 | - | - |
| Gender minorities | ||||
| Transgender women | 51/183 | 28.9 | - | - |
| Other gender minority | 8/183 | 4.4 | - | - |
| Sex worker registration status | ||||
| Unregistered | - | - | 133/192 | 69.3 |
| Registered | - | - | 59/192 | 30.7 |
| Employment Status | ||||
| Unemployed | 30/183 | 16.4 | 101/192 | 52.6 |
| Self-employed/employed/student | 153/183 | 83.6 | 91/192 | 47.4 |
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.
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%CI:1.61-6.43) per 100 person-years.
Table 2:
HIV Status at baseline and seroconversion over 24 months
| HIV status at baseline | Seroconversion over 24 months of follow up | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| Negative | Living with HIV | Seroconverted | Incidence | ||||||
| Population | n/N | % | n/N | % | P value | n/N | % | Rate | 95% CI |
| Sexual/Gender Minority Cohort | 111/183 | 60.7 | 73/183 | 39.9 | 0.397 | 8/108 | 7.4 | 3.21 | 1.61-6.43 |
| Cisgender MSM | 76/124 | 61.3 | 47/123 | 38.2 | 4/76 | 5.3 | - | - | |
| Gender minority | 32/59 | 54.2 | 26/58 | 44.8 | 4/32 | 12.5 | - | - | |
| Sex worker cohort | 118/186 | 63.4 | 68/186 | 36.6 | 0.875 | 4/118 | 3.3 | 1.32 | 0.50-3.52 |
| Not registered | 82/130 | 63.1 | 48/130 | 36.9 | 1/82 | 1.2 | - | - | |
| Registered | 36/56 | 64.3 | 20/56 | 35.7 | 3/36 | 8.3 | - | - | |
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 is reported in Supplementary Table 3. Among SGMs 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). SGMs living with HIV had an increased odds of experiencing perceived healthcare stigma (aOR:3.51; 95%CI:1.75,7.06) and anticipated stigma (aOR:2.85; 95%CI:1.06,7.67) over the 6 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.
Table 3:
Stigma among sexual and gender minorities who have sex with men and female sex workers by HIV status over 24 months
| Perceived healthcare stigma | Anticipated healthcare stigma | Enacted healthcare stigma | Perceived family stigma | Perceived friend stigma | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| aOR | 95% CI | aOR | 95% CI | aOR | 95% CI | aOR | 95% CI | aOR | 95% CI | |
| Sexual and gender minority cohort** | ||||||||||
| Longitudinal chi-squared p-value* | P<0.001 | P<0.001 | P=0.878 | P=0.784 | P=0.047 | |||||
| Visit | ||||||||||
| Visit 1 | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref |
| Visit 2 | 0.74 | 0.38-1.43 | - | - | 0.32 | 0.11-0.89 | 0.85 | 0.49-1.43 | 0.77 | 0.33-1.79 |
| Visit 3 | 0.52 | 0.24-1.15 | 0.44 | 0.17-1.14 | 1.00 | 0.50-1.96 | 1.52 | 0.93-2.46 | 1.43 | 0.67-3.08 |
| Visit 4 | 0.12 | 0.03-0.49 | 0.28 | 0.09-0.84 | 0.87 | 0.37-2.06 | 1.28 | 0.76-2.14 | 0.93 | 0.42-2.04 |
| Visit 5 | 0.24 | 0.07-0.85 | 0.13 | 0.03-0.62 | 0.88 | 0.32-2.37 | 1.26 | 0.70-2.26 | 0.98 | 0.41-2.36 |
| Visit 6 | 0.09 | 0.02-0.37 | 0.06 | 0.01-0.41 | 0.61 | 0.28-1.31 | 0.83 | 0.50-1.40 | 0.15 | 0.03-0.67 |
| Living with HIV at baseline | 3.51 | 1.75-7.06 | 2.85 | 1.06-7.67 | 1.01 | 0.52-1.98 | 1.08 | 0.67-1.76 | 1.46 | 0.78-2.74 |
| Gender minority | 1.77 | 0.92-3.43 | 2.21 | 0.84-5.76 | 0.97 | 0.53-1.93 | 1.23 | 0.75-1.67 | 1.24 | 0.87-2.29 |
| Female sex workers*** | ||||||||||
| Longitudinal chi-squared p-value* | P=0.043 | P=0.104 | P=0.395 | P=0.076 | P=0.006 | |||||
| Visits | ||||||||||
| Visit 1 | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref |
| Visit 2 | 1.47 | 0.80-2.70 | 1.27 | 0.66-2.42 | 3.13 | 1.18-8.35 | 0.83 | 0.53-1.28 | 0.38 | 0.19-0.78 |
| Visit 3 | 0.62 | 0.27-1.42 | 0.45 | 0.16-1.30 | 1.27 | 0.41-3.89 | 0.83 | 0.53-1.29 | 0.35 | 0.16-0.43 |
| Visit 4 | 0.54 | 0.22-1.34 | 0.42 | 0.13-1.35 | 2.30 | 0.86-6.15 | 0.80 | 0.48-1.34 | 0.26 | 0.11-0.59 |
| Visit 5 | 0.45 | 0.17-1.18 | 0.18 | 0.04-0.89 | 0.97 | 0.28-3.38 | 0.77 | 0.47-1.27 | 0.34 | 0.15-0.79 |
| Visit 6 | 0.84 | 0.41-1.69 | 0.94 | 0.42-2.12 | 1.30 | 0.42-3.97 | 0.59 | 0.37-0.94 | 0.38 | 0.19-0.78 |
| Living with HIV at baseline | 0.75 | 0.38-1.44 | 0.93 | 0.43-2.00 | 0.62 | 0.29-1.31 | 0.79 | 0.47-1.24 | 1.02 | 0.54-1.91 |
| Registered | 0.93 | 0.56-1.54 | 0.85 | 0.42-1.71 | 0.89 | 0.46-1.65 | 0.99 | 0.63-1.56 | 1.51 | 0.84-2.72 |
crude longitudinal chi squared for trend
SGM model adjusted for age, education level, gender, HIV status at visit 1
sex worker model adjusted for age, education level, registration status, HIV status at visit 1
Antiretroviral therapy and viral suppression over 24 months
Crude numbers and proportions of self-reported ART adherence and viral suppression by study visit is reported in Supplementary Table 3. 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 6 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 to non-registered.
Table 4:
Current treatment and viral suppression among those living with HIV at baseline
| Self-Reported ART treatment | Viral Suppression | |||
|---|---|---|---|---|
| aOR* | 95% CI | aOR* | 95% CI | |
| Sexual and gender minority cohort* | ||||
| Longitudinal chi-squared p-value* | 0.383 | 0.028 | ||
| Visit | ||||
| Visit 1 | Ref | Ref | Ref | Ref |
| Visit 2 | 0.84 | 0.16-4.32 | 6.00 | 2.77-13.01 |
| Visit 3 | 1.66 | 0.24-11.51 | 4.18 | 1.89-9.26 |
| Visit 4 | - | - | 4.69 | 2.03-10.87 |
| Visit 5 | - | - | 3.65 | 1.50-8.90 |
| Visit 6 | 1.01 | 0.18-5.62 | 3.10 | 1.27-7.51 |
| Gender minority | 0.53 | 0.17-1.63 | 0.54 | 0.21-1.40 |
| Female sex worker cohort** | ||||
| Longitudinal chi-squared p-value* | 0.822 | 0.357 | ||
| Visits | ||||
| Visit 1 | Ref | Ref | Ref | Ref |
| Visit 2 | 0.86 | 0.24-3.09 | 1.05 | 0.60-1.85 |
| Visit 3 | - | - | 0.88 | 0.45-1.72 |
| Visit 4 | 4.95 | 0.24-102.54 | 0.96 | 0.42-2.20 |
| Visit 5 | 1.23 | 0.20-7.37 | 1.19 | 0.57-2.48 |
| Visit 6 | 1.25 | 0.23-6.87 | 1.75 | 0.63-4.81 |
| Registered | 0.48 | 0.11-2.09 | 0.33 | 0.14-0.82 |
crude longitudinal chi squared for trend
Sexual/gender minority model adjusted for age, education level, gender
Female sex worker model adjusted for age, education level, registration status
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).
Table 5:
Viral suppression changes associated with stigma exposure
| Viral Suppression | ||
|---|---|---|
| aOR** | 95% CI | |
| Sexual and gender minority cohort* | ||
| Stigma | ||
| Perceived healthcare stigma | 2.78 | 1.39-5.55 |
| Anticipated healthcare stigma | 3.14 | 0.61-16.21 |
| Enacted healthcare stigma | 0.42 | 0.18-0.99 |
| Perceived family stigma | 1.47 | 0.69-3.16 |
| Perceived friend stigma | 1.93 | 0.58-6.44 |
| Gender minority | 0.54 | 0.21-1.40 |
| Female sex worker cohort* | ||
| Stigma | ||
| Perceived healthcare stigma | 0.62 | 0.21-1.82 |
| Anticipated healthcare stigma | 4.02 | 1.25-12.94 |
| Enacted healthcare stigma | 1.20 | 0.44-3.27 |
| Perceived family stigma | 0.84 | 0.34-2.07 |
| Perceived friend stigma | 0.93 | 0.38-2.29 |
| Registered | 0.38 | 0.15-1.01 |
adjusted for visit, education, age
Discussion
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 non-interventional cohorts among key populations in Senegal and viral suppression among sexual and gender minorities 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 sexual and gender minority and sex worker cohorts, highlighting maintained resiliency among cohort participants despite no reduction in enacted stigma in the healthcare setting [28]. The clinical component of the integrated stigma mitigation intervention provided training for healthcare providers on non-stigmatizing 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[32–38]. 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. Sexual and gender minorities living with HIV had an increased odds of reporting anticipated and perceived stigmas over the follow up period when compared to 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[39–41]. Given high levels of intersectional stigmas observed here, stigma reduction interventions should be integrated into HIV programs to address the specific needs of sexual and gender minorities living with HIV and potentially improve uptake of services.
HIV incidence among participants in this cohort was relatively low compared to previous non-interventional longitudinal cohorts in Senegal, suggesting a potential benefit of integrated stigma mitigation interventions in HIV prevention [42]. 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[28]. A recent study estimated that among key populations living with HIV in Senegal, approximately half of female sex workers and one in ten sexual and gender minorities 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 [28]. Despite no change in reported treatment, viral suppression improved among sexual and gender minorities during the study period, suggesting potential improved adherence to treatment.
Viral suppression for sexual and gender minorities 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 sexual and gender minorities in the cohort. Primary resistance mutations were observed among sexual and gender minorities at baseline of this study[43]. 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[44]. Given the role of stigma in limiting retention in ART programs, sexual and gender minorities 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 sexual and gender minorities living with HIV in Senegal.
Viral suppression was positively associated with perceived healthcare stigma among sexual and gender minorities. 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[28]. 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 loss 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.
Conclusions
This 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 in order to effectively improve HIV-related prevention and treatment outcomes among key populations with diverse identities.
Supplementary Material
Acknowledgments
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 United States Agency for International Development (USAID) under Cooperative Agreement No. AID-OAA-A-13-00089. Manuscript 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: SDB, FMD, DD, CN, SM, CTK, NLD, DC. Study design: SDB, FMD, DD, CTK, NLD, DC, NT. Protocol development: BL, GT, KC, CL, SK, NLD, SDB, FMD; Study activities and follow up: GT, KC, BL, SK, CL, SDB, FMD, DD, IB. Conceptual development of the analysis and manuscript: CEL SDB OO; Manuscript development: CEL, SDB, OO. Data Analysis: OO, CEL, SK. Manuscript review and contributions: all authors.
Conflicts of Interest and Source of Funding: The authors have no confiicts of interest to disclose. Funding HIV Prevention 2.0 (HP2): Achieving an AIDS-Free Generation in Senegal is supported by the United States Agency for International Development (USAID) under Cooperative Agreement No. AID-OAA-A-13-00089. National Institutes of Mental Health under grant R01MH110358, Validation of Stigma Metrics for Marginalized Men. Manuscript development was supported by a 2019-2021 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.
References
- 1.Buchbinder SP, Liu AY. CROI 2019: advances in HIV prevention and plans to end the epidemic. Topics in antiviral medicine 2019; 27(1):8–25. [PMC free article] [PubMed] [Google Scholar]
- 2.Baral S, Rao A, Sullivan P, Phaswana-Mafuya N, Diouf D, Millett G, et al. The disconnect between individual-level and population-level HIV prevention benefits of antiretroviral treatment. The lancet HIV 2019; 6(9):e632–e638. [DOI] [PubMed] [Google Scholar]
- 3.UNAIDS. Global AIDS update 2019—communities at the centre.
- 4.Link BG, Phelan JC. Conceptualizing Stigma. Annual Review of Sociology 2001; 27(1):363–385. [Google Scholar]
- 5.Goffman E Stigma: notes on the management of spoiled identity. 1963.
- 6.Bowleg L The problem with the phrase women and minorities: intersectionality-an important theoretical framework for public health. American journal of public health 2012; 102(7):1267–1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Turan JM, Elafros MA, Logie CH, Banik S, Turan B, Crockett KB, et al. Challenges and opportunities in examining and addressing intersectional stigma and health. BMC medicine 2019; 17(1):7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Nyatsanza T, Wood L. Problematizing official narratives of HIV and AIDS education in Scotland and Zimbabwe. SAHARA J : journal of Social Aspects of HIV/AIDS Research Alliance / SAHARA , Human Sciences Research Council 2017; 14(1):185–192. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Perez-Brumer AG, Reisner SL, McLean SA, Silva-Santisteban A, Huerta L, Mayer KH, et al. Leveraging social capital: multilevel stigma, associated HIV vulnerabilities, and social resilience strategies among transgender women in Lima, Peru. Journal of the International AIDS Society 2017; 20(1):21462. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Bwirire LD, Fitzgerald M, Zachariah R, Chikafa V, Massaquoi M, Moens M, et al. Reasons for loss to follow-up among mothers registered in a prevention-of-mother-to-child transmission program in rural Malawi. Transactions of the Royal Society of Tropical Medicine and Hygiene 2008; 102(12):1195–1200. [DOI] [PubMed] [Google Scholar]
- 11.Byakika-Tusiime J, Crane J, Oyugi JH, Ragland K, Kawuma A, Musoke P, et al. Longitudinal antiretroviral adherence in HIV+ Ugandan parents and their children initiating HAART in the MTCT-Plus family treatment model: role of depression in declining adherence over time. AIDS and behavior 2009; 13 Suppl 1:82–91. [DOI] [PubMed] [Google Scholar]
- 12.Crowell TA, Keshinro B, Baral SD, Schwartz SR, Stahlman S, Nowak RG, et al. Stigma, access to healthcare, and HIV risks among men who sell sex to men in Nigeria. Journal of the International AIDS Society 2017; 20(1):21489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Turan JM, Bukusi EA, Onono M, Holzemer WL, Miller S, Cohen CR. HIV/AIDS stigma and refusal of HIV testing among pregnant women in rural Kenya: results from the MAMAS Study. AIDS and behavior 2011; 15(6):1111–1120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Rodriguez-Hart C, Nowak RG, Musci R, German D, Orazulike I, Kayode B, et al. Pathways from sexual stigma to incident HIV and sexually transmitted infections among Nigerian MSM. AIDS (London, England) 2017; 31(17):2415–2420. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Rahangdale L, Banandur P, Sreenivas A, Turan JM, Washington R, Cohen CR. Stigma as experienced by women accessing prevention of parent-to-child transmission of HIV services in Karnataka, India. AIDS care 2010; 22(7):836–842. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Fay H, Baral SD, Trapence G, Motimedi F, Umar E, Iipinge S, et al. Stigma, health care access, and HIV knowledge among men who have sex with men in Malawi, Namibia, and Botswana. AIDS and behavior 2011; 15(6):1088–1097. [DOI] [PubMed] [Google Scholar]
- 17.Hladik W, Barker J, Ssenkusu JM, Opio A, Tappero JW, Hakim A, et al. HIV infection among men who have sex with men in Kampala, Uganda--a respondent driven sampling survey. PloS one 2012; 7(5):e38143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Peitzmeier S, Mason K, Ceesay N, Diouf D, Drame F, Loum J, et al. A cross-sectional evaluation of the prevalence and associations of HIV among female sex workers in the Gambia. International journal of STD & AIDS 2014; 25(4):244–252. [DOI] [PubMed] [Google Scholar]
- 19.Lyons CE, Schwartz SR, Murray SM, Shannon K, Diouf D, Mothopeng T, et al. The role of sex work laws and stigmas in increasing HIV risks among sex workers. Nature communications 2020; 11(1):773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Nyblade L, Reddy A, Mbote D, Kraemer J, Stockton M, Kemunto C, et al. The relationship between health worker stigma and uptake of HIV counseling and testing and utilization of non-HIV health services: the experience of male and female sex workers in Kenya. 2017; 29(11):1364–1372. [DOI] [PubMed] [Google Scholar]
- 21.Peitzmeier SM, Grosso A, Bowes A, Ceesay N, Baral SD. Associations of Stigma With Negative Health Outcomes for People Living With HIV in the Gambia: Implications for Key Populations. Journal of acquired immune deficiency syndromes (1999) 2015; 68 Suppl 2:S146–153. [DOI] [PubMed] [Google Scholar]
- 22.Mann JM. Statement at an informal briefing on AIDS to the 42nd session of the United Nations General Assembly. Journal of the Royal Statistical Society Series A (Statistics in Society) 1988; 151(1):131–136. [Google Scholar]
- 23.Braveman P, Gruskin S. Defining equity in health. J EpidemiolCommunity Health 2003; 57(4):254–258. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.UNAIDS. Action on Social Drivers to End AIDS and Extreme Poverty. In. World Bank Main Complex, Washington, D.C; 2014. [Google Scholar]
- 25.Stangl AL, Lloyd JK, Brady LM, Holland CE, Baral S. A systematic review of interventions to reduce HIV-related stigma and discrimination from 2002 to 2013: how far have we come? Journal of the International AIDS Society 2013; 16(3 Suppl 2):18734. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.UNAIDS, UNAIDS Senegal. 2018.
- 27.UNAIDS. Senegal. 2018.
- 28.Lyons CE, Ketende S, Diouf D, Drame FM, Liestman B, Coly K, et al. Potential Impact of Integrated Stigma Mitigation Interventions in Improving HIV/AIDS Service Delivery and Uptake for Key Populations in Senegal. Journal of acquired immune deficiency syndromes (1999) 2017; 74 Suppl 1:S52–s59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Stahlman S ST, Sullivan PS, Ketende S, Lyons C, Charurat ME, Drame FM, Diouf D, Ezouatchi R, Kouanda S, Anato S, Mothopeng T, Mnisi Z, Baral SD. The Prevalence of Sexual Behavior Stigma Affecting Gay Men and Other Men Who Have Sex with Men Across Sub-Saharan Africa and in the United States. JMIR public health and surveillance 2016; 2(2):e35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Fitzgerald-Husek A, Van Wert MJ, Ewing WF, Grosso AL, Holland CE, Katterl R, et al. Measuring stigma affecting sex workers (SW) and men who have sex with men (MSM): A systematic review. 2017; 12(11):e0188393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Cuzick J A Wilcoxon-type test for trend. Statistics in medicine 1985; 4(1):87–90. [DOI] [PubMed] [Google Scholar]
- 32.Pisal H, Sutar S, Sastry J, Kapadia-Kundu N, Joshi A, Joshi M, et al. Nurses' health education program in India increases HIV knowledge and reduces fear. The Journal of the Association of Nurses in AIDS Care : JANAC 2007; 18(6):32–43. [DOI] [PubMed] [Google Scholar]
- 33.Wu S, Li L, Wu Z, Liang LJ, Cao H, Yan Z, et al. A brief HIV stigma reduction intervention for service providers in China. AIDS patient care and STDs 2008; 22(6):513–520. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Kaponda CP, Jere DL, Chimango JL, Chimwaza AF, Crittenden KS, Kachingwe SI, et al. Impacts of a peer-group intervention on HIV-related knowledge, attitudes, and personal behaviors for urban hospital workers in Malawi. The Journal of the Association of Nurses in AIDS Care : JANAC 2009; 20(3):230–242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Ezedinachi EN, Ross MW, Meremiku M, Essien EJ, Edem CB, Ekure E, et al. The impact of an intervention to change health workers' HIV/AIDS attitudes and knowledge in Nigeria: a controlled trial. Public health 2002; 116(2):106–112. [DOI] [PubMed] [Google Scholar]
- 36.Norr KF, Ferrer L, Cianelli R, Crittenden KS, Irarrazabal L, Cabieses B, et al. Peer group intervention for HIV prevention among health workers in Chile. The Journal of the Association of Nurses in AIDS Care : JANAC 2012; 23(1):73–86. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Uys L, Chirwa M, Kohi T, Greeff M, Naidoo J, Makoae L, et al. Evaluation of a health setting-based stigma intervention in five African countries. AIDS patient care and STDs 2009; 23(12):1059–1066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Khuat TO AK, Pulerwitz J, Ogden J, Nyblade L. Improving hospital-based quality of care in Vietnam by reducing HIV-related stigma and discrimination, a Horizons final report. In. Washington, DC: Population Council; 2008. [Google Scholar]
- 39.Bauer GR. Incorporating intersectionality theory into population health research methodology: Challenges and the potential to advance health equity. Social Science & Medicine 2014; 110:10–17. [DOI] [PubMed] [Google Scholar]
- 40.Larson E, George A, Morgan R, Poteat T. 10 Best resources on… intersectionality with an emphasis on low-and middle-income countries. Health Policy and Planning 2016. [DOI] [PubMed] [Google Scholar]
- 41.Bowleg L The Problem With the Phrase Women and Minorities: Intersectionality—an Important Theoretical Framework for Public Health. American journal of public health 2012; 102(7):1267–1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Drame FM, Crawford EE, Diouf D, Beyrer C, Baral SD. A pilot cohort study to assess the feasibility of HIV prevention science research among men who have sex with men in Dakar, Senegal. Journal of the International AIDS Society 2013; 16 Suppl 3:18753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Leye N Leveraging HIV-1 resistance patterns to guide the implementation of treatment programs for MSM living with HIV in Senegal: HIV Prevention 2.0. In: 9th IAS Conference on HIV Science Paris, France; 2017. [Google Scholar]
- 44.Gupta RK, Jordan MR, Sultan BJ, Hill A, Davis DH, Gregson J, et al. Global trends in antiretroviral resistance in treatment-naive individuals with HIV after rollout of antiretroviral treatment in resource-limited settings: a global collaborative study and meta-regression analysis. Lancet (London, England) 2012; 380(9849):1250–1258. [DOI] [PMC free article] [PubMed] [Google Scholar]
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