The effect on HIV transmission and cost-effectiveness of programmes for female sex workers in East, Central, and Southern Africa: a modelling study.

BACKGROUND: HIV prevalence and incidence has declined in East, Central, and Southern Africa (ECSA), but remains high among female sex workers (FSWs). Sex worker programmes have the potential to considerably increase access to HIV testing, prevention, and treatment. We aimed to quantify these improvements by modelling the potential effect of sex worker programmes at two different intensities on HIV incidence and key health outcomes, and assessed the programmes' potential cost-effectiveness in order to help inform HIV policy decisions. METHODS: Using a model previously used to review policy decisions in ECSA, we assumed a low-intensity sex worker programme had run from 2010 until 2023; this resulted in care disadvantages among FSWs being reduced, and also increased testing, condom use, and willingness to take pre-exposure prophylaxis (PrEP). After 2023, three policy options were considered: discontinuation, continuation, and a scale-up of the programme to high-intensity, which would have a broader reach, and higher influences on condom use, antiretroviral therapy (ART) adherence, testing, and PrEP use. Outputs of the key outcomes (the percentage of FSWs who were diagnosed with HIV, on ART, and virally suppressed; the percentage of FSWs with zero condomless partners, and HIV incidence) were compared in 2030. The maximum cost for a sex worker programme to be cost-effective was calculated over a 50-year time period and in the context of 10 million adults. The cost-effectiveness analysis was conducted from a health-care perspective; costs and disability-adjusted life-years were both discounted to present US$ values at 3% per annum. FINDINGS: Compared with continuing a low-intensity sex worker programme until 2030, discontinuation of the programme was calculated to result in a lower percentage of FSWs diagnosed (median 88·75% vs 91·37%; median difference compared to continuation of a low-intensity programme [90% range] 2·03 [-4·49 to 10·98]), a lower percentage of those diagnosed currently taking ART (86·35% vs 88·89%; 2·38 [-3·69 to 13·42]), and a lower percentage of FSWs on ART with viral suppression (87·49% vs 88·96%; 1·17 [-6·81 to 11·53]). Discontinuation of a low-intensity programme also resulted in an increase in HIV incidence among FSWs from 5·06 per 100 person-years (100 p-y; 90% range 0·52 to 22·21) to 4·05 per 100 p-y (0·21 to 21·15). Conversely, comparing a high-intensity sex worker programme until 2030 with discontinuation of the programme resulted in a higher percentage of FSWs diagnosed (median 95·81% vs 88·75; median difference compared to discontinuation [90% range] 6·36 [0·60 to 18·63]), on ART (93·93 vs 86.35%; median difference 7·13 [-0·65 to 26·48]), and with viral suppression (93·21% vs 87·49; median difference 7·13 [-0·65 to 26·48]). A high-intensity programme also resulted in HIV incidence in FSWs declining to 2·23 per 100 p-y (0·00 to 14·44), from 5·06 per 100 p-y (0·52 to 22·21) if the programme was discontinued. In the context of 10 million adults over a 50-year time period and a cost-effectiveness threshold of US$500 per disability-adjusted life-year averted, $34 million per year can be spent for a high-intensity programme to be cost-effective. INTERPRETATION: A sex worker programme, even with low-level interventions, has a positive effect on key outputs for FSWs. A high-intensity programme has a considerably higher effect; HIV incidence among FSW and in the general population can be substantially reduced, and should be considered for implementation by policy makers. FUNDING: Wellcome Trust.

A risk-differentiated, community-led intervention to strengthen uptake and engagement with HIV prevention and care cascades among female sex workers in Zimbabwe (AMETHIST): a cluster randomised trial.

BACKGROUND: Female sex workers remain disproportionately affected by HIV. The aim of this study was to determine the effect of risk-differentiated, peer-led support for female sex workers in Zimbabwe on the risk of HIV acquisition and HIV transmission from sex among female sex workers. METHODS: In this cluster randomised, open-label, controlled study, 22 clinics dedicated to female sex workers co-located in government health facilities throughout Zimbabwe were allocated (1:1, through restricted randomisation) to usual care or AMETHIST intervention. Usual care comprised HIV testing, pre-exposure prophylaxis (PrEP), referral to government antiretroviral therapy (ART) services, contraception, condoms, syndromic management of sexually transmitted infections, health education, legal advice, and peer support. AMETHIST added peer-led microplanning tailored to individuals' risk and participatory self-help groups. All cisgender women (aged >18 years) who had sold sex within the past 30 days and lived or worked within trial cluster areas were eligible. Intervention status was not masked to programme implementers but was masked to survey teams and laboratory staff. After 28 months, a respondent-driven sampling (RDS) survey was done in the female sex worker population around each clinic, which measured the primary outcome, the combined proportion of female sex workers in the surveyed population at risk of transmitting HIV (ie, were HIV positive, not virally suppressed, and not consistently using condoms) or at risk of acquiring HIV (ie, were HIV negative and not consistently using condoms or PrEP). We report prespecified analyses of the disaggregated proportions of female sex workers in the surveyed population at risk of either transmission or acquisition of HIV. Analyses were prespecified, RDS-weighted, and age-adjusted. This trial is registered with the Pan African Clinical Trials Registry, PACTR202007818077777. FINDINGS: The AMETHIST intervention was started on May 15, 2019, and data were collected from June 1, 2019, until Dec 13, 2021. The RDS survey was done from Oct 18 to Dec 13, 2021, with 2137 women included in the usual care group (11 clusters) and 2131 in the AMETHIST intervention group (11 clusters) after excluding survey seeds (n=132) and women with missing key data (n=44). 1973 (46·2%) of the 4268 female sex workers surveyed were living with HIV; of these, 863 (93·5%; RDS-adjusted) of 931 women in the intervention group and 927 (88·8%) of 1042 in the usual care group were virologically suppressed. 287 (22·4%) of 1200 HIV-negative women in the intervention group and 194 (15·7%) of 1096 in the usual care group reported currently taking PrEP, of whom only two (0·4%) of 569 had protective tenofovir diphosphate concentrations in dried blood spots (>700 fmol/dried blood punch). There was no effect of the intervention on the primary endpoint of risk of both HIV transmission and acquisition (intervention group n=1156/2131, RDS-adjusted proportion 55·3%; usual care group n=1104/2137, RDS-adjusted proportion 52·7%; age-adjusted risk difference -0·9%, 95% CI -5·7% to 3·9%, p=0·70). For the secondary outcomes, the proportion of women living with HIV at risk of transmission was low and significantly reduced in the intervention group (n=63/931, RDS-adjusted proportion 5·8%) compared with the usual care group (103/1041, 10·4%), with an age-adjusted risk difference of -5·5% (95% CI -8·2% to -2·9%, p=0·0003). Risk of acquisition among HIV-negative women was similar in the intervention (n=1093/1200, RDS-adjusted proportion 92·1%) and the usual care group (1001/1096, 92·2%), with an age-adjusted risk difference of -0·6% (95% CI -4·6 to 3·4, p=0·74). INTERPRETATION: There was no overall benefit of the intervention on combined risk of transmission or acquisition. Viral load suppression in women living with HIV was high and appeared to be further improved by AMETHIST, suggesting potential for impressive uptake and adherence to ART in vulnerable and mobile populations. Sustaining treatment and reinvigorating prevention remain crucial. FUNDING: The Wellcome Trust and the Bill & Melinda Gates Foundation. TRANSLATIONS: For the Shona and Ndebele translations of the abstract see Supplementary Materials section.

Using a Programme Science approach to substantially reduce the risk of HIV transmission and acquisition in sex transactions among female sex workers in Zimbabwe.

INTRODUCTION: We used a Programme Science platform, to generate evidence to support the implementation of programmes for sex workers in Africa. Female sex workers are estimated to make up 1.6% (1.3%-1.8%) of the population of women aged 15-49 years in Zimbabwe. We highlight how programme science can be used to help distinguish between when, where and with whom programmes need to be implemented and discuss two case studies that exemplify implementing better (Case study 1 (1 June 2019-30 June 2021) Optimizing implementation of a risk differentiated microplanning intervention) and implementing differently (Case study 2 (1 October 2016-30 September 2022) Reorientating implementation of DREAMS for young women selling sex). METHODS: Zimbabwe's nationally scaled programme for sex workers was established in 2009 in partnership with sex workers to provide comprehensive services for sex workers and generate evidence for programme design, implementation and scale up. Since inception, comprehensive data have been collected from all sex workers seeking services. As the scope of service provision has expanded so has the scope of data collection and analysis. At enrolment, sex workers are assigned an alphanumeric unique identifier which links consultations within and across programme sites. We conduct descriptive analyses of the Key Population (KP) programme data to guide programme implementation and redesign, embedding programmatic qualitative enquiry as required. RESULTS: Two case studies describing different approaches to programme optimization are presented. In the first, an optimization exercise was used to strengthen programme implementation ensuring that the KP programme got back on track after SARS-COV-2. In the second, an in-depth review of research and programme data led to a re-orientation of the DREAMS programme to ensure that young women at the highest risk of HIV acquisition were enrolled and had access to DREAMS social support interventions in turn strengthening their uptake of HIV prevention. CONCLUSIONS: Optimizing and sustaining HIV care and treatment programmes requires effective delivery with sufficient scale and intensity for population impact. Our programme science approach guided the scale up of the KP programme in Zimbabwe, providing evidence to support strategy, implementation and ongoing management, and importantly helping us distinguish between when we needed to just implement, implement better or implement differently.

Temporal trends in, and risk factors for, HIV seroconversion among female sex workers accessing Zimbabwe's national sex worker programme, 2009-19: a retrospective cohort analysis of routinely collected HIV testing data.

BACKGROUND: The frequency of new HIV infections among female sex workers in sub-Saharan Africa is poorly understood. We used routinely collected data that enable unique identification of repeat HIV testers to assess temporal trends in seroconversion and identify associated risk factors for female sex workers accessing Sisters with a Voice, Zimbabwe's national sex worker programme. METHODS: We pooled HIV testing data gathered between Sept 15, 2009, and Dec 31, 2019, from 36 Sisters programme sites in Zimbabwe. We included female sex workers aged 16 years or older with an HIV-negative test and at least one subsequent programme test. We calculated HIV seroconversion rates (using the midpoint between the HIV-positive test and the last negative test as the seroconversion date) and estimated rate ratios to compare 2-year periods by using Poisson regression, with robust SEs to account for clustering by site and adjusting for age and testing frequency to assess temporal trends. We did sensitivity analyses to explore assumptions about seroconversion dates and the effects of variation in follow-up time on our conclusions. FINDINGS: Our analysis included data for 6665 female sex workers, 441 (7%) of whom seroconverted. The overall seroconversion rate was 3·8 (95% CI 3·4-4·2) per 100 person-years at risk. Seroconversion rates fell with time since first negative HIV test. After adjustment, there was evidence of a decrease in seroconversion rates from 2009 to 2019 (p=0·0053). In adjusted analyses, being younger than 25 years, and having a sexually transmitted infection diagnosis at a previous visit, were significantly associated with increased seroconversion rates. Our findings were mostly robust to sensitivity analyses, but when 1 month before an HIV-positive test was used as the seroconversion date, seroconversion rates no longer fell with time. INTERPRETATION: We identified high rates of seroconversion shortly after linkage to programme services, which emphasises the need to strengthen HIV prevention programmes from first contact with female sex workers in Zimbabwe. New infections among female sex workers remain challenging to measure, but longitudinal analysis of routine testing data can provide valuable insights into seroconversion rates and associated risk factors. FUNDING: UN Population Fund, Deutsche Gesellschaft für Internationale Zusammenarbeit, the Bill & Melinda Gates Foundation, The Global Fund to Fight AIDS, Tuberculosis and Malaria, US President's Emergency Plan for AIDS Relief, US Agency for International Development, and the Elton John AIDS Foundation.

HIV prevalence, risk behaviour, and treatment and prevention cascade outcomes among cisgender men, transgender women, and transgender men who sell sex in Zimbabwe: a cross-sectional analysis of programme data.

BACKGROUND: There is a paucity of evidence on HIV vulnerabilities and service engagements among people who sell sex in sub-Saharan Africa and identify as cisgender men, transgender women, or transgender men. We aimed to describe sexual risk behaviours, HIV prevalence, and access to HIV services among cisgender men, transgender women, and transgender men who sell sex in Zimbabwe. METHODS: We did a cross-sectional analysis of routine programme data that were collected between July 1, 2018, and June 30, 2020, from cisgender men who sell sex, transgender women who sell sex, and transgender men who sell sex, as part of accessing sexual and reproductive health and HIV services provided through the Sisters with a Voice programme, at 31 sites across Zimbabwe. All people who sell sex reached by the programme had routine data collected, including routine HIV testing, and were referred using a network of peer educators. Sexual risk behaviours, HIV prevalence, and HIV services uptake during the period from July, 2018, to June, 2020, were analysed through descriptive statistics by gender group. FINDINGS: A total of 1003 people who sell sex were included in our analysis: 423 (42·2%) cisgender men, 343 (34·2%) transgender women, and 237 (23·6%) transgender men. Age-standardised HIV prevalence estimates were 26·2% (95% CI 22·0-30·7) among cisgender men, 39·4% (34·1-44·9) among transgender women, and 38·4% (32·1-45·0) among transgender men. Among people living with HIV, 66·0% (95% CI 55·7-75·3) of cisgender men, 74·8% (65·8-82·4) of transgender women, and 70·2% (59·3-79·7) of transgender men knew their HIV status, and 15·5% (8·9-24·2), 15·7% (9·5-23·6), and 11·9% (5·9-20·8) were on antiretroviral therapy, respectively. Self-reported condom use was consistently low across gender groups, ranging from 26% (95% CI 22-32) for anal sex among transgender women to 32% (27-37) for vaginal sex among cisgender men. INTERPRETATION: These unique data show that people who sell sex and identify as cisgender men, transgender women, or transgender men in sub-Saharan Africa have high HIV prevalences and risk of infection, with alarmingly low access to HIV prevention, testing, and treatment services. There is an urgent need for people-centred HIV interventions for these high-risk groups and for more inclusive HIV policies and research to ensure we truly attain universal access for all. FUNDING: Aidsfonds Netherlands.

HIV prevention in individuals engaged in sex work.

PURPOSE OF REVIEW: People who sell sex remain at disproportionate risk of acquiring HIV and should be prioritized for evidence-based HIV prevention programmes delivered at sufficient scale and intensity for effectiveness. Although new biomedical tools are becoming available, many basic lessons learned early in the HIV pandemic remain salient today and need renewed attention. RECENT FINDINGS: New preexposure prophylaxis formulations, distribution systems, and delivery mechanisms are being successfully trialled and implemented, adding to well established prevention tools such as male and female condoms and lubricants. The importance of social support networks and community ownership of programmes has been consistently reaffirmed. Serious challenges remain in optimizing HIV prevention for sex workers, including providing services at the scale and intensity necessary for population level impact, addressing culturally sensitive issues of gender identity and sexual orientation, and protecting adolescents and young people who may sell sex. Pervasive social stigma, often reinforced by criminalization and police harassment, further constrain sex workers' access to available services and prevention tools. SUMMARY: Meaningful community engagement and addressing the multiple social determinants of vulnerability at individual, community, and structural levels remain at the core of preventing HIV among people involved in selling sex.

Interpreting declines in HIV test positivity: an analysis of routine data from Zimbabwe's national sex work programme, 2009-2019.

INTRODUCTION: Early diagnosis of HIV is critical for epidemic control. To achieve this, successful testing programmes are essential and test positivity is often used as a marker of their performance. The aim of this study was to analyse trends and predictors of HIV test positivity over time and explore how an understanding of seroconversion rates could build on our interpretation of this indicator among female sex workers in Zimbabwe. METHODS: We analysed HIV test data from Zimbabwe's nationally scaled sex work programme between 2009 and 2019. We defined test positivity as the proportion of all tests that were HIV positive and measured new diagnoses by estimating seroconversion rates among women with repeat tests, defined as an HIV-positive test after at least one HIV-negative test in the programme. We used logistic regression to analyse test positivity over three time-periods: 2009-2013, 2014-2017 and 2018-2019, adjusting for potential confounding by demographic factors and the mediating effects of time since last HIV test. We calculated the seroconversion rates for the same time-periods. RESULTS: During the 10-year study period, 54,503 tests were recorded in 39,462 women. Between 2009 and 2013, 18% of tests were among women who reported testing in the previous 6 months. By 2018-2019, this had increased to 57%. Between 2018 and 2019, test positivity was 9.6%, compared to 47.9% for 2009-2013 (aOR 6.08 95% CI 5.52-6.70) and 18.8% for 2014-2017 (aOR 2.17 95% CI 2.06-2.28). Adjusting for time since last test reduced effect estimates for 2009-2013 (aOR 4.03 95% CI 3.64-4.45) and 2014-2017 (aOR 1.97 95% CI 1.86-2.09) compared to 2018-2019. Among 7573 women with an initial HIV-negative test in the programme and at least one subsequent test, 464 tested HIV positive at a rate of 3.9 per 100 pyar (95% CI 3.5-4.2). CONCLUSIONS: Test positivity decreased among women testing through the programme over time, while seroconversion rates remained high. These declines were partly driven by changes in individual testing history, reflecting comprehensive coverage of testing services and greater knowledge of HIV status, but not necessarily declining rates of seroconversion. Understanding testing history and monitoring new HIV infections from repeat tests could strengthen the interpretation of test positivity and provide a better understanding of programme performance.

"It went through the roof": an observation study exploring the rise in PrEP uptake among Zimbabwean female sex workers in response to adaptations during Covid-19.

INTRODUCTION: Sisters with a Voice (Sisters), a programme providing community-led differentiated HIV prevention and treatment services, including condoms, HIV testing, pre-exposure prophylaxis (PrEP) and antiretroviral therapy linkage for sex workers, reached over 26,000 female sex workers (FSW) across Zimbabwe in 2020. Zimbabwe's initial Covid "lockdown" in March 2020 and associated movement restrictions interrupted clinical service provision for 6 weeks, particularly in mobile clinics, triggering the adaptation of services for the Covid-19 context and a scale up of differentiated service delivery (DSD) models. PrEP service delivery decentralized with shifts from clinical settings towards community/home-based, peer-led PrEP services to expand and maintain access. We hypothesize that peer-led community-based provision of PrEP services influenced both demand and supply-side determinants of PrEP uptake. We observed the effect of these adaptations on PrEP uptake among FSW accessing services in Sisters in 2020. METHODS: New FSW PrEP initiations throughout 2020 were tracked by analysing routine Sisters programme data and comparing it with national PrEP initiation data for 2020. We mapped PrEP uptake among all negative FSW attending services in Sisters alongside Covid-19 adaptations and shifts in the operating environment throughout 2020: prior to lockdown (January-March 2020), during severe restrictions (April-June 2020), subsequent easing (July-September 2020) and during drug stockouts that followed (October-December 2020). RESULTS AND DISCUSSION: PrEP uptake in 2020 occurred at rates <25% (315 initiations or fewer) per month prior to the emergence of Covid-19. In response to Covid-19 restrictions, DSD models were scaled up in April 2020, including peer demand creation, community-based delivery, multi-month dispensing and the use of virtual platforms for appointment scheduling and post-PrEP initiation support. Beginning May 2020, PrEP uptake increased monthly, peaking at an initiation rate of 51% (n = 1360) in September 2020. Unexpected rise in demand coincided with national commodity shortages between October and December 2020, resulting in restriction of new initiations with sites prioritizing refills. CONCLUSIONS: Despite the impact of Covid-19 on the Sisters Programme and FSW mobility, DSD adaptations led to a large increase in PrEP initiations compared to pre-Covid levels demonstrating that a peer-led, community-based PrEP service delivery model is effective and can be adopted for long-term use.

Potential reduction in female sex workers' risk of contracting HIV during coronavirus disease 2019.

Female sex workers' livelihoods in Zimbabwe have been severely impacted by the coronavirus disease 2019 pandemic due to closure of entertainment venues. Competition over fewer clients has reduced ability to negotiate condom use. At the same time as partner numbers have decreased, frequency of reported condomless sex has not increased, suggesting potential reduction in overall HIV and sexually transmitted infection risk and an opportunity for programmes to reach sex workers with holistic social and economic support and prevention services.

Effect of Prices, Distribution Strategies, and Marketing on Demand for HIV Self-testing in Zimbabwe: A Randomized Clinical Trial.

Importance: HIV self-testing is a promising approach for increasing awareness of HIV status in sub-Saharan Africa, particularly in Zimbabwe, where HIV prevalence is 13%. Evidence is lacking, however, on the optimal pricing policies and delivery strategies for maximizing the effect of HIV self-testing. Objective: To assess demand for HIV self-testing among adults and priority-population subgroups under alternative pricing and distribution strategies. Design, Setting, and Participants: This randomized clinical trial recruited study participants between February 15, 2018, and April 25, 2018, in urban and rural communities in Zimbabwe. A factorial design was used to randomize participants to a combination of self-test price, distribution site, and promotional message. Individuals and their household members had to be at least 16 years old to be eligible for participation. This intention-to-treat population comprised 3996 participants. Interventions: Participants were given a voucher that could be redeemed for an HIV self-test within 1 month at varying prices (US $0-$3) and distribution sites (clinics or pharmacies in urban areas, and retail stores or community health workers in rural areas). Vouchers included randomly assigned promotional messages that emphasized the benefits of HIV testing. Main Outcomes and Measures: Proportion of participants who obtained self-tests in each trial arm, measured by distributor records. Results: Among the 4000 individuals enrolled, 3996 participants were included. In total, the mean (SD) age was 35 (14.7) years, and most participants (2841 [71.1%]) were female. Self-testing demand was highly price sensitive; 260 participants (32.5%) who were offered free self-tests redeemed their vouchers, compared with 55 participants (6.9%) who were offered self-tests for US $0.50 (odds ratio [OR], 0.14; 95% CI, 0.10-0.19), a reduction in demand of more than 25 percentage points. Demand was below 3% in the $1, $2, and $3 groups, which was statistically significantly lower than the demand in the free distribution group: in pooled analyses, demand was considerably lower among participants in higher-than-$0 price groups compared with the free distribution group (2.8% vs 32.5%; OR, 0.05; 95% CI, 0.04-0.07). In urban areas, demand was statistically significantly higher with pharmacy-based distribution compared with clinic-based distribution (6.8% vs 2.9%; adjusted OR, 2.78; 95% CI, 1.74-4.45). Price sensitivity was statistically significantly higher among rural residents, men, and those who had never received testing before. Promotional messages did not influence demand. Conclusions and Relevance: This study found that demand for HIV self-testing in Zimbabwe was highly price sensitive, suggesting that free distribution may be essential for promoting testing among high-priority population groups; additionally, pharmacy-based distribution was preferable to clinic-based distribution in urban areas. Trial Registration: ClinicalTrials.gov identifier: NCT03559959.