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Optimizing the impact of key population programming across the HIV cascade Guest Editors: R. Cameron

Optimizing the impact of key population programming across the HIV cascade

Guest Editors: R. Cameron Wolf, Trista Bingham, Greg Millett, Rose Wilcher Supplement Editor: Marlène Bras

Wolf, Trista Bingham, Greg Millett, Rose Wilcher Supplement Editor: Marlène Bras Volume 21, Supplement 5, July

Volume 21, Supplement 5, July 2018

Wolf, Trista Bingham, Greg Millett, Rose Wilcher Supplement Editor: Marlène Bras Volume 21, Supplement 5, July

Acknowledgements

The Guest Editors – R. Cameron Wolf, Trista Bingham, Greg Millett, and Rose Wilcher – would like to thank all of the authors who submitted expressions of interest and full manuscripts and worked so hard throughout the selection process, which was very rigorous. We wish that many more studies could have been included, but hope that this effort to compile the latest evidence for key populations responses will continue in the future. We also wish to thank the Journal of the International AIDS Society for the support and guidance throughout the process.

Support

This supplement grew out of a collaborative effort between technical advisors at the U.S. President’s Emergency Plan for AIDS Relief (PEPFAR) and the Foundation for AIDS Research (amfAR). It was supported by multiple agencies including the United States Agency for International Development (USAID) and PEPFAR through the Linkages across the Continuum of HIV Services for Key Populations Affected by HIV project (LINKAGES, Cooperative Agreement AID-OAA-A-14-00045); PEPFAR through the Centers for Disease Control and Prevention (CDC); and amfAR. Its contents are solely the responsibility of the authors and do not necessarily represent the official position of the funding agencies.

Optimizing the impact of key population programming across the HIV cascade

Guest Editors: R. Cameron Wolf, Trista Bingham, Greg Millett, Rose Wilcher Supplement Editor: Marlène Bras

Contents

Building the evidence base to optimize the impact of key population programming across the HIV cascade R Cameron Wolf, Trista Bingham, Greg Millett and Rose Wilcher

1

Gaps and opportunities: measuring the key population cascade through surveys and services to guide the HIV response Avi Joseph Hakim, Virginia MacDonald, Wolfgang Hladik, Jinkou Zhao, Janet Burnett, Keith Sabin, Dimitri Prybylski and Jesus Maria Garcia Calleja

7

Estimating the contribution of key populations towards spread of HIV in Dakar, Senegal Christinah Mukandavire, Josephine Walker, Sheree Schwartz, Marie-Claude Boily, Leon Danon, Carrie Lyons, Daouda Diouf, Ben Liestman, Nafissatou Leye Diouf, Fatou Drame, Karleen Coly, Remy Serge Manzi Muhire, Safiatou Thiam, Papa Amadou Niang Diallo, Coumba Toure Kane, Cheikh Ndour, Erik Volz, Sharmistha Mishra, Stefan Baral and Peter Vickerman

13

Think global, act local: the experience of Global Fund and PEPFAR joint cascade assessments to harmonize and strengthen key population HIV programmes in eight countries Tiffany A Lillie, James Baer, Darrin Adams, Jinkou Zhao and R Cameron Wolf

23

Blue-Ribbon Boys: factors associated with PrEP use, ART use and undetectable viral load among gay app users across six regions of the world George Ayala, Glenn-Milo Santos, Sonya Arreola, Alex Garner, Keletso Makofane and Sean Howell

32

Cost and cost-effectiveness analysis of pre-exposure prophylaxis among men who have sex with men in two hospitals of Thailand Chutima Suraratdecha, Robyn M Stuart, Chomnad Manopaiboon, Dylan Green, Cheewanan Lertpiriyasuwat, David P Wilson, Patcharaporn Pavaputanon, Prin Visavakum, Patama Monkongdee, Thana Khawcharoenporn, Phiphatthananon Tharee, Chonticha Kittinunvorakoon and Michael Martin

39

Achieving the first 90 for key populations in sub-Saharan Africa through venue-based outreach: Challenges and opportunities for HIV prevention based on PLACE study findings from Malawi and Angola Michael E Herce, William M Miller, Agatha Bula, Jessie K Edwards, Pedro Sapalalo, Kathryn E Lancaster, Innocent Mofolo, Maria Lúcia M Furtado and Sharon S Weir

47

Social network methods for HIV case-finding among people who inject drugs in Tajikistan Maxim Kan, Danielle B Garfinkel, Olga Samoylova, Robert P Gray and Kristen M Little

57

Uptake of HIV self-testing and linkage to treatment among men who have sex with men (MSM) in Nigeria: A pilot programme using key opinion leaders to reach MSM Waimar Tun, Lung Vu, Osasuyi Dirisu, Adekemi Sekoni, Elizabeth Shoyemi, Jean Njab, Sade Ogunsola and Sylvia Adebajo

65

From conventional to disruptive: upturning the HIV testing status quo among men who have sex with men in Vietnam Kimberly E Green, Bao N Vu, Huong TT Phan, Minh H Tran, Huu V Ngo, Son H Vo, Trang M Ngo, Anh H Doan, Tham T Tran, Trang NN Nguyen, An Bao, Lan TX Hang, Thanh M Le, Tung T Doan, Linh H Dang and Giang TT Ha

74

What would you choose: Online or Offline or Mixed services? Feasibility of online HIV counselling and testing among Thai men who have sex with men and transgender women and factors associated with service uptake Nittaya Phanuphak, Tarandeep Anand, Jureeporn Jantarapakde, Chattiya Nitpolprasert, Kanittha Himmad, Thanthip Sungsing, Deondara Trachunthong, Sangusa Phomthong, Petchfa Phoseeta, Sumitr Tongmuang, Pravit Mingkwanrungruang, Dusita Meekrua, Supachai Sukthongsa, Somporn Hongwiangchan, Nutchanin Upanun, Jiranuwat Barisri, Tippawan Pankam and Praphan Phanuphak

82

Changes in engagement in HIV prevention and care services among female sex workers during intensified community mobilization in three sites in Zimbabwe, 2011 to 2015 Tendayi Ndori-Mharadze, Elizabeth Fearon, Joanna Busza, Jeffrey Dirawo, Sithembile Musemburi, Calum Davey, Xeno Acharya, Sibongile Mtetwa, James R Hargreaves and Frances Cowan

95

Self-testing, communication and information technology to promote HIV diagnosis among young gay and other men who have sex with men (MSM) in Brazil Raquel B De Boni, Nena Lentini, Ana CFS Santelli, Aristides Barbosa Jr., Marly Cruz, Trista Bingham, Vanda Cota, Renato Girade Correa, Valdiléa G Veloso and Beatriz Grinsztejn

106

Can a national government implement a violence prevention and response strategy for key populations in a criminalized setting? A case study from Kenya Parinita Bhattacharjee, Giuliana J Morales, Timothy M Kilonzo, Robyn L Dayton, Reuben T Musundi, Janet M Mbole, Serah J Malaba, Bernard E Ogwang, Shajy K Isac, Stephen Moses and Helgar K Musyoki

109

Measuring intersecting stigma among key populations living with HIV: implementing the people living with HIV Stigma Index 2.0 Barbara A Friedland, Laurel Sprague, Laura Nyblade, Stefan D Baral, Julie Pulerwitz, Ann Gottert, Ugo Amanyeiwe, Alison Cheng, Christoforos Mallouris, Florence Anam, Aasha Jackson and Scott Geibel

115

Author Index

118

Wolf RC et al. Journal of the International AIDS Society 2018, 21 (S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146

(S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146 EDITORIAL
(S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146 EDITORIAL

EDITORIAL

Building the evidence base to optimize the impact of key population programming across the HIV cascade

R Cameron Wolf 1 § , Trista Bingham 2 , Greg Millett 3 and Rose Wilcher 4

§ Corresponding author: R. Cameron Wolf, USAID Office of HIV/AIDS, Washington, DC, USA. Tel: +1 571 451 3058. (cwolf@usaid.gov )

Keywords: key populations; men who have sex with men; sex workers; people who inject drugs; transgender persons; HIV; service delivery; implementation science

Received 18 May 2018; Accepted 24 May 2018

Copyright © 2018 The Authors. Journal of the International AIDS Society published by John Wiley & sons Ltd on behalf of the International AIDS Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

1 | GLOBAL CONTEXT

The most recent global HIV data have brought great optimism that controlling the HIV epidemic could become a reality. These encouraging data show overall declines in both AIDS- related deaths and new HIV infections worldwide [ 1]. Recent data also demonstrate impressive gains toward the global 90- 90-90 targets. As of 2016, an estimated 70% of all people liv- ing with HIV (PLHIV) globally knew their HIV status. Among those who had been diagnosed, 77% were accessing antiretro- viral therapy, and 82% of people on treatment had achieved viral suppression [1 ]. Despite this progress, the optimism is tempered by concern that reducing HIV incidence rates must be further accelerated to guarantee epidemic control [2 ]. Moreover, the recent gains have not been uniform. While global data indicate important achievements in addressing the epidemic among key popula- tions defined by the World Health Organization (WHO) as men who have sex with men (MSM), sex workers, transgender people, people who inject drugs (PWID), and prisoners [3 ] these gains still lag far behind those made in the general pop- ulation. UNAIDS estimates that 44% of all new HIV infections among adults worldwide occur among key populations and their partners [1 ]. In generalized epidemic contexts of sub- Saharan Africa, key populations and their sexual partners account for 25% of new HIV infections, while in concentrated epidemic settings, they account for as much as 80% of infec- tions [1]. Globally, sex workers, MSM and PWID are 10, 24 and 24 times more likely, respectively, to acquire HIV com- pared with the general population ages 15 years and older [4 ]. Transgender women are 49 times more likely to be living with HIV and prisoners are five times more likely to be living with HIV compared to other adults [4,5 ].

2 | GROWTH IN SUPPORTING HIV

PROGRAMMES FOR KEY POPULATIONS

Evidence of the disproportionate epidemiological burden that members of key populations shoulder has been met with important policy developments and funding commitments. In 2014, the Global Fund to Fight AIDS, Tuberculosis and Malaria launched the Key Populations Action Plan, reflecting its commitment to help meet their HIV prevention, care and treatment needs and rights [6 ]. That same year, WHO released consolidated guidelines on HIV prevention, diagnosis, treatment and care for key populations [3 ]. These guidelines were updated in 2016 to reflect the urgent call to treat all individuals regardless of CD4 count and to provide pre-expo- sure prophylaxis (PrEP) to those at substantial risk [7]. Addi- tional global implementation guidance and programmatic tools soon followed to support key population programme design and scale up [8-12 ]. The Presidents Emergency Plan for AIDS Relief (PEPFAR) has also launched specific initiatives to expand key popula- tionsaccess to and retention in HIV services. Through pro- grammes such as the Key Populations Challenge Fund, the Key Populations Implementation Science Initiative and the Local Capacity Initiative, PEPFAR supported work to under- stand and better serve key populations, as well as to strengthen capacity of key population-led organizations to address the epidemic in their communities [13 ]. Moreover, PEPFAR recognizes that ensuring key populations have access to and increase their use of comprehensive packages of health and social services is essential for achieving epidemic control [14 ]. Finally, the UNAIDS HIV Prevention 2020 Roadmap deems combination prevention programmes for key populations nec- essary to accelerate declines in new HIV infections at country

Wolf RC et al. Journal of the International AIDS Society 2018, 21 (S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146

level. The Roadmap calls for combination prevention pro- grammes that are evidence-informed, community-owned, and human rights-based; implemented at scale; and tailored to the specific needs of key populations [15 ].

3 | KEY POPULATIONS, DATA

CHALLENGES AND THE HIV CASCADE

These commitments are critical to advancing a more effective response. However, progress translating commitments into improved outcomes for key populations has been hindered by persistent barriers, such as stigma (including self-stigma), dis- crimination, and punitive legal and policy environments. In addition, the field faces ever-present data challenges with key populations, who often do not self-disclose their current or former status as key population members. Consequently, they may be included as members of the general populationand their contribution to HIV transmission underreported and unrecognized. Alternatively, they may be connected to key population community services in one place but receive test- ing or treatment services anonymously in another, making it difficult for programmes to track and support clients across multiple service points. The limited population-based data that are available show that testing and treatment coverage among key populations remains disproportionately low with no key population group close to achieving 90-90-90 targets [1,16 ]. This has led to calls for improving outcomes for key populations through data-driven interventions. Indeed, this supplement grew out of the urgent need to share the emerging evidence from both new and evolving service delivery interventions for key populations. The HIV prevention, care and treatment cascade has been globally adopted as a useful framework for guiding key popula- tion programming (Figure 1 ) [8 ]. It can indicate where pro- grammatic efforts are falling short in reaching and retaining key populations across the continuum of care, and thereby

pinpoint areas for intensified work. Moreover, this cascade model highlights the importance of engaging and building capacity of communities to lead efforts to reach, test, treat, and retain key populations in services, as well as the need to tackle structural barriers including stigma, discrimination, violence, gender-based bias and, in many cases, criminalization. Cutting across the cascade is the need to ensure program- matic efforts are rights based and that confidentiality, safety and security are respected. Achieving epidemic control will not be possible without more robust and rapid progress in delivering evidence-based interventions that improve key populations access to and uptake of HIV services across the cascade. Fundamental to that progress is the generation and use of key population- specific cascade data. The recently relaunched Key Popula- tions Atlas from UNAIDS represents an important step in that direction [17 ]. This tool brings together country-specific data on a variety of indicators disaggregated by key popula- tion group. We need to complement this with better data from a variety of methodological approaches that identify strategies effective at reaching and engaging key populations at different points along the HIV cascade, and allow targeted investments in programming at those points where they are most needed.

4 | TOWARDS A MORE EFFECTIVE

RESPONSE FOR KEY POPULATIONS

Recognition of these needs has led to advances in monitoring key populations uptake of services across the cascade to identify leaksin the system, as well as more sophisticated analysis and use of data to identify solutions and strengthen programming [18,19 ]. In addition, a number of key popula- tion-focused implementation science studies are underway across a range of geographies to evaluate the effectiveness of new approaches, outreach strategies and delivery modali- ties in overcoming structural obstacles and improving service

in overcoming structural obstacles and improving service Figure 1. Cascade of HIV prevention, care, and treatment

Figure 1. Cascade of HIV prevention, care, and treatment services for key populations

Wolf RC et al. Journal of the International AIDS Society 2018, 21 (S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146

uptake and retention with different key population groups [20 ]. As programming is scaled up globally, it is critical that we maximize public health impact by sharing the latest evidence of what works to engage key populations in targeted preven- tion, treatment, and retention programmes. The contents of this supplement represent high-quality articles from a range of multidisciplinary efforts to advance key population science and practice across the cascade. They offer new evidence and data-driven strategies for improving programming with MSM, sex workers, transgender people and PWID across diverse geographies. The supplement does not contain articles addressing prisoners as they require significantly different approaches from key populations in communities outside incarcerated settings.

5 | DATA APPROACHES TO IMPROVE CASCADE MONITORING

Five of the papers in this supplement describe methods and analyses specific to key populations that can be used to refine and focus interventions. The data generated from these approaches are important to guide strategic planning, resource allocation and programme quality improvement initiatives. The supplement opens with a commentary by Hakim et al . in which the authors make the case for why we need better key population cascade data and how we can get it [21 ]. They argue that targeted bio-behavioural surveys represent an important source of data to guide the epidemic response but have been underutilised to monitor and inform key population service delivery efforts. While there may be sampling concerns and other limitations to these types of surveys, the authors underscore that bio-behavioural survey data are critical to tri- angulate with available programme data for a comprehensive assessment of the reach and impact of services for key popu- lations. An article by Mukandavire et al . presents a new methodol- ogy to estimate the contribution of onward HIV transmission among key populations to the overall HIV dynamic in Dakar, Senegal [22 ]. They report that the contribution of commercial sex to HIV transmission is diminishing; however, unprotected sex between men contributed to 42% of transmissions between 1995 and 2005, and increases to an estimated 64% in the 2015 to 2025 period. The authors posit that this dynamic may also be observed in other low- and middle- income countries where the contribution of MSM to overall HIV transmission may be under-appreciated. To better refine key population programming at country level, Lillie et al . describe a partnership between PEPFAR and The Global Fund to conduct key populations cascade assess- ments [23 ]. By jointly participating in these assessments, major funders and national stakeholders are able to better align pack- ages of services, training, geographic coverage, innovations, data collection and quality improvement efforts. These cascade assessments were completed in eight countries: Malawi, Cameroon, Swaziland, Haiti, Angola, Nepal, Cote d Ivoire and Botswana. For this commentary, the authors review common challenges and recommendations made at the programme, national and donor level at each step in the cascade.

Using data collected from an online survey implemented through the gay social networking application, Hornet, Ayala et al . describe determinants of HIV service uptake among a global sample of MSM [24 ]. Of the 10,774 HIV-negative respondents, 13% reported PrEP use. Among HIV-positive respondents (n = 1243), both ART use and undetectable viral load (UVL) were associated with older age, a recent sexually transmitted infection (STI) test or STI treatment; and aware- ness of unlikely HIV transmission with UVL. The findings underscore the importance of STI testing and treatment as well as information about HIV transmissibility (U = U) for encouraging PrEP and ART use. This study is noteworthy for its innovative use of a gay dating app to rapidly generate data from a large online community of MSM that can be used for advocacy and tailored programme decision-making. Finally, Suraratcheda et al . contribute the first estimates on the costs and cost-effectiveness of providing oral PrEP for MSM in Thailand [25 ]. Costing studies related to key popula- tion programming are extremely limited yet costing data are critical for effective programme planning. This paper makes an important first contribution for the Asia-Pacific region by esti- mating the annual costs (US$223 to US$331 per MSM per year, including demand creation activities) and cost-effective- ness of PrEP under several delivery scenarios. While providing PrEP to all MSM over the next five years would have greater epidemiological and economic benefit to Thailand, the authors conclude that providing PrEP to high-risk MSM would be the most cost-effective approach.

6 | IMPROVING RECRUITMENT,

TESTING UPTAKE AND CASE FINDING

The supplement features two articles that broaden our under- standing of strategies for improving the reach of prevention services and uptake of HIV testing among previously unreached key population members. Herce et al . report data from two bio- behavioural surveys in Malawi and Angola that illustrate the value of providing venue-based outreach and testing services in hotspots,where people including MSM, FSWs and transgen- der people meet and seek sex partners [26 ]. Over 70% of the individuals diagnosed with HIV through the venue-based approach were not previously aware of their status, indicating that this was effective at increasing testing uptake and case finding among these populations. A study by Kan et al . from Tajikistan compares the effective- ness of three network-based approaches to recruitment and case finding among PWID [27 ]. The approaches include two respondent-driven sampling (RDS) strategies one restricted and the other unrestricted and an active case-finding (ACF) strategy that involves direct outreach by peers who are living with HIV or current/former PWID. Collectively, these approaches identified 190 new cases of HIV in an eight-month period, linked 80% of them to confirmatory testing, and initiated 87.5% of the confirmed positives on treatment. While RDS strategies were more effective than ACF in detecting new HIV cases, the ACF approach attracted a higher proportion of first- time testers. This finding led the authors to note that both strate- gies are likely needed to achieve their case-finding goals among PWID in this setting.

Wolf RC et al. Journal of the International AIDS Society 2018, 21 (S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146

7 | INNOVATIONS IN HIV TESTING MODALITIES AND LINKAGE TO

TREATMENT

Recognizing that innovations in HIV testing options are needed to improve coverage, three articles in the supplement examine feasibility, acceptability, and effectiveness of new HIV testing

modalities. Tun et al . present the results of a pilot intervention to distribute oral HIV self-testing kits to MSM through key opinion leaders in Lagos, Nigeria [ 28 ]. This study found that not only is oral self-testing feasible and highly acceptable among MSM in this urban population, but also that effective linkage to treatment can be achieved for those who test positive through self-testing with active follow-up and access to a trusted MSM-friendly com- munity clinic that offers HIV treatment.

In a study from Vietnam, Green et al . explore HIV testing

interventions through MSM lay providers and HIV self-testing, promoted through online channels and face-to-face interac- tions [29 ]. The study found that more than half of the MSM who sought lay- or self-testing were first-time testers. These new testing strategies resulted in higher detection of new HIV cases (6.8%) compared to conventional facility-based test- ing (estimated at 1.6%), while those linked to testing from social media interventions presented with even higher HIV-

positive people (11.6%). Moreover, 90% of those identified as positive were successfully registered for ART.

A study from Thailand also demonstrates the promise of

leveraging technology and self-testing to improve reach and testing uptake among MSM and transgender women [30 ]. In this study, Phanuphak et al . explore preferences among three different modalities of HIV testing including: (1) offline HIV counselling and testing; (2) online pre-test counselling and off- line HIV testing; and (3) online counselling and online, super- vised, HIV self-testing. The study demonstrated that online

counselling coupled with online, supervised, HIV self-testing is feasible and acceptable. In addition, the online strategy pro- duced the highest proportion of first time testers (47.3%) and had the highest HIV prevalence (15.9%). Being a transgender woman and spending more than four hours per day on social media increased a participants likelihood to self-select for online counselling and HIV testing.

8 | TAKING COMMUNITY-LED PROGRAMMING ACROSS THE

CONTINUUM TO SCALE

Two papers in the supplement report outcomes from large- scale, key population-led efforts to improve outcomes across the cascade. Ndori-Mharadze et al . report results from an evaluation of Sisters with a Voice, Zimbabwes nationally scaled comprehensive programme for FSWs, following intensi- fied community mobilization activities [ 31 ]. The findings demonstrate that early peer mobilization efforts to familiarize community members with tailored HIV services were associ- ated with improved outcomes, notably increases in HIV test- ing frequency, knowledge of HIV status and increased linkage to ART. Results of an innovative HIV self-testing component within a broader, community-wide implementation science project in

Curitiba, Brazil demonstrated feasibility and improved HIV diagnosis among young MSM who had not previously tested for HIV [32 ]. Based on their findings, De Boni et al . report on the expansion and tailoring of the Internet-based self-testing platform to increase HIV testing coverage among MSM in S~ao Paulo, Brazil s largest metropolitan area with the highest num- ber of new HIV infections.

9 | ADDRESSING STRUCTURAL BARRIERS

Due to the criminalized and stigmatized nature of key popula- tions globally, sex workers, MSM, PWID and transgender peo- ple are often afraid to visit healthcare services and, when they do go, are reluctant to disclose their sexual histories for fear of rejection, derision or other negative reactions from provi- ders [33,34 ]. In addition, the perpetration of violence against key populations is frequent and often severe. Experiences of violence not only increase the risk of key populations acquir- ing HIV but also deeply affect their desire and ability to get tested for HIV and adhere to HIV treatment [35,36 ]. Two papers in this supplement address structural barriers to better HIV-related outcomes. Bhattacharjee et al . describe successful efforts to integrate violence prevention and response services into the national key population programme in Kenya [37 ]. Drawing on programme data over a four-year period, this paper contributes important evidence that it is possible to address violence against key populations under the leadership of the national government, even in an environ- ment where sex work, same-sex sexual practices and drug use are criminalized [ 38 ]. A commentary by Friedland et al . reflects on the evolution of the PLHIV Stigma Index, which at the end of 2017 had interviewed more than 100,000 PLHIV in 90 countries [39 ]. The paper describes efforts at updating the new PLHIV Stigma Index 2.0 to better capture HIV-related and key popu- lation-related stigma, within the context of modern global test- ing and treatment guidelines. The updated tool was pilot- tested through a community-led process in Cameroon, Sene- gal and Uganda, and provides essential evidence and opportu- nities for communities in other countries to more effectively document stigma and advocate for and implement stigma miti- gation interventions as part of human rights-affirming HIV responses.

10 | MOVING AHEAD

These papers provide much-needed contributions to the evi- dence base for key population programming across the HIV prevention, care and treatment cascade. Our hope is that this supplement will compel funders, policymakers, implementers and other stakeholders to do more now to champion data- driven programming. One common theme that emerges from this supplement is that we should establish and scale-up inno- vative, community-led services, while expanding the integra- tion and options for key populations within the health system. In addition, we will not make sustainable improvements in outcomes if we do not better address the stigma,

Wolf RC et al. Journal of the International AIDS Society 2018, 21 (S5):e25146 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25146/full | https://doi.org/10.1002/jia2.25146

discrimination and violence that key populations experience at the hands of family, community members, health care pro- viders and the state. As more evidence on key population programmes emerges, it is critical that the international community catalyse these advances with supportive policies that promote widespread uptake of effective approaches. Important studies are ongoing through the PEPFAR Key Populations Implementation Science and amfAR Implementation Science Grants initiatives, from which we anticipate more rich data designed to fill further gaps in our understanding of how to implement better ser- vices for key populations. After more than three decades in the fight against HIV, plans to end the HIV epidemic through goals such as UNAIDS 90-90-90 have been adopted by governments, major donors, and stakeholders globally. Investments to address the epi- demic among key populations should be central to these efforts. With ever-present threats of stigma, discrimination, violence, and other human rights abuses, the gains that have been made among key populations are precarious. The urgency of continuing to maintain focus on these groups can- not be understated. To leave no one behind, the substantial progress that has been made to date against the epidemic will need to be bolstered with rigorous, key population-specific data collection and use, with partnerships focused on vigi- lance, courage, tolerance and commitment.

AUTHORS AFFILIATIONS

1 U.S. Agency for International Development, Office of HIV/AIDS, Washington, DC, USA; 2 U.S. Centers for Disease Control and Prevention, Atlanta, GA, USA; 3 AmfAR, The Foundation for AIDS Research, New York, NY, USA; 4 FHI 360, LINKAGES Project, Durham, NC, USA

COMPETING INTERESTS

The authors have no other funding or conflicts of interest to disclose.

AUTHORS CONTRIBUTIONS

RCW, TB, GM and RW all contributed to the preparation of the first draft. All authors approved the final manuscript.

ACKNOWLEDGEMENTS

The authors acknowledge important ongoing efforts underway through the PEPFAR Key Populations Implementation Science and amfAR Implementation Science Grants initiatives. The authors also thank Billy Pick (USAID) for his input on this editorial.

FUNDING

This manuscript was supported by multiple agencies including the United States Agency for International Development (USAID) and the U.S. President s Emer- gency Plan for AIDS Relief (PEPFAR) through the Linkages across the Contin- uum of HIV Services for Key Populations Affected by HIV project (LINKAGES, Cooperative Agreement AID-OAA-A-14-00,045); PEPFAR through the Centers for Disease Control and Prevention (CDC); and amfAR, the Foundation for AIDS Research. The content is solely the responsibility of the authors and does not necessarily represent the official views of any of the funding agencies.

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Hakim AJ et al. Journal of the International AIDS Society 2018, 21 (S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119

(S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119 COMMENTARY
(S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119 COMMENTARY

COMMENTARY

Gaps and opportunities: measuring the key population cascade through surveys and services to guide the HIV response

Avi Joseph Hakim 1 § , Virginia MacDonald 2 , Wolfgang Hladik 1 , Jinkou Zhao 3 , Janet Burnett 4 , Keith Sabin 5 , Dimitri Prybylski 1 and Jesus Maria Garcia Calleja 2

§ Corresponding author: Avi Hakim, Clifton Rd, NE, Atlanta, GA 30303, USA. Tel: +1 404 639 8858. ( Hxv8@cdc.gov )

Abstract

Introduction: The UNAIDS 90-90-90 targets to diagnose 90% of people living with HIV, put 90% of them on treatment, and for 90% of them to have suppressed viral load have focused the international HIV response on the goal of eliminating HIV by 2030. They are also a constructive tool for measuring progress toward reaching this goal but their utility is dependent upon data availability. Though more than 25% of new infections are among key populations (KP)- sex workers, men who have sex with men, transgender people, people who inject drugs, and prisoners- and their sex partners, there is a dearth of treatment cascade data for KP. We assess the availability of cascade data and review the opportunities offered by biobehavioral and pro- gramme data to inform the HIV response. Discussion: The emphasis on the collection of treatment cascade data among the general population in higher prevalence countries has not led to a similar increase in the availability of cascade data for KP. The limited data available for KP highlight large gaps in service uptake across the cascade, particularly in the first 90, awareness of HIV status. Biobehavioral surveys (BBS), with linked population size estimation, provide population-based data on the treatment cascade and should be con- ducted every two to three years in locations with services for KP. With the inclusion of viral load testing, these surveys are able to monitor the entire treatment cascade among KP regardless of whether these populations access HIV services targeting the general population or KP. BBS also reach people accessing services and those who do not, thereby providing a unique opportunity to learn about barriers to service uptake including stigma and discrimination. At the same time high-quality pro- gramme data can play a complementary role in identifying missed opportunities that can be addressed in real-time. Conclusions: Data are more important than ever for guiding the HIV response toward reaching 90-90-90 targets and elimi- nating HIV, particularly in the face of decreased funding for HIV and specifically for KP. Timely high-quality BBS data can be triangulated with high-quality programme data to provide a comprehensive picture of the epidemic response for KP.

Keywords: Key populations; 90-90-90 cascade; surveillance; surveys; programme monitoring

Received 15 December 2017; Accepted 12 May 2018 Copyright © 2018 World Health Organization; licensee IAS. This is an open access article distributed under the terms of the Creative Commons Attribution IGO License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In any reprodu ction of this article, there should not be any suggestion that WHO or this article endorse any specific organization or products. The use of the WHO logo is not permitted.

1 | INTRODUCTION

UNAIDS 90-90-90 targets provide a valuable framework to guide the HIV response and monitor progress towards ending the epidemic [ 1]. These targets of having 90% of people living with HIV (PLHIV) aware of their infection, with 90% of them on antiretroviral therapy (ART), and 90% of them with sup- pressed viral load were conceived so that they could be informed through programme or survey data [ 2]. Though pro- gramme data exist about the number of HIV tests conducted and the number of people on ART, estimates of ART coverage are largely based on models such as Spectrum, and until recently, little has been known about population viral suppres- sion [3]. However, the international embrace of the 90-90-90 targets has spurred surveys to collect data towards these indicators [ 4,5]. It has also led to a recognition that the key populations treatment cascade should be expanded to include

outreach prevention and testing services as this is where many key population members first engage with the health system [6,7 ]. In order to elucidate progress toward UNAIDS targets, the US President s Emergency Plan for AIDS Relief (PEPFAR) is assessing national and sub-national 90-90-90 cascades among the general population in more than one dozen high HIV prevalence countries through the Population-based HIV Impact Assessment (PHIA) [8 ]. These surveys are seen as the best available method for nationally representative estimates of progress toward 90-90-90 targets. Results from Zimbabwe, Malawi and Zambia have highlighted the need to focus efforts on diagnosing infections because once diagnosed, countries are making good progress at linking and retaining people on antiretroviral treatment and suppressing viral load [9,10 ]. Data from Swaziland have confirmed the potential of combination prevention efforts and increasing treatment coverage in

Hakim AJ et al. Journal of the International AIDS Society 2018, 21 (S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119

reducing HIV incidence [11,12 ]. However, while population- based national and sub-national 90-90-90 cascade data are quickly becoming available for the general population in higher prevalence countries, no population-based surveys provide cascade data for key populations sex workers (SW), men who have sex with men (MSM), transgender people (TP), and people who inject drugs (PWID). The lack of survey-derived cascade data for key populations is striking missed opportu- nity given that a larger number of biobehavioral surveys (BBS) have been conducted among key populations than among the general population [ 13-18 ]. In the absence of BBS data, key population programme data are often insufficient to fill data gaps about the cascade. These data are limited by the challenges of tracking individuals from community-based interventions to health facilities, and from facility to facility, particularly if that facility does not utilize key population unique client codes [ 19,20 ]. In some settings, people may not feel comfortable reporting their sexual or drug injecting practices or identities and in others it may not be safe to collect such data due to stigma and discrimination. This lack of data impedes the effective targeting of services by population, location, and intervention need, and measuring of progress toward epidemic control. We conducted a litera- ture search in PubMed and reviewed reports for PEPFAR and Global Fund-supported surveys to identify surveys reporting at least two elements of the 90-90-90 cascade. We compare general population and key population cascades and their availability; and review the opportunities offered by BBS and programme data as well as their limitations.

2 | DISCUSSION

2.1 | A tale of two responses: progress towards

general population and key population epidemic control

The immense progress combating HIV in the general popula- tion, evidenced by PHIA results, has been rightly celebrated but simultaneously underscores how far there is to go with key populations. It is well established that the risk of HIV acquisition is far higher among key populations than the gen- eral population, that HIV prevalence is higher among key pop- ulations, and that key populations access to HIV services is low [21-24 ]. Even within the same country, recent national population-based surveys (e.g. PHIA and Kenya AIDS Indicator Survey) and population-based BBS among key populations put in stark contrast the disparities in the 90-90-90 cascades between general population and key population members in the same country. They further illustrate the low coverage among key populations or the absence of key population cas- cade data in other countries (Table 1). Of great importance is that no cascade data exist for transgender people apart from in combination with MSM and no publicly available data exist for prisoners. As BBS should be conducted in locations with key population services and populations of sufficient size for sampling, the number of sites contributing to key population estimates are indicated below [5]. Only in Malawi and South Africa is the proportion of PLHIV self-reporting being aware of their HIV infection higher in a key population group (female sex workers, FSW, in this case) than the general population, though the South African key

population survey occurred two years after the general population survey during which time services may have been expanded. Another explanation is that the FSW surveys were conducted in urban areas while the general population data represents the entire country, and HIV testing access, and therefore awareness, may be higher in urban than rural areas. The limited BBS viral load in Table 1 may reflect the avail- ability of viral load testing. The scale-up of viral load testing for treatment monitoring in many resource-limited settings will aid in estimating viral load measures in surveys. Where access to viral load testing is limited, investigators can send dried blood spots or plasma serum to other laboratories (e.g. in the capital or to another country) for testing while making an effort to return viral load results to survey participants. Similar to the general population, the largest gap in 90-90- 90 key population cascades above is among the proportion of people self-reported to be living with HIV and aware of their infection. Where data exist, self-reported awareness of HIV infection is lowest among MSM. While linkage to treatment is comparable between populations, it is still lower among key populations, and viral suppression data suggest that treatment adherence or retention may also be lower among key popula- tions compared to the general population, signifying that all three steps in the key population cascade need attention, with priority on diagnosis. Structural factors such as continued discrimination and criminalization of key populations impede access to health ser- vices and willingness to conduct surveys. Barriers to timely BBS include political will and funding as services are priori- tized over strategic information to guide them, and the gen- eral population over key populations. The representativeness and timeliness of data are extre- mely important for maximizing their utility. The data in Table 1 come from respondent-driven sampling surveys for key popu- lations and nationally representative cluster-based household surveys for the general population, both of which are able to provide representative data about the target population. Though other data may exist, they are of lesser quality (i.e. utilized non-probability probability sampling methods or were restricted to a key population sub-group) and therefore not included. Table 1 reveals that key population BBS may not be conducted with sufficient frequency (i.e. every two to three years), and the publication dates of the data presented sug- gest that results may take a considerable amount of time to be released [5 ]. Survey-derived treatment cascades do not exist for key populations in all other resource-constrained countries. At a basic level, many southern African countries have no BBS data at all on men who have sex with men. In addition, Table 1 illustrates that where data do exist, data on the gen- eral population are generally more recent than on key popula- tions. Key populations can play a critical role advocating for data collection. Kenya conducted BBS among key populations and a national general population survey in 2012 but only measured the cascade in the general population survey [33 ]. While another national survey will be conducted in 2018, no survey was planned amongst female sex workers, men who have sex with men, or transgender people until recent advo- cacy efforts by civil society resulted in the allocation of resources for such surveys.

Hakim AJ et al. Journal of the International AIDS Society 2018, 21 (S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119

Table 1. General population and key population 90-90-90 cascades

 

First 90:

Second 90:

Third 90: virally suppressed, of those on ART

 

Year of data collection

 

self-reported

self-reported on ART of those diagnosed

Country

Population

Sites

diagnosed

Cameroon [ 25 ] Cameroon [ 25 ] India [ 26 ] India [ 26 ] Kenya [ 27 ] Malawi [ 10]

FSW

5

2015 to 2016 2015 to 2016 2012 to 2013

52%

81%

a

MSM/TP

5

42%

63%

a

MSM

12

30%

53%

63%

PWID

15

2012 to 2013

41%

44%

83%

General population

National

2012 62.4%

 

71.9%

79.8%

General population

National

2015 to 2016

72.7%

89.6%

91.2%

Mozambique [ 28 ] General population Mozambique [ 29 ] FSW Mozambique [ 29 ] MSM Mozambique [ 29 ] PWID

National

2015 34.3%

 

77.3%

a

3

2011 to 2012

22.3%

52.5%

a

3

2011

8.8%

39.8%

a

2

2014 63.2%

 

44.9%

a

Papua New Guinea [ 15 ] South Africa [ 30 ] South Africa [ 31 ] Swaziland [ 32] Uganda [ 14] Uganda [ 13] Zambia [ 10] Zimbabwe [ 9 ] Zimbabwe [ 16 ]

FSW

1

2016 38.9%

84.4%

54.6%

General population

National

2012

37.8% male/55.0% female 25.7% male/34.7% female a

FSW

1

2014 to 2015 2016 to 2017

82%

48%

a

General population

National

84.7%

87.4%

91.9%

FSW

1

2012 37.5%

 

67.7%

51.6%

MSM

1

2012 to 2013 2015 to 2016 2015 to 2016

20.2%

75.0%

58.3%

General Population

National

66.0%

85.0%

89.3%

General Population

National

72.9%

86.8%

86.5%

FSW

14

2013

64.0%

67.7%

77.8%

a Data not available.

2.2 | A tale of two cascades: population-based and

programme-based

Population-based surveys in the form of BBS are an essential part of key population surveillance and should be conducted every two to three years to measure changes in the epi- demic and the impact of the response [2,5 ]. BBS have many advantages. Foremost is their ability to obtain data on people regardless of whether they are accessing HIV services, allow- ing the development of representative estimates of service coverage, including outreach and prevention services such as pre-exposure prophylaxis, and 90-90-90 cascades for the sur- vey location [2]. By asking questions of participants about non-engagement in services, BBS allow an understanding of the characteristics and reasons why people are not testing for HIV, not on treatment, or not virally suppressed, informa- tion that is essential for increasing HIV service coverage. Such reasons may include perceived or experienced stigma, cost, not knowing where to test, or feeling not at risk [13,34,35 ]. BBS can also facilitate the production of popula- tion size estimates. They are often challenged, however, by the time required for planning, implementation, data analysis, and report writing, as well as budget constraints. Structural factors such as stigma and criminalization may also impede participation in BBS. This can be assessed through formative assessment and non-response interviews during BBS, and mitigated by early engagement of key populations in survey planning.

It may be tempting to use data from general population sur- veys in place of BBS data to characterize the HIV epidemic; however, such efforts are fraught with many challenges and the surveys are only conducted in a subset of countries. Key populations may be less likely to be sampled in household sur- veys due to homelessness, or informal or clandestine living arrangements. Many ministries of health are reluctant to include questions about same-sex sexual activity, transgender people, or even the gender of sex partners in household sur- veys, particularly when these are criminalized. Where key pop- ulations are sampled and questions about their practices and identities are included in a survey, they may not disclose them to interviewers. Taken together, these factors may bias key population cascades obtained in general population surveys. Finally, individual surveys may not have sufficient power to disaggregate data by key population. As surveys such as PHIA are powered for national incidence estimation and subnational viral load suppression for the general population, they lack the power to estimate the same for key populations who make up a small proportion of the population. General population sur- veys do, however, offer a unique opportunity to estimate national and subnational key population size through the use of the network scale-up method. Such estimates may facilitate the expression of key population cascades when combined with high quality programme data. Whereas BBS reach people accessing services and those who do not, programme data only describes those accessing services. In addition, key population programme data only

Hakim AJ et al. Journal of the International AIDS Society 2018, 21 (S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119

describe those key population members who access services at key population-friendly facilities that disaggregate data by population rather than all key population members living with HIV (KPLHIV) who access services, leaving an incomplete pic- ture of KPLHIV who access services. Stigma continues to hin- der uptake of services by key populations and disclosure of key population practices and identities among those who do access them, resulting in low programme coverage and conse- quently, inadequate data for drawing conclusions about the population [36-40 ]. And in some countries, the provision of services to key populations has been barred, effectively excluding the possibility of using programme data to inform cascades [41 ]. BBS can help highlight the detrimental effects of such policies and structural barriers. They can further assess mental health measures and the mediating role between exposure to stigma, violence, and discrimination, and practices, identities, and service uptake. The 2017 WHO Biobehavioral Survey Guidelines for Populations at Risk for HIV offers questions for investigators to include in order to measure these and other important topics, including shame and social cohesion [ 5]. High-quality programme or service data that are individual- ized and deduplicated can provide important information about the number and sub-groups of people accessing services and their ART outcomes [42 ]. This can help service providers monitor interventions to verify that they are efficiently reach- ing the right people in the right places and that interventions are functioning as planned. When programme data reveal that the number of new people reached with outreach services decreases over time, when the testing yield declines, or when patients do not collect medicine, providers can respond in real time to changes in the population and their needs. Short sur- veys using audio-computer assisted personal interviews can also be integrated into routine services to obtain behavioural data on individuals accessing services. Such surveys have been used at a testing facility for men who have sex with men in Uganda (e.g. the Know Your Sero-Status, KYSS, survey) as well as at one of Ugandas largest general population testing facili- ties, Mildmay Clinic. A unique client code can be used to track people and their practices and serostatus over time. These data should not be used to replace BBS as they only repre- sent people already accessing services. Furthermore, sentinel sites are ill-suited for key population surveillance because their very nature, for instance as an sexually transmitted infec- tions clinic, make them associated with service uptake and HIV, and the resulting data are biased. Despite these advantages, data quality can vary widely and routine programme data only provide information about ser- vice uptake and health status. Detailed behavioural data that can inform service delivery generally are not collected. Track- ing individuals, and linkage to and retention on treatment can also be challenging. Double counting of individuals accessing services at the same site, or at multiple sites or providers may inflate the reach of services or skew testing yield. The genera- tion of unique client codes, as many key population services have done, may improve data quality but may also create chal- lenges when trying to assess the number of key population members accessing services at key population-friendly or gen- eral population services that do not use these unique identi- fiers or collect information about key population status. This is further limited where stigma or fear lead key population

members not to disclose their defining risk practice or identity [43-46 ]. Noting the significance of confidentiality and security issues for key populations, WHO does not recommend the inclusion of key population groups on patient monitoring records [47 ]. In addition, where it may seem that people diag- nosed with HIV are not linked to treatment or that people on ART have defaulted, it may also be the case that individuals chose to seek services elsewhere [48-50 ]. These silent trans- fers may prompt policy makers and service providers to target resources at a problem that may not exist. In addition, without a robust population size estimate, it is nearly impossible to estimate outreach coverage, the starting point of the key pop- ulation cascade. The triangulation of both BBS and programme data has great potential to guide service providers and policy makers in the epidemic response [51-53 ]. Together, these data, collected using different methods and data sources, may be able to pro- vide a comprehensive picture of the epidemic response, with programme monitoring revealing trends in service provision and missed opportunities, and BBS data on the reach and impact of services. For instance, programme data showing high loss to follow up and BBS data showing high ART coverage and viral suppression, may reveal that people are simply changing service providers, possibly even to general population sites, thereby suggesting that fewer resources are needed to identify and reengage those who were thought to be lost to follow up and retain others. The higher than expected viral suppression may also suggest a reduction in HIV incidence. While triangulation exercises should be updated regularly as new data become available, they are not common and the pro- duction of a report or publication is even less common. It is imperative that key population members play a mean- ingful role in the collection and use of data about and for them. Formative assessments provide key populations with an important role in informing BBS. They should also be included as collaborators and investigators, and where appropriate, data collectors. In Papua New Guinea, survey results were shared with key population members ahead of public release and their feedback and recommendations were incorporated into survey reports, including in the form of statements from key population organizations [54,55 ]. Such engagement enhances a sense of ownership of the results by these groups and their ability to use the data for advocacy.

3 | CONCLUSIONS

The HIV treatment cascade is a valuable tool for measuring progress toward epidemic control and when measured through BBS, elucidating barriers, structural and otherwise, to service utilization. While there are many gaps in measuring the cascade, there are also many opportunities for data collec- tion and use. Though BBS of key populations are recom- mended to be conducted every two to three years, in practice they occur less frequently or not at all [5 ]. Meanwhile, their importance for monitoring the epidemic will increase as coun- tries get closer to reaching 95-95-95. Many efficiencies can be found to expedite data collection and facilitate timely data availability and use, in turn decreas- ing costs of data collection and service provision. These effi- ciencies include starting surveys with more seeds, utilizing

Hakim AJ et al. Journal of the International AIDS Society 2018, 21 (S5):e25119 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25119/full | https://doi.org/10.1002/jia2.25119

audio computer-assisted self-interviews that require fewer staff and decrease bias, and developing analytic programs dur- ing data collection [56-58 ]. Incorporating BBS into national surveillance strategies and making them routine activities implemented every two to three years can help enhance the timeliness, standardization, quality, and utility of data. Follow- ing the example of the ARISTOTLE study which showed the cost effectiveness of their survey and intervention, other sur- veys are now beginning to assess the cost effectiveness of BBS resulting from their critical role in diagnosing and (re)link- ing people to ART, including those who have stopped being on ART [59 ]. Between survey rounds, programme data can indicate whether services are reaching more people and areas for improvement in programme quality. In the context of decreas- ing funding from external donors in countries with concen- trated epidemics, it becomes ever more important to use data to inform the response and make an investment case for national and donor resources.

AUTHORS AFFILIATIONS

1 Division of Global HIV and Tuberculosis, US Centers for Disease Control and Prevention, Atlanta, GA, USA; 2 World Health Organization, Geneva, Switzerland; 3 The Global Fund to Fight AIDS, Tuberculosis and Malaria, Geneva, Switzerland; 4 Division of HIV/AIDS Prevention, US Centers for Disease Control and Preven- tion, Atlanta, GA, USA; 5 United Nations Joint Programme for HIV/AIDS, Geneva, Switzerland

COMPETING INTERESTS

We have no competing interests to report.

AUTHORS CONTRIBUTIONS

AH, WH, DP and KS conceived of this manuscript. AH and WH contributed sub- stantially to the writing. VM, JZ, JB, KS, DP and JC reviewed the manuscript.

ACKNOWLEDGEMENTS

FUNDING

This paper has been supported in part by the President s Emergency Plan for AIDS Relief (PEPFAR) through the Centers for Disease Control and Prevention (CDC).

DISCLAIMER

The findings and conclusions in this paper are those of the authors and do not necessarily represent the official position of the funding agencies.

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Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126 RESEARCH ARTICLE
http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126 RESEARCH ARTICLE

RESEARCH ARTICLE

Estimating the contribution of key populations towards the spread of HIV in Dakar, Senegal

Christinah Mukandavire 1 , Josephine Walker 1 , Sheree Schwartz 3 , Marie-Claude Boily 2 , Leon Danon 1,9 , Carrie Lyons 3 , Daouda Diouf 4 , Ben Liestman 3 , Nafissatou Leye Diouf 5 , Fatou Drame 4 , Karleen Coly 3 , Remy Serge Manzi Muhire 3 , Safiatou Thiam 8 , Papa Amadou Niang Diallo 7 , Coumba Toure Kane 5 , Cheikh Ndour 7 , Erik Volz 2 , Sharmistha Mishra 6 , Stefan Baral 2 and Peter Vickerman 1 §

§ Corresponding author: Peter Vickerman, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK. Tel: +44 7821196359.

( peter.vickerman@bristol.ac.uk)

Abstract

Introduction: Key populations including female sex workers (FSW) and men who have sex with men (MSM) bear a dispropor- tionate burden of HIV. However, the role of focusing prevention efforts on these groups for reducing a country s HIV epidemic is debated. We estimate the extent to which HIV transmission among FSW and MSM contributes to overall HIV transmission in Dakar, Senegal, using a dynamic assessment of the population attributable fraction (PAF). Methods: A dynamic transmission model of HIV among FSW, their clients, MSM and the lower-risk adult population was parame- terized and calibrated within a Bayesian framework using setting-specific demographic, behavioural, HIV epidemiological and antiretroviral treatment (ART) coverage data for 1985 to 2015. We used the model to estimate the 10-year PAF of commercial sex between FSW and their clients, and sex between men, to overall HIV transmission (defined as the percentage of new infec- tions prevented when these modes of transmission are removed). In addition, we estimated the prevention benefits associated with historical increases in condom use and ART uptake, and impact of further increases in prevention and treatment. Results: The model projections suggest that unprotected sex between men contributed to 42% (2.5 to 97.5th percentile range 24 to 59%) of transmissions between 1995 and 2005, increasing to 64% (37 to 79%) from 2015 to 2025. The 10-year PAF of commercial sex is smaller, diminishing from 21% (7 to 39%) in 1995 to 14% (5 to 35%) in 2015. Without ART, 49% (32 to 71%) more HIV infections would have occurred since 2000, when ART was initiated, whereas without condom use since 1985, 67% (27 to 179%) more HIV infections would have occurred, and the overall HIV prevalence would have been 60% (29 to 211%) greater than what it is now. Further large decreases in HIV incidence (68%) can be achieved by scaling up ART in MSM to 74% coverage and reducing their susceptibility to HIV by two-thirds through any prevention modality. Conclusions: Unprotected sex between men may be an important contributor to HIV transmission in Dakar, due to subopti- mal coverage of evidence-informed interventions. Although existing interventions have effectively reduced HIV transmission among adults, it is crucial that further strategies address the unmet need among MSM.

Keywords: population attributable fraction; HIV; female sex workers; men who have sex with men; clients; condom use; key populations

Additional Supporting Information may be found online in the Supporting information tab for this article.

Received 15 December 2017; Accepted 16 May 2018 Copyright © 2018 The Authors. Journal of the International AIDS Society published by John Wiley & sons Ltd on behalf of the International AIDS Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

1 | INTRODUCTION

Key populations (KP) such as female sex workers (FSW) and men who have sex with men (MSM) bear a disproportionate burden of HIV [1-5]. The HIV-associated vulnerabilities experi- enced by KP are thought to play an important role in the trans- mission of HIV in low HIV prevalence settings, but less so in settings with generalized HIV epidemics. Existing analyses sug- gest that FSW and their clients contribute less than 30% [1,3]

and 10% [6] of prevalent HIV infections among adults in sub- Saharan Africa (SSA), respectively, although these analyses only considered the proportion of prevalent infections that were among clients or FSW. In addition, recent reviews of the UNAIDS Modes of Transmission (MOT) model [7,8] suggest that the role of KP is small in SSA, with the cumulative percentage of new annual infections due to KP generally being less than 25%. These estimations of the role of KP to HIV epidemics do not incorporate the full chain of transmission originating from

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

KPs, such that a male who becomes infected by another male could then infect a female, resulting in the initial male not only contributing to the MSM HIV epidemic but also the hetero- sexual epidemic. Indeed, for commercial sex, these analyses conflict with emerging dynamic modelling analyses suggesting that > 90% of all HIV transmissions to date are directly or indirectly due to sex work in the low-to-moderate prevalence HIV epidemics of Burkina Faso, Cote d Ivoire and Benin, and over 65% in the higher-prevalence HIV epidemic in Kenya [9-14 ]. These analyses challenge the conventional wisdom and existing epidemiological tools such as the MOT model. In con- trast, two recent studies for Nigeria and Cote dIvoire suggest MSM contribute little (< 10%) to these HIV epidemics [ 14,15 ]. This is despite MSM experiencing a high HIV burden [4,16,17 ] and engaging in sexual partnerships with women, so contribut- ing bridging infections to the wider population [18 ]. Limita- tions in existing evidence emphasizes the urgent need to improve our estimates of the contribution of KP to HIV epi- demics in SSA; this basic epidemiological measure is crucial for prioritizing HIV programming. Senegal has a low HIV prevalence among adults (0.4% in 2016) [19 ], thought to be due to a comprehensive response to the epidemic [20 ]. Nevertheless, the HIV burden among KP is much higher (5.9% in FSW and 29.7% in MSM in 2016) [21-27 ]. Despite the low prevalence of HIV in the adult popu- lation and high prevalence among KP, current estimates sug- gest that commercial sex and sex between men contribute little (< 15%) to existing HIV transmission in Senegal [3,8], although these estimations were limited as they did not incor- porate the dynamic aspect of transmission. To remedy these limitations, we undertook a dynamic model assessment of the contribution of commercial sex and sex between men to HIV transmission in Dakar, Senegal. We also estimated the impact of historical increases in the coverage of antiretroviral therapy (ART) and condom use among KP, and the potential impact of further uptake of prevention and treat- ment interventions.

2 | METHODS

2.1 | Model description

We developed a dynamic HIV transmission model to evaluate the extent to which FSW, clients of FSW (referred to as cli- ents hereafter) and MSM contribute to the overall HIV epi- demic in Dakar, Senegal. The model did not include people who inject drugs because of their low prevalence in Dakar (< 0.07% of the adult population [28 ]). The model considers adults (15 to 49 years), and divides the population into six sub-populations: low-risk females and males, clients, FSW, young MSM (< 30 years) and old MSM ( 30 years) (Figure 1). Transgender women (TGW) were not explicitly included in the model because of insufficient data to parameterize this risk population. Low-risk individuals are defined as people who are not MSM and do not report commercial sex. Individuals enter the modelled population in the low-risk groups when they become sexually active, at a rate that bal- ances non-HIV deaths and reflects population growth. Low- risk males and females can become clients and FSW at speci- fied rates, with both practising commercial sex for an average duration. Similarly, MSM transition from the low-risk male

(a)
(a)
Similarly, MSM transition from the low-risk male (a) (b) Uninfected Recruitment Φ On ART (c) Acute
Similarly, MSM transition from the low-risk male (a) (b) Uninfected Recruitment Φ On ART (c) Acute
Similarly, MSM transition from the low-risk male (a) (b) Uninfected Recruitment Φ On ART (c) Acute
(b) Uninfected Recruitment Φ On ART
(b)
Uninfected
Recruitment
Φ
On ART

(c)

Acute HIV

Acute HIV Progression Chronic HIV HIV death

Progression

Acute HIV Progression Chronic HIV HIV death

Chronic HIV

Acute HIV Progression Chronic HIV HIV death

HIV death

Acute HIV Progression Chronic HIV HIV death

Infec on

Λ
Λ

Loss to follow up

Treatment HIV death Low-risk female Clients of FSW
Treatment
HIV death
Low-risk
female
Clients
of FSW
Low-risk male
Low-risk
male
Female sex workers
Female
sex
workers

Young and old men who have sex with men

sex workers Young and old men who have sex with men Figure 1. Model schematic illustrating

Figure 1. Model schematic illustrating the (a) movement of indi- viduals in and out of different sub-populations (male and female low-risk, clients, female sex workers (FSW), younger and older men who have sex with men (MSM), (b) stratification of the pop- ulation with respect to HIV infection and (c) sexual interactions which can result in HIV transmission among female, male, FSW, their clients and MSM. Blue arrow in Figure 1c shows com- mercial sex and all other arrows show sex with main and casual partners.

population, and age from the young to the old MSM group, but remain as MSM until death. The model captures HIV transmission among the sub-popu- lations through vaginal and anal sex (VI and AI, respectively) between all males and females, and AI within the MSM group (Figure 1 ). The model stratifies the population with respect to HIV infection and disease progression (Figure 1b). Upon infec- tion, susceptible individuals acquire acute HIV infection before progressing to chronic infection. Chronically-infected individuals experience HIV-related mortality, but can also be recruited onto ART, which reduces HIV-related mortality. Indi- viduals on ART can be lost to follow up, whereupon they

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

return to the chronic infection stage. All sub-populations also experience non - HIV-related death. The model incorporates HIV transmission due to main, casual and commercial sexual partnerships. Commercial partnerships occur between FSW and their clients, while main and casual partnerships between men only occur among MSM. All other heterosexual main and casual partnerships occur between all groups. The risk of HIV transmission for each individual is related to the HIV prevalence of their sexual partners, with the HIV transmission risk being elevated if they have acute infec- tion, and reduced if they are on ART. Transmission risk is also related to the frequency of sex between different partnerships and is reduced through condom use. The consistency of condom use is time dependent and varies by type of partnership. The model assumes some males are circumcised, which reduces the risk of HIV acquisition. We assume heightened transmission risk in the initial stages of an HIV epidemic to capture the effects of risk heterogeneity. The model is described in Data S1.

2.2 | Model parameterization and calibration

Recent model parameter and calibration data for FSW, clients and MSM were obtained from three integrated behavioural and biological assessment (IBBA) surveys undertaken in Dakar, Senegal, from 2015 to 2016 [25 ] (client data are unpublished). Sexual behaviour data related to FSW, clients and MSM came from these surveys. The survey used to parameterize the MSM component of the model also included some TGW.

In addition, older IBBA surveys were used to determine whether risk behaviour has changed over time, and how the HIV epidemic in different risk groups has evolved. Importantly, this included trends in condom use for different risk groups. However, differences in the behavioural measures used made it difficult to evaluate how behaviours changed over time, and so uncertainty was incorporated into those trends. Adult pop- ulation HIV-related epidemiological and sexual behaviour data were obtained from the Demographic Health Surveys (DHS) for 2005 and 2010 [29,30 ]. Table S1 gives a summary of IBBA surveys used in the modelling, while the model parame- terization is summarized in Table 1 and included in full in Table S2. Based on data from numerous FSW and client IBBA surveys between 1985 and 2016 [26,31-36 ], and national data on increases in condom distribution between 1988 and 1997 [37 ], condom use during commercial VI sex between FSW and their clients (Figure 2 a) was assumed to increase from negligi- ble levels in 1985 [33 ], up to a high stable level from 1998 onwards between 54 and 90% [24,26,34 ]. This large range was based on the difference between client- and FSW- reported condom use estimates in 2015 to 2016. Similarly, based on data from MSM IBBA surveys, condom use in last sex act for male partners of MSM was assumed to be negligi- ble in 1985, low (10% to 30%) in 2001 [38 ], up to 70 to 85% by 2003 to 2007 [22,39,40 ] and constant thereafter (Figure 2 b) (2016 survey). The Data S1 and Figure S1 include further details on the condom use assumptions.

Table 1. Parameters used for female sex workers (FSW), their clients and men who have sex with men (MSM) in 2016

Model parameter

FSW

Clients

Young MSM ( <30 years)

Old MSM ( 30 years)

Size estimates (% of adult

0.5% (0.3 to 0.9%)

5.1% (1.8 to 12.1%)

1.2% (0.8 to 2.3%)

women or men)

HIV-1 prevalence

5.9% (1.8 to 10.0%)

1.2% (0.5 to 2.4%)

28.6% (19.8 to 37.5%) a

37.0% (14.8 to 59.2%)

Level of viral suppression in

individuals living with HIV

Frequency of partners per year

Commercial (FSW/Clients)

73.7% (60.9 to 84.2%)

NA

516.4 (368.2 to 691.2) b 69.6 (62.4 to 78.0)

35.4% (23.9 to 48.2%)

Main heterosexual

0.58 (0.47 to 0.73)

1.9 (1.3 to 2.6)

0.88 (0.39 to 1.5)

0.88 (0.39 to 1.5)

Casual heterosexual

0.96 (0.48 to 1.6)

0.6 (0.15 to 1.4)

2.3 (0.55 to 5.1)

2.3 (0.55 to 5.1)

Main (MSM sex)

0.71 (0.59 to 0.83)

0.71 (0.59 to 0.83)

Casual (MSM sex)

5.4 (2.5 to 9.2)

4.8 (1.3 to 9.2)

% of commercial sex acts that are anal c

4.1% (2.1 to 6.5%)

5.1% (3.8 to 6.5%)

Frequency of vaginal sex acts per year

Main heterosexual partners

98.3 (78.5 to 117.5)

97.3 (73.6 to 124.6)

65.3 (56.2 to 74.4)

65.3 (56.2 to 74.4)

Casual heterosexual partners

6.2 (4.2 to 8.2)

3.8 (2.1 to 5.9)

4.5 (2.6 to 6.4)

4.5 (2.6 to 6.4)

Frequency of anal sex acts per year

Main heterosexual partners

9.9 (3.6 to 15.6)

6.6 (3.4 to 11.1)

5.2 (1.6 to 9.4)

5.2 (1.6 to 9.4)

Casual heterosexual partners

0.49 (0.12 to 1.2)

0.33 (0.097 to 0.75)

0.52 (0.04 to 1.0)

0.52 (0.04 to 1.0)

Frequency of anal sex for men with men per year (MSM sex)

Main partnerships of MSM

105.6 (91.0 to 120.6)

105.6 (91.0 to 120.6)

Casual partnerships of MSM

7.6 (6.7 to 8.2)

15.2 (13.2 to 16.4)

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

(a) FSW 1985 1995 2005 2015 Condom use % (commercial partners) 0 20 40 60
(a)
FSW
1985
1995
2005
2015
Condom use % (commercial partners)
0
20
40
60
80
100

Time (years)

(b) MSM

1985 1995 2005 2015 Condom use % (male partners) 0 20 40 60 80 100
1985 1995
2005
2015
Condom use % (male partners)
0
20
40
60
80
100

Time (years)

Figure 2. Modelled condom use trends for (a) female sex workers (FSW) and (b) men who have sex with men (MSM). (a) FSW condom use with commercial partners for vaginal intercourse. Assume condom use for anal intercourse is half that of vaginal intercourse for all years. (b) MSM condom use with regular and casual male partners. We assume some bias in reporting so all rates have been multiplied by a bias factor of 0.7 to 1.0 lower bound of 0.7 chosen to give overall lower bound of 0.5, as seen in figure.

Senegal population size estimates for 1980 to 2020 and gender-specific death rates were obtained from UNDP [ 41 ], with population growth rates being fit to this data. Population size estimates for FSW and MSM were produced as part of the 2015 IBBA surveys using the service multiplier and unique object methods [42 ]. The population size of clients was estimated through balancing the overall demand for commer- cial sex of FSW with that of clients (see Data S1). ART data for the Senegal population came from the World Bank and UNAIDS [43,44 ] (Figure S2), suggesting ART cover- age increased from negligible levels in 2000 to 40% of individu- als living with HIV in 2015. For FSW, these coverage trends were scaled up because the 2016 IBBA found 74% of FSW liv- ing with HIV were virally suppressed (unpublished data from 2016 FSW survey [25 ]). ART recruitment rates were calibrated to give the trends in ART coverage. Other HIV biological param- eters came from literature (Table S2). Uncertainty ranges were assigned to most model parame- ters, with most parameters being fixed over time except for the rate of ART recruitment, levels of condom use and frequency of sex for MSM with their male partners, which data suggest increased from 2007 to 2016 [21,25 ]. To incorporate uncer- tainty, 10,000 parameter sets were randomly sampled from their uncertainty ranges (Table S2 and Table 1 ). For each parameter set, the model was run while including temporal increases in condom use, ART coverage and the frequency of

sex for male MSM partners. Any run producing HIV prevalence projections that agreed with early IBBA HIV prevalence data for FSW (1990 or 1995) and clients (1999) and recent HIV preva- lence data for young MSM from 2014 to 2016 were selected as a model fit. These data suggested a HIV prevalence of 2.0 to 10.0% in 1990 and 5.0 to 15.0% in 1995 in FSW, 1.1 to 5.5% in clients (1999) and 9.7 to 37.7% in MSM, with these prevalence estimates shown in Figure 3 (data sources in Table S1). The wide range for MSM is due to contrasting estimates from two IBBA surveys in 2014 and 2016. Other HIV prevalence data for all sub-groups are also shown in Figure 3. The model was not calibrated to these data, but instead the data were used to vali- date the accuracy of the model projections.

2.3 | Analyses

2.3.1 | Contribution of commercial sex and sex

between men to HIV transmission

To estimate the contribution of commercial sex between FSW and clients and sex between men to the overall HIV epidemic (re- ferred to as population attributable fraction or PAF), model fits were used to estimate the proportion of new HIV infections that would be prevented by setting the transmission probability for com- mercial sex or sex between men to zero over a specific time period. This was estimated for 1 or 10 years from 1995, 2005 and 2015.

2.3.2 | Impact of existing interventions

Model fits were used to explore the likely impact of historical increases in ART coverage and condom use on the evolution of the HIV epidemic for different population sub-groups. This was determined by re-running the model fits, but with no ART and/or condom use.

2.3.3 | Impact of scaling up interventions

We then assessed the impact of increasing the coverage of ART among MSM from 2017 to 2030, such that the proportion of MSM living with HIV who are virally suppressed increases to the same coverage as FSW (74%) by 2020. This increase in ART coverage was also considered among low-risk individuals. To capture the possible effect of introducing pre-exposure pro- phylaxis for HIV (PrEP) and/or further increases in condom use, we also investigated the impact of an intervention that reduces an individual s average risk of becoming HIV positive. This was estimated by reducing by a third the susceptibility to HIV trans- mission among (i) MSM, (ii) FSW or (iii) all low-risk individuals. This is roughly equivalent to putting 40% of MSM on PrEP (as- suming 85% effectiveness [46,47 ]), 50% of FSW on PrEP (as- suming 66% effectiveness [47,48 ]) or reducing the number of unprotected sex acts by 40% through increased condom use (assuming 82.5% effectiveness per sex act). We also assumed a scenario where both were achieved for MSM (PrEP and con- dom use), reducing susceptibility by two-thirds.

2.3.4 | Uncertainty analysis

We performed linear regression analyses of covariance (ANCOVA) [49 ] to determine which parameters contribute most to the variability in the 10-year PAF estimates for com- mercial sex and sex between men for 2015.

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

(a)

(b)

40 Model runs (median) Model runs (95%CI) 30 Data (with 95%CI) 20 10 0 1985
40
Model runs (median)
Model runs (95%CI)
30
Data (with 95%CI)
20
10
0
1985
1995
2005
2015
HIV prevalence FSW (%)
15 Model runs (median) Model runs (95%CI) Data (with 95%CI) 10 5 0 1985 1995
15
Model runs (median)
Model runs (95%CI)
Data (with 95%CI)
10
5
0
1985
1995
2005
2015
HIV prevalence clients (%)

Time (years)

(c) (d) 100 100 Model runs (median) Model runs (95%CI) Data (with 95%CI) 80 80
(c)
(d)
100
100
Model runs (median)
Model runs (95%CI)
Data (with 95%CI)
80
80
60
60
40
40
20
20
0
0
1985
1995
2005
2015
HIV prevalence young MSM (%)
HIV prevalence old MSM (%)

(e) Time (years)

(f)

Time (years) Model runs (median) Model runs (95%CI) Data (with 95%CI) 1985 1995 2005 2015
Time (years)
Model runs (median)
Model runs (95%CI)
Data (with 95%CI)
1985
1995
2005
2015

Time (years)

2.0 2.0 Model runs (median) Model runs (95%CI) Model runs (median) Model runs (95%CI) 1.5
2.0
2.0
Model runs (median)
Model runs (95%CI)
Model runs (median)
Model runs (95%CI)
1.5
Data (with 95%CI)
1.5
Data (with 95%CI)
1.0
1.0
0.5
0.5
0.0
0.0
1985
1995
2005
2015
1985
1995
2005
2015
Time (years)
Time (years)
HIV prevalence female (%)
HIV prevalence male (%)

Figure 3. A comparison of model fits with HIV prevalence estimates from 1985 to 2020 for (a) female sex workers (FSW) (b) clients of FSW, (c) younger men who have sex with men (MSM) (<30 years old), (d) older MSM ( 30 years old) and (e) female and (f) male overall adult populations. Continuous black line shows median projections from all the model fits, with dashed lines and grey shaded areas showing 95% credibility intervals. Red points and lines show data with 95% confidence intervals.

3 | RESULTS

3.1 | Existing epidemiological insights

Two hundred model runs agreed with the HIV prevalence cali- bration data from FSW, clients and MSM. Despite only being calibrated to one-third of the prevalence estimates (5/17 data points), these model fits agreed closely with observed HIV prevalence trends for all groups (Figure 3). These model fits suggest the HIV prevalence among FSW, clients and the adult population has been in steady decline since the mid-90s, but may have increased recently among MSM.

3.2 | Contribution of commercial sex and sex

between men to HIV transmission

For the 10 years from 1995, a median of 42.1% (2.5 to 97.5%, percentile range 23.7 to 59.0%) of new HIV

infections could have been prevented (10-year PAF) if the risk due to sex between men had been removed over this period, respectively, with this increasing to 64.1% (37.4 to 79.4%) by 2015 (Figure 4). The increase in the 10-year PAF for sex between men in 2015 is due to the increase in the frequency of AI sex acts between MSM over this time per- iod. Much of this effect of MSM is due to their heterosex- ual partnerships with females, such that removing this risk prevents 37.1% (18.7 to 51.3%) of HIV infections over 10 years from 2015 (Figure 4). In contrast, the 10-year PAF for commercial sex was 20.6% (7.3 to 38.7%) and 13.6% (4.8 to 35.0%) for 1995 and 2015 respectively (Fig- ure 4). For sex between men, one-year PAFs were lower than 10-year PAFs, but were similar for commercial sex (Table 2 ). The analysis of covariance showed that many parameters contributed to the uncertainty in the PAF estimates (Data

S1).

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

Population attributable fraction % (10 year)

100

80

60

40

20

0

Sex between men Commercial sex Heterosexual sex for MSM Non−commercial sex for FSW & clients

 

Sex between low risk groups

 
Sex between low risk groups  
sex Heterosexual sex for MSM Non−commercial sex for FSW & clients   Sex between low risk
sex Heterosexual sex for MSM Non−commercial sex for FSW & clients   Sex between low risk

1995

2005

2015

Figure 4. Ten-year population attributable fraction (PAF) for sex between men (blue), commercial sex (red), heterosexual sex for men who have sex with men (MSM) (purple), non-com- mercial sex for female sex workers (FSW) and their clients (grey), and sex between low-ri sk groups (green). The PAF is estimated as the proportion of all HIV infections prevented over 10 years from 1995, 2005 or 2015 if the HIV transmis- sion risk due to a specific ty pe of sexual behaviour is removed. The box plots signify the uncertainty (middle line is median, limits of boxes are the 25% and 75% percentiles and whiskers are 2.5% and 97.5% percentile range) in the PAF esti- mates due to uncertainty in the model parameters.

3.3 | Impact of existing interventions

Model projections (Figure 5) suggest that if there had been no ART scale-up since 2000, in relative terms, the HIV prevalence in FSW in 2015 would have been 13.5% (6.1 to 23.8%) higher, 7.0% (4.0 to 11.0%) higher in MSM and 5.7% (2.2 to 10.2%) higher overall. In contrast, if condom use had not increased in the mid- to late-1990s, the HIV prevalence in MSM would have been 56.6% (27.9 to 160.3%) higher in 2015, 2.1 times (1.5 to 6.8) higher in FSW and 60.2% (28.9 to 210.9%) higher in the general population (Figure 5). In terms of new HIV infections, with- out ART scale-up, 49.0% (32.3 to 71.3%) more HIV infec- tions would have occurred in Dakar since 2000 when ART was introduced, whereas without any condom use since the mid-1980s, 66.5% (27.2 to 178.5%) more HIV infections would have occurred.

3.4 | Impact of scaling up interventions

Scaling up ART among MSM such that 74% are virally sup- pressed by 2020 (35.4% of MSM living with HIV are currently virally suppressed) would decrease the overall HIV incidence in Dakar by 14.7% (4.9 to 47.1%) by 2030 (Figure 6). If the HIV susceptibility in MSM is also reduced by a third then inci- dence would decrease by 43.9% (14.9 to 76.0%), while it decreases by 68.3% (42.0 to 88.6%) if susceptibility reduces by 66%. This captures what could be achieved from putting 40% of HIV-negative MSM on PrEP and reducing the number of non-condom protected sex acts by 40%. However, further decreases in FSW or general population susceptibility (by a third) or increases in ART coverage in the general population (so 74% are virally suppressed) will not add much more impact, with these interventions in combination decreasing the overall incidence by 82.4% (62.4 to 93.3%). This is due to the small contribution of these groups to HIV transmission in Dakar.

4 | DISCUSSION

Our findings suggest that unprotected anal sex between men, both through individuals who identify as cis-male and TGW, may be the main contributor to the HIV epidemic in Dakar, Senegal, with up to 64% of new HIV infections being pre- ventable if the HIV prevention and treatment needs of these individuals could be met. Conversely, unlike other low HIV prevalence settings in SSA, much fewer (< 15%) HIV infections are attributable to commercial sex between FSW and their cli- ents [10,11,14 ]. The greater role of MSM in Dakar is partly due to their greater number compared to FSW (1.2% of adult males compared to 0.5% of adult females in 2015) and much higher HIV prevalence (29.7% for MSM compared to 6.6% for FSW in 2016), with this disparity being due to long-term pre- vention activities among FSWs in Dakar, but not MSM. In addition, the heterosexual activity of MSM is also important; stopping this mode of transmission could prevent 37% of new HIV infections from 2015 to 2025. These results are useful for planning intervention strategies going forward, with most impact being achieved from expand- ing interventions among MSM, including cis-male and TGW. These data suggest that increasing ART provision to MSM could reduce HIV incidence by 15% if the proportion of MSM living with HIV who are virally suppressed doubled from 35%

Table 2. Population attributable fraction for sex between men and commercial sex. The population attributable fraction is defined as the proportion of HIV infections prevented if the HIV transmission risk due to sex between men or commercial sex was removed from 1995, 2005 or 2015 for 1 or 10 years

1995

2005

2015

PAF (1 year)

Sex between men

36.2% (21.5% to 52.5%)

28.9% (13.3% to 42.8%)

51.4% (27.3% to 66.7%)

Commercial sex

19.8% (8.3% to 38.7%)

21.6% (8.8% to 36.9%)

13.8% (5.1% to 31.1%)

PAF (10 years)

Sex between men

42.1% (23.7% to 59.0%)

44.6% (20.5% to 61.4%)

64.1% (37.4% to 79.4%)

Commercial sex

20.6% (7.3% to 38.7%)

20.3% (7.6% to 40.1%)

13.6% (4.8% to 35.0%)

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

(a)

Baseline (median) Baseline (95%CI) Data (with 95%CI) No ART No condom use 1985 1995 2005
Baseline (median)
Baseline (95%CI)
Data (with 95%CI)
No ART
No condom use
1985 1995
2005
2015
HIV prevalence FSW (%)
0
10
20
30
40

(b)

Time (years)

Baseline (median) Baseline (95%CI) Data (with 95%CI) No ART No condom use 1985 1995 2005
Baseline (median)
Baseline (95%CI)
Data (with 95%CI)
No ART
No condom use
1985 1995
2005
2015
HIV prevalence MSM (%)
0
20
40
60
80
100

(c)

Time (years)

Baseline (median) Baseline (95%CI) Data (with 95%CI) No ART No condom use 1985 1995 2005
Baseline (median)
Baseline (95%CI)
Data (with 95%CI)
No ART
No condom use
1985 1995
2005
2015
Overall HIV prevalence (%)
0.0
0.5
1.0
1.5
2.0

Time (years)

Figure 5. Projections of the impact of removing existing levels of antiretroviral therapy (ART) and condom use on HIV prevalence trends for (a) female sex workers (FSW), (b) all men who have sex with men (MSM) and (c) overall general population prevalence. Fig- ures show baseline (median with 95% credibility intervals) trends, and median trends with no effect of ART (median-blue) or no con- dom use (median-orange).

to 74%. In addition, reducing their susceptibility to HIV infec- tion could also have important benefits, with the successful introduction of PrEP among MSM possibly reducing HIV inci- dence by a further 30 percentage points, and an expansion of condom use having similar benefits. Such interventions, on

their own and in combination with ART scale-up have been shown to be effective [46,50-53 ], cost-effective[ 54,55 ] and feasible among MSM, and so their expansion should not be delayed. As same-sex practices remain criminalized in Senegal, and MSM face discrimination [56 ], it is also important that effective stigma mitigation interventions are combined with these interventions to ensure their effectiveness [25 ]. Our findings suggest little impact is achieved from reducing risk or increasing ART coverage among other population sub- groups, including FSW, further emphasizing the need to focus new interventions on MSM. However, this is contingent on sustained high levels of condom use and ART uptake among FSW. That is, our results do not suggest that efforts should be transferred from existing interventions to refocus on MSM interventions, but rather that additional efforts are focused on MSM. Indeed, our projections emphasize existing interventions have had considerable impact, halving HIV prevalence com- pared to what it could have been in 2017.

5 | STRENGTHS AND LIMITATIONS

Strengths of our analysis include the use of detailed setting-spe- cific data from numerous bio-behavioural surveys among FSW, their clients and MSM from 1985 to 2015, as well as two gen- eral population surveys from 2005 and 2010. In addition, the inclusion of MSM in our modelling improves on previous models that have frequently ignored MSM based on assumptions of decreased relevance across Sub-Saharan Africa [57 ], and rarely included them in dynamic PAF estimates [9,58 ]. Lastly, another key strength in our analyses is the accuracy of our model pro- jections compared to data that were not fitted, which included two-thirds of available HIV prevalence estimates. Despite using best available data, this model has several limitations. It did not incorporate any commercial sex among MSM due to limited data. Fortunately, including commercial sex among MSM would not have changed our general results since the HIV infections would still be attributed to same-sex practices. The model also did not explicitly include TGW because of insufficient data to do so. However, the 2016 MSM survey used to parameterize and calibrate the model included some TGW, as did the MSM size estimation data used by the model, and so their contribution was cap- tured to an extent by the model. Moving forward, these analyses and associated bio-behavioural surveys need to better assess gender identity to enable a better assessment of their role in HIV transmission. The modelling was also limited by uncertainty in many model parameters. In addi- tion, differences in the condom use and behavioural mea- sures used by studies made it hard to evaluate temporal changes in risk. To account for these uncertainties, we asso- ciated wide ranges to all uncertain parameters and trends in condom use and risk behaviours, and used Bayesian fit- ting methods to account for and constrain this uncertainty through calibrating to HIV prevalence data. Importantly, our findings were robust to this uncertainty. Another limitation of our analysis was the relative simplicity of the model with respect to HIV natural history, the portrayal of ART and heterogeneity in sexual behaviours among each sub-population. Although greater detail has been included in other models, there is no consensus on the appropriate level

Mukandavire C et al. Journal of the International AIDS Society 2018, 21 (S5):e25126 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25126/full | https://doi.org/10.1002/jia2.25126

Scale to Reduce Baseline up

MSM

two FSW susceptibility

susceptibility

of susceptibility

coverage

in

2020

a third

a by third Scale

2020

thirds

by a third

susceptibility

ART

by

low risk to 74% by

by

by Reduce

up ART

74%

MSM

low risk groups

Reduce

MSM

Reduce

of

of

0.8 0.6 0.4 0.2 0.0 Overall HIV incidence per 1000 pyrs
0.8
0.6
0.4
0.2
0.0
Overall HIV incidence
per 1000 pyrs
0.6 0.4 0.2 0.0 Overall HIV incidence per 1000 pyrs Figure 6. Effect of changes in

Figure 6. Effect of changes in antiretroviral therapy (ART) coverage or susceptibility to infection (due to pre-exposure prophylaxis (PrEP) or increases in condom use) from 2017 to 2030 on overall projected HIV incidence per 1000-person years in 2030. The plots show median and 95% credibility intervals of the projections. Sce- narios included are additive on top of the previous scenarios from left to right, firstly including baseline projections, then projections with scale-up of ART coverage in men who have sex with men (MSM) from 2017 such that 74% of MSM living with HIV are virally suppressed by 2020 (same as female sex workers (FSW)), reduce susceptibility of MSM by 33% and then 66% (similar to increase condom use or PrEP coverage in MSM), reducing susceptibility of FSW by 33%, scale-up ART coverage in low risk such that 74% are virally suppressed by 2020 and reduce susceptibility of low-risk groups by 33%.

of complexity for specific models. One specific simplification is not stratifying MSM by whether they normally have insertive or receptive anal sex. This was done to avoid overly complicat- ing the model, which should not have affected our results because they have the same sexual behaviour with females; the main indirect mechanism for MSM contributing to overall HIV transmission. Lastly, the model only considered Dakar. Although this limits the generalizability of the findings, it does increase the likely pre- cision of the modelling because we did not make generalizing assumptions to produce an average portrayal of the Senegal epi- demic. Despite the limited scope of the analysis, it is still likely that the results are relevant to the whole of Senegal because the HIV prevalence in MSM is generally high and increasing, while it is lower and decreasing among FSW. In addition, our analyses are also likely relevant to other West African settings with growing epidemics in MSM, similar or lower HIV prevalence in FSW [3,4 ], and similar reporting of heterosexual sex among MSM [59 61 ].

6 | CONCLUSION AND IMPLICATIONS

Previous analyses have shown a large role for commercial sex in some sub-Saharan HIV epidemics [ 10-14 ], but this is the first to suggest that MSM, including individuals who identify as cis-male and TGW, could also be having an important role in some lower- and middle-income country settings, where other analyses have suggested a small role [14,15,62 ]. This is likely due to the

different behavioural and epidemiological situation among MSM in Dakar compared to these other settings. Although existing interventions have been successful in reducing HIV transmission, including early increases in condom use and recent scale-up of ART among FSW, public health efforts are now needed to address the ongoing unmet need among MSM. This unmet need is resulting in MSM in Senegal and other settings in SSA experi- encing uncontrolled HIV epidemics with high prevalence [57 ], which is driving HIV transmission in this setting and could be elsewhere. Scaling up prevention and treatment interventions for MSM should now be a high priority, with these initiatives needing to be sensitive to the legal context, and associated stig- mas or discrimination that MSM experience. Without this policy shift, the HIV epidemics among MSM in Senegal and elsewhere in SSA are unlikely to decrease.

AUTHORS AFFILIATIONS

1 Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK; 2 Department of Infectious Disease Epidemiology, Imperial College, London, UK; 3 Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA; 4 Enda Sante, Dakar, Senegal; 5 Institut de Recherche en Sant e, de Surveillance Epidemiologique et de Formations, Dakar, Senegal; 6 St Michaels Hospital, University of Toronto, Toronto, Canada; 7 Divi- sion de La Lutte Contre Le Sida et Les IST, Ministry of Health, Dakar, Senegal; 8 Department of Health, National AIDS Council of Senegal, Dakar, Senegal; 9 Col- lege of Engineering, Mathematics and Physical Sciences, University of Exeter, Exeter, UK

COMPETING INTERESTS

The authors have no competing interests.

AUTHORS CONTRIBUTIONS

PV, MCB, SB, SM and SS conceptualized the study. CM performed the model analyses and wrote the first draft of the manuscript with PV. CM and LD devel- oped the model and reviewed the literature for data sources for the model, helped by the Senegal and JHU team. PV supervised the model analyses. SB, SS, DD, CL, BL, NLD, FD, KC, RSMM, ST, PAND, CT and CN collected or con- tributed data for the modelling. JW and LD undertook data analyses for param- eterizing and calibrating the model. All authors contributed to data interpretation, writing the manuscript and approved the final version.

ACKNOWLEDGEMENTS

FUNDING

This publication resulted in part from research funded by a supplement to the Johns Hopkins University Center for AIDS Research, an NIH-funded pro- gramme (P30AI094189) with support specifically from the Office of AIDS Research (OAR). The programme also received support from Linkages across the Continuum of HIV Services for Key Populations Affected by HIV project (LINKAGES, Cooperative Agreement AID-OAA-A-14-00,045) and the parent study HIV Prevention 2.0 (HP2): Achieving an AIDS-Free Generation in Sene- gal (AID-OAA-A-13-00,089). The supplement, LINKAGES and HP2 received support from the United States Agency for International Development (USAID) and the U.S. Presidents Emergency Plan for AIDS Relief (PEPFAR). PV also acknowledges support from the National Institute of Health Research Health Protection Research Unit in the Evaluation of Interventions. SM is supported by a Canadian Institutes of Health and Ontario HIV Treatment Network Research New Investigator Award. The content is solely the respon- sibility of the authors and does not necessarily represent the official views of any of the funding agencies.

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the online version of this article:

Data S1. Supplementary materials. Table S1. Details of surveys used to parameterise and cali- brate the model for different risk groups in Dakar

Table S2. (a) Demographic, sexual and behavioural parameters

of female sex workers, clients, MSM and low risk populations.

(b) HIV epidemiological parameters Figure S1. Modelled condom use trends for female sex work- ers (FSW) and men who have sex with men (MSM). (a) FSW condom use with commercial partners for vaginal intercourse.

Assume condom use for anal intercourse (AI) is half that of vaginal intercourse (VI) for all the years. (b) FSW condom use with main partners for VI. Condom use for anal intercourse (AI) with main partners is assumed to be 0.6 to 1.0 times that for VI. FSW condom use with casual partners for VI is 1 to

1.5 times that for main partners VI; AI with casual partners is

0.6 to 1.0 times that for VI with casual partners. (c) MSM con-

dom use with male regular and casual partners. Assume some

bias in reporting so all rates are multiplied by a bias factor of

0.7 to 1.0 lower bound of 0.7 chosen to give overall lower

bound of 0.5. (d) MSM condom use with female main and casual partners. Condom use is assumed to be the same for

VI and AI.

Figure S2. ART coverage in Senegal from 2000 from UNAIDS AIDS info [44] and World Bank [43] Figure S3. Analysis of covariance results of parameters that contribute more than 4% variability to the 2015 (a) 10-year commercial sex PAF and (b) 10-year MSM PAF.

Lillie TA et al. Journal of the International AIDS Society 2018, 21 (S5):e25125 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25125/full | https://doi.org/10.1002/jia2.25125

(S5):e25125 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25125/full | https://doi.org/10.1002/jia2.25125 COMMENTARY
(S5):e25125 http://onlinelibrary.wiley.com/doi/10.1002/jia2.25125/full | https://doi.org/10.1002/jia2.25125 COMMENTARY

COMMENTARY

Think global, act local: the experience of Global Fund and PEPFAR joint cascade assessments to harmonize and strengthen key population HIV programmes in eight countries

Tiffany A. Lillie 1 § , James Baer 2 , Darrin Adams 3 , Jinkou Zhao 4 and R. Cameron Wolf 5

§ Corresponding author: Tiffany A. Lillie, FHI 360, 1825 Connecticut Avenue NW, Washington, DC 20009, USA. Tel: +1 202 884 8851. ( tlillie@fhi360.org )

Abstract

Introduction: The Global Fund and the US President s Emergency Plan for AIDS Relief (PEPFAR) are major donors to HIV services with key populations (KPs) to achieve the UNAIDS 95-95-95 epidemic control goals. The programmes they fund are

not always well aligned or coordinated, decreasing their effectiveness. Joint assessments are designed and led by LINKAGES,

a project funded by PEPFAR and the US Agency for International Development, to improve coordination among donors and

on-the-ground implementation of KP HIV programmes. Joint assessments help identify barriers that prevent KPs from access-

ing interventions along the cascade of prevention, diagnosis and treatment services, and provide recommendations to improve and align programmes. Detailed reports from eight assessments in Malawi, Cameroon, Swaziland, Haiti, Angola, Nepal, Cote^ d Ivoire and Botswana were analysed for thematic challenges, and recommendations are presented. The purpose of the paper

is to identify commonalities across KP HIV programmes that were found through the assessments so others can learn and

then strengthen their programmes to become more effective. Discussion: The joint cascade assessments offered countries feedback on HIV programme challenges and recommendations for strengthening them at national, subnational and local levels. Shared intervention areas included: (1) robust population size estimates to inform service delivery targets and to budget resources for KP outreach; (2) accessible and KP-friendly services most relevant to individuals to increase retention in the HIV cascade; (3) decentralized, community-based services for HIV testing and antiretroviral therapy, and new approaches including self-testing and PrEP; (4) addressing structural issues of stigma, discrimination and violence against KPs to create a more enabling environment; and (5) more effective and continual tracking of KPs across the cascade, and coordinated, harmonized monitoring tools and reporting systems between donor- funded and national programmes. Conclusions: The assessment teams and country stakeholders viewed the assessments as a best practice for coordinating donor- funded programmes that may overlap or inefficiently serve KPs. Global and national HIV programmes need investments of time, resources, and commitment from stakeholders to continually course-correct to align and improve programmes for sustained impact. The type of continued partnership demonstrated by the joint assessments is key to address HIV among KPs globally.

Keywords: HIV; key populations; assessment; donors; collaboration

Received 11 December 2017; Accepted 16 May 2018 Copyright © 2018 The Authors. Journal of the International AIDS Society published by John Wiley & sons Ltd on behalf of the International AIDS Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

1 | INTRODUCTION

In all countries affected by the HIV epidemic, key populations (KPs) including sex workers, men who have sex with men (MSM), people who inject drugs, transgender people, and peo- ple in prisons and other closed settings bear a dispropor- tionate burden of HIV infection [1-5 ] and face formidable barriers to accessing services for HIV prevention, diagnosis, treatment and care. These barriers include stigma and discrim- ination, restrictive laws, violence and human-rights violations [6 ]. Many KP HIV programmes have insufficient scale, scope and quality to overcome these barriers. KPs are a high priority in efforts to prevent new HIV infections and achieve the

ambitious UNAIDS 95-95-95 treatment goals by 2030 [ 7]. The Global Fund to Fight AIDS, Tuberculosis and Malaria (GF) and the US President s Emergency Plan for AIDS Relief (PEP- FAR) are working to improve KP programmes based on World Health Orga