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Adolescent girls and young women: key populations for HIV epidemic control

Adolescent girls and young women: key populations for HIV epidemic control Introduction: At the epicentre of the HIV epidemic in southern Africa, adolescent girls and young women aged 1524 contribute a disproportionate 30% of all new infections and seroconvert 57 years earlier than their male peers. This agesex disparity in HIV acquisition continues to sustain unprecedentedly high incidence rates, and preventing HIV infection in this age group is a pre-requisite for achieving an AIDS-free generation and attaining epidemic control. Discussion: Adolescent girls and young women in southern Africa are uniquely vulnerable to HIV and have up to eight times more infection than their male peers. While the cause of this vulnerability has not been fully elucidated, it is compounded by structural, social and biological factors. These factors include but are not limited to: engagement in age-disparate and/or transactional relationships, few years of schooling, experience of food insecurity, experience of gender-based violence, in- creased genital inflammation, and amplification of effects of transmission co-factors. Despite the large and immediate HIV prevention need of adolescent girls and young women, there is a dearth of evidence-based interventions to reduce their risk. The exclusion of adolescents in biomedical research is a huge barrier. School and community-based education programmes are commonplace in many settings, yet few have been evaluated and none have demonstrated efficacy in preventing HIV infection. Promising data are emerging on prophylactic use of anti-retrovirals and conditional cash transfers for HIV prevention in these populations. Conclusions: There is an urgent need to meet the HIV prevention needs of adolescent girls and young women, particularly those who are unable to negotiate monogamy, condom use and/or male circumcision. Concerted efforts to expand the prevention options available to these young women in terms of the development of novel HIV-specific biomedical, structural and behavioural interventions are urgently needed for epidemic control. In the interim, a pragmatic approach of integrating existing HIV prevention efforts into broader sexual reproductive health services is a public health imperative. Keywords: HIV prevention; adolescent girls; young women; prevention interventions. Received 22 August 2014; Revised 27 November 2014; Accepted 18 December 2014; Published 26 February 2015 Copyright: – 2015 Dellar RC et al; licensee International AIDS Society. This is an Open Access article distributed under the terms of the Creative Commons Attribution 3.0 Unported (CC BY 3.0) License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. nearly 30% of all new HIV infections in the region [1,5,6]. In Introduction Southern Africa is at the epicentre of the global HIV epi- South Africa, this percentage translates to 113,000 new demic, bearing almost 40% of the global burden of infection infections in young women per year, more than four-times despite being home to less than 2% of the global population the number contributed by their male peers (Figure 1) [5]. [1]. In this endemic setting, the dominant mode of transmis- Such disproportionately high HIV incidence in young women sion is through heterosexual sex. UNAIDS has described the compared to young men is explained by a striking and char- epidemic as a generalized and hyper-endemic to reflect the acteristic feature of the HIV epidemic in this region: the age continued unprecedentedly high (10%) population preva- sex disparity in HIV acquisition, wherein young women lence [1,2]. However, generalizability should not be equated acquire HIV around five to seven years earlier than young to uniformity, as significant heterogeneity exists in terms of men, often synonymously with sexual debut (Figure 2) [5,7]. As a result of the agesex disparity in HIV acquisition, HIV where and in whom HIV infections occur, with certain localities and populations being consistently more vulnerable to infec- prevalence in young women is high, and represents a sub- stantial treatment burden [5,8]; for example, between 2009 tion than others [1,3]. Focusing HIV prevention efforts on such high-incidence locations and populations is likely to enable the and 2013, 27% of women less than 20 years attending ante- greatest gains to be made in altering current epidemiological natal clinics in a rural sub-district of KwaZulu-Natal were found to be HIV positive (unpublished). On a population level, the high trajectories toward control of the HIV epidemic [4]. An important key population in the southern African incidence in young women is sustaining intergenerational trans- setting is young women aged 1524 years, who contribute mission of HIV and contributes to the overall disproportionate 64 Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 HIV incidence (%) by age and sex burden of HIV in women compared to men [9]. Indeed, 3.0 approximately 60% of all people living with HIV in sub-Saharan 2.5 Africa are women [1]. Clearly, achieving the goal of an ‘‘AIDS- free generation’’ depends on reducing the burden of new 2.0 infection in this key population [10]. 1.5 However, despite the imperative to prevent HIV acquisition in young women, there remains a paucity of evidence-based 1.0 interventions available to this population. Indeed, current 0.5 options are typically limited to promotion of abstinence (or delayed sexual debut), behaviour change, and condom use, 0.0 Female 15–24 Male 15–24 Female 25+ Male 25+ all of which are somewhat challenging given the underlying Age and sex gender-power dynamics of the southern African setting [10]. Further, whilst there has been great optimism following the recent demonstrations of the prevention potential of antire- Proportion of new infections by age and sex trovirals (ARVs)  both prophylactically to prevent HIV acqui- sition (pre-exposure prophylaxis, or PrEP) and for treatment to minimise onward transmission (treatment as prevention, TasP)  to date none of the PrEP trials have included par- Female 15–24 ticipants B18 years of age, and as such it seems unlikely that 26% 28% Male 15–24 these advances will be of benefit to the full range of those considered young women (see Box 1) in the immediate future Female 25+ [10,11]. Male 25+ 6% Box 1. Defining young women. 40% The standard definition of young women includes all those falling within the ages of 1524 years. As such, most epidemiological data, and much of the discussion here, is presented in terms of this age stratification. Figure 1. Disproportionate HIV incidence in young women in South Africa. It is, however, important to note that between these Adapted from Shisana et al. [5]. ages, young women undergo significant transitions in lifestyle, maturity, and legal rights which will place them HIV prevalence by age and sex, South Africa 2012 at different vulnerabilities at different time points. Females Males It is likely that the significance of the B18 years vs. 18 years divide will increase in significance with the rollout of PrEP, as few safety studies for PrEP interven- tions have been conducted in adolescents B18 years. As such, we would like to encourage the use of this and other sub-strata by those reporting on HIV surveillance in young people. Moreover, a crucial step in addressing the public health 0–14 15–19 20–24 25–29 30–34 35–39 40–44 45–49 50–54 55–59 60+ imperative to reduce HIV acquisition in young women is the Age group (years) validation of the safety of existing technologies and interven- tions for HIV prevention in young women B18 years [10,12]. HIV prevalence by age and sex, KwaZulu Natal high school students 2010 Concurrently, a concerted effort is required to better under- Males Females stand both the biological and structural factors driving the heightened vulnerability to HIV infection in young women more broadly. Such efforts, in parallel with a consolidation of the evidence obtained from adolescent- and youth-focused HIV prevention interventions and programmes conducted to date, should serve to inform the development of more efficacious interventions. The objective of this review is to provide an overview of the state-of-the-science of HIV prevention in young women and <16 16–17 18–19 >19 adolescent girls to inform policy and research direction. Age group (years) Specifically, we aim to (1) summarise the various behavioural and biological factors that predispose adolescent girls and Figure 2. Agesex disparity in HIV acquisition. Adapted from Shisana et al. [5] and Abdool Karim et al. [8]. young women to HIV infection, (2) briefly review the evidence HIV prevalence (%) HIV prevalence (%) HIV incidence (%) Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 from previous HIV prevention interventions targeted toward young women become infected after just a few coital en- adolescent girls and young women, and (3) discuss future counters, and on a population level, acquisition seems almost directions for HIV prevention in adolescent girls and young synonymous with sexual debut [17,36]. As such, there has women. been significant investigation into potential biological fac- tors that might augment behavioural risk, and a number of mechanisms have been hypothesised to result in heightened Discussion vulnerability to infection in young women, compared both to Why are adolescent girls and young women so vulnerable men and to older women. to HIV infection? For example, a number of studies focused on sero- Socio-behavioural associations of HIV infection in adolescent discordant couples have highlighted a higher per-act risk of girls and young women HIV acquisition in women compared to men [3740]. A portion Arguably the most convincing driver of the agesex disparity of this effect may be attributed to the higher viral load typically in HIV acquisition observed in sub-Saharan Africa is the high observed in men, but the phenomena may also be explained prevalence of intergenerational relationships between young at least in part by physical factors that result in increased women and older men [13,14]. The aggregating prevalence of exposure to HIV in women, compounded both from the com- HIV with increasing age means that, ceterius paribus, a young paratively larger surface area of the cervico-vaginal mucosa girl engaging in a sexual relationship with an older man is at and from the increased HIV mucosal exposure time (semen can much higher risk of HIV acquisition compared to a young remain in the female genital tract up to three days post-coitus) girl engaging with a male peer (Figure 2) [5]. Further, a young [41,42]. The higher per-act risk of HIV acquisition in women woman engaging in a relationship with an older man may be could also result from the relatively high levels of activation less likely to negotiate condom use given the gender-power of the immune cells in the female genital tract, the increased dynamics in the southern African setting, further augment- expression of HIV co-receptors in cervical cells compared ing her risk [13,15]. Consistent with these data, a number to foreskin cells, and/or a mucosal surface more likely to of studies have demonstrated that engagement in an age- acquire micro-abrasions during sex: together, these factors disparate or intergenerational relationship is strongly asso- result in more accessible portals for HIV entry in women ciated with increased HIV prevalence in young women [35,4346]. [13,1618]. Further work is needed to understand how this Further, young women are more susceptible to HIV infection association may be changing over time with increasing ARV compared to older women, and there are a number of bio- therapy (ART) coverage, and survival of both HIV infected logical factors that have been promulgated to explain this age- men and women over 25 years of age. variability in vulnerability. For example, the immature cervix Understanding the complex factors that drive adolescent has a greater proportion of genital mucosa exposed to HIV girls and young women to engage in sexual relationships that is highly susceptible to infection, and young women with older men is challenging, but may be critical in terms have relatively high levels of genital inflammation which have of adequately addressing the prevention needs of these consistently been reported to increase HIV acquisition risk key populations. In many cases, young women have reported [23,35,4749]. feeling flattered by the attention of older men, and many re- When considering the apparently uniquely high per-act lationships are likely to be built on genuine romantic con- HIV acquisition risk in young women, it is also necessary to nections [19,20]. In other instances, young women may be consider other relevant contextual factors that may mediate motivated primarily by the increased financial or social capital available through engaging in relationships with older men; the infection environment, including other sexually trans- indeed, many adolescent girls and young women report in- mitted infections (STIs) and contraceptive use. For example, volvement in these ‘‘transactional relationships,’’ which have many bacterial and viral STIs are associated with increased significant additional implications for HIV risk [21,22]. risk of HIV infection, and are much more prevalent in young Beyond engagement in age-disparate relationships, other women compared to young men [50,51]. A recent school- risk factors for HIV infection in young women include early based survey conducted in rural KwaZulu-Natal, South Africa, sexual debut, few years of schooling, food insecurity, loss found the trend in herpes simplex virus-2 (HSV-2) acquisition of a family member, and experience of gender-based violence to mirror the agesex disparity in HIV infection, with young [8,17,2328]. Many of these factors may mediate their ef- female students acquiring HSV-2 soon after sexual debut, and fects on HIV acquisition via increasing the relative value a more than three-fold higher prevalence of HSV-2 compared of financial capital available through engagement in transac- to their male peers (Figure 3) [8]. Interestingly, recent HSV-2 tional relationships with older men [21,2932]. However, infection may confer the greatest impact in terms of in- independent pathways of risk mediation are also likely to exist. creasing vulnerability to HIV, such that the female genital Food insecurity, for example, may also make young women tract in the immediate years following HSV-2 acquisition may biologically more susceptible to HIV [33]. be particularly susceptible to HIV infection [52,53]. Beyond STIs, other biological risk factors may also be amplified in young women. For example, one study has shown Possible biological mechanisms for heightened vulnerability that the use of the hormonal contraceptive depot medrox- to HIV infection in adolescent girls and young women yprogesterone acetate (DMPA) increases the risk of HIV The per-coital act HIV incidence rate in adolescent girls and young women is so high that it seems unlikely that it can be acquisition in young women (1824 years), while decreasing explained by behavioural risk alone [34,35]. Indeed, many HIV acquisition risk in older women (]25 years) [54]. Further, 66 Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 HSV-2 prevalence by age and sex, KwaZulu Natal behavioural intervention. However, the burden of HIV in high school students 2010 school-attending adolescents, while lower than out-of-school Males Females adolescents, remains significant, and thus there is also con- cern that the results might point to differential desirability bias by trial arm, which questions the validity of significant changes in self-reported markers of behaviour change re- ported by other studies. The data from school-based trials also underscore that while knowledge is a pre-requisite 10 for HIV prevention, it is in itself insufficient to prevent HIV infection. <16 16–17 18–19 >19 Age group (years) Attempts to make health services youth-friendly Other interventions to prevent HIV infection in young people Figure 3. Agesex disparity in HSV-2 acquisition. have focused on health systems strengthening in an effort to Adapted from Abdool Karim et al. [8]. address barriers to healthcare access by increasing the pro- vision of high-quality, youth-friendly HIV and SRH services. although establishing causal relationships is challenging, Such interventions are potentially critical, as there is sig- intra-vaginal cleaning practices are more prevalent in younger nificant demand for more comprehensive SRH services that women, suggesting these women are consequently more likely recognise the inter-relationships between HIV and broader to have an altered vaginal flora, potentially heightening their SRH and thus the importance of integrated service delivery HIV susceptibility [55,56]. [1,57]. Together these biological factors may create a ‘‘perfect Interventions to make health services more youth-friendly storm’’ of conditions in recently sexually debuted adoles- have typically focused on a different combinations of training cent girls and young women in southern Africa making them of service providers, outreach activities, and provision of uniquely vulnerable to HIV infection when exposed to the mobile services targeted toward specific high-risk adolescent virus via engaging in unprotected sex with an HIV-positive populations [66,7577]. Many of these interventions have partner. been successful in terms of increasing uptake of services Effectiveness of current HIV prevention interventions by young people. However, similarly to in-school interven- available to adolescent girls and young women tions, there is a notable dearth of biological-outcome-based In-school interventions assessment. Schools provide convenient venues for HIV prevention edu- cation, and not surprisingly a vast number of youth-targeted Community-level interventions HIV, STI, and pregnancy prevention programmes operate in HIV prevention interventions implemented at the community schools throughout sub-Saharan Africa [57]. The effectiveness level are highly heterogeneous, including sporting events, of such programmes in young people in sub-Saharan Africa mentoring and youth centres [78]. Evaluation of these in- has been the subject of a considerable number of systematic terventions highlights their largely positive impact on knowl- reviews [5871]. To summarise the evidence, several pro- edge and attitudes to HIV. However, these interventions grammes have been demonstrated to be effective in improv- often fail to reach the most HIV vulnerable populations, and ing knowledge and attitudes concerning HIV and the uptake of evaluation designs are generally weak. Only one study to our HIV testing. These data follow a general trend in sub-Saharan knowledge has assessed HIV incidence, and this study reported Africa of increasing comprehension and understanding about no evidence of effectiveness [79]. HIV in young people [1]. Those interventions demonstrating the most success are characterised by a number of factors, Conditional cash transfers including but not limited to: iterative and context-specific Cash transfers to young people that incentivise safer behaviour session programmes, HIV prevention and sexual and repro- have recently emerged as a new strategy to reduce young ductive health (SRH) curricula that include tasks focused people’s vulnerability to HIV [1,80]. The evidence in support of toward more general skills and knowledge development, the efficacy of this strategy is limited but promising. Indeed, and delivery by trained facilitators [57]. In contrast, abstinence- a recent randomized controlled trial in Lesotho demonstrated only and peer-led in-school interventions tend to be ineffective that a programme of financial incentives reduced the prob- [57,62]. ability of acquiring HIV by 25% over two years [81]. Similarly, an Despite some apparent successes, few rigorously con- independent randomized controlled trial in Malawi reported ducted trials have assessed the impact of interventions that those female high school students who received con- on biological outcomes, including HIV, STI and/or pregnancy ditional cash transfers (CCTs) were 64% less likely to be HIV incidence. Those trials that have demonstrated no significant infected compared to those who were not [82]; however, effects of any school-based intervention on these biological baseline HIV infection was not measured. These data suggest outcomes, in spite of reporting positive impacts on self- reported behaviour change in adolescents [7274]. These a potential for CCT to prevent HIV in young people, and results may stem from the relatively strong prevention effect outcomes of current research in the field such as HPTN 068 of being in school itself, which may dwarf the effect of any are eagerly awaited. HSV-2 prevalence (%) Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 Gaps and future directions more than 44,000 infections in one year. Implementation and Despite the large and immediate need for HIV prevention policy science are urgently needed to translate research on in adolescent girls and young women, there is a dearth of PrEP effectiveness into averted infections. Further, there is evidence-based interventions available to them to reduce also work to be done in ensuring that on rollout, the state- of-the-science of prevention is not lagging behind in adoles- their risk. Given the diversity of epidemics within and between cents B18 years because of restrictive ethico-legal guidelines countries, in order to develop more efficacious youth-focused that often prevent them from participating in biomedical prevention interventions, a sound understanding of the local research in spite of their substantial need [6,10]. epidemic is required as well as the bio-behavioural nexus This review was restricted to considering HIV prevention in that renders adolescent girls and young women more vulner- adolescent girls and young women. However, the treatment able to HIV infection. The significant SRH needs of young needs resulting from the unprecedentedly high HIV incidence women should be central to the design of new interventions, rates in these key populations should not be underestimated: as integration of services is the backbone of a pragmatic ap- in Lesotho for example, almost a quarter of all young people proach to address needs now, even as we refine, develop and aged 1524 years are infected with HIV [1]. Adolescent- test new and novel approaches [1,83]. A careful review of focused HIV prevention interventions should also seek to previous interventions and their evaluations is needed to meet the needs of HIV-positive young people who face ensure maximum gains. Most notably, it is critical that any significant barriers to care. Indeed, of note is that adoles- future intervention should be rigorously assessed for effec- cents (1019 years) are the only age group in which AIDS tiveness in controlled trials with biological outcomes prior deaths have risen between 2001 and 2012 [1]. to wide-scale implementation to maximise efficiency and effectiveness of resource allocation. Many researchers would benefit from engaging the young women themselves as part- Conclusions ners in intervention design and implementation, and certainly Meeting the HIV prevention and SRH needs of adolescent encouraging male partner buy-in and female empowerment girls and young women who are at uniquely high risk of HIV will also be important in those settings where gender-power acquisition is a public health and moral imperative and a dynamics augment HIV risk. requirement to meet the laudable goals of achieving an AIDS- A further important direction for future research should be free generation and/or epidemic control. However, despite to develop interventions targeted to hard-to-reach young this imperative, evidence-based prevention options available people who might be missed by school- or community-based to adolescent girls and young women remain limited, and even interventions. The evidence for the best practice in reaching as efforts get underway to develop more efficacious interven- such populations is particularly limited, despite their often tions, they are likely to take many years to reach fruition. greater risk of HIV acquisition. However, our own experiences Immediate action is therefore needed to facilitate this key highlight that some important components of making service population to mediate their own risk, including as first steps provision palatable and attractive to hard-to-reach adoles- rollout of PrEP, adolescent enrolment in biomedical HIV cents include anonymized testing, flexible clinic hours and prevention trials, and provision of accessible and integrated adaptions of respondent-driven sampling. Concurrently, ef- SRH-HIV prevention services. forts should be made to keep adolescents in school. The task of developing and evaluating new HIV prevention interven- Authors’ affiliations tions  particularly those programmes that aim to address Centre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, the underlying social vulnerabilities  is substantial, and will South Africa; Department of Epidemiology, Mailman School of Public Health, potentially require decades of concentrated action, during Columbia University, New York, NY, USA which time adolescent girls and young women will continue Competing interests to become infected in their hundreds of thousands. As such, The authors declare that no competing interests exist. it is a moral imperative to effectively deliver what we know works now. The most pressing example of a technology that Authors’ contributions we know works but is not being delivered is PrEP, which was RD, SD, and QAK conceptualized the article. RD prepared the final draft, with contributions and revisions made by SD and QAK. All authors have read and developed specifically with young women in southern Africa approved the final version. in mind: designed to allow them to exercise their rights over their health and take control over their own risk without Author information dependence on their sexual partners. While the number of RD is a research fellow at CAPRISA supported by the CAPRISA Training Programme. randomized controlled trials demonstrating the effectiveness Acknowledgements of PrEP continues to grow, this success has yet to be translated CAPRISA was established as part of the Comprehensive International Program of into product availability in southern Africa. Undeniably, PrEP Research on AIDS (CIPRA) and is supported by the National Institute of Allergy is not 100% effective, is limited by adherence and would and Infectious Disease (NIAID), National Institutes of Health (NIH) and the US Department of Health and Human Services (DHHS) (grant# 1 U19AI51794). benefit from improvements currently in development; how- ever, one has to question where the threshold of evidence References required for rollout of current forms of PrEP to young women 1. UNAIDS. Global report: UNAIDS report on the global AIDS epidemic 2013 in southern Africa lies. A simple calculation highlights that [cited 2014 Aug 14]. Available from: http://www.unaids.org/en/media/unaids/ even with a 39% efficiency, rollout of Tenofovir gel to young contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_ women aged 1524 years in South Africa alone might prevent 2013_en.pdf 68 Dellar RC et al. 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Adolescent girls and young women: key populations for HIV epidemic control

Journal of the International AIDS Society , Volume 18 (2Suppl 1) – Feb 26, 2015

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Abstract

Introduction: At the epicentre of the HIV epidemic in southern Africa, adolescent girls and young women aged 1524 contribute a disproportionate 30% of all new infections and seroconvert 57 years earlier than their male peers. This agesex disparity in HIV acquisition continues to sustain unprecedentedly high incidence rates, and preventing HIV infection in this age group is a pre-requisite for achieving an AIDS-free generation and attaining epidemic control. Discussion: Adolescent girls and young women in southern Africa are uniquely vulnerable to HIV and have up to eight times more infection than their male peers. While the cause of this vulnerability has not been fully elucidated, it is compounded by structural, social and biological factors. These factors include but are not limited to: engagement in age-disparate and/or transactional relationships, few years of schooling, experience of food insecurity, experience of gender-based violence, in- creased genital inflammation, and amplification of effects of transmission co-factors. Despite the large and immediate HIV prevention need of adolescent girls and young women, there is a dearth of evidence-based interventions to reduce their risk. The exclusion of adolescents in biomedical research is a huge barrier. School and community-based education programmes are commonplace in many settings, yet few have been evaluated and none have demonstrated efficacy in preventing HIV infection. Promising data are emerging on prophylactic use of anti-retrovirals and conditional cash transfers for HIV prevention in these populations. Conclusions: There is an urgent need to meet the HIV prevention needs of adolescent girls and young women, particularly those who are unable to negotiate monogamy, condom use and/or male circumcision. Concerted efforts to expand the prevention options available to these young women in terms of the development of novel HIV-specific biomedical, structural and behavioural interventions are urgently needed for epidemic control. In the interim, a pragmatic approach of integrating existing HIV prevention efforts into broader sexual reproductive health services is a public health imperative. Keywords: HIV prevention; adolescent girls; young women; prevention interventions. Received 22 August 2014; Revised 27 November 2014; Accepted 18 December 2014; Published 26 February 2015 Copyright: – 2015 Dellar RC et al; licensee International AIDS Society. This is an Open Access article distributed under the terms of the Creative Commons Attribution 3.0 Unported (CC BY 3.0) License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. nearly 30% of all new HIV infections in the region [1,5,6]. In Introduction Southern Africa is at the epicentre of the global HIV epi- South Africa, this percentage translates to 113,000 new demic, bearing almost 40% of the global burden of infection infections in young women per year, more than four-times despite being home to less than 2% of the global population the number contributed by their male peers (Figure 1) [5]. [1]. In this endemic setting, the dominant mode of transmis- Such disproportionately high HIV incidence in young women sion is through heterosexual sex. UNAIDS has described the compared to young men is explained by a striking and char- epidemic as a generalized and hyper-endemic to reflect the acteristic feature of the HIV epidemic in this region: the age continued unprecedentedly high (10%) population preva- sex disparity in HIV acquisition, wherein young women lence [1,2]. However, generalizability should not be equated acquire HIV around five to seven years earlier than young to uniformity, as significant heterogeneity exists in terms of men, often synonymously with sexual debut (Figure 2) [5,7]. As a result of the agesex disparity in HIV acquisition, HIV where and in whom HIV infections occur, with certain localities and populations being consistently more vulnerable to infec- prevalence in young women is high, and represents a sub- stantial treatment burden [5,8]; for example, between 2009 tion than others [1,3]. Focusing HIV prevention efforts on such high-incidence locations and populations is likely to enable the and 2013, 27% of women less than 20 years attending ante- greatest gains to be made in altering current epidemiological natal clinics in a rural sub-district of KwaZulu-Natal were found to be HIV positive (unpublished). On a population level, the high trajectories toward control of the HIV epidemic [4]. An important key population in the southern African incidence in young women is sustaining intergenerational trans- setting is young women aged 1524 years, who contribute mission of HIV and contributes to the overall disproportionate 64 Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 HIV incidence (%) by age and sex burden of HIV in women compared to men [9]. Indeed, 3.0 approximately 60% of all people living with HIV in sub-Saharan 2.5 Africa are women [1]. Clearly, achieving the goal of an ‘‘AIDS- free generation’’ depends on reducing the burden of new 2.0 infection in this key population [10]. 1.5 However, despite the imperative to prevent HIV acquisition in young women, there remains a paucity of evidence-based 1.0 interventions available to this population. Indeed, current 0.5 options are typically limited to promotion of abstinence (or delayed sexual debut), behaviour change, and condom use, 0.0 Female 15–24 Male 15–24 Female 25+ Male 25+ all of which are somewhat challenging given the underlying Age and sex gender-power dynamics of the southern African setting [10]. Further, whilst there has been great optimism following the recent demonstrations of the prevention potential of antire- Proportion of new infections by age and sex trovirals (ARVs)  both prophylactically to prevent HIV acqui- sition (pre-exposure prophylaxis, or PrEP) and for treatment to minimise onward transmission (treatment as prevention, TasP)  to date none of the PrEP trials have included par- Female 15–24 ticipants B18 years of age, and as such it seems unlikely that 26% 28% Male 15–24 these advances will be of benefit to the full range of those considered young women (see Box 1) in the immediate future Female 25+ [10,11]. Male 25+ 6% Box 1. Defining young women. 40% The standard definition of young women includes all those falling within the ages of 1524 years. As such, most epidemiological data, and much of the discussion here, is presented in terms of this age stratification. Figure 1. Disproportionate HIV incidence in young women in South Africa. It is, however, important to note that between these Adapted from Shisana et al. [5]. ages, young women undergo significant transitions in lifestyle, maturity, and legal rights which will place them HIV prevalence by age and sex, South Africa 2012 at different vulnerabilities at different time points. Females Males It is likely that the significance of the B18 years vs. 18 years divide will increase in significance with the rollout of PrEP, as few safety studies for PrEP interven- tions have been conducted in adolescents B18 years. As such, we would like to encourage the use of this and other sub-strata by those reporting on HIV surveillance in young people. Moreover, a crucial step in addressing the public health 0–14 15–19 20–24 25–29 30–34 35–39 40–44 45–49 50–54 55–59 60+ imperative to reduce HIV acquisition in young women is the Age group (years) validation of the safety of existing technologies and interven- tions for HIV prevention in young women B18 years [10,12]. HIV prevalence by age and sex, KwaZulu Natal high school students 2010 Concurrently, a concerted effort is required to better under- Males Females stand both the biological and structural factors driving the heightened vulnerability to HIV infection in young women more broadly. Such efforts, in parallel with a consolidation of the evidence obtained from adolescent- and youth-focused HIV prevention interventions and programmes conducted to date, should serve to inform the development of more efficacious interventions. The objective of this review is to provide an overview of the state-of-the-science of HIV prevention in young women and <16 16–17 18–19 >19 adolescent girls to inform policy and research direction. Age group (years) Specifically, we aim to (1) summarise the various behavioural and biological factors that predispose adolescent girls and Figure 2. Agesex disparity in HIV acquisition. Adapted from Shisana et al. [5] and Abdool Karim et al. [8]. young women to HIV infection, (2) briefly review the evidence HIV prevalence (%) HIV prevalence (%) HIV incidence (%) Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 from previous HIV prevention interventions targeted toward young women become infected after just a few coital en- adolescent girls and young women, and (3) discuss future counters, and on a population level, acquisition seems almost directions for HIV prevention in adolescent girls and young synonymous with sexual debut [17,36]. As such, there has women. been significant investigation into potential biological fac- tors that might augment behavioural risk, and a number of mechanisms have been hypothesised to result in heightened Discussion vulnerability to infection in young women, compared both to Why are adolescent girls and young women so vulnerable men and to older women. to HIV infection? For example, a number of studies focused on sero- Socio-behavioural associations of HIV infection in adolescent discordant couples have highlighted a higher per-act risk of girls and young women HIV acquisition in women compared to men [3740]. A portion Arguably the most convincing driver of the agesex disparity of this effect may be attributed to the higher viral load typically in HIV acquisition observed in sub-Saharan Africa is the high observed in men, but the phenomena may also be explained prevalence of intergenerational relationships between young at least in part by physical factors that result in increased women and older men [13,14]. The aggregating prevalence of exposure to HIV in women, compounded both from the com- HIV with increasing age means that, ceterius paribus, a young paratively larger surface area of the cervico-vaginal mucosa girl engaging in a sexual relationship with an older man is at and from the increased HIV mucosal exposure time (semen can much higher risk of HIV acquisition compared to a young remain in the female genital tract up to three days post-coitus) girl engaging with a male peer (Figure 2) [5]. Further, a young [41,42]. The higher per-act risk of HIV acquisition in women woman engaging in a relationship with an older man may be could also result from the relatively high levels of activation less likely to negotiate condom use given the gender-power of the immune cells in the female genital tract, the increased dynamics in the southern African setting, further augment- expression of HIV co-receptors in cervical cells compared ing her risk [13,15]. Consistent with these data, a number to foreskin cells, and/or a mucosal surface more likely to of studies have demonstrated that engagement in an age- acquire micro-abrasions during sex: together, these factors disparate or intergenerational relationship is strongly asso- result in more accessible portals for HIV entry in women ciated with increased HIV prevalence in young women [35,4346]. [13,1618]. Further work is needed to understand how this Further, young women are more susceptible to HIV infection association may be changing over time with increasing ARV compared to older women, and there are a number of bio- therapy (ART) coverage, and survival of both HIV infected logical factors that have been promulgated to explain this age- men and women over 25 years of age. variability in vulnerability. For example, the immature cervix Understanding the complex factors that drive adolescent has a greater proportion of genital mucosa exposed to HIV girls and young women to engage in sexual relationships that is highly susceptible to infection, and young women with older men is challenging, but may be critical in terms have relatively high levels of genital inflammation which have of adequately addressing the prevention needs of these consistently been reported to increase HIV acquisition risk key populations. In many cases, young women have reported [23,35,4749]. feeling flattered by the attention of older men, and many re- When considering the apparently uniquely high per-act lationships are likely to be built on genuine romantic con- HIV acquisition risk in young women, it is also necessary to nections [19,20]. In other instances, young women may be consider other relevant contextual factors that may mediate motivated primarily by the increased financial or social capital available through engaging in relationships with older men; the infection environment, including other sexually trans- indeed, many adolescent girls and young women report in- mitted infections (STIs) and contraceptive use. For example, volvement in these ‘‘transactional relationships,’’ which have many bacterial and viral STIs are associated with increased significant additional implications for HIV risk [21,22]. risk of HIV infection, and are much more prevalent in young Beyond engagement in age-disparate relationships, other women compared to young men [50,51]. A recent school- risk factors for HIV infection in young women include early based survey conducted in rural KwaZulu-Natal, South Africa, sexual debut, few years of schooling, food insecurity, loss found the trend in herpes simplex virus-2 (HSV-2) acquisition of a family member, and experience of gender-based violence to mirror the agesex disparity in HIV infection, with young [8,17,2328]. Many of these factors may mediate their ef- female students acquiring HSV-2 soon after sexual debut, and fects on HIV acquisition via increasing the relative value a more than three-fold higher prevalence of HSV-2 compared of financial capital available through engagement in transac- to their male peers (Figure 3) [8]. Interestingly, recent HSV-2 tional relationships with older men [21,2932]. However, infection may confer the greatest impact in terms of in- independent pathways of risk mediation are also likely to exist. creasing vulnerability to HIV, such that the female genital Food insecurity, for example, may also make young women tract in the immediate years following HSV-2 acquisition may biologically more susceptible to HIV [33]. be particularly susceptible to HIV infection [52,53]. Beyond STIs, other biological risk factors may also be amplified in young women. For example, one study has shown Possible biological mechanisms for heightened vulnerability that the use of the hormonal contraceptive depot medrox- to HIV infection in adolescent girls and young women yprogesterone acetate (DMPA) increases the risk of HIV The per-coital act HIV incidence rate in adolescent girls and young women is so high that it seems unlikely that it can be acquisition in young women (1824 years), while decreasing explained by behavioural risk alone [34,35]. Indeed, many HIV acquisition risk in older women (]25 years) [54]. Further, 66 Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 HSV-2 prevalence by age and sex, KwaZulu Natal behavioural intervention. However, the burden of HIV in high school students 2010 school-attending adolescents, while lower than out-of-school Males Females adolescents, remains significant, and thus there is also con- cern that the results might point to differential desirability bias by trial arm, which questions the validity of significant changes in self-reported markers of behaviour change re- ported by other studies. The data from school-based trials also underscore that while knowledge is a pre-requisite 10 for HIV prevention, it is in itself insufficient to prevent HIV infection. <16 16–17 18–19 >19 Age group (years) Attempts to make health services youth-friendly Other interventions to prevent HIV infection in young people Figure 3. Agesex disparity in HSV-2 acquisition. have focused on health systems strengthening in an effort to Adapted from Abdool Karim et al. [8]. address barriers to healthcare access by increasing the pro- vision of high-quality, youth-friendly HIV and SRH services. although establishing causal relationships is challenging, Such interventions are potentially critical, as there is sig- intra-vaginal cleaning practices are more prevalent in younger nificant demand for more comprehensive SRH services that women, suggesting these women are consequently more likely recognise the inter-relationships between HIV and broader to have an altered vaginal flora, potentially heightening their SRH and thus the importance of integrated service delivery HIV susceptibility [55,56]. [1,57]. Together these biological factors may create a ‘‘perfect Interventions to make health services more youth-friendly storm’’ of conditions in recently sexually debuted adoles- have typically focused on a different combinations of training cent girls and young women in southern Africa making them of service providers, outreach activities, and provision of uniquely vulnerable to HIV infection when exposed to the mobile services targeted toward specific high-risk adolescent virus via engaging in unprotected sex with an HIV-positive populations [66,7577]. Many of these interventions have partner. been successful in terms of increasing uptake of services Effectiveness of current HIV prevention interventions by young people. However, similarly to in-school interven- available to adolescent girls and young women tions, there is a notable dearth of biological-outcome-based In-school interventions assessment. Schools provide convenient venues for HIV prevention edu- cation, and not surprisingly a vast number of youth-targeted Community-level interventions HIV, STI, and pregnancy prevention programmes operate in HIV prevention interventions implemented at the community schools throughout sub-Saharan Africa [57]. The effectiveness level are highly heterogeneous, including sporting events, of such programmes in young people in sub-Saharan Africa mentoring and youth centres [78]. Evaluation of these in- has been the subject of a considerable number of systematic terventions highlights their largely positive impact on knowl- reviews [5871]. To summarise the evidence, several pro- edge and attitudes to HIV. However, these interventions grammes have been demonstrated to be effective in improv- often fail to reach the most HIV vulnerable populations, and ing knowledge and attitudes concerning HIV and the uptake of evaluation designs are generally weak. Only one study to our HIV testing. These data follow a general trend in sub-Saharan knowledge has assessed HIV incidence, and this study reported Africa of increasing comprehension and understanding about no evidence of effectiveness [79]. HIV in young people [1]. Those interventions demonstrating the most success are characterised by a number of factors, Conditional cash transfers including but not limited to: iterative and context-specific Cash transfers to young people that incentivise safer behaviour session programmes, HIV prevention and sexual and repro- have recently emerged as a new strategy to reduce young ductive health (SRH) curricula that include tasks focused people’s vulnerability to HIV [1,80]. The evidence in support of toward more general skills and knowledge development, the efficacy of this strategy is limited but promising. Indeed, and delivery by trained facilitators [57]. In contrast, abstinence- a recent randomized controlled trial in Lesotho demonstrated only and peer-led in-school interventions tend to be ineffective that a programme of financial incentives reduced the prob- [57,62]. ability of acquiring HIV by 25% over two years [81]. Similarly, an Despite some apparent successes, few rigorously con- independent randomized controlled trial in Malawi reported ducted trials have assessed the impact of interventions that those female high school students who received con- on biological outcomes, including HIV, STI and/or pregnancy ditional cash transfers (CCTs) were 64% less likely to be HIV incidence. Those trials that have demonstrated no significant infected compared to those who were not [82]; however, effects of any school-based intervention on these biological baseline HIV infection was not measured. These data suggest outcomes, in spite of reporting positive impacts on self- reported behaviour change in adolescents [7274]. These a potential for CCT to prevent HIV in young people, and results may stem from the relatively strong prevention effect outcomes of current research in the field such as HPTN 068 of being in school itself, which may dwarf the effect of any are eagerly awaited. HSV-2 prevalence (%) Dellar RC et al. Journal of the International AIDS Society 2015, 18(Suppl 1):19408 http://www.jiasociety.org/index.php/jias/article/view/19408 | http://dx.doi.org/10.7448/IAS.18.2.19408 Gaps and future directions more than 44,000 infections in one year. Implementation and Despite the large and immediate need for HIV prevention policy science are urgently needed to translate research on in adolescent girls and young women, there is a dearth of PrEP effectiveness into averted infections. Further, there is evidence-based interventions available to them to reduce also work to be done in ensuring that on rollout, the state- of-the-science of prevention is not lagging behind in adoles- their risk. Given the diversity of epidemics within and between cents B18 years because of restrictive ethico-legal guidelines countries, in order to develop more efficacious youth-focused that often prevent them from participating in biomedical prevention interventions, a sound understanding of the local research in spite of their substantial need [6,10]. epidemic is required as well as the bio-behavioural nexus This review was restricted to considering HIV prevention in that renders adolescent girls and young women more vulner- adolescent girls and young women. However, the treatment able to HIV infection. The significant SRH needs of young needs resulting from the unprecedentedly high HIV incidence women should be central to the design of new interventions, rates in these key populations should not be underestimated: as integration of services is the backbone of a pragmatic ap- in Lesotho for example, almost a quarter of all young people proach to address needs now, even as we refine, develop and aged 1524 years are infected with HIV [1]. Adolescent- test new and novel approaches [1,83]. A careful review of focused HIV prevention interventions should also seek to previous interventions and their evaluations is needed to meet the needs of HIV-positive young people who face ensure maximum gains. Most notably, it is critical that any significant barriers to care. Indeed, of note is that adoles- future intervention should be rigorously assessed for effec- cents (1019 years) are the only age group in which AIDS tiveness in controlled trials with biological outcomes prior deaths have risen between 2001 and 2012 [1]. to wide-scale implementation to maximise efficiency and effectiveness of resource allocation. Many researchers would benefit from engaging the young women themselves as part- Conclusions ners in intervention design and implementation, and certainly Meeting the HIV prevention and SRH needs of adolescent encouraging male partner buy-in and female empowerment girls and young women who are at uniquely high risk of HIV will also be important in those settings where gender-power acquisition is a public health and moral imperative and a dynamics augment HIV risk. requirement to meet the laudable goals of achieving an AIDS- A further important direction for future research should be free generation and/or epidemic control. However, despite to develop interventions targeted to hard-to-reach young this imperative, evidence-based prevention options available people who might be missed by school- or community-based to adolescent girls and young women remain limited, and even interventions. The evidence for the best practice in reaching as efforts get underway to develop more efficacious interven- such populations is particularly limited, despite their often tions, they are likely to take many years to reach fruition. greater risk of HIV acquisition. However, our own experiences Immediate action is therefore needed to facilitate this key highlight that some important components of making service population to mediate their own risk, including as first steps provision palatable and attractive to hard-to-reach adoles- rollout of PrEP, adolescent enrolment in biomedical HIV cents include anonymized testing, flexible clinic hours and prevention trials, and provision of accessible and integrated adaptions of respondent-driven sampling. Concurrently, ef- SRH-HIV prevention services. forts should be made to keep adolescents in school. The task of developing and evaluating new HIV prevention interven- Authors’ affiliations tions  particularly those programmes that aim to address Centre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, the underlying social vulnerabilities  is substantial, and will South Africa; Department of Epidemiology, Mailman School of Public Health, potentially require decades of concentrated action, during Columbia University, New York, NY, USA which time adolescent girls and young women will continue Competing interests to become infected in their hundreds of thousands. As such, The authors declare that no competing interests exist. it is a moral imperative to effectively deliver what we know works now. The most pressing example of a technology that Authors’ contributions we know works but is not being delivered is PrEP, which was RD, SD, and QAK conceptualized the article. RD prepared the final draft, with contributions and revisions made by SD and QAK. All authors have read and developed specifically with young women in southern Africa approved the final version. in mind: designed to allow them to exercise their rights over their health and take control over their own risk without Author information dependence on their sexual partners. While the number of RD is a research fellow at CAPRISA supported by the CAPRISA Training Programme. randomized controlled trials demonstrating the effectiveness Acknowledgements of PrEP continues to grow, this success has yet to be translated CAPRISA was established as part of the Comprehensive International Program of into product availability in southern Africa. Undeniably, PrEP Research on AIDS (CIPRA) and is supported by the National Institute of Allergy is not 100% effective, is limited by adherence and would and Infectious Disease (NIAID), National Institutes of Health (NIH) and the US Department of Health and Human Services (DHHS) (grant# 1 U19AI51794). benefit from improvements currently in development; how- ever, one has to question where the threshold of evidence References required for rollout of current forms of PrEP to young women 1. UNAIDS. Global report: UNAIDS report on the global AIDS epidemic 2013 in southern Africa lies. A simple calculation highlights that [cited 2014 Aug 14]. Available from: http://www.unaids.org/en/media/unaids/ even with a 39% efficiency, rollout of Tenofovir gel to young contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_ women aged 1524 years in South Africa alone might prevent 2013_en.pdf 68 Dellar RC et al. 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