Introduction
Adolescent adherence to antiretroviral medication remains lower than adult rates in both high [1,2] [3] [4] [5] [6] [7]
In 2013, a systematic review [8] [9] [10] [11] [12] [13] + cell count. Since this review, a further three studies have been identified, with mixed results. In a hospital in Thailand, 260 children and adolescents aged 6–19 years (228 over 10 years old) showed no associations between HIV disclosure and ART adherence, using measures of pill count, CD4+ cell count or viral load [14] P = 0.008) [15] P < 0.03) [16]
These studies are of great value in the field of adolescent HIV care. However, it is notable that – despite 62% of HIV-positive adolescents living in Southern and Eastern Africa [17] N = 376 adolescents come from this region, with only N = 441 adolescents studied in all African studies combined. In addition, all studies sampled only adolescents attending healthcare facilities, thus excluding adolescents not actively retained in care. This study augments existing evidence by testing associations of adolescent HIV-status disclosure and ART adherence. It uses a large, community-traced adolescent sample in South Africa that includes those lost-to-follow-up, and intermittent/nonattenders of clinic appointments.
Disclosure is increasingly understood not as a single event, but as a complex and dynamic process [18,19] [20] [21] [22,23]
Materials and methods
This study used iterative quantitative and qualitative methods, following recommendations for research approaches of HIV diagnosis among children [7,24]
Participants and procedures
The Eastern Cape is South Africa's poorest province, with an antenatal HIV-prevalence of 29.1% [95% confidence interval (95% CI) 27.3–30.9] [25] n = 32) were identified. Subsequent to this mapping exercise, the national health policy of decentralization of HIV treatment programmes resulted in an increase of the clinic sample (n = 39 facilities). Within these facilities, all adolescents aged 10–19 years who had ever initiated ART and who had a first or last name and address or village/township recorded were identified. All adolescents were either met at clinics or followed up in their homes, to ensure inclusion regardless of clinic attendance or loss-to-follow-up. Of an initial n = 1102, 351 were excluded due to mis-recorded age, false names or addresses, or having moved to another province, 40 adolescents or caregivers refused to participate, and 27 adolescents had died. Six hundred and eighty-four ART-initiated adolescents were interviewed.
Voluntary informed consent was obtained from caregivers and adolescents for a 90-min interview (refusal rate 5.5%). Permission to record interviews and focus groups was requested from all qualitative participants. No incentives were provided, but all participants were given a pack containing a snack, toothbrush and toothpaste, and all received a certificate acknowledging participation. To prevent adolescents being identified or stigmatized through participating in HIV-related research, the study was presented as focusing on the needs of adolescents using public health services, and adolescents in neighbouring homes were also interviewed (n = 259, not included in these analyses).
Participants for the qualitative study were purposively recruited from the quantitative sample on the basis of consent and availability to participate in in-depth research and reported experience of HIV disclosure and ART initiation. Seventy-two in-depth interviews were conducted with 43 HIV-positive teenagers: twenty-six adolescents were interviewed once (26 interviews), twelve adolescents were interviewed twice (24 interviews), six adolescents were interviewed three times (18 interviews), and one adolescents was interviewed four times (4 interviews). 30 interviews were conducted with 22 caregivers of HIV-positive adolescents: One caregiver was interviewed three times (3 interviews), three caregivers were interviewed twice (six interviews), and 21 caregivers were interviewed once (21 interviews). Four focus groups were conducted with adolescent girls, adolescent boys, adolescent girls and boys combined and caregivers of HIV-positive adolescents. Eighteen months of direct participant observation and healthcare worker interviews were conducted at the family planning, antenatal care, antiretroviral and trauma units of five public health facilities (three hospitals and two health centres).
Questionnaires, interview schedules and consent forms were translated from English into Xhosa, and reviewed subsequent to back-translation. Adolescents participated in the language of their choice. Interviewers were trained in conducting research with HIV-affected adolescents. Confidentiality was maintained, except in cases of significant harm or when participants requested assistance. Where participants reported recent abuse, rape or risk of significant harm, referrals were made to child protection and health services, with follow-up support. Ethical protocols were approved by the Universities of Cape Town and Oxford, the Provincial Departments of Health and Education and ethical review boards of participating hospitals.
Quantitative measures
ART adherence was measured by adolescent self-report [26] [27] [28] [29]
Opportunistic infection symptoms associated with nonadherence were measured as sores on the body or face, tuberculosis symptoms (coughing blood and night sweats), shingles and mouth ulcers [30] [31]
Adolescent knowledge of HIV-status was initially assessed from clinic records and healthcare worker report and then checked with primary caregivers in the consent process. However, discrepancies in record-keeping and caregiver report meant that it was essential to check whether adolescents understood their status [32]
Potential cofactors included socio-economic and household factors of adolescent age, sex, language, urban/rural location and formal/informal housing, measured using items adapted from the South African census. Household assets were measured using an index of access to the eight highest socially perceived necessities for children, corroborated by more than 80% of the population in the nationally representative SA Social Attitudes Survey [33] [34] [35]
Analyses
Analyses used an iterative approach. Initial qualitative findings identified potentially important themes that were included as cofactors in quantitative analyses. Subsequent to this, qualitative analyses investigated themes arising from the quantitative findings. Qualitative interviews were recorded and transcribed in full or (where participants preferred not to be recorded) written notes were taken. Thematic codes were developed from the data, based on the principles of grounded theory [36]
Quantitative analyses were conducted in three stages in SPSS 22, using the sample of adolescents who had ever initiated ART (n = 684). Prior to analyses, socio-demographics were assessed (Table 1 ). Then, rates of self-reported past-week nonadherence were calculated, and associations with having two or more opportunistic infection symptoms were tested using logistic regressions and controlling for socio-demographics (sex, age, language, location, formal/informal housing and access to necessities) (Table 2 ).
Table 1: Socio-demographic characteristics by HIV-status knowledge.
Table 2: Association of self-reported past-week adherence to concurrent more than two opportunistic symptoms (shingles, mouth ulcers, tuberculosis symptoms).
Second, associations between adolescent knowledge of HIV-positive status and ART-adherence were tested in multivariate hierarchical logistic regressions, following Hosmer and Lemershow tests [37] Table 3 ). In the initial model, all potential predictors and cofactors were included (child age, sex, language, urban/rural location, informal housing, household access to basic necessities, presence of biological caregiver, maternal and paternal orphanhood, perinatal or horizontal infection, pill burden and past-year changes of medication, clinic or hospital care, travel time to clinic and visiting clinic alone/accompanied). In the second model, all factors associated at p-value less than 0.1 with adherence were included, and in the final model, all factors associated at p-value less than 0.05 were shown.
Table 3: Associations between HIV status knowledge and self-reported past-week full adherence (full sample).
Third, associations of age of disclosure and ART-adherence were examined for perinatally infected adolescents who knew their status (n = 362 of 540 perinatally infected) (Table 4 ). Horizontally infected adolescents were excluded as the processes of point-of-care testing do not entail family/healthcare worker choice about whether and when to disclose. The WHO guidelines recommend disclosure by the age of 12 for perinatally infected adolescents, and so associations between disclosure under age 12 and adherence were examined in multivariate logistic regression, using the same process and cofactors as on the full sample above.
Table 4: Associations between adherence and disclosure aged under 12 for perinatally HIV-infected adolescents who are aware of their status.
Results
Socio-demographic factors are summarized in Table 1 . Children were 10–19 years old (mean 13.4, SD 2.67), 52% female and 79% perinatally infected. Ninety-six percent of adolescents spoke Xhosa as a first language, and 18% lived in informal ‘shack’ housing while the remainder lived in rural traditional or urban formal structures. Sixty-seven percent lacked basic necessities and 45% lived with a biological parent. Maternal/paternal orphanhood was 45 and 29%, respectively, and 15% were double orphans. Seventy percent of ART-initiated adolescents knew their HIV-status.
Self-reported nonadherence in the past week was 36%. Independent of socio-demographics, past-week full adherence was associated with lower likelihood of adolescents experiencing two or more of concurrent shingles, mouth ulcers or tuberculosis symptoms [odds ratio (OR) 0.55; 95% CI 0.40–0.76, P < 0.001] (Table 2 ).
Associations of adolescent knowledge of status to adherence
In the final adjusted model, adolescent knowledge of their HIV-status doubled the odds of past-week full adherence (OR 2.18; 95% CI 1.47–3.24, P < 0.001), independent of all cofactors of age, sex, location, ethnicity, informal housing, poverty, biological caregiver relationship, maternal/paternal orphanhood, perinatal infection, medication burden, changes in medication, clinic type, travel time to clinic and lone/accompanied clinic attendance. Full adherence was negatively associated with being older (OR 0.85; 95% CI 0.80–0.91, P < 0.001) and longer travel time to the clinic (OR 0.72; 95% CI 0.57–0.89, P < 0.005) (Table 3 ).
Associations of younger-age disclosure to nonadherence
In the final adjusted model, among perinatally infected adolescents who knew their status (n = 362), disclosure prior to age 12 was associated with past-week full adherence (OR 2.07; 95% CI 1.34–5.22, P < .005), independent of all cofactors of age, sex, location, ethnicity, informal housing, poverty, biological caregiver relationship, maternal/paternal orphanhood, perinatal infection, medication burden, changes in medication, clinic type, travel time to clinic and lone/accompanied clinic attendance. Full adherence was also negatively associated with longer travel time to the clinic (OR 0.54; 95% CI 0.39–0.73, P < 0.001) (Table 4 ).
Qualitative findings identified largely positive experiences of disclosure that may explain associations with higher adherence. In both home and clinic settings, disclosure provided opportunities to ask challenging questions, to express feelings of anxiety, shame and anger, and to improve treatment literacy. Disclosure was often reported as a dialogue, and efforts were made to modify information in accordance with the age, emotional maturity and clinical history of individual children or adolescents. In some healthcare settings, disclosure could also facilitate access to other forms of support such as social grants or support groups.
Many reports of disclosure included locally adapted analogies that healthcare workers used with the aim of explaining the virus and enhancing patient self-efficacy. In the most common of these analogies, healthcare workers described HIV as a tsotsi [gangster], the adolescent as a policeman and ART as a weapon: ‘When you drink them [ART], it puts the HIV in jail’, explained a doctor, [direct observation, Hospital X, 2014]. A doctor recounted: ‘At that point I also explain to them that they have a future, and they can live until they are old. They can go to university, and have a car, and have babies, and get married, and do all of the things that they want to do, as long as they take the ARVs’. In a few cases, strategies to induce fear during disclosure processes were reported to be counter-productive. Where adolescents were threatened with social censure, illness or death should they default from ART, disclosure processes were characterized by anxiety, anger and risks of prompting rebellion through ART defaulting.
Qualitative findings may also help to understand why earlier disclosure was associated with positive outcomes of higher adherence among perinatally infected adolescents. Healthcare workers described earlier disclosure as reducing levels and extent of deception: ‘That's why I know it's better if you tell them earlier, at age ten or eleven … When we’ve told older children, their reaction is worse … Firstly, you’ve lied to them, and they feel very, very hurt by that. And secondly, they are in such a difficult stage of their lives, to add to that, ‘Now you’ve got HIV’, and all the implications of that, it slays them’. [Hospital Y 2014].
However, qualitative findings also indicated that understandings of disclosure may vary between healthcare workers, caregivers and adolescents. For some adolescents, disclosure was only partially understood at first: ‘My grandmother said that I will take these pills until I die, because they are my life. And she said I have HIV. At that time I didn’t understand. I only understood when I was eleven years old … I thought she was kidding with me, but I took them anyway because I was sick and I thought the tablets were for my fever’ (14-year old HIV-positive girl, 17 December 2014). Complexities also emerged in the process of undertaking the quantitative research, which identified discrepant perceptions of disclosure. These were primarily cases in which clinics and caregivers reported that adolescents were unaware of their status, but adolescents identified that they were fully aware. For these adolescents, status knowledge had occurred through a range of processes, including ‘googling’ their medication, learning about HIV treatment at school, asking older cousins or siblings and having been told by a previous, now-deceased caregiver.
Discussion
Around 2.1 million adolescents worldwide are currently living with HIV, of which 1.3 million live in Southern and Eastern Africa [17] [38] [39]
This study provides strong empirical support that full disclosure to adolescents of their HIV-positive status is associated with higher ART adherence. Amongst perinatally infected adolescents, early disclosure prior to age 12 is associated with further improved adherence. Adherence was associated with reduced opportunistic infection symptoms. It is clear that paediatric disclosure is important, ideally undertaken early, and may be insufficiently utilized as a means to improve treatment outcomes.
Findings also suggest that paediatric disclosure can be done well in a low-resource context and in a range of government health facilities. Qualitative findings report that healthcare workers and caregivers are responsive to the incremental nature of disclosure, and that adolescents may require multiple opportunities to comprehend the meaning of their status. This aligns with HIV literature suggesting that disclosure is a multistage process rather than an event [40] [41] [23]
These findings add to a mixed but small literature. Of the seven known studies worldwide, only two include samples of over 100 adolescents and find either no associations between disclosure and adherence in Thailand [14] [16] [10,12,15] [42] [40]
However, findings, and those of other studies in the region [18] [43,44] [45,46]
This study has a number of limitations. Firstly, although all disclosure had taken place prior to reporting of past-week adherence, the cross-sectional nature of the data limits corroboration of causal pathways. Secondly, only self-reported measures of adherence were available, due to infrequent testing of viral load and CD4+ cell count in low-resource health services. Thirdly, some of the qualitative findings, such as potential negative effects of ultimatum-based disclosure, were unable to be substantiated by testing in the quantitative data. And fourthly, of the 1075 living adolescents originally recorded in clinic records, 351 were unable to be traced due to false names or addresses given, or migration. This reflects the challenges facing both HIV-research and HIV-services serving a highly stigmatized and mobile young population. Despite these limitations, this study has notable strengths. It is the largest known study of ART adherence and disclosure among adolescents, and it is the only known study to use community-tracing in order to include adolescents not actively engaged in clinical care. Of 724 adolescent-caregiver dyads approached, refusal rates were very low at 5%. Self-reported adherence was strongly associated with lower rates of multiple opportunistic infection symptoms. Disclosure definitions followed guidelines requiring both naming and basic understanding of HIV [40]
Adolescent adherence to ART remains a major challenge. But adherence is also a gateway to reducing HIV-mortality, preventing onwards transmission and limiting viral resistance. Disclosure of HIV status to children and adolescents may be daunting, particularly for families negotiating stigma, illness and bereavement [47]
Acknowledgements
This was a collaborative study between the Universities of Oxford and Cape Town, UNICEF, the South African National Departments of Health, Basic Education and Social Development, Pediatric AIDS Treatment for Africa and local CBOs the Raphael Centre, Small Projects Foundation and Keiskamma Trust. The authors would particularly like to thank Julia Rosenfeld, Maya Isaacohn, Marija Pantelic, Janina Steinert, Lizzy Button, Craig Carty, Gerry Boon, Luntu Galo, Sheree Goldswain, Justus Hofmeyr, Sibongile Mandondo and Nicoli Nattrass. This project would not be possible without excellent fieldworkers. We thank the healthcare workers, families and most of all we thank the adolescents who participated in this study.
This work was supported by the Nuffield Foundation under Grant CPF/41513, the International AIDS Society through the CIPHER grant (155-Hod), the Philip Leverhulme Trust (PLP-2014-095), the Economic and Social Research Council (IAA-MT13-003) and the Clarendon-Green Templeton College Scholarship (Elona Toska). Additional support for Lucie Cluver and Franziska Meinck was provided by the European Research Council (ERC) under the European Union's Seventh Framework Programme (FP7/2007-2013)/ ERC grant agreement no. 313421. Additional support for Rebecca Hodes was provided by South Africa's National Research Foundation and the University of Cape Town's Humanities Faculty.
Conflicts of interest
Authors declare no conflict of interest in conducting and publishing this research.
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