A review of transition experiences in perinatally and behaviourally acquired HIV-1 infection; same, same but different?

Abstract Introduction: Despite sharing common psychosocial and developmental experiences, adolescents living with perinatally and behaviourally acquired HIV-1 infection are different in terms of timing of HIV infection and developmental stage at infection. Therefore, it is of interest to identify similarities and differences between these two groups of adolescents living with HIV in their experiences, facilitators and barriers during the transition process. Methods: A detailed literature search of peer-reviewed published papers was conducted on PubMed to identify relevant original research or viewpoints published up to September 2016. Conference abstracts and other unpublished data sources were not included. Results: Existing published literature, mainly using qualitative methods, explores the transition from paediatric to adult healthcare provision, as experienced by these two groups of young people. Reports highlight the variation and similarities in their experiences and challenges of transition. Findings from the USA and Europe predominate, while experience from Africa and Asia is lacking, despite the importance of these regions in the global epidemic. Conclusions: Published transition data remain limited, and there are few studies focusing on behaviourally infected adolescents and key population groups (e.g. adolescents who use drugs, lesbian/gay/transgender individuals). Robust definitions of the transition process and standardized outcome measures are required to facilitate cross-study and geographic comparisons.


Introduction
Recent estimates [1,2] suggest that there were 1.8 million adolescents living with HIV in 2015, with 250,000 new infections in this group. The ratio between perinatal and behavioural infections is generally unknown [3]. However, a UNAIDS estimate in 2013 suggested that among adolescents living with HIV in the 25 countries contributing the majority of AIDS-related deaths among this age group, around half were infected through mother-to-child transmission, and half through sexual and unsafe injection transmission [4].
In higher-resourced settings, adolescents with perinatally acquired HIV are usually seen by paediatric healthcare providers, and by the time of transition of care to adult services are more likely, when compared to their behaviourally infected peers, to have advanced disease, physical and neurocognitive deficits, HIV-1-associated drug resistance, and drug side effects [5][6][7][8][9][10][11]. Global guidelines recommend commencing ART in all age groups [12,13] and hence many perinatally infected children are highly treatment experienced as they enter adolescence. There has been increasing recognition of the emergence of resistance mutations to first-line therapy in resourced-limited settings where access to viral load monitoring and to second-line regimens remains challenging [14,15].
In contrast, adolescents with behaviourally acquired HIV may be seen from diagnosis in adult services, particularly where adolescent services are poorly developed and paediatric care ceases, depending on the setting, between 12 and 18 years of age. As such, they will not experience transition of healthcare provision from paediatric to adult services; yet, they too will be experiencing multiple transitions from childhood to adulthood during this time. Exposure groups at greater risk of HIV acquisition during adolescence include young heterosexual women, men who have sex with men (MSM), transgender adolescents, and those who sell sex and use drugs [16][17][18][19]. Risk factors for HIV acquisition in adolescents include: increased number of sexual partners, younger age of sexual debut, previous STIs, mental health diagnosis, poverty, homelessness, and drug and alcohol use [16][17][18][19]. As they enter adult care, behaviourally infected adolescents are more likely to be in early stages of disease, the majority with normal prior physical and cognitive development, requiring simpler first-line treatment regimens. However, they may continue to engage in high-risk behaviours and may have difficulties in accepting their diagnosis and treatment [5][6][7].
In addition to the shared challenges due to the psychosocial and developmental changes of adolescence and the stigma associated with HIV infection, adolescents in both groups frequently lack adequate emotional support, including from family members. This stems in part from difficulty in disclosing their HIV status to relatives or friends, and in the perinatally infected group because many have lost one or both parents to 20]. Furthermore, adolescents in key populations may have to confront the additional stigma and discrimination related to their drug use or sexual orientation not only among individual healthcare providers, but also within healthcare systems and policy levels [1,21].
This narrative literature review describes key differences and similarities in transition experiences between populations of HIV-positive youth by mode of infection, what is known about their outcomes in adult care, and future research priorities.

Methods
We searched PubMed for published English language literature on adolescent transition up to September 2016 using the following search terms: "Adolescent" AND "HIV" AND "Transition"). Of 270 citations retrieved, we focused on any study exploring facilitators and barriers of the transition process among adolescents or young adults living with HIV, and among healthcare workers. We paid particular attention to findings reported by mode of transmission, and we excluded papers which provided only quantitative outcomes in one risk group.
Multiple barriers and facilitators to successful transition were identified in the research studies. Amongst identified barriers, the strong attachment between adolescents and the paediatric provider was the most commonly identified factor [22,25,28,30,32,34,35,37,44], which applied to both perinatally and behaviourally infected adolescents. This was reported by adolescents themselves who expressed not wanting to leave their paediatric team, and by the healthcare professionals who cited concerns regarding the adolescents' ability to self-manage within the healthcare environment of adult services [20,21,[23][24][25]32,33]. This attachment has been explained by the positive long-term relationship between adolescents and providers, the protective care of paediatric providers [26], and the lack of preparation for transition within the healthcare system (e.g. requiring provider time) and for the patient (e.g. knowledge and skills to live independently) [25,26,28,30,33,37,43]. When transition occurred despite sufficient preparation, this attachment led to feelings of loss [25], with some adolescents finding it more difficult to build good relationships with the adult provider.
However, a comprehensive transition programme that was centred around the adolescent and included a formal written policy, time for education and skill development (especially around disease knowledge, scheduling of appointments and medication adherence), and a readiness assessment, was reported to be a facilitator of the transition process [5, 24,25,27,30,33,34,41,43,44]. Transition programmes that focussed on helping adolescents build their competence and independence further seemed to improve transition outcomes [23][24][25]30,32,41,42]. A common theme was for adolescents to have some control over the transition process, and for it to be geared to the adolescent's individual readiness to transition.
A commonly cited barrier was the negative perceptions among both groups of adolescents and their guardians about adult healthcare providers [22,26,28,30,33,37]. These arose from differences between adult and paediatric services in terms of patient load, expectation of patient autonomy, length and frequency of appointments, clinic setting and patient population [26,30,32,33,[41][42][43]45]. Developing good relationships with adult providers to facilitate transition has been achieved in some settings by integrating adult healthcare professionals into the paediatric clinic, arranging for adolescents to visit the adult provider before transfer, and seeing the same adult clinician each visit [24,[28][29][30]32,33,43,44]. Education for adult healthcare providers around the needs of adolescents, including communication styles and awareness of the potential neurocognitive impact of perinatally acquired HIV and the impact on autonomy, self-care and information processing, further supported the transition process [24,[28][29][30]32,33,43,44]. Another important issue were the psychosocial challenges faced by all adolescents that are further complicated by living with HIV. Hence, papers highlighted how adolescents needed a comprehensive integrated package of support from healthcare providers encompassing mental health [5,27,31,35], sexual and reproductive health [43], substance abuse services and social support integrated within their HIV care [30,33,37]. Whilst paediatric services were typically multidisciplinary in structure, adult services were sometimes "fragmented", with limited resources, skills and experience in dealing with the complex and varied psychosocial needs of adolescents living with HIV [24,33]. Multidisciplinary support in adult care, especially for mental health, may improve continuity of care and therefore could facilitate the transition process [27,33,41,43]. In young men who have sex with men, an individual's resilience or coping ability was affected by the strength of their immediate surrounding support network, and important factors influencing successful transition included the level of physical illness, age and developmental stage at the time of their HIV [31].
Confidentiality and fears concerning onward disclosure were highlighted as important barriers to the transition process. Due to their negative perception and/or experience of HIV-associated stigma, adolescents expressed concern about privacy in adult services [26,30,37,[42][43][44]. Adolescents with behavioural infection were particularly concerned about onward disclosure of their HIV status to their families [30], which could lead to poor family support around the transition period. In contrast, perinatally infected adolescents frequently had to negotiate transition alone due to being orphans, creating a very difficult setting for transition compared to other chronic diseases of childhood where the parents have been shown to be key facilitators in the process [47]. In addition, for many perinatally infected adolescents, adult services were often offered within a sexual health setting, before they had become sexually active, which created discomfort and was a regular reminder that they were living with a sexually transmissible infection. System-level issues including lack of social support for housing, transportation and financial resources also negatively affected the transition process and were cited as common barriers to remaining in care [30,33,34,[41][42][43]45].

Discussion and conclusions
This narrative review of published studies highlights the commonalities in transition experiences for adolescents with perinatally and behaviourally acquired HIV, and the multitude of factors which may be associated with positive and negative transition outcomes in these groups. Common barriers to transition included strong attachments between adolescents and paediatric providers, and negative perceptions of adult healthcare providers. Positive facilitators included having clear policies around transition, education and skills development for providers and patients, assessment of readiness to transition, shared appointments between paediatric and adult providers, and specific training for adult providers on communicating with adolescents. Psychosocial challenges, including stigma, levels of family support, and mental health, were varied and differed by population group, as did the need for different aspects of multidisciplinary care packages.
The studies reviewed highlight the paucity of published data on HIV-specific transition, and particularly studies focusing on behaviourally infected adolescents. Additionally, the lack of standard definitions/endpoints for assessing successful transition complicates interpretation of existing data. This applies to both quantitative (retention, CD4 count, viral load, HIV-1 associated resistance mutations, AIDS and non-AIDS mortality, morbidity) and qualitative (patient and healthcare provider experience, autonomy and self-care) studies. Tracking transition outcomes is further complicated by the lack of robust systems that monitor patients after transfer to adult care [42,43].
Most published findings were from higher resourced settings (mainly the USA and Europe), while data from Africa and Asia are lacking and of particular importance, as these regions have the largest burden of HIV disease with limited resources. Furthermore, there is a need to investigate the impact of cultural differences and the experiences of key population groups on transition outcomes. Understanding the expectations and experiences of adolescents and young adults as they go through transitional care will provide important knowledge to improve current practice.
The priority medical and psychosocial outcomes following any transitional care model are to ensure retention in HIV care, facilitate long-term self-care, and to provide ongoing holistic support to promote health and wellbeing. Young people living with HIV need systems they can trust that offer them open access and understand the need for dialogue around the specific challenges they face. If we are to achieve the UNAIDS global targets of zero AIDS deaths and zero new infections, adolescents and young adults must be respectfully and appropriately engaged in care that is tailored to their complex needs. Patterns of healthcare and health-seeking behaviours established in adolescence can form a framework for lifelong service utilization, and should be nurtured and guided as we seek to help them transition to adult life.