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Clinical Science

Mental Health and Functional Competence in the Cape Town Adolescent Antiretroviral Cohort

Hoare, Jacqueline PhDa; Phillips, Nicole MSocScia; Brittain, Kirsty MPHb,c; Myer, Landon PhDb,c; Zar, Heather J. PhDd,e; Stein, Dan J. PhDa,f

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: August 1, 2019 - Volume 81 - Issue 4 - p e109-e116
doi: 10.1097/QAI.0000000000002068

Abstract

INTRODUCTION

In adolescents living with HIV (PHIV+), psychosocial development and behavior are profoundly affected, with concerns related to functioning and mental health.1 Functioning encompasses overall competencies, the ability to interact with their environment, fulfill role, social activities, relationships with friends and family, and the ability to navigate problems constructively. A review of mental health of PHIV+ suggested that they experience emotional and behavioral problems, including psychiatric disorders, at higher-than-expected rates, often exceeding other high-risk groups.2 The mental health of PHIV+ may be linked to HIV disease, to adolescence in general, or to psychosocial problems generated by the interaction between HIV, the adolescent, and their environment.3 AIDS-related mortality among PHIV+ has risen by 50% despite the scale-up of antiretroviral therapy (ART).4 Poor ART adherence is likely to play a role in the increase of AIDS-related deaths among adolescents and has shown to be associated with psychosocial and mental health difficulties.4 Data from reviews, although based on very limited studies, suggest that attention-deficit hyperactivity disorder (ADHD), anxiety, and depression are all highly prevalent in PHIV+.5 Apathy is a well-recognized neuropsychiatric symptom in adults with HIV6; however, there is no literature on motivation/apathy in PHIV+.7 Apathy has been described in adults living with HIV without cognitive impairment and depression.6 Apathy could be a cause of poor adherence and poor functioning in activities of daily living in PHIV+, as has been described in adult HIV.

Determinants of impaired adolescent health internationally are factors such as low household income and lack of education. Safe and supportive families and schools, together with positive and supportive peers, are important in helping adolescents develop to their full potential and attain the best health in adulthood.8 Low household income, overcrowding, family disruption, caregiver depression, and school failure are all recognized risk factors for poor adolescent mental health.9,10 Loss is frequently both recurrent and cumulative for PHIV+. Not only are they dealing with the possible loss of their own life, but in the case of perinatally acquired infection, they are also dealing with the loss of immediate family members.11 Adolescents orphaned by AIDS are more likely to have depression, peer relationship problems, posttraumatic stress, and conduct problems than adolescents orphaned by other causes.12 The drivers of poor mental health in PHIV+ are understudied in South Africa and may include structural factors such as family resources and assents, HIV-related stigma, and traumatic life events. Understanding the factors associated with poor mental health and functioning in PHIV+ living in South Africa would be important to inform future holistic adolescent-friendly ART services.

Due to the historically high mortality rate in young children with perinatally acquired HIV in South Africa, in part due to the later rollout of ART around 2004, the first generation of perinatally HIV-infected children in South Africa are entering adolescence, and may face a number of mental health challenges, but there are limited data investigating a wide range of mental health outcomes including motivation and functioning. Psychosocial development and behavior during adolescence are influenced by HIV, with concerns related to treatment adherence, stigmatization, risk taking, and the position of young people within family and social support systems. There are potentially complex—but still poorly understood—interactions between each of these factors; research across multiple domains is required to understand the health and development of PHIV+ in this context. The overall goal of Cape Town Adolescent Antiretroviral Cohort (CTAAC) is to investigate markers of chronic disease processes and progression in PHIV+ including mental health and functioning longitudinally over a 3-year period. The current study is a baseline descriptive study investigating a wide range of mental health measures and functioning in PHIV+ enrolled in CTAAC, including the effect of orphanhood on mental health measures, and the associations between demographic life stressors, HIV-related stigma, treatment, and clinical data with mental health measures.

METHODS

A study of baseline mental health measures in a subgroup of PHIV+ enrolled in the CTAAC, a prospective cohort study to investigate HIV disease progression over 3 years. Adolescents were recruited from public sector health care service from across Cape Town. Inclusion criteria were adolescents, aged 9–11 years, with perinatally transmitted HIV, who had been on ART for at least 6 months, knew their HIV status, and where informed parental consent and participant assent were obtained. Controls were HIV-negative, age-, sex-, and ethnicity-matched. Controls were recruited for the same public health care services as the PHIV+. Controls were excluded if they had known preexisting disease or if informed consent and assent were not obtainable. All youth screened for the control cohort underwent rapid HIV testing before enrollment to confirm negative status.

Exclusion criteria were based on the inclusion of neuroimaging studies (not reported on here): an uncontrolled medical condition, such as poorly controlled diabetes mellitus, epilepsy, or active tuberculosis requiring admission; an identified CNS condition (other than HIV), such as TB meningitis or bacterial meningitis, documented cerebrovascular accident; lymphoma; a history of head injury with of loss of consciousness greater than 5 minutes, or any radiological evidence of skull fracture; a history of perinatal complications such as hypoxic ischemic encephalopathy or neonatal jaundice requiring exchange transfusion, or neurodevelopment disorder not attributed to HIV.

Adolescents were enrolled from August 2013 to April 2015 at the Research Centre for Adolescent and Children Health at Red Cross Children's Hospital, South Africa. Ethical approval was obtained from the University of Cape Town's Faculty of Health Sciences research ethics committee.

Measures

Baseline demographic and clinical data were obtained at enrollment. A general physical examination was performed by a medical officer, which included anthropometry and Tanners pubertal staging. Other covariates including medical history were extracted from medical records or measured at study visit. Questionnaires were administered by study staff to child/parent or guardian dyads at enrollment. Where appropriate, separate questionnaires were administered to adolescents and their accompanying parent/guardian. Interviews were conducted in the participant's home language, in private rooms by trained counselors with extensive experience working with PHIV+ and a parent or guardian. We have used each of these measures in the local population, with evidence of good reliability in isiXhosa speaking populations.10,13 Caregiver depression was measured using the Center for Epidemiological Studies-Depression. The life events questionnaire focuses on recent stressful life events (ie, those occurring in the past 12 months). HIV-related stigma questions rated between 1 = Not at all and 3 = All the time.

Baseline Health and Sociodemographics

Baseline health and sociodemographic questionnaires were conducted to obtain general health information, medical history, and data on ancestry, language, education, and treatment. PHIV+ and caregivers were asked to report on whether they had missed any ART doses in the past month. Updated routine CD4 and viral load results and ART regimen and date of initiation of ART were abstracted from routine care records.

Family Resources, Support, and Assets

The Family Resources Scale and Family Support Scales were used to gather information about the family's perceived access to resources and support. Higher scores on the scales indicate perceived better resources and better support. For our purposes, a composite asset index score was calculated based on access to household and financial resources, for a maximum score of 17.

Beck Youth Inventories (BYI-II)

This self-report scale has 5 inventories, which may be used separately or in combination to assess a child's experience of depression, anxiety, anger, disruptive behavior, and self-concept. The inventories are intended for use with children and adolescents between the ages of 7–18 years. The inventories are structured in line with DSM-IV-TR criteria. The BYI-II has been used with success in only a few sub-Saharan African studies. Scores were standardized according to the manual reported norms for sex and age.

Children's Motivation Scale

This 16-item instrument14 was used to measure the adolescent's motivation levels, or tendency toward apathy. For each item, the parent was asked to state how often his/her child engaged in self-motived activities. For example, if a statement read “Starts playing (games, activities) on his/her own,” the parent would select one of the following options: 0 (never or rarely occurs), 1 (1–3 times during a month), 2 (1–3 times per week), 3 (4–6 times per week), or 4 (1 or more times a day). The scale produces a raw score, which is interpreted along a spectrum.

The Conner's Parent's Rating Scale (CPRS)

The CPRS is one of the most popular rating scales used by professionals today for parent rating to diagnose ADHD.15 The CPRS addresses 4 factors: conduct problem, hyperactivity, inattentive–passive, and hyperactivity index. The scale produces a raw score, which is interpreted along a spectrum.

Child Behavior Checklist (CBCL)

This 113-item instrument16 is one of the most widely used and psychometrically sound measures for assessing child behavioral and emotional problems and psychopathology. In this study, it was used to measure internalizing and externalizing problems experienced by the child. It was also used to measure total problems experienced by the child, as well as the child's total competence. Parents were asked to rate items according to how much each given statement applied to their children: 0 (not true), 1 (somewhat or sometimes true), or 2 (very true or often true). Examples of some statements are: “Acts too young for his/her age” and “Can't concentrate, can't pay attention for long.” The CBCL raw score was converted into T-scores using the ABESA software for scoring the CBCL. The CBCL has been used successfully to measure child behavior problems in South African children.

Statistical Analysis

Data were analyzed using Stata 12 (StataCorp Inc., College Station, TX). Mann–Whitney U tests were used to compare the HIV-infected group with controls for all baseline demographics and clinical characteristics, as presented in Table 1. Likewise, the Mann–Whitney U test was used to compare the difference in clinical cutoff scores between the groups, as presented in Table 3. We compared mental health measures between PHIV+ and HIV-uninfected adolescents in linear regression models adjusted for adolescent age, sex, and current grade at school. Among PHIV+, we explored independent associations between sociodemographic HIV-related stigma, life stressors, clinical (CD4, viral load, hospitalizations, and ART line) and caregiver-related variables, and mental health measures in multivariable linear regression models, controlling for possible confounding variables.

T1
TABLE 1.:
Baseline Demographic and Clinical Characteristics of CTAAC Cohort

A sample size of at least 40 adolescents in each group was based on detecting a significant difference in mean depressive symptoms; the proposed sample size would allow >80% power to detect differences of >0.05.

RESULTS

Two hundred four PHIV+ and 44 matched controls were enrolled. Age, sex, ethnicity, education, and household income were similar between PHIV+ and uninfected adolescents Table 1. PHIV+ were more likely to have had repeated grades at school, have a caregiver with depression, have lost both biological parents, and have delayed breast development and shorter stature than the uninfected group. Most PHIV+ were on first-line ART with a mean CD4 count of 953 cells/mm3, median viral load of 0 IU/mL, and duration of ART of 7 years. Of the data that are available from medical records (PHIV+ and controls; n = 232), 97 participants (42%) have record of a prior hospitalization. Noting that participants could have been hospitalized more than once for different reasons, these hospitalizations were documented as being for asthma (5%), TB (32%), pneumonia (53%), heart problems (3%), kidney problems (1%), malnutrition (16%), psychiatric reasons (2%), meningitis (3%), and other reasons (25%). In terms of mental health histories, 5% of those who have medical history data available have a recorded mental health issue.

PHIV+ had poorer functional competence when compared with well-matched uninfected adolescents. There were a number of significant differences in mental health measures with PHIV+ having poorer self concept and motivation (Table 2), higher levels of depressive, disruptive behavior, and ADHD symptoms (Table 2). ADHD symptoms were no longer significant after adjusting for age, sex, and current grade at school. The CBCL and BYI-II have clinical cut-off scores above or below which the symptoms are thought to be clinically significant. Central tendency statistics by group for the primary mental health outcome measures are presented in a supplementary table. (see Supplementary Table, Supplemental Digital Content, https://links.lww.com/QAI/B350). Table 3 presents the numbers and percentages of adolescents with clinically significant symptoms on the various subscales of the CBCL and the BYI-II. PHIV+ had higher rates of clinically significant poorer functional competence, poor self-concept, depression, anger, and disruptive behavior. Within the PHIV+ group, orphanhood was significantly associated with higher levels of disruptive behavior on a χ2 analysis (F = 22.22, P = 0.08, Cramer's V = 0.180).

T2
TABLE 2.:
CTAAC Cohort Baseline Functional Competence and Mental Health Measures, Association With Living With HIV
T3
TABLE 3.:
Number of Adolescents With Clinically Significant Mental Health Disorders Within the CTAAC Cohort and Differences Between the Groups

Within the PHIV+, factors associated with mental health symptoms and poorer functioning were mostly sociodemographic factors such as male sex, repeating a grade at school, caregiver not being a biological parent, poorer caregiver quality of life, less family resources, less family support, and less family assets Table 4. More stressful life events was associated with more anxiety, depression, anger, disruptive behavior and ADHD symptoms, and internalizing, externalizing, and total problems. More HIV-related stigma was associated with depression, anger, and disruptive behavior. Current CD4 cell count and viral load were not associated with any of the mental health symptoms. Previous hospitalizations were not associated with any of the mental health outcomes. Having had an HIV-related illness was associated with poorer total competence. Age of initiation of ART was associated with self-concept, and failing first-line ART (currently being on second- or third-line ART) was associated with internalizing and externalizing behavior problems.

T4
TABLE 4.:
Factors Associated With Mental Health Outcomes Among Adolescents Living With HIV

DISCUSSION

Our descriptive study of CTAAC baseline functioning and mental health measures found adolescents living with HIV to have poorer functional competence when compared to uninfected peers. There were also a number of significant differences in mental health measures, with PHIV+ having poorer self-concept and motivation and higher levels of disruptive behavior, depression, and ADHD symptoms. However, the ADHD symptoms were no longer significant after adjusting for age, sex, and current grade at school. When examining the mental health and functioning measures that provide clinical cutoff scores, PHIV+ had higher rates of clinically significant poorer functional competence, poor self-concept, depression, anger, and disruptive behavior. Within the PHIV+ group, the loss of both biological parents was associated with higher levels of disruptive behavior. Within the group of PHIV+, factors associated with mental health symptoms and poorer functioning were mostly sociodemographic factors and stressful life events. More HIV-related stigma was associated with depression, anger, and disruptive behavior. Age of initiation of ART was associated with self-concept, and failing first-line ART was associated with internalizing and externalizing behavior problems.

Chronic illness can interfere with the functional competence of adolescents and make them more vulnerable to psychological and social problems.17 We found significant problems in functional competence using the CBCL total competence subscale in our PHIV+ cohort. The impact of HIV surpasses that of virtually all other chronic conditions, and may be compounded by the stigma associated with HIV infection.18 Stigma, living with chronic illness, bereavement, and caretaker changes are well-documented challenges facing perinatally HIV-infected youth. With high rates of neurocognitive disorders, despite treatment with ART, youth may have multiple challenges to negotiating life problems.13 Assessing functioning in adolescents has yielded mixed results, with some studies finding no differences in adaptive functioning between infected and noninfected adolescents.19 Ideally, a better measure of functioning would be individual school- and home-based assessments conducted by an occupational therapist; however, in a resource-limited setting, we rely on self-report measures.

Adolescence is a period in which mental health problems if present are likely to emerge.20 Previous studies have reported higher rates of depression and anxiety in youth living with HIV than found in our study.21 A review found average prevalences of 28.6% for ADHD, 24.3% for anxiety disorders, and 25% for depression.5 Higher rates of ADHD have previously been described in HIV-infected youth22 in developing countries and children with other types of chronic illnesses.23 The CTAAC baseline cohorts are young adolescents (9–11 yrs old), which may account for the lower levels of mental health problems reported here. The CTAAC cohort included measures of mental health problems less commonly investigated such as anger, disruptive behavior, self-concept, and motivation, with more problems reported in the PHIV+. Self-concept is defined as an individual's beliefs and knowledge about his/her personal attributes and qualities.24 It has been found that a positive self-concept has direct protective effects on the development of depressive symptoms in the chronically ill.25 Poor self-concept has previously been linked to problem behavior, depression, and anxiety,24 symptoms reported with increased rates in the adolescents living with HIV in this study. Less youth depression has been associated with more social support seeking, higher youth self-esteem, and lower internalized stigma.26 Worryingly higher levels of depression in PHIV+ have been associated with increased risk behavior.27 The emergence of mental health problems and sexual risk behavior can be detrimental to the health and well-being of HIV infected youth and may place others at risk for secondary HIV transmission, creating a significant public health challenge.22 In PHIV+, higher levels of anger have been directly associated with elevated psychological distress and avoidant coping, and indirectly associated with greater HIV disease severity.34 Poor mental health may also lead to denial of infection, apathy/low motivation, and hopelessness, resulting in medication refusal. Apathy has been shown to impact on everyday function, medication adherence, and treatment outcome in adults.28–30 It may manifest even without significant cognitive impairment,30 possibly a sign of early HIV-related CNS disease. In adolescents, low motivation may impact on school and daily functioning, and influence later quality of life.

Within the CTAAC PHIV+ cohort, loss of both biological parents was significantly associated with higher levels of disruptive behavior. Loss of parent/s living with HIV has previously been associated with significantly more emotional distress and problem behaviors.31 Exposure to violence in the home and the community is high in South Africa. Orphaned children living with HIV have been found to experience more violence than children unaffected by HIV. Interpersonal violence in the home has predicted child depression, lower self-esteem, and behavioral problems.32

The specific role of HIV in relation to mental symptoms remains unclear. In this study, current CD4 cell count and viral load were not associated with mental health outcomes. CD4 count and HIV RNA viral load have in previous studies not been associated with the presence or absence of mental health problems.33 Factors associated with mental health symptoms and poorer functioning in this study were mostly sociodemographic factors such as repeating a grade at school, caregiver not being a biological parent, poorer caregiver quality of life, less family resources, less family support, and less family assets. In addition, stressful life events and HIV-related stigma were associated with mental health symptoms. Although studies are limited with mixed findings, a review found that parental health and mental health, stressful life events, and community disorder have been associated with worse mental health outcomes, whereas parent–child involvement and communication, peer, parent, and teacher social support have been associated with better function.2 Failing first-line ART was associated with internalizing and externalizing behavior problems. The direction of the relationship due to the cross-sectional nature of this study is unclear. A limitation of this study is that reasons for switching to second- or third-line treatment were not always possible to obtain. Whether this was due to drug resistance or chronic poor treatment adherence is unknown.

Limitations of the current study are that we cannot determine the causality of mental health symptoms. It is likely that multiple factors are involved, including variables such as adolescence, the progression of NeuroHIV disease, the effects of ART, or other environmental or psychosocial effects on behavior, including the stress of having a stigmatized, chronic, and potentially fatal illness. There may also be physical and psychosocial characteristics of HIV-infected mothers who transmitted the virus to their babies that may influence long-term youth mental health. However, this study reports on a wide range of mental health symptoms, including the first report of significant apathy in PHIV+. Although the current study reports on cross-sectional data only, CTAAC is a longitudinal study, which will be able to provide information on mental health 3 years later, such as predictive factors, stability of diagnosis, duration of diagnosis, and the association of mental health with HIV disease progression.

CONCLUSIONS

Mental health problems are commonly associated with PHIV+. These findings emphasizing the importance of mental health symptoms and associated functional impairment in children and adolescents with perinatally acquired HIV. They provide an important foundation for addressing additional questions such as how mental health influences the various components of adherence to treatment and risk-taking behavior over time. Psychosocial function has been given relatively limited attention; however, these issues may be just as critical as biomedical and socioeconomic factors for the success of treatment.35 These findings highlight the importance of screening for mental health symptoms, HIV-related stigma, sociodemographic risk factors, and recent life stressors in ART clinics. Mental health and ART services should be integrated into one adolescent friendly service because PHIV+ are likely to face future physical and psychological health consequences related to the cognitive and functional competence challenges they face if mental health care is not made a priority in the fight against HIV.1 This care may need to take into account that parents or caregivers share the infection. Adolescents with behaviorally acquired HIV in South Africa are likely to be exposed to similar sociodemographic and recent life event risk factors for the development of mental health problems. It is not clear whether PHIV+ are at higher or similar risk for the development of mental health problems in comparison with behaviorally/recently acquired HIV. Factors unique to PHIV+ would be longer duration of illness and ART exposure, increased risk of orphanhood, and exposure to HIV during critical developmental periods.

ACKNOWLEDGMENTS

The authors thank all participating adolescents and their caregivers, and study staff for their commitment to this work.

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Keywords:

HIV; adolescents; mental health; functioning; orphan

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