Adherence to antiretroviral therapy among adolescents living with HIV in Jamaica

doi:10.21203/rs.3.rs-1537907/v1

Objective:

To characterize adherence patterns to antiretroviral therapy (ART) and identify factors affecting optimal adherence among adolescents living with HIV (ALHIV) in Kingston, Jamaica during the Covid-19 pandemic.

Design and Methods:

During August-October 2021, we conducted a cross-sectional study on adherence (no missed doses in preceding four days) among adolescents 10-18 years attending three outpatient departments in the Kingston Metropolitan Area. Adherence factors were evaluated using a self-administered, interviewer-assisted structured questionnaire. Biochemical and clinicopathological information were retrieved from patients’ medical records. Multivariate logistic regression was used to determine likelihood of adherence for given adherence factors.

Results:

Of 65 participating clients, 92.3 % were perinatally infected, mean (SD) age 15.4 (2.0) years and 61.5% were female. Overall self-reported adherence was 66.1% (43/65) and higher among adolescents in residential care versus family care (p=0.002). Median (IQR) viral load 19 copies/ml/10³ (IQR 19-51) was lower (p=0.010) and median (IQR) CD4⁺count 701 cells per µL (IQR 501-1052) higher (p= 0.016) among adolescents in residential care compared to family care. Adherence was 4 times more likely among adolescents at UHWI (OR=4.53, 95% CI (1.25, 16.43), knowledgeable about ARVs (OR= 4.31, (1.09,17.04), and with reduced appointments due to Covid-19 pandemic (OR= 5.36, (1.09, 26.41) and 4 times less likely if cared for by relatives, experiencing side effects, higher pill burden or hospitalized with complications.

Conclusions:

Medication, caregiver-related and health system management factors are both enablers and barriers of adherence for ALHIV, and the importance of caregivers’ support, treatment literacy and simplified treatment regimens are highlighted.

Human immunodeficiency virus infection/Acquired immunodeficiency syndrome (HIV/AIDS) accounted for approximately 38 million people living with HIV, 1.7 million new infections, 690,000 AIDS-related deaths and children aged 0–14 years representing 9% of new infections (1, 2). In Jamaica AIDS is a leading cause of death in 15 to 49 age group and the second leading cause of death in children aged 1 to 4 years (3). The vulnerable populations (men who have sex with men, commercial sex workers and heterosexuals engaging in high-risk sexual behaviors), and those presenting late with opportunistic infections are particularly at risk. Cumulatively, over 34,125 HIV cases and 9,517 deaths attributed to AIDS were reported in Jamaica between 1982 and 2015, 1250 deaths in children 0–19 years (4), with continued rise in new infections to date (5).

Increased access to and utilization of highly active antiretroviral therapy in HIV-infected children has been facilitated through international funding, and established unified parallel treatment programmes for paediatric HIV in the Kingston Metropolitan area and centers island-wide through collaborative efforts between the Kingston Paediatric and Perinatal HIV/AIDS Programme and National HIV/AIDS Programme, Ministry of Health, Jamaica since 2003 (6, 7). The consequent outcomes of improved survival and reduction in HIV-attributable morbidity among children and adolescents necessitates further strengthening of adherence particularly among adolescents living with HIV (ALHIV) who are less likely compared to other age groups to achieve viral load suppression (8, 9, 10), internationally benchmarked at 62% adherence (11).

Among 1.8 million children (0–14 years) and 5 million young adults (15–25 years) living with HIV (12), increased access to antiretroviral therapy (ART) has resulted in growing numbers of perinatally-infected and behaviourally-infected adolescents surviving to late adolescence and adulthood (13, 14, 15, 16, 17). Majority ALHIV (82%) globally reside in Africa, highest prevalence in Sub-Saharan countries (18, 19), and female predominance (20, 21). Higher HIV prevalence among female adolescents, gay, bisexual boys and transgender adolescents call for urgent interventions to mitigate risk in these vulnerable groups. ALHIV have lower rates of retention in care and viral suppression resulting in increased HIV-attributable mortality especially in 15–19 age group (22, 23, 24, 25, 26, 27).

Adherence is the single most important factor determining the success of ART, optimal efficacy requiring at least 95% (8, 9, 10). Sub-optimal adherence results in treatment failure, development of viral resistance, and subsequent negative outcomes for survival and morbidity (28, 29). Monitoring measures include directly observed therapy, pharmacy reporting, patient reports, clinic appointment checks, and biomedical markers such as viral load levels (6). Self-reported surveys recalling missed doses over the last four days have been shown to be valid and reliable (30, 31, 32).

Transition from paediatric HIV services to the adult care is a vulnerable window associated with disengagement from care, and decreased viral suppression rates (33), and poor adherence is considered a risk-taking behavior common during adolescent development (34).

Across developed and developing country settings, barriers to adherence include complicated regimens, pill burden, forgetfulness, falling asleep, suspicions of treatment, access to medication, work and family responsibilities, fear of disclosure, life stages, negative experiences with ART and poor health literacy, being orphaned, poor adult support, lack of economic resources, and health system delays (35, 36, 37). Facilitators include positive effects of ART, acceptance of diagnosis, sense of self-worth, understanding need for adherence, reminder tools, simple regimen, strong family, peer and health support system, permanency planning, having married parents, parent also on ART, ART/HIV literacy, and rewards for adherence. Early paediatric ART regimes had frequent dosing, high pill/volume burden and toxicities (38, 39) but these barriers are currently mitigated by simpler, coformulated regimes, reduced pill burden and dosing frequency, and improved side effect profiles, hence optimising adherence and virological suppression (40, 41).

Globally, the Covid-19 pandemic disrupted health care systems, hospitals were overwhelmed and non-essential services, including outpatient activities scaled back or suspended (42). Internationally the progress toward HIV epidemic control has been derailed, but strategies have been implemented to mitigate effects of the Covid-19 pandemic (43).

ALHIV are vulnerable to the developmental, social, and environmental factors that affect adherence to ART. Access to newer combination therapies with reduced side effect profiles and optimized management approaches, and the Covid-19 pandemic have prevailed since adherence was last evaluated in ALHIV in Jamaica (6). Against this background and limited data on ART adherence from resource-limited settings, we aimed to characterize current adherence patterns among ALHIV attending outpatient clinics in Kingston, Jamaica, and assess perception of the impact of the prevailing COVID-19 pandemic on adherence.

Study Design

This cross-sectional study was designed to evaluate adherence among ALHIV 10–18 years old receiving treatment at outpatient clinics in Kingston, Jamaica.

Study Setting

During August to October 2021, this study was conducted at the Infectious Diseases clinics of three institutions in the Kingston Metropolitan Area: The University Hospital of the West Indies (UHWI), the Comprehensive Health Centre (CHC) and the Bustamante Hospital for Children (BHC) (44, 45). Using unified protocols, children and adolescents living with HIV/AIDS have been managed through the Jamaica Perinatal, Paediatric and Adolescent HIV/AIDS (JaPPAAIDS) programme in collaboration with the Ministry of Health and Wellness, Jamaica.

Participants and Sampling

Eighty-three clients fulfilled the age criteria for participation at the institutions [UHWI (10–18 years) 42; CHC (13-18years) 31; BHC (10–12 years) 10]. All patients (and parents/guardians) were approached except for those not disclosed of HIV status and with significant intellectual disability (not capable of answering questionnaire) or too ill to participate.

Written informed consent was obtained from all subjects and their legal guardian(s).

Procedure

Recruitment

Adolescents and caregivers fulfilling the inclusion/exclusion criteria were recruited at the time they accessed outpatient care at the UHWI, BHC and CHC. Patients were first informed of the study by the clinic nurse without being notified that they would be questioned about adherence. The researcher (RD) then discussed the purpose and procedure of the study with those interested adolescents and their parents (if less than 18 years old) and sought written informed consent from parents or legal guardians (for participants under 18 years) adolescents 18 years, and assent from adolescents under 18 years for whom parental consent had been obtained.

Patients who missed their clinic appointment were contacted via telephone by the nurse in charge/clinic manager, as per the usual protocol of the respective clinics, and informed of the study. If interested, consent forms were read to the participants (RD) and verbal consent obtained by the researcher in the presence of a witness, with the call on speaker phone.

Considering the COVID-19 pandemic, strategies were devised to optimize participation in this study. Patients whose appointments were outside of the study period, were identified through the respective databases of the various sites by the nurses in charge/clinic managers. They were contacted by the nurse manager and if interested then given a secret passcode. The passcode was used to correctly identify the client when contacted by the investigator. Verbal consent was then obtained as described previously in the presence of a witness prior to administering the questionnaire.

Data collection procedure and Instruments

A 45-item self-administered, interviewer-assisted structured questionnaire developed through literature review and researchers’ clinical experience, was utilized to collate data regarding socio-demographic characteristics, clinical information, ART regimen and adverse effects, adherence pattern, facilitators and barriers to adherence and perception of Covid-19 impact on adherence to treatment and care. Self-reported adherence was measured utilizing modified questions from a standardized tool of the AIDS Clinical Trial Group (ACTG), and defined as no missed doses in the preceding four days (31). The questionnaire was pre-tested (and modified) on adolescent clients living with other chronic illnesses (eg. diabetes mellitus) to optimise the instrument’s face validity.

Onsite participants had the questionnaire administered in a private space in the clinic to maintain confidentiality and standard government-mandated Covid-19 protocols were implemented. Remote participants were interviewed via telephone or video following verbal consent in a setting of their choice. Confidentiality was assured and there was no digital recording of the interview. The average time for completion of the questionnaire was 30–40 minutes.

Clinical data and biochemical markers of adherence [CDC clinical and immunological classification, mode of transmission, duration on ARV, HIV viral load, CD 4 + count, comorbidities, hospitalisations] were extracted from the patient’s medical records.

Data Management

Data security was assured through storage of hard data in a locked filing cabinet only accessible to the investigators. Client identifiers were removed and replaced by unique study numbers before electronic data were entered into an encrypted electronic spreadsheet and password protected.

Data Analysis

Using the Statistical Programme for Social Sciences (SPSS) version 25.0, descriptive statistics summarized sociodemographic and clinical characteristics and perception of COVID-19 pandemic impact. Independent sample student’s t-test and Mann-Whitney U test were used to compare clinical and sociodemographic characteristics between adolescents by residential status and adherence pattern. Pearson’s chi-squared and/or Fisher’s Exact tests assessed factors affecting adherence. Significant factors were explored in a logistic regression model. A p-value < 0.05 was considered statistically significant.

Ethical Approval

Ethical approval was received from the Mona Campus Research Ethics Committee, and the South East Regional Health Authority Ethics Committee. All methods were carried out in accordance with relevant guidelines and regulations or declaration of helsinki.

Written informed consent was obtained from all subjects and their legal guardian(s).

Sixty-five of 83 age-eligible candidates participated in the study (response rate 78.3%). Nine candidates were excluded due to failure to meet eligibility criteria (intellectual disability or non-disclosure), 8 could not be contacted by the nurse manager or primary researcher and 1 candidate declined to participate (undisclosed reason). Majority of participants resided in Kingston & St. Andrew 38 (58.5%), and 31(47.7%) accessed care at the Comprehensive Health Centre. Of the 8 participants who could not be contacted, 6 were female and 2 male, all treated at UHWI and under family care.

There was female predominance 40(61.5%), and majority 60(92.3%) had been infected through vertical transmission. Participants’ mean (SD) age at enrolment was 15.4 (2.0) years, and 52(80.0%) were categorized as CDC category B and C . Majority of the participants had family-based care 44(67.7%), with 26(40.0%) adolescents cared for by either or both parents. Sixty (92.3%) mothers and 17(26.2%) fathers were HIV positive; 48(72.9%) biological parents were currently alive. Twenty-five (38.5%) participants reported their parents were on ART.

Most participants were on ART for greater than 10 years 54(83.1%). Sixty respondents (92.3%) reported receiving special instructions on how to take medication. Majority 63(96.9%) reported being educated about their diagnosis and importance of adherence by health care provider, 59(90.8%) thought they needed their medication to remain healthy and 62(95.4%) were able to afford their medication. Only 23(35.4%) reported using a reminder method, 83% of who set an alarm reminder, and 16(32.7%) received rewards (monetary) for adherence. Only 5(7.7%) had disclosed their diagnosis to family/friends. Majority 40(61.5%) felt supported by family, and 20(30.8%) received peer support. Of the 65 respondents, 6(9.2%) admitted to alcohol use, while only 1(1.5%) had tried cigarette smoking.

Overall self-reported adherence with ART (no missed doses over the past four days) was 66.1% among 43 ALHIV and higher in adolescents in residential facilities (94.7%) versus those in family care (54.3%) (p= 0.002).

The overall median (IQR) CD4⁺count 701 (501-1052) cells per µL was higher among those in residential care (p= 0.016) (Table 1). The overall median (IQR) viral load was 19 (19-2212) copies/mL and disproportionately lower among those in residential care, the majority of who (68%) had viral loads less than 20 copies/mL. Thirty-two (52%) participants had undetectable viral loads. There was no statistical difference in age, duration on ART, CDC clinical category by residential status (Table 1).

Table 1. Clinicopathological and biochemical characteristics of adolescents on antiretroviral therapy by mode of caregiving

Mode of caregiving

p-value

Characteristic

Residential care

Family care

Age (years), Mean (SD)

Median (IQR)

(N=65)

16.10 (1.8)

17 (13.7-17)

15.43 (2.0)

16 (14.5-18)

0.226

CD4 count (µl/ml)

Median (IQR)

(N=61)

960 (675-1286)

435 (96-916)

0.016

Viral load (copies/mL)*

Median (IQR)

(N=62)

19 (19-51)

192 (19-6700)

0.010

Years on ART n (%)

(N=65)

<5

5-10

>10

0 (0.0%)

1 (5.0%)

18(95.0%)

7 (15.0%)

3 (6.50%)

36 (78.50%)

0.186

CDC clinical category

n (%) (N=65)

A

B

C

3 (15.8)

13 (68.4)

10 (21.7)

26 (56.6)

0.673

*Viral loads quoted as undetectable or below level of detection (< 20 copies/mL) were quantified as 19.0 copies/mL.

Adherence was associated with attending UHWI clinic (p<0.05), living in residential facility (p<0.001), knowledgeable of ART name (p<0.05), experiencing few side effects (p<0.05), not admitted for HIV-related complications (p<0.01), and having reduced appointments impacted by COVID-19 (p<0.05). Adherence was not associated with gender, age, CDC clinical stage, parental HIV and survival status, education attainment, years on ART, HIV/ART education, adherence reminder, ART affordability, adherence reward, disclosure to family/friends, nor family/peer support.

Significant factors were further explored using logistic regression to assess likelihood of adolescents’ adherence to their ARV regimen (Table 2). Adherence was four times more likely among adolescents managed at UHWI (OR= 4.53, 95% CI (1.25, 16.43), adolescents who can name/describe ARVs (OR= 4.31, (1.09,17.04), and those who had reduced appointments due to the Covid-19 pandemic (OR= 5.36, (1.09, 26.41) and four times less likely if under the care of relatives other than parents, experiencing side effects or hospitalized with complications (Table 2). When all factors were included in the same model/equation to adjust for possible confounder effect, only “admitted for complications” was statistically significant (p=0.05). The logistic regression model was statistically significant (p=0.014), the model explained 53% of the variance in adherence and correctly classified 81% of cases.

Table 2. Multiple logistic regression analysis on factors associated with adherence among ALHIV on ART

Covariate	OR (95% OR)	p-value
Treatment site
CHC	1.00 (Reference)
UHWI	4.53 (1.25, 16.43)	0.022
BHC	0.82 (0.17, 3.95)	0.808
Primary caregiver
Parents	1.00 (Reference)
Self	0.44 (0.02, 8.29)	0.587
State	NA
Other (relative/partner)	0.21 (0.06, 0.75)	0.016
Can name/describe ARV
No	1.00 (Reference)
Yes	4.31 (1.09, 17.04)	0.037
Experience side effects
No	1.00 (Reference)
Yes	0.28 (0.09, 0.92)	0.035
Admitted for complications
No	1.00 (Reference)
Yes	0.19 (0.06, 0.65)	0.008
Covid reduced appointments
No	1.00 (Reference)
Yes	5.36 (1.09, 26.41)	0.039

Since adherence among adolescents in residential care approached 100%, further analysis was conducted specifically on adolescents in family care to explore barriers and facilitators in this group. Adherence was associated with parent(s) as primary caregiver (p<0.001), not admitted for complications (p=0.005), and ARV regimen (pill burden) (p=0.025). The logistic regression model showed adherence was increased among adolescents under parental care (OR=5.565, 95%CI 1.001, 12,485) (p=0.05).

None of the respondents felt that Covid-19 affected their access to ART, majority 44/46 (95.6%) perceived that adherence was not affected, and 6(13%) experienced reduced clinic appointments.

Self-reported adherence with ART among ALHIV attending ambulatory services in Kingston, Jamaica was low, with only two-thirds achieving optimal self-reported adherence (no missed dose in the preceding four days). Adherence was significantly higher among adolescents receiving state based/residential care compared to those in family-based care. The higher self-reported adherence in residential-based care adolescents was congruent with their higher median CD4⁺ counts and maximally suppressed viral load.

The suboptimal level of adherence places ALHIV at risk for drug resistance, treatment failure, and reduced future therapeutic options with subsequent disease progression (11). Our findings of low-level adherence are not surprising, and are congruent with findings among adolescents in other settings in North America (47), Ethiopia (37), and South Africa (10). Behaviourally-infected adolescents age 12-18 years in America followed longitudinally had self-reported adherence 69% at the initial visit and median time to nonadherence was 12 months (47), similar to our mainly vertically infected ALHIV. A cross sectional study among Ethiopian ALHIV 13-19 years had self-reported adherence of 79.1%, but these findings were not validated by more objective measures (37). South African ALHIV age 11-19 years were less adherent compared to adults and had lower rates of virological suppression and immunological recovery (10). A systematic review of adherence from 53 countries (both developed and lesser developed countries), involving over 10,000 ALHIV was 62.3%, using pooled analysis from eligible studies (11), shared/had results similar to our findings.

Children residing in state-based facilities follow a strict protocol for taking medication, enhanced by directly observed therapy (DOT). The benefit of DOT is highlighted in the superior immunologic and virological markers observed in ALHIV treated in residential facilities. This finding highlights the need for family centred support to replicate DOT and other supportive measures in the family home. Multisystemic therapy, an intensive home-based family therapy previously employed for treatment of antisocial behaviour, has shown favourable results in improving HIV knowledge and adherence outcomes among caregivers and children dealing with HIV (48).Also suggested as an option to improve outcomes for family care is a ‘day-clinic’ which provides multi-disciplinary multifaceted holistic treatment to paediatric patients on ART (49).

Factors positively associated with adherence in this study included adolescents’ ability to name/describe their medication, being managed at the UHWI, those whose appointments were reduced by Covid-19 pandemic, and having parents as primary caregiver among those in family-based care. Barriers included relatives as caregivers, a history of experiencing side effects of ART, being hospitalized with complications and a higher pill burden. The higher adherence seen in patients at UHWI may be explained by the majority of participants being in residential care and benefitting from directly observed therapy.

Adolescents with reduced appointments due to the pandemic had better adherence, however this subset of patients were those historically with good adherence and congruent immunological markers, and were allowed by the clinic staff to have fewer visits.

The positive impact knowledge of ART regimen has on adherence was previously reported at the UHWI by White et al (6) and is an important contributor to developing health literacy.

Poorer adherence among those who experience side effects and higher pill burden is similar with other studies (35,36,39) and highlights options for simpler, ideally single tablet regimens with low side effect profiles that enhance adherence among adolescents (41).

Health care system related factors seem less of a concern for adherence in this study, as majority respondents reported being educated about their diagnosis, and only a small percentage cited challenges with medication affordability. The access to and affordability of medication is enhanced through the National HIV/AIDS Programme, Jamaica (6,7). A consistent approach to psychoeducation and reinforcement is needed, as six respondents were either unsure or didn’t think they needed their medication to remain healthy.

Our study found no associationwith use of reminder tools, rewards for adherence, peer support group participation, with adherence, unlike other studies (35,36). The small sample size of our study may have been a confounding factor. Globally, health care systems including outpatient care have been affected by the Covid-19 pandemic (44), but our participants perceived no significant impact on their access to treatment and care, and expressed that the pandemic encouraged them to be more adherent due to fear of contracting Covid-19. Self-reported adherence was probably prone to recall bias and over-reporting, but the correlates of maximally suppressed viral loads and higher CD4⁺ counts among adherent adolescents substantiated the self-report. We targeted the outpatient services with majority of ALHIV in Kingston, however there were other facilities managing ALHIV in Kingston and wider Jamaica hence the findings are not generalizable. Data from clients who were not contactable and missing medical records would have been useful to characterize adherence patterns. These missing clients were all treated at the UHWI and under family care and thus could have introduced selection bias. Ideally a longitudinal study design and follow up of adolescents as they transition to adults would have provided more informative data.

Overall adherence level was 66.1% among a cohort of primarily vertically transmitted ALHIV in Kingston, Jamaica. Optimal adherence was more likely among those managed at specific treatment sites, knowledgeable about ARVs, and those with reduced/adjusted appointments due to Covid-19 pandemic, and less likely if cared for by relatives, experiencing ARV side effects, pill burden or hospitalized with complications. The importance of caregiver support during the teen years and supportive, client-centred health care systems during the pandemic are highlighted by these findings. Targeted multisystemic therapy and multi-disciplinary, multifaceted holistic treatment approaches are needed to mitigate barriers and optimise adherence among ALHIV as they transition the adolescent period.

ALHIV

adolescents living with HIV

ART

antiretroviral therapy

ARV

antiretrovial

BHC

Bustamante Hospital for Children

CHC

Comprehensive Health Centre

CI

confidence interval

CDC

Centers for Disease Control and Prevention

HIV/AIDS

Human immunodeficiency virus infection/Acquired immunodeficiency syndrome

IQR

interquartile range

OR

odds ratio

SD

standard deviation

UHWI

University Hospital of the West Indies

Ethics approval and consent to participate

Ethical approval was received from the Mona Campus Research Ethics Committee, and the South East Regional Health Authority Ethics Committee.

Written Informed consent was obtained from all subjects and their legal guardian(s)

Consent for publication

Not applicable

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Competing interests

The authors declare that they have no competing interests

Funding

There are no sources of funding for the research reported. The design of the study and collection, analysis, and interpretation of data and writing the manuscript were done by the research team.

Authors' contributions

RD conceptualised the paper, wrote the proposal, conducted the study procedure, analysed and interpreted the data and was a major contributor in writing the manuscript. AH supervised the development of the proposal and conduct of the study, assisted in data interpretation and edited the manuscript. KLO supervised the conduct of aspects of the study, reviewed and edited the manuscript. RP supervised the development of the proposal and conduct of the study and was a major contributor in writing and editing the manuscript. All authors read and approved the final manuscript.

Acknowledgements

The authors graciously acknowledge the nurse managers (especially Nurse Jacynth Moore) and healthcare personnel at the outpatient services of the University Hospital of the West Indies, Bustamante Hospital for Children and Comprehensive Health Centre, Kingston, Jamaica for facilitating introductions and access to the participating clients.

Authors' information

No additional information.

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No competing interests reported.

Adherence to antiretroviral therapy among adolescents living with HIV in Jamaica

Status:

Version 1

Abstract

Introduction

Methodology

Study Design

Study Setting

Participants and Sampling

Procedure

Recruitment

Data collection procedure and Instruments

Data Management

Data Analysis

Ethical Approval

Results

Discussion

Conclusion

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1