African Journal of AIDS Research ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/raar20 Antiretroviral therapy adherence and viral suppression among HIV-infected adolescents and young adults at a tertiary hospital in Ghana Isaac Justice Kobina Biney, Kofi Adesi Kyei, Vincent Jessey Ganu, Ernest Kenu, Peter Puplampu, Steven Manortey & Margaret Lartey To cite this article: Isaac Justice Kobina Biney, Kofi Adesi Kyei, Vincent Jessey Ganu, Ernest Kenu, Peter Puplampu, Steven Manortey & Margaret Lartey (2021) Antiretroviral therapy adherence and viral suppression among HIV-infected adolescents and young adults at a tertiary hospital in Ghana, African Journal of AIDS Research, 20:4, 270-276, DOI: 10.2989/16085906.2021.1998783 To link to this article: https://doi.org/10.2989/16085906.2021.1998783 Published online: 14 Dec 2021. Submit your article to this journal Article views: 7 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=raar20 African Journal of AIDS Research 2021, 20(4): 270–276 Copyright © NISC (Pty) Ltd AJAR ISSN 1608-5906 EISSN 1727-9445 https://doi.org/10.2989/16085906.2021.1998783 Research Article Antiretroviral therapy adherence and viral suppression among HIV-infected adolescents and young adults at a tertiary hospital in Ghana Isaac Justice Kobina Biney1 , Kofi Adesi Kyei2* , Vincent Jessey Ganu1 , Ernest Kenu1,3, Peter Puplampu1 , Steven Manortey4 & Margaret Lartey1,5 1Fevers Unit, Department of Medicine, Korle Bu Teaching Hospital, Accra, Ghana 2School of Biomedical and Allied Health Sciences, University of Ghana, Accra, Ghana 3School of Public Health, University of Ghana, Accra, Ghana 4Ensign College of Public Health, Kpong, Ghana 5School of Medicine and Dentistry, University of Ghana, Accra, Ghana *Correspondence: k.adesi@kbth.gov.gh With the introduction of antiretroviral therapy (ART), many HIV-infected children are growing into adolescence and adulthood. A facility-based cross-sectional study was conducted at the Fevers Unit of one of the teaching hospitals in Ghana. The Morisky Medication Adherence Scale (MMAS-8) and pill count were used to assess adherence, while measured viral load levels of participants were used to assess viral suppression. The rate of viral suppression (<400 copies/ml) was 68.2%. Participants with high MMAS-8 scores were 8.4 times more likely to be virally suppressed compared to those with low MMAS-8 scores (OR = 8.4, p = 0.003, 95% CI: 2.11–33.48). The commonest reason for missing doses of their antiretroviral drugs (ARVs) was forgetfulness. Efforts must be made by all stakeholders involved in HIV care to engage adolescents and young adults living with HIV (AYALHIV) on personal and/or group levels to help identify and improve particular ART adherence issues so as to increase viral suppression rates. Keywords: HAART, HIV, medication, resistance, viral load Introduction and young adults are those in the 20–24-year age bracket (World Health Organisation [WHO], 2013). Adolescents Adolescents and young adults have gained account for five per cent of all PLHIV and 12 per cent of new remarkable attention among persons living with human adult HIV infections (Govender et al., 2018; WHO, 2013). immunodeficiency virus (PLHIV) because they constitute In Ghana, the 2015 HIV prevalence among the general the only group where HIV-associated mortality is going up population was 1.62% (Dako-Gyeke et al., 2016). There despite the introduction of highly active antiretroviral therapy were 2 214 new infections among children 0–19 years and (HAART). The aim of the study was to determine the rate of the HIV prevalence rate among the 20–24-year group was adherence to antiretroviral therapy (ART) and related factors 0.46% (Dako-Gyeke et al., 2016; UNAIDS, 2017). as well as the rate of viral suppression among adolescents The introduction of HAART has been a major breakthrough and young adults living with HIV (AYALHIV) at an HIV clinic for PLHIV, but sustained optimal adherence is needed for the in Ghana. Although AIDS-related death and disease rates best outcome (Machtinger & Bangsberg, 2013). The main have generally and drastically reduced over the years with challenge to ARV treatment is HAART non-adherence which the advent of HAART, the proportion of the disease burden adversely affects clinical, immunological and virological cannot be underestimated. outcomes of patients (Chandwani et al., 2012; Machtinger & Bangsberg, 2013; Mini et al., 2012). Studies have reported Background that effective antiretroviral therapy should result in at least a The mortality rate among persons living with HIV (PLHIV) 10-fold decrease in HIV-1 RNA copies/mL in the first month has reduced over the years with the advent of highly active and suppression to <50 copies/mL by 24 weeks (Hammer antiretroviral therapy (HAART) (Govender et al., 2018). In et al., 2008; McMahon et al., 2013). A recent study has 2014, 2.0 million adolescents were reported to be living reported viral suppression as early as 12 weeks for a new with HIV worldwide, out of which over 82% were attributed regimen containing Dolutegravir (Walmsley et al., 2013). to be living in sub-Saharan Africa (Govender et al., 2018). Many factors affect the ability of HAART to suppress Adolescents are individuals in the 10–19-year age group viral replication such as inadequate drug exposure or African Journal of AIDS Research is co-published by NISC (Pty) Ltd and Informa UK Limited (trading as Taylor & Francis Group) African Journal of AIDS Research 2021, 20(4): 270–276 271 dosing, viral resistance and inadequate adherence to of 129 was obtained. An estimated 10% non-response rate therapy (Bennett et al., 2008). It has been reported that was added to give a total sample size of 142. Purposive adherence to chronic medication among adolescents sampling was conducted for AYALHIV attending the clinic. is lower compared with younger children or adults Participants were briefed about the study and those who (Adejumo et al., 2015; Wamboldt et al., 2002). With the met the inclusion criteria and consented were recruited. increasing population of adolescents and young adults The procedure was repeated on each clinic day until the in Ghana, observations have indicated the existence expected sample was obtained. of non-adherence to medication, thus poor HIV RNA suppression among this population. Adherence for the Data collection adolescents and young adults may differ in several ways. Data on sociodemographic characteristics and ART were For example, those in boarding schools with limited collected using a pre-tested structured questionnaire. caregiver support may not be adherent to medication The eight item Morisky Medication Adherence Scale schedules as compared to those who live with their parents (MMAS-8) with scores ranging from 1–8 was used to or caregivers and attend day schools (Kim et al., 2014). assess self-reported adherence (Al-Qazaz et al., 2010; The young adults may, however, discontinue medication Tan et al., 2014). Scoring on the MMAS-8 is as follows: for lack of parental control, especially when the biological less than 6 for low, equal or greater than 6 but less than 8 parents are dead (Kim et al., 2014). for medium, and exactly 8 for high (Al-Qazaz et al., 2010; There is limited data on adherence to HAART and viral Tan et al., 2014). For this study, a minimum score of 6 was suppression among adolescents and young adults living considered good adherence (Peyre et al., 2016). A pill with HIV (AYALHIV) in West Africa with the possible risk count was conducted by a trained pharmacist. Participants of developing drug resistance from poor adherence. In had their leftover pills assessed against their last clinic visit this resource-limited setting, knowledge of medication ARV supply. Discrepancies in pill count between the pills adherence issues among this population could inform policy available at the present clinic visit and those supplied at for interventions to improve the situation and avert the the last clinic visit were used to assess adherence. The development of drug resistance in this population. researchers used the announced pill count. Recently measured viral load levels of study participants were Materials and methods retrieved from their medical records. Viral load reports that were at most six months old from the date that the test was A facility-based, cross-sectional study with a quantitative done were considered recent. approach was conducted at the HIV clinic of the Fevers Unit in the study centre. The Fevers Unit offers both in-patient Data analysis and out-patient care for over 18 000 persons living with HIV, Data were entered, cleaned and analysed using STATA including over 200 AYALHIV. The HIV clinic conducts three Statistical software package (v. 2007). Scores from the out-patient clinics per week for adults and one out-patient MMAS-8 were analysed and presented as frequencies clinic for AYALHIV per week. This study was conducted over and percentages. Continuous variables were presented a five-month period (December 2017–April 2018) among as means and standard deviations. Simple bivariate AYALHIV who accessed health services at the HIV clinic. logistic regression analysis using self-reported medication Recruitment of the participants was based on two criteria. adherence on viral load levels was done. The significance The first was a minimum of two years after ART initiation, level for all analyses was set at a p-value less than 0.05. followed by the presence of a caregiver to give consent for participants under 18 years old, and assent from the Ethical consideration individual. This study was reviewed and approved by the ethics and The criteria of at least two years after initiation of ART was protocol review committee of the University of Ghana, adopted because the measurement of baseline viral load College of Health Sciences (CHS-Et/M.3–P.3.6/2018) and levels before the initiation of HAART is not a requirement at approval was also obtained from the head of the unit of the HIV clinic. However, two years after ART initiation is an the teaching hospital. The study has been performed ample time period to adequately achieve viral suppression in accordance with the ethical standards laid down in an as studies have reported a minimum of 12 weeks (McMahon appropriate version of the 2000 Declaration of Helsinki as et al., 2013). Again, two years after ART initiation helps to well as the Declaration of Istanbul 2008. The Institutional achieve the expected sample size required for the study Review Board (IRB) of the Ensign College of Public since a handful of the participants had been on HAART Health in Ghana assessed the research as meeting the for only six months. Only those still alive two years after requirements and complying with standards for data the initiation of HAART were interviewed. All individuals collection at the hospital. Approval was therefore granted in who were acutely ill and had co-infections at the time of November 2017 and was further accepted by the teaching recruitment were excluded from the study. hospital. Written informed consent was obtained from the Sampling participants and caregivers of participants below 18 years, The sample size for the study was calculated using the together with assent where applicable. All study participants CDC Epi Info7 following a population size of 200, a 95% consented before participating in the data collection activity. confidence level, 62.3% adherence rate among AYALHIV Any details that could disclose the identity of the subjects (Kim et al., 2014) and a 5% margin of error. A sample size under the study were omitted. 272 Biney, Kyei, Ganu, Kenu, Puplampu, Manortey & Lartey Results medication adherence (p = 0.020), while the other Sociodemographic characteristics demographic characteristics were insignificant (Table 4). A A total of 136 AYALHIV consented to participate in the simple logistic regression analysis revealed that participants study, giving a response rate of 95.8%. Their ages ranged with high adherence scores were 8.4 times more likely to between 14–24 years, with a mean of 18.47±3.26. Ninety- be virally suppressed than those with low adherence scores three (68.38%) of the participants were adolescents and (OR = 8.4, p = 0.003, 95% CI: 2.11–33.48) (Table 5). 43 (31.62%) were young adults. Approximately 52% of the participants were female. Almost 92% of participants were Table 2: Medication adherence assessment using MMAS-8 students, out of which 43% were in senior high school and (N = 136) 14.71% in tertiary institutions (Table 1). The range of duration on ART was 2 to 22 years (mean = 7.37, SD = 4.84). MMAS-8 Item Yes No Adherence to antiretroviral therapy n (%) n (%) The total of ART adherence using the MMAS-8 for the Do you sometimes forget to take your 81 (59.56) 55 (40.44)medicine? participants was 78.67%, which was high adherence. The Over the past two weeks, were there 30 (20.06) 106 (79.94) average adherence score obtained by participants was any days you did not take your 6.27±1.79. Approximately 60% of participants provided a medicine? “Yes” response to the question “Do you sometimes forget Have you ever stopped your medicine 23 (16.91) 113 (83.09) to take your medicine?” in the MMAS-8. Twenty-three without telling your doctor? (16.91%) participants confirmed that they stopped taking When you travel, do you sometimes 19 (13.97) 117 (86.03) their medications without informing their caregiver (Table 2). forget to bring your medicine? Only 97 out of 136 AYALHIV had a pill count done during Did you take all your medicine 125 (91.91) 11 (8.09) the study period due to the unavailability of pill containers for yesterday? assessment. The rate of adherence to antiretroviral therapy When you feel your symptoms are 24 (17.65) 111 (82.35)under control, do you sometimes stop using pill count was 93.81% (91/97) (Figure 1). The reasons taking medicine? for missing ARVs included forgetfulness (50.37%), change Taking meds every day is a real 34 (25) 102 (75) in daily routine (7.41%), side effects of ARVs (3.70%), inconvenience for some people. Do perceived stigma from peers (2.22%) and depression you ever feel hassled about sticking (1.48%). to your treatment plan? Do you have pill counts done during 97 (71.3) 39 (28.7) Viral suppression this period? Only 110 out of 136 AYALHIV had a recently measured viral load documented. Approximately 68% of them had viral Table 3: Bivariate analysis of factors associated with HIV viral load load levels less than 400 RNA copies/ml with a range of <20 (<400 vs ≥400), (N = 129) copies/ml to 335 850 copies/ml. There was a statistically significant association between self-reported adherence Viral load (MMAS-8) and viral suppression (p = 0.003). There was Characteristic p-value<400 ≥400 no significant association between viral suppression and MMAS8 N N 0.003 other variables (Table 3). A significant association was Low 6 12 found between one’s religious affiliation and self-reported Medium 48 18 High 21 5 Pill count 0.427 Table 1: Sociodemographic characteristics of adolescent and As expected 67 23 young adult populations living with HIV* (N = 136) More than expected 2 2 Less than expected 1 1 Characteristic Category n (%) Age group 0.526 Age group 10–19 years 93 (68.38) 10–19 years 49 25 20–24 years 43 (31.62) 20–24 years 26 10 Gender Male 66 (48.53) Religious affiliation 0.111 Female 70 (51.47) Christianity 71 30 Educational level None 4 (2.21) Islam 4 5 Primary 8 (5.88) Gender 0.910 JHS 47 (34.56) Male 33 15 SHS 58 (42.65) Female 42 20 Tertiary 20 (14.71) Educational status 0.113 Ethnicity Akan 61 (44.85) None 1 2 Ga/Dangme 20 (14.71) Primary 5 1 Ewe 30 (22.06) Junior high school 20 15 Other 25 (18.38) Senior high school 34 15 Religion Christian 122 (89.71) Tertiary 15 2 Islamic 14 (10.29) Employment status 0.306 Employment status Unemployed 124 (91.18) Unemployed 69 30 Employed 12 (8.82) Employed 6 5 African Journal of AIDS Research 2021, 20(4): 270–276 273 60% 50% 50% 40% 30% 20% 15% 10% 10% 8% 6% 3% 4% 2% 2% 2% 0% REASON FOR MISSING ANTIRETROVIRAL THERAPY Figure 1: Bar chart showing commonest reason for missing antiretroviral therapy Table 4: Bivariate analysis using MMAS-8 and selected variables Discussion of adolescent and young adult populations* The ART adherence rate determined using the MMAS-8 MMAS-8 was 78.7%, while use of the pill count, the adherence rate Characteristic p-value Low Medium High was 93.8%. The rate of viral suppression (<400 copies/ml) Age group 0.073 among our study participants was found to be 68.2%. The 10–19 years 21 56 16 findings of the ART adherence rate of 78.7% in this study is 20–24 years 8 20 15 higher than the global rate of 62% but lower than the 84% Gender 0.711 reported in Africa (Kim et al., 2014; Nachega et al., 2010; Male 14 35 17 Tan et al., 2014). In addition, the adherence rate in this Female 15 41 14 study was higher than the 65% reported in another study Religious affiliation 0.020 conducted in the United States of America (Chandwani et Christian 23 73 26 al., 2012), although it was lower than findings of 93% in a Islam 6 3 5 Educational status 0.445 study conducted in Uganda (Wiens et al., 2012). However, None 0 2 0 a similar adherence rate of 79% was reported in a study Primary 1 4 4 conducted in Brazil among adolescents living with HIV (Filho Junior high school 10 25 12 et al., 2008). The difference observed could be as a result Senior high school 14 35 9 of the different adherence measurement scales used in Tertiary 4 10 6 the various studies. Whereas other medication adherence Employment status 0.916 assessment tools measure self-reported adherence Unemployed 27 69 28 spanning a period of a few days (1–3 days) to three months Employed 2 7 3 and is dose adherent, the MMAS-8 measures behaviour adherence from when the individual begun ART (Gokarn et al., 2012). Table 5: Measure of effect on viral suppression from self-reported The rate of adherence using pill count in this study was adherence (MMAS-8) 93.81%, which is lower than the 97% that was reported among Ugandan adolescents (Wiens et al., 2012) but MMAS-8 OR p-value 95% CI higher than the 60% reported among Romanian young Low (reference) 1 – – adults (Dima et al., 2013). The differences observed may Medium 5.33 0.003 1.74–16.34 be attributable to the fact that, over time, patients get used High 8.4 0.003 2.11–33.48 to a pill count and often tend to please health care staff by PERCENTAGE 274 Biney, Kyei, Ganu, Kenu, Puplampu, Manortey & Lartey presenting the required number of pills and/or empty pill Conclusion containers during an announced pill counting exercise as opposed to an unannounced pill count. Considering the fact Medication adherence was high among AYALHIV at the that the average duration on antiretroviral therapy was 7.4 study site, with 79% and 94% for self-report and pill count years, it may support the familiarity of pill counting among respectively. However, viral load suppression was measured the AYALHIV over time. at 68%. Self-reported medication adherence was an The commonest reason for missing ARVs in this study independent predictor of viral suppression. High medication was forgetfulness. This is consistent with an earlier adherence increases the odds of viral suppression by eight. qualitative study among adolescents at the study site where Sustained optimum adherence among AYALHIV is key in forgetfulness and perceived stigmatisation post-disclosure attaining and maintaining viral suppression. This ensures were identified as the commonest barrier to ART adherence a reduction in risk of HIV transmission, the prevention of (Garvie, Lawford, Banet, 2009). In a systematic review of HIV-related mortality and an improvement in overall clinical qualitative studies on adherence to ART, forgetfulness was outcomes. The commonest reason stated for missing daily identified as a major contributor to non-adherence (Vervoort ART was forgetfulness; however, the health care team et al., 2007). and the cohort have formed a common group where daily Contrary to the expectation of more than 90% viral reminders are posted to prompt the entire cohort to take their suppression among PLHIV, only 68% of AYALHIV ARVs in an attempt to curb forgetfulness. Efforts should also were virally suppressed. This could be explained by the be made by all stakeholders involved in HIV care in Ghana sub-optimal adherence levels observed among them when to engage the AYALHIV on personal and/or group levels, an earlier study established that medication adherence is helping to identify and improve particular ART adherence a strong independent predictor of virological suppression issues to increase viral suppression rates. (OR 3.41, 95% CI: 2.29–5.06) (Ankrah et al., 2016). The The findings should prompt policy makers such as the findings of this study on self-reported medication adherence AIDS Commission and implementers such as the National and viral load levels are consistent with an earlier study in AIDS Control programme, health workers and peer Latin America among children infected with HIV (Duarte et counsellors to develop interventional and support strategies al., 2015). In that study, it was reported that the probability to improve adherence and ultimately viral suppression of having a viral load measure < 400 copies/ml at 12 months among AYALHIV. was more than four times higher among those with perfect adherence than those with less than perfect adherence. Acknowledgements —Our appreciation goes to all study Another study among HIV-infected adults in Nigeria showed participants and their caregivers for their immense support during that a higher self-rated score of recent adherence was the study period. Our profound gratitude goes to Elaine Dovi of associated with lower odds of raised viral loads (Greig et al., the study site who conducted the pill count for the study. We also 2013), which is consistent with the findings of this study. express our heartfelt thanks and appreciation to the staff of the Infectious Disease Unit of the study site. As a result of forgetfulness contributing to non-adherence in our cohort, the rate of viral suppression of 68.2 % found in our study was lower than the UNAIDS global 90% target ORCID iDs (90-90-90) for PLHIV (UNAIDS, 2014). The low level of viral suppression observed among the study population may be Isaac Justice Kobina Biney – https://orcid.org/0000-0003-0824-896X a reflection of the true state of medication adherence. The Kofi Adesi Kyei – https://orcid.org/0000-0003-3485-5368 rate of viral suppression (<400 RNA copies/ml) observed Vincent Jessey Ganu – https://orcid.org/0000-0001-8649-4344 in the Ghanaian AYALHIV in this study was the same as Peter Puplampu – https://orcid.org/0000-0001-8589-5779 the rate of viral load suppression of 68% observed among Steven Manortey – https://orcid.org/0000-0001-5783-6595 black adolescents aged 16–23 years with HIV-1 in the USA (Garvie, Lawford & Flynn, 2009). However, the viral load References suppression rate observed in this study was lower than the 79% among Ugandan adolescents (10–19 years) (Bakeera- Adejumo, O. A., Malee, K. M., Ryscavage, P., Hunter, S. J., & Taiwo, Kitaka et al., 2008), the 82% in South Africa among AYALHIV B. O. (2015). Contemporary issues on the epidemiology and (16–24 years) (Mutevedzi et al., 2011) and the 94% among antiretroviral adherence of HIV-infected adolescents in sub-Saharan adolescents in Botswana (Ndiaye et al., 2013). 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