Introduction

The COVID-19 pandemic has led to massive disruptions to economies, health systems, and social life across the globe. Emerging evidence indicates detrimental effects of the COVID-19 pandemic on health funding, systems, and access, which may exacerbate vulnerabilities among children and youth in sub-Saharan Africa [1–7]. Adolescents living with HIV (ALHIV, ages 10–19), who are already at higher risk of poor health outcomes relative to younger and older people living with HIV (PLHIV), are strongly influenced by structural barriers to care and social determinants of health [8–11]. Complex adolescent-specific challenges to adhering to antiretroviral therapy (ART) and remaining in HIV care [9, 11] may therefore be compounded during the pandemic [4, 12–17].

Given the significant vulnerabilities and specific healthcare needs of ALHIV, the COVID-19 pandemic could have significant effects on adolescent well-being and HIV outcomes [18, 19]. Further, adolescents are at high risk for mental health challenges related to HIV stigma, isolation, and trauma [8, 20–22], and these may be heightened during disruptions to schooling, work, and social activities during the pandemic. Economic downturns resulting from the pandemic may leave ALHIV and their families vulnerable to food or housing insecurity, which can further complicate engagement in HIV care. Such consequences, seen in prior crises, must be characterized and addressed in the current pandemic, in preparation for future, inevitable occurrences [23].

Kenya reported its first case of COVID-19 on March 13, 2020 [24], and has experienced three “waves” of increased COVID-19 incidence: in July/August, 2020; October/November 2020; and as of this writing a third wave was occurring in March/April 2021 [25, 26]. Kenya implemented several mitigation strategies in March 2020, including border closures; a ban on international travel, social gatherings, closures of schools, religious places, bars, and restaurants; movement restrictions; and a curfew [27]. Some restrictions were lifted in June 2020; however, the most recent wave of the pandemic has prompted reinstatement of movement restrictions, closures, and a curfew [27, 28]. A prior large-scale crisis in Kenya—the 2007–2008 post-election crisis—prompted similar restrictions and resulted in challenges to retention in HIV care and ART adherence among PLHIV, impacting viral suppression and drug resistance [23, 29–33]. The effect of the ongoing COVID-19 pandemic on PLHIV in Kenya is not yet fully known.

Amid increasing COVID-19 case numbers in Kenya [25–27], we assessed effects of the pandemic on the social, economic, HIV care, physical, and mental wellbeing of ALHIV who were either retained in care or lost to program (LTP) at enrollment in an ongoing prospective study. We hypothesized that ALHIV may experience significant psychosocial effects of the pandemic, and that ALHIV with histories of care disengagement may be particularly vulnerable amid health system, economic, and social disruptions.

Methods

Results

The parent study is comprised of 378 ALHIV, including 308 who were retained in care and 70 who had been LTP at initial enrollment. Of this cohort, phone surveys were completed with 334 ALHIV or their caregivers (Table 1), including 275/308 (89.3%) participants from the retained group and 59/70 (84.3%) from the LTP group. Among all adolescents, the median age was 17.1 years (interquartile range 15.1–19.6) at the time of the survey. Females comprised 51.5%. Ninety-one percent of survey respondents were adolescents themselves; 8.7% of all respondents were primary caregivers to ALHIV in the ACE cohort. A greater proportion of surveys were completed by caregivers for ALHIV in the LTP group (27.1% vs. 4.7%, p<0.001).

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Table 1. Participant characteristics, COVID-19 knowledge, and preparedness among adolescents living with HIV in western Kenya, with comparisons by engagement cohort at enrollment in parent study.

https://doi.org/10.1371/journal.pone.0257210.t001

A number of survey findings were similar between the two groups, and are therefore presented for the total cohort. Statistically significant differences between the groups are specified.

Social and economic situation

At the time phone surveys were conducted, ALHIV were staying primarily at their usual residence (66.1% among LTP, 78.2% among retained); others had gone to a rural home (20.3% among LTP, 11.3% among retained); had gone to a relative (6.8% among LTP, 4.7% among retained); or were living in a group home or institution (5.1% among LTP, 2.9% among retained; Table 2). A greater proportion of LTP adolescents had left their usual residence, though this was not statistically significant (33.9% vs. 21.8%, p = 0.189).

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Table 2. Caregiver- and adolescent-reported social and economic impacts of the COVID-19 pandemic among adolescents living with HIV in western Kenya, with comparisons by engagement cohort at enrollment in parent study.

https://doi.org/10.1371/journal.pone.0257210.t002

A greater proportion of LTP adolescents were not enrolled in school (37.3% among LTP vs. 14.9% among retained, p<0.001), or were no longer doing school work (45.8% among LTP vs. 36.4% among retained, p = 0.017).

Prior to the pandemic, 35 (10.5%) of adolescents were working or earning income, primarily in the informal sector (94.1%) and mostly in public-facing jobs (77.1%). Of these, 26 (74.3%) adolescents lost their job or income during the pandemic. Over a third of adolescents (120, 35.9%) had relied on someone else at home who lost a job or lost income during the pandemic.

In total, 135 adolescents (40.4%) did not have enough food either some (121, 36.2%) or most (14, 4.2%) of the time. Adolescents’ primary sources of food during the pandemic were stores or markets (72.9% among LTP vs. 88.0% among retained, p = 0.007), their own farms (53.6%), a relative’s or friend’s farm (13.8%), or other sources (2.4%), which included food distributions from church groups, AMPATH, or other organizations.

In open-ended responses regarding major life changes during the pandemic, respondents emphasized challenges from being out of school, missing socialization with peers, as well as lacking money for food or basic needs, and a lack of work for themselves or their families.

Access to antiretroviral therapy

Regarding their ART medications, 99.4% of adolescents currently had ART with them or where they have been sheltering (Table 3). Two adolescents in the LTP group did not have ART; they had experienced 90 days and 330 days without ART, respectively. Of those with ART, 4.2% reported having less than a one-week supply. Seventeen percent of adolescents had concerns about running out of ART during the pandemic, and 5.1% reported skipping medication doses due to concerns about running out of ART medications. More adolescents in the LTP group (6.8%) than in the retained group (0.7%, p = 0.010) reported greater difficulties refilling medications during the pandemic. Challenges included lacking transportation (n = 4); curfew or travel restrictions (1); fear of traveling (1); restrictions on entering hospital site (1); and medication stock-out (1).

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Table 3. Caregiver- and adolescent-reported ART access and adherence among adolescents living with HIV during the COVID-19 pandemic in western Kenya, with comparisons by engagement cohort at enrollment in parent study.

https://doi.org/10.1371/journal.pone.0257210.t003

Health status, health-seeking behavior, and healthcare access

Among respondents, 44 (13.2%) adolescents had felt ill at some point in the preceding 2 months. Of these, 36 (80%) sought care at the HIV clinic (n = 19), a hospital (n = 10), or a pharmacist (n = 7) (Table 4). Five adolescents were continuing to feel unwell at the time of the survey. Illness symptoms at any point during the prior 2 months included: fever (9.6%), cough (9.9%), shortness of breath (3.0%), fatigue (4.8%), body aches (7.2%), congestion (12.0%), sore throat (3.6%), vomiting (2.1%), or diarrhea (4.2%). One adolescent had been hospitalized during the previous 2 months, for severe malaria.

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Table 4. Caregiver- and adolescent-reported health status and health-seeking behavior among adolescents living with HIV during the COVID-19 pandemic in western Kenya, with comparisons by engagement cohort at enrollment in parent study.

https://doi.org/10.1371/journal.pone.0257210.t004

Eight adolescents (2.4%) had been tested for COVID-19 at any time. No adolescents had been told by a medical provider that they had COVID-19. Nine adolescents (2.7%) had reportedly had close contacts who had been ill, including four who reported contacts with individuals diagnosed with COVID-19.

Eighteen adolescents (5.4%) experienced greater difficulties than usual in accessing medical care. These included challenges due to limited access to transportation (11), lack of money for medications (4), fear of traveling (3), travel restrictions (1), or clinic closures or stock-outs (1).

Mental health

Adolescent scores on the PHQ-2 were categorized as 0–2 (94.4%) vs. 3 or higher (5.6%), with those 3 or higher meeting the threshold for further evaluations for possible depression (Table 5). Similarly, scores on the GAD-2 ranged from 0–2 (94.8%) to 3 or higher (5.2%), with those 3 or higher meeting the threshold for further evaluations for possible anxiety.

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Table 5. Responses to mental health screening questionnaires among adolescents living with HIV in western Kenya during the COVID-19 pandemic, with comparisons by engagement cohort at enrollment in parent study.

https://doi.org/10.1371/journal.pone.0257210.t005

Discussion

In this cross-sectional survey of ALHIV currently or previously enrolled in HIV care, we observed multiple large-scale effects of the COVID-19 pandemic on schooling, income, and financial and food security for ALHIV and their households. More than a third of participants were no longer doing any school work. Of those who had been working, most had lost a job or lost income due to the pandemic. More than a third had experienced the loss of income for a family member on whom they relied, and more than 40% experienced food insecurity. Despite widescale economic, social, and healthcare challenges, few adolescents reported lacking ART, and we observed relatively low proportions of reported ART adherence challenges. Amid significant societal disruptions in western Kenya, and globally, during an unprecedented pandemic, it is and will remain essential to address the economic and social dimensions of the pandemic, particularly as they affect ALHIV, young people, and other vulnerable groups. Identifying areas and opportunities to further strengthen health systems to sustain HIV care engagement and access is of critical ongoing importance.

Surveyed ALHIV who were LTP at enrollment in the parent study had notable differences from the retained group, including being older, with a greater proportion of females, enrolled at the Rafiki Center, and initially enrolled in HIV care in later calendar years. The Rafiki Center serves a long-standing cohort of ALHIV, and includes a clinic population with particularly complex medical and social vulnerabilities, including orphaned and street-connected youth. Later age at HIV care enrollment may signal greater medical vulnerability and barriers to engagement, and both females and older adolescents have been observed to have risks for disengagement [10, 41, 42]. In this study we examined how these groups with differing care engagement at enrollment in the parent study experienced a range of impacts of the COVID-19 pandemic.

By some measures, greater social, economic, and health challenges associated with the pandemic were observed among ALHIV LTP at enrollment into the parent study compared to those engaged in HIV care. These included that among LTP ALHIV, a greater proportion had stopped schooling, or had left their usual residence due to the pandemic. Further, a larger proportion of LTP ALHIV experienced greater difficulties filling ART medications during the pandemic, or had forgotten to take ART in the past 3 days. Such differences might relate to underlying social vulnerabilities that drive disengagement from HIV care and which may exacerbate the impact of societal disruptions during the COVID-19 pandemic [8, 9, 11, 34]. At the same time, large proportions of all ALHIV in this study were experiencing financial or food insecurity and/or interruptions to school or work, reflecting widescale challenges affecting adolescents and their households. Further findings include that LTP ALHIV were less likely to avoid visitors or social gatherings. It is unclear if this finding may possibly relate to any underlying differences in social factors, such that they were less able to avoid visitors or social gatherings, or different sources of information regarding COVID-19, with the LTP group reporting higher proportions of e.g. WhatsApp or Facebook as main sources of information, and lower use of TV news or newspaper sources as compared to the retained group. In either case, further work may be needed for infection prevention messaging and interventions to mitigate risk of COVID-19 exposure to vulnerable ALHIV.

Very few studies have been conducted regarding the impacts of the COVID-19 pandemic among ALHIV or in sub-Saharan Africa, despite the particular vulnerability of this population, most of whom are living in eastern and southern Africa [43, 44]. One study of ALHIV in Kenya also found significant social and economic impacts [45]. The present study included a cohort of ALHIV with recent care disengagement, a group for whom the pandemic effects appeared to be more significant, as well as some more detailed assessments than in the previous study. Both studies strongly emphasize the urgent, acute economic and social impacts of the pandemic experienced by ALHIV in this setting.

As phone surveys were initiated in this and other PLHIV cohorts in the IeDEA East Africa Region, emergent needs of this population were immediately apparent. The majority of participants in this study were given referrals to either social work, clinical teams, or partnering community organizations, to address immediate needs including those food security, access to ART, costs of transportation to clinic, needs for pregnant adolescents, or other acute concerns regarding access to healthcare or education. Further, initial survey findings were used to support an emergency philanthropic effort at AMPATH, which included food distribution and economic support to PLHIV, as well as funding for health system capacity for managing COVID-19 patients. The health system was exceedingly strained by several factors, including patient care needs, limited availability of PPE, and by the deaths of several clinicians and staff. For ALHIV, a previously adolescent-dedicated clinic was re-purposed as a COVID-19 isolation ward, necessitating the temporary relocation of adolescent HIV services to a main clinic site which was not solely for adolescent care. This change, coupled with some turnover or sharing of clinic staff, as well as the loss of in-person adolescent support groups, presented multiple challenges to HIV care for adolescents. Severe stressors on health systems in the context of the pandemic limit their capacity to respond to the needs of PLHIV. We observed ways in which ALHIV may be particularly vulnerable amid widescale challenges to the health system.

Some findings from this study may point to areas of resilience in both the health system and among ALHIV to sustain HIV care engagement during a massively disruptive period. Among the cohort that was reached for this study, only two adolescents did not have ART with them; and 14 (4.2%) had less than one week of medication remaining. Both HIV care teams and the research team undertook intensive efforts from the start of the pandemic to ensure continued ART access among ALHIV in this group. These included outreach phone calls; provision of multi-month refills, ensuring refills, labs, or transfer of care at local facilities when needed; and working to ensure access to ART and to basic needs. At AMPATH, youth peer mentors had critical roles in ensuring access to ART and supporting retention among adolescents during this period, and have served to promote resilience in HIV clinical care during this crisis. The sustained ART access in this group may be compared with a study which demonstrated sustained ART provision for people treated for HIV in primary clinics in South Africa during the strict initial lockdown period [46].

Meanwhile, we observed that a minority of participants reported receiving official communication from their HIV clinic about COVID-19. We note that it is possible that some participants had been contacted but may not have considered such contacts as formal communications or as explicitly regarding COVID-19. It is also possible that the clinic had attempted to contact but was unable to reach others. There may be opportunities for further enhancing health system communications, including 2-way communications to identify and respond to patient needs, particularly for potentially vulnerable populations including people living with HIV. Enhanced communication may be needed both to disseminate health information, such as when symptoms may be managed at home, if appropriate, and to be responsive to emerging needs, during a crisis period such as this.

Regarding adherence, a slightly lower proportion of adolescents reported ART adherence challenges than in previous studies. Overall proportions of taking a dose >1 hour late in the last 7 days, missing at least 1 dose in the past 7 days, and forgetting to take ART within the last 3 days were 19.5%, 6.3%, and 6.3%, respectively. Studies of adolescent- or caregiver-reported adolescent adherence to ART in this setting have previously noted slightly higher proportions of taking ART >1 hour late in the last 7 days (26–29%); missing at least 1 dose in the past 7 days (16–18%); and forgetting to take ART within the last 3 days (8%) [47–49]. It is possible that respondents were less likely to report adherence challenges in phone surveys than in in-person studies. Nevertheless, this finding suggests that ALHIV in this group did not experience a higher degree of ART adherence challenges than is typical, and may have even had slightly better adherence as a group during this period. While some adolescents noted barriers to adherence, such as being around new household members to whom they had not disclosed their status, others described in open-ended items experiencing improved adherence or re-starting ART during this period. Described facilitators to adherence included motivation to stay healthy amid the pandemic, and not being in school (where anticipated stigma from peers may deter adherence). Several described multiple efforts taken by the clinic to sustain ART access and engage adolescents around any barriers to adherence or care, all of which may have helped promote adherence. Clinic efforts included frequent communication and support by phone and use of peer mentors in additional roles to support adolescent engagement. Further research is needed to understand impacts on ART adherence over the time course of the pandemic.

During a prior humanitarian crisis of the 2007–2008 post-election conflict in Kenya, impacts were observed on pediatric ART adherence and loss to follow-up [33]. It was noted, however, that perhaps the effects were not as great as would have been expected given the scope of conflict and displacement in western Kenya [33]. Then, as in now, it became apparent that while children and adolescents with HIV are vulnerable to large-scale crises disrupting care engagement, the resilience and responsiveness of the health program in these emergencies critically enabled sustained pediatric HIV care [30, 33]. Proactively building on and strengthening key supports such as systems for tracking and following up patients, provision of multidisciplinary support including peer support, and optimizing use of mobile phones for care support and coordination can further support care continuity during future periods of social crises or disruptions.

On mental health screens, 5–6% of adolescent respondents met thresholds to further evaluate for possible depression or anxiety, while greater numbers reported any degree of health symptoms on individual PHQ-2 and GAD-2 items (13.1%-15.1%). A separate study conducted with ALHIV in western Kenya during the COVID-19 pandemic found that 5–6% of ALHIV had PHQ-9 scores consistent with mild to severe depression; compared with 21% of young adults (20–24 years old) [45]. Limited data are available regarding the prevalence of mental health disorders among ALHIV in African countries [22]. A recent pilot study in this population reported depression 3.3% and anxiety 6.7% on baseline assessments [47]. Larger studies among ALHIV in Kenya and other countries in the region have found higher rates of depression (17.8%-25%) and anxiety (32.3%) [50–53]. Challenges exist measuring mental health across global settings, and there is a need to rigorously evaluate and validate mental health instruments for use with this population [22]. As we noted for self-reported adherence, while it is possible that use of these instruments in phone surveys may have limited sensitivity to detect mental health symptoms, given that the measured prevalence of symptoms was lower than might have been expected in this population and in a challenging time period, we must also consider the resilience of this group of ALHIV. Further study may clarify factors promoting mental health among ALHIV over this period, and should include longitudinal assessments of mental health.

As was the case before the COVID-19 pandemic, strategies are needed to support engagement in care and positive mental health among PLHIV across settings. Important areas of intervention include provision of social, economic, nutritional, and mental health support, upholding human rights, and addressing health disparities [3, 14, 54]. There may be important roles for mobile strategies for provision of HIV or mental health care, as well as for decentralized HIV care and multi-month ART refills [14, 15, 17]. On a practical level, this includes developing strategies for clinics to identify and respond to emerging needs of PLHIV, to adapt clinic services to virtual/phone modalities or longer follow-up times, and to facilitate in-person care when needed [18, 55, 56]. As adolescents have unique vulnerabilities, ensuring continuation of adolescent-dedicated services, including social and peer support, and adapting these services as feasible during the pandemic, is critical [18]. More broadly, children and young people living in sub-Saharan Africa may experience an array of social and health impacts from the pandemic, including those living with HIV, TB, or other health conditions, and approaches are needed to mitigate the broad impacts of the pandemic for young people, including on their education and healthcare access [3, 5].

Our study has several limitations. First, responses were self-reported and therefore prone to social desirability and other reporting biases. It is therefore possible that some impacts of the pandemic may be under-reported, including those related to ART adherence or mental health symptoms. Second, while we reached 88.4% of participants in the parent study, the response rate was lower among those recently LTP (84%), and some surveys were completed by primary caregivers which may be subject to measurement error. It is possible, if not likely, that social and economic impacts, as well as impacts on health access and ART adherence may be greater among the LTP ALHIV or caregivers who could not be reached. Nevertheless, the inclusion of a cohort of adolescents with histories of recent care disengagement is valuable, and we noted some important differences in effects of the pandemic affecting this group. We note that over the time course that surveys were conducted, some factors changed related to the pandemic and the healthcare response. For example, in later surveys, some respondents reported receiving food through a food distribution effort that was prompted by initial surveys. A further limitation is that in this study we do not have comparable data with other groups, such as PLHIV, or adolescents who do not have HIV infection, and therefore we cannot draw conclusions about the psychosocial impacts of the pandemic on ALHIV as compared to other populations in Kenya. Finally, we note that the comparisons in this study by engagement history are not explanatory, but rather describe responses according to baseline engagement groups; and as unadjusted analyses they do not control for confounding factors.

In this study we were able to examine ALHIV cohorts according to recent histories of care disengagement, as determined at their enrollment in an ongoing prospective study. This study does not reflect their current engagement in care, which might have changed during the pandemic. We observed that most ALHIV in this study, including those in the LTP cohort, had access to ART, which may reflect either recent care re-engagement and/or the efforts of the care program and the study team to ensure ART access. With the onset of the COVID-19 pandemic, HIV programs in this setting worked to ensure that all PLHIV had access to ART, including providing multi-month refills and refills at local dispensaries, and deferring clinic visits when appropriate. The study team also liaised with all ALHIV in this cohort to understand acute needs and ensure access to ART. Engagement in HIV care is not a static outcome; there is “churn” over time for individuals into and out of care [57–59]. It is valuable to understand how previous disengagement relates to health outcomes over time, and this study provides a “snapshot” of ALHIV health during a crisis period. It will be important to assess the trajectories of adolescents over the course of the pandemic, with regard to their re-engagement or disengagement from care over time, given the significant economic, healthcare, and social challenges wrought by the pandemic.

Conclusions

The COVID-19 pandemic has had devastating effects on education, and financial and food security for ALHIV and their households in western Kenya. ALHIV who experienced challenges with care retention before the pandemic may be especially vulnerable. Given the extent of educational, financial, and food security impacts of the pandemic, there is a risk for potential lasting effects of the pandemic which compromise adolescent health and trajectories into stable adulthoods. In this context, HIV treatment programs should consider approaches to support immediate and ongoing needs for patients and families, such as through nutritional or financial supports. At the same time, we observed sustained ART access, and lower self-reported adherence challenges or mental health symptoms than might have been anticipated, potentially signaling resilience and strengths of the ALHIV in this study and their care programs. It will be important to continue to assess these effects of the pandemic over time for ALHIV and to develop proactive supports for this vulnerable group during this crisis.

Acknowledgments

We acknowledge and thank the adolescents and caregivers who participated in this research and who generously provided their essential perspectives and insights.