Megan Schoenbauer1, Melissa Saftner1, Scovia Nalugo Mbalinda2, Tom Ngabirano2
1School of Nursing, University of Minnesota
2Makerere University, Department of Nursing, College of Health Sciences
Abstract
Currently, 1.6 million people in Uganda are living with HIV, with most new infections occurring in adolescents. The COVID-19 pandemic also disproportionately affected adolescents, disrupting their access to HIV care. This study examined these interruptions using Bronfenbrenner’s Social Ecological Model, analyzing factors such as sex, financial status, education, family size and government policy.
A secondary analysis was conducted using data from a parent study of 154 adolescents (ages 15-20) receiving HIV treatment at Nsambya Home Care in Kampala. Between September and December 2022, 80 females and 74 males completed a COVID-19 impact questionnaire addressing healthcare disruptions, medical care concerns, distress and financial hardship. The average age was 17.9 years. Females were more likely than males to report interruptions in general care and in HIV care, though 95% of participants denied experiencing delays in care. However, 66% worried that the pandemic would impact their HIV care, with financial instability linked to difficulty in accessing HIV medication. The results of this study demonstrate that factors such as sex and financial status influence the extent to which COVID-19 affected HIV care in Uganda. Understanding the impact of COVID-19 on care, such as interruptions in medication therapy, can help healthcare providers better support adolescents living with HIV during public health crises.
Author Summary
There are 1.6 million people living with Human Immunodeficiency Virus (HIV) in Uganda, with most new infections found in adolescents. This study was conducted to examine the interruptions in care COVID-19 caused for adolescents living with HIV in Uganda. Participants completed a COVID-19 impact questionnaire between September and December 2022. Females were more likely than males to report interruption to care, although 95% of participants disagreed that their care had been disrupted or delayed. However, 66% reported fearing how the pandemic would impact their HIV care. Those who reported an inability to purchase basic necessities were more likely to report difficulty accessing HIV medications. The results of this study demonstrate that sex and financial status impacted the effects that COVID-19 had on HIV care in Uganda. Understanding the influence of COVID-19 on HIV care can help healthcare providers better support adolescents living with HIV during public health crises.
Introduction
There are approximately 38 million people living with Human Immunodeficiency Virus (HIV) worldwide (Joint United Nations Programme on HIV/AIDS 2022). However, the disease is disproportionately concentrated in eastern and southern Africa, which together account for 54% of all cases (UNAIDS 2022). In Uganda alone, there are currently 1.6 million people living with HIV, with most new infections found in adolescents (UNICEF 2023). Although HIV was once viewed as a terminal diagnosis, advancements in treatment now allow individuals to live long lives with the condition, making its management comparable to that of other chronic illnesses. In Uganda, efforts have increasingly focused on sustaining a high quality of life for those living with HIV through consistent access to antiretroviral therapy (ART) (UNICEF 2023). Many national programs prioritize the prevention of vertical transmission from pregnant individuals to their infants and treating those infected perinatally. As a result, childhood survival rates among children with HIV have increased by 50% (UNICEF 2023), contributing to an unprecedented number of adolescents living with the virus. While Uganda has made notable progress in reducing new infections and expanding treatment access, the COVID-19 pandemic disrupted care for many young people living with HIV (YPLWH), making it more difficult to attend routine medical appointments and obtain timely ART refills (Linnemayr et al. 2021).
Adolescents represent a particularly vulnerable group within Uganda’s HIV epidemic, with adolescent girls accounting for nearly two-thirds of all new infections in the country (UNICEF 2023). Without timely and consistent treatment, HIV can progress to Acquired Immunodeficiency Syndrome (AIDS), which remains a serious threat despite an overall decline in AIDS-related deaths. Alarmingly, the number of adolescents in Uganda who died from AIDS doubled between 2000 and 2017 (UNICEF 2023). Furthermore, the COVID-19 pandemic has exacerbated these challenges, through direct disruptions such as lockdowns and through secondary effects such as civil unrest and the diversion of health resources to other public health priorities (UNAIDS 2022). These disruptions have disproportionately affected adolescents, further compromising their access to critical services like ART and routine clinical follow-up appointments (Staden et al. 2022). Beyond the physical health consequences, the pandemic has also taken a toll on the mental health and psychosocial well-being of young people, adding another layer of complexity to HIV care and support during this period (Magson et al. 2021).
The Impacts of the COVID-19 Pandemic on HIV Care
A study of Ugandan adults with HIV in September 2020 found that 76% felt their ability to attend clinic visits had been impacted by the pandemic, and 54% believed that attending in person would increase their chances of contracting COVID-19 (Linnemayr et al. 2021). Travel to clinics was impacted not only by fear of the disease but also by nationwide policies intended to prevent the spread of COVID-19. A national lockdown was implemented on March 25th, 2020, forcing most public transportation and taxi services to shut down (Wagner et al. 2021). Transportation restrictions left many patients with no way to reach their appointments and strictly enforced curfews meant those who left the clinic late at night faced the threat of police violence (Linnemayr et al. 2021).
Inability to attend clinic appointments also reduced the likelihood of patients refilling their ART medications, until the lockdown was lifted in September 2020 (Linnemayr et al. 2021). For one of the largest HIV clinics in Uganda (Mildmay), there was a substantial drop in monthly visits, with visits in May 2020 totaling only 45% of the previous year’s (Wagner et al. 2021). ART medications are essential to prevent the spread of HIV and to prevent worsening illness from the virus. Adolescents have lower rates of ART adherence than the general population, and maintaining therapeutic relationships with healthcare providers is essential to combat this (Staden et al. 2022). The pandemic also exacerbated food insecurity, which may have contributed to increased ART nonadherence, as most ART medications must be taken with food (Wagner et al. 2021). Of the 324 patients surveyed from Mildmay, 194 (60%) reported increased food insecurity as a result of the pandemic, and 26 (8%) reported missing a dose of ART due to lack of food (Wagner et al. 2021).
Psychosocial Effects of COVID-19
Though the pandemic adversely affected mental health worldwide, it had a greater effect on those with chronic health conditions like HIV(Pettinicchio et al. 2021). People who already devoted more of their resources and energy to maintaining their health faced heightened worry, and the worry of being infected by COVID-19 led to poorer mental health outcomes (Pettinicchio et al. 2021). A survey of Canadian adults living with disabilities and chronic health conditions found that 38.2% reported increased anxiety, 38.9% increased stress and 18.2% increased despair during the pandemic (Pettinicchio et al. 2021). The negative financial and economic impacts of the pandemic further exacerbated these mental health struggles (Pettinicchio et al. 2021).
For chronically ill adults in the U.S., resource loss during the pandemic included not only economic resources, but also interpersonal resources like companionship, psychological resources like hope and physical health resources (McElroy‐Heltzel et al. 2022). As those living with chronic illness often have fewer resources to begin with, this loss led to increased anxiety, depression,and distress (McElroy‐Heltzel et al. 2022). However, perceived social support improved mental health outcomes. Chronically ill study participants in the U.S. who perceived themselves as being able to overcome adversity were protected from more severe mental health declines (McElroy‐Heltzel et al. 2022). Personal traits like optimism and resilience showed that participants could draw on their past experiences to cope (McElroy‐Heltzel et al. 2022).
Adolescents with HIV have had to navigate living with a complex chronic illness during a pandemic and the psychosocial effects of isolation during a developmental time when peer relationships are critical (Staden et al. 2022). Adolescents with HIV are at the intersection of two groups heavily impacted by COVID-19, and their developmental stage leads them to rely on peers for emotional support and development (Magson et al. 2021). An increased desire to be independent from their parents causes them to spend more time with peers, but lockdowns make this difficult. Adolescents who were separated from their peers due to the pandemic may be at increased risk of psychosocial disorders including generalized anxiety, social anxiety and depression (Magson et al. 2021). While young people (18-25 years old) from South Africa were most concerned about having basic needs met during the pandemic, they also expressed similar concerns to younger adolescents, including concerns about when schools would re-open, uncertainty about the future and the challenges of anxiety and depression (Gittings et al. 2021).
Financial Impacts of COVID-19
People living with HIV (PLWH) are particularly vulnerable to the economic impacts of the COVID-19 pandemic. They are more likely to face employment discrimination, have higher rates of unemployment and are more likely to work in the informal economy, which is not regulated or protected by the government (International Labour Organization 2020). Many PLWH around the world struggle with out-of-pocket healthcare expenses, and COVID-19 further increased the burden. One study of men who have sex with men living with HIV in Thailand found that the pandemic had negatively impacted their finances (Nitpolprasert et al. 2022). Multiple men stated that they feared contracting COVID-19 would force an HIV disclosure to their colleagues or employers, which could lead to employment discrimination. Nineteen of the 26 participants experienced financial stress or inability to afford basic necessities due to job loss or reduction in income since the start of the pandemic. In the search for new jobs, they feared mandatory HIV testing. This study found that the most serious impact of the COVID-19 pandemic to date for this population was on socio-economic status (Nitpolprasert et al. 2022).
Framework
This study was analyzed using Bronfenbrenner’s Social Ecological Model, also known as the Bioecological Systems Theory. The model originally recognized four different levels that influence health behaviors, which interact with and reinforce each other (Onwuegbuzie et al. 2013). In healthcare settings today, the original four levels are most commonly referred to as individual, interpersonal, organizational and community (Golden and Earp 2012). A fifth level, shown in Figure 1, has been added since the initial development and is included in some variations of the model (Golden and Earp 2012). The policy level takes into account national, territorial and local policies and their enforcement.
Figure 1. Levels of the Social Ecological Model
We examined multiple levels of Bronfenbrenner’s Social Ecological Model and their effects on HIV care for YPLWH. Interruptions in HIV care can be related to various factors at different levels, including the desire to avoid unwanted side effects of ART (individual), treatment costs (individual and organizational), limited appointment slots with providers (organizational), distance from care (community) and discrimination related to HIV status (community) (Dubrocq and Rakhmanina 2018). This study included questions related to general medical care interruptions, HIV care interruptions and fears of further interruptions related to COVID-19. Data collection occurred between September and December of 2022, by which time the participants had been living through the pandemic with HIV for over two years. This study aims to examine the level of interruption caused by the COVID-19 pandemic for adolescents living with HIV in Uganda, to fill the research gap for this particular subpopulation that consists of Ugandan adolescents.
Research Questions
How many adolescents had difficulty accessing HIV medications, decided not to attend an in-person HIV appointment or treatment or did not seek emergency care due to COVID-19?
How many adolescents agree or strongly agree that their HIV care or follow-up has been disrupted or delayed, and how does that compare to interruptions to their general medical care?
Is the experience of interruption of care associated with increased fear of further disruption?
Did adolescents who faced pandemic-related financial difficulties also face greater disruption to their HIV care?
Research Purpose Statement
The purpose of this study was to measure the level of interruption that the COVID-19 pandemic caused for HIV care for adolescents in Uganda. At the time of writing, no previous studies have been found that examine this topic. Much of the research up to this point on people living with HIV during the COVID-19 pandemic has been in populations other than adolescents, even though adolescents make up a significant portion of those infected with HIV (UNAIDS 2022). Though dedicating resources to novel viruses and outbreaks is an essential part of disaster response, unintended consequences for YPLWH must be examined to better prepare for future pandemics. There is currently a research gap on how adolescents specifically were affected during the pandemic, and there is little understanding of how HIV care for adolescents in Uganda was influenced.
Adolescents make up a significant proportion of those living with HIV across the world, and there are currently 1.6 million people living with HIV in Uganda, so this is a large population missed by previous researchers. By identifying the main consequences of the pandemic and how they differed by sex and financial status, this study fills the research gap in the understanding of how COVID-19 affected adolescents with HIV.
Materials and Methods
Study Design
This study was a secondary analysis of a prior research study. The primary study was a quantitative, cross sectional study conducted by Melissa Saftner and a team of researchers from the University of Minnesota and Makerere University in Kampala, Uganda.
Primary Study
The primary study examined adolescent readiness to transition to adult HIV care and COVID-19 impacts on HIV care. Their target population was Ugandan adolescents, and they recruited a convenience sample of 156 participants aged 15-20 years living with HIV in Uganda. All participants were in active antiretroviral treatment through Nsambya Home Care (NHC), an HIV ART treatment program in Kampala, Uganda. Study participants were required to be aware of their HIV status. Participants and parents/guardians of potentially eligible participants were informed about the study by program counselors at NHC, and those who were interested were referred to a study team member for further information and consent. The present study includes all participants from the parent study, excluding two who had begun participating in the study but did not finish it.
Study Procedures
Researchers described the study procedures, including risks and benefits, to interested participants. Participants 18 years and older completed a written informed consent form, and participants below the age of 18 provided assent after their caregivers provided written informed consent. Participants then completed a short demographic questionnaire on an electronic tablet through REDcap (Harris et al. 2009) to allow the research team to characterize the sample and examine potential differences in answers based on categories such as age or sex. Finally, participants completed the Self-Management and Transition to Adulthood with Rx Treatment (STARx) (Ferris et al. 2015) and COVID-19 surveys. Participants received reimbursement for transportation and time for research participation in the form of 15,000 Ugandan shillings (approximately 4 USD). Data were collected between September and December of 2022 and were de-identified to protect the privacy and confidentiality of participants. To validate a tool such as the STARx, including the assessment of its psychometric properties and to conduct factor analysis, methodological guidelines recommend a sample size of approximately 150 to 200 participants as a general rule of thumb, with 100 participants being viewed as adequate (Sapnas and Zeller 2002). Researchers purposefully sampled an even mix of males and females and both 15-17 and 18-20 year olds to understand the differences between sexes and age groups.
Ethics
The primary study was approved by the University of Minnesota Institutional Review Board (#00012756) and the Joint Council Research Centre (#JCRC-2021-15). It was also reviewed and approved by the Uganda National Council for Science and Technology (#SS1134ES).
Measures
This secondary analysis used two of the parent study surveys. The first survey given to participants contained 20 sociodemographic questions. These included select all that apply questions (e.g., whom do you live with), open-ended questions (e.g., how did you acquire HIV) and multiple-choice questions (e.g., who is responsible for your daily needs). The next part of the survey was a modified version of the Self-Management and Transition to Adulthood with Rx Treatment (STARx) questionnaire, the responses to which were not used for this study.
The final part of the survey was the COVID-19 impact questionnaire. Survey measures were drawn from an existing survey to report the impact of COVID-19 on the health and well-being of cancer patients, the COVID-19: Impact of the Pandemic and HRQOL in Cancer Patients and Survivors. That survey was developed in 2020 to assess the impact of the pandemic on cancer patients and survivors (Penedo et al. 2020). As the first studies utilizing this survey were published in 2022, data on its reliability and validity are not yet available. However, two Ugandan faculty members from Makerere University reviewed the questionnaire used in the parent study and provided feedback to improve its face validity. The survey included 39 items related to participants’ quality of life and psychosocial adaptation during the pandemic and 15 items related to the impact of COVID-19 on participants’ HIV-specific care. Survey items were divided into seven domains: COVID-19-specific distress, healthcare disruptions and concerns about medical care, disruption to daily activities and social interactions, financial hardship, perceived benefits of COVID-19, functional social support and perceived stress management/ability to manage stress. These survey items were framed using Bronfenbrenner’s Social Ecological Model to study individual, organizational and community impacts.
We focused on three domains: healthcare disruption and concerns about medical care, COVID-19-specific distress and financial hardship. Questions in the healthcare disruption section included “My general medical care or follow-up has been disrupted or delayed,” with answer options ranging from strongly agree to strongly disagree, and, “Due to COVID-19, did you decide not to: seek emergency care in an urgent care facility or emergency room,” with yes/no answer options. Questions in the COVID-19-specific distress section included, “I fear how the COVID-19 pandemic will impact my HIV care,” with answer options ranging from “Strongly Agree” to “Strongly Disagree.” Questions in the financial hardship section included “Due to COVID-19, my household income has…,” with answer options including increased, decreased or not changed and “My family has not been able to purchase or obtain basic necessities,” with answer options ranging from “Strongly Agree” to “Strongly Disagree.”
Data Analysis
Data were analyzed using the SAS, version 9.4. Descriptive statistics were used to describe the sample characteristics on variables such as age, sex, self-rating of health status, education, how the participant acquired HIV and how long they have been on ART. The proportions of adolescents who had difficulty accessing medications, HIV appointments and emergency care were then reported using means. Breaking down the sample with these descriptive statistics allowed the researchers to use Pearson’s Chi-Square test to determine if there was a difference between expected and observed data and if there was a statistically significant relationship between the variables. Pearson’s Chi-Square test was used to study three of the research questions: the association between fear of disruption of care and experienced disruption of care, how many adolescents experienced disruptions or delays in their HIV care or follow-up versus how many experienced interruptions to their general medical care, and financial difficulty and level of interruption. The sample was divided by sex and age for analysis purposes.
Results
The final sample (n = 154) had an average age of 17.9 (SD = 1.7). Thirty-six percent of the sample was 15-17 years old (nl = 56), and 64% was 18-20 years old (nb = 98). Females held a slight majority (52%, nf = 80) over males (48%, nm = 74). The average female was slightly older (18.1, SD = 1.7) than the average male (17.7, SD = 1.7). Participants had an average of 5.6 people (SD = 2.95) living in their homes. Table 1 contains additional demographic information for the sample.
Table 1. Sample Demographics by Sex
Interruption to HIV Care
The first research question that guided this study was how many adolescents had difficulty accessing HIV medications, had decided not to attend an in-person HIV appointment or treatment or did not seek emergency care due to COVID-19. The second was how many adolescents agree or strongly agree that their HIV care or follow-up has been disrupted or delayed and how that compared to interruptions to their general medical care.
Approximately 21% of participants had difficulty accessing HIV medications due to the pandemic. However, only 6.5% reported that their general medical care had been disrupted or delayed, and only 5.2% stated that about their HIV care. Twelve percent reported they chose not to attend an in-person HIV appointment due to COVID-19, and 5.8% chose not to seek urgent or emergency care. Females were more likely than males to report disruption or delay in general medical care (p = .030, nf = 80, nm = 74) and HIV care (p = .015, nf = 80, nm = 74). There was not a significant difference in reported interruption of medical care (p = .243, nl = 56, nb = 98) or HIV care (p = .885, nl = 56, nb = 98) between the age groups of 15-17 years old and 18-20 years old.
Psychological and Financial Impacts
This study also sought to examine whether experiencing interruptions in care led to increased fear of further disruption and if adolescents who encountered pandemic-related financial difficulties also faced greater disruption to their HIV care. Despite most participants reporting that their care had not been disrupted or delayed, 66% reported fear of how the pandemic would impact their HIV care. Experiencing interruption in care was not associated with increased fear of disruption, 95% CI [-.022, .067]. Males were more likely than females to report fear of the pandemic’s impact on their HIV care (p = .039, nf = 80, nm = 74). There was no significant difference in reported fear between the age groups of 15-17 year olds and 18-20 year olds (p = 0.167,nl = 56, nb = 98).
Forty-seven percent of participants reported that they or a family member had lost their primary income due to the pandemic, and 55.8% reported a decrease in household income. Seventy-nine percent came from families that had experienced financial difficulties, and 10.4% had not been able to purchase or obtain basic necessities like food or personal care products. Adolescents who reported an inability to purchase basic necessities were more likely to have difficulty accessing HIV medications due to COVID-19 (p < .001, ny = 32, nn = 122), with 32 answering “yes” to “Due to COVID-19, did you have difficulty accessing your HIV medications?” and 122 answering “no.” Loss of primary income (p = .116, ny = 32, nn = 122), decrease in household income (p = .507, ny = 32, nn = 122), and financial difficulty (p = .372, ny = 32, nn = 122) were not associated with increased reporting of difficulty accessing medications. Inability to purchase basic needs, loss of primary income, decrease in household income and experiencing financial difficulty were not associated with an increase in reports of HIV care or follow-up disruptions or delays. Neither sex or age group was more likely to report negative financial impacts due to the pandemic.
Discussion
The first research question addressed the number of adolescents who had difficulty accessing HIV medications, decided not to attend an in-person HIV appointment or treatment or decided not to seek emergency care due to COVID-19. Twenty-one percent of participants reported difficulty accessing HIV medications due to the pandemic. This was nearly double the number who reported that they chose not to attend an in-person HIV appointment due to COVID-19 (11.7%) and significantly more than those who chose not to seek urgent or emergency care (5.8%). This differs from a 2020 study with Ugandan adults living with HIV, which found that 14% of participants faced negative effects on ART adherence, but 76% experienced difficulty getting to clinic appointments (Linnemayr et al. 2021). These differences may suggest that adolescents were less concerned with contracting COVID-19 than they were with missing in-clinic appointments. Alternatively, the timing of the two studies could have had an impact on the level of fear related to contracting COVID-19.
Although adolescents chose to attend scheduled in-person appointments when possible, they still faced many practical barriers to accessing care. A national lockdown imposed in March 2020 shut down public transportation and limited private cars to one person per vehicle (Wagner et al. 2021). Since the minimum age for obtaining a driver’s license in Uganda is 18 years old and having a personal vehicle is costly, young adolescents had no easy way to get to a pharmacy or clinic (Uganda Driver Licensing System 2023). A study of 324 Ugandan adults found that the risk of running out of ART went from 5% before the national lockdown to 25% in June 2020 (Wagner et al. 2021). This is similar to the 20.8% of adolescents in this study who had difficulty accessing medications due to the pandemic. HIV care and follow-up must be continuous so that people living with the virus can get the antiretroviral medication they need, maintain their health and prevent the spread of the virus.
The second research question examined how many adolescents agree or strongly agree that their HIV care or follow-up has been disrupted or delayed and how that compared to interruptions to their general medical care. Five percent of participants stated that their HIV care had been disrupted or delayed, and 6.5% reported that about their general medical care. This was surprisingly low given higher levels reported in previous studies. Data from an EHR system at Mildmay Uganda, a hospital in Kampala, found that clinic visits had decreased by over 50% at the beginning of the national lockdown (Wagner et al. 2021). Risk of running out of ART increased from 5% to 25% (Wagner et al. 2021). Another study of Ugandan adults found that 76% agreed or strongly agreed that COVID-19 impacted their ability to come into the clinic for their appointments (Linnemayr et al. 2021). Differences may come from the fact that these studies were performed earlier in the pandemic before vaccines were available and when fear of COVID-19 may have been increased.
While very few participants reported that their general medical care or HIV care had been disrupted or delayed, females were more likely than males to report disruption. Adolescent females may have faced increased responsibilities during the pandemic, as domestic chores and family care activities primarily fall to female family members in Uganda (Farago et al. 2021). Additionally, 14% of girls are married by the time they are 15, and almost half are by age 18 (Farago et al. 2021). Girls and women are expected to prioritize the needs of others above their own in typical marital norms, so individual healthcare may be deemed less important. Females may also have reported care interruptions at higher rates because they are more likely than males to seek care in the first place (Himmelstein and Sanchez 2016).
The third research question asked if experiencing interruption of care led to an increased fear of further disruption. Though few participants reported that their care had been disrupted or delayed, 66% reported fear of how the pandemic would impact their HIV care. Experiencing interruption in care was not associated with an increased fear of disruption. Males were more likely than females to report fear of the pandemic’s impact on their HIV care, which may be related to the fact that men and boys are primarily responsible for earning household income in Uganda (Farago et al. 2021). Ugandan adolescents also characterize men as “dominant, financial providers, protectors, and decision makers” (Farago et al. 2021, para. 7). As these data reflect, these patriarchal stereotypes are harmful to both adolescent boys and girls. Because men are also less likely to seek healthcare due to factors like avoiding dependence and valuing bravery (Himmelstein and Sanchez 2016), adolescent boys may be at increased risk of care disruption.
Finally, the fourth research question examined if adolescents who faced pandemic-related financial difficulties also faced greater disruption to their HIV care. Almost half of participants reported that they or a family member had lost their primary income due to the pandemic, and more than half reported a decrease in household income. Adolescents who reported an inability to purchase basic necessities were more likely to have difficulty accessing HIV medications due to COVID-19. This may have been related to a number of factors, including inability to afford private transportation to pick up medications and difficulty making in-clinic appointments for medication refills. Since ART should also be taken with food, adolescents who faced food insecurity may not have taken their ART to avoid unwanted side effects (Wagner et al. 2021). Changes in daily schedules due to the pandemic may also have interrupted adolescent’s regular routines, leading them to forget to take medications (Wagner et al. 2021).
Nurses should consider a variety of factors like sex and financial status impacting patient adherence to medication, disruption to overall care and fear of interruption. Since a much higher proportion of participants reported difficulty getting medications than reported interruptions to HIV care, this may signify that difficulty accessing medications is the norm rather than the exception. Though Ugandan citizens can access healthcare for free, their public healthcare is significantly underfunded (Zikusooka et al. 2009). This forces those of lower socioeconomic status to rely on poorer quality services, which may be severely impacted by public health emergencies, while those who can afford to seek private healthcare may face fewer interruptions (Zikusooka et al. 2009). Infrastructure to support preventative healthcare and ensure ongoing access to healthcare for those with chronic conditions is an essential investment to prepare for future outbreaks.
Limitations
This study utilized a convenience sample of patients from Nsambya Home Care, an HIV ART treatment program in Kampala, Uganda. As this clinic is located in a busy area of the nation’s capital, it is unclear how experiences may differ for patients receiving care from other clinics throughout the pandemic. Patients from this clinic may not accurately represent all adolescents living with HIV in Uganda, impacting the generalizability of study results. For example, patients living close to the nation’s capitol and receiving care there may have faced different challenges than patients receiving care in more rural areas of the country. Because the sample was not randomly identified, study recruiters also could have missed specific patient populations who were not in the clinic on days that researchers were. As a result, study findings may over represent those who were not experiencing disruptions to care due to the clinic-based recruitment.
Although our sample was well balanced between males and females (48% and 52%), it does not represent HIV rates in Ugandan adolescents. HIV prevalence among 15-24-year-olds is estimated to be 4.2% for women and 2.4% for men (U.S. Embassy in Uganda 2017). A larger sample size that was more representative of population infection rates could have highlighted sex-related differences that were not found in this study.
Data collection for this study occurred from September to December of 2022. On September 20th, an outbreak of Sudan Ebola virus was declared by the Ugandan Ministry of Health (Bwire et al. 2023). By the end of the outbreak in January 2023, there were a total of 164 cases and 55 deaths. This may have impacted participants in a number of different ways; fear of Ebola and its impacts could have overshadowed fear of COVID-19, leading to a decrease in perceived impacts of COVID-19. Conversely, a return to lockdown and outbreak status may have brought back strong memories of the COVID-19 lockdown, leading to an increase in perceived impacts. Patients who were especially concerned about or impacted by Ebola may not have been able to attend clinic appointments, causing them to miss the opportunity to enroll in the study. Because data collection occurred at a unique moment in history, this could impact the validity of the study findings (Webling Library 2023).
As this study asked direct quantitative questions, we have no qualitative data related to the rationale for differences between responses. This can make it difficult to hypothesize what caused statistically significant results. Qualitative interviews with participants could have offered further insights into the impacts of the COVID-19 pandemic and helped clarify unexpected differences in results.
Conclusions
The results of this study suggest that this population of adolescents struggled with multiple negative consequences of COVID-19, which interfered with their HIV care. Despite not reporting the same level of impact other populations have experienced, participants reported a high level of fear of the pandemic’s consequences. Reported interruptions in care varied by sex and financial status. Males were more likely to report fear of interruptions to their care. Difficulty accessing ART was the highest reported interruption in care, with higher rates in those who were unable to purchase basic necessities. Females were more likely than males to report disruptions in care.
Recommendations
Future nursing practice should take these results into account. Multidisciplinary teams, including social workers, should be involved in care for every patient to ensure that financial status is not limiting their access to care. Nurses should also advocate for governmental policies that ensure equal access, especially during public health emergencies. Public health and government officials should consider these barriers when developing policies for crisis response, so that patients do not lose access to care. This could include building technology systems to conduct telehealth appointments, recruiting community workers trained in infection control to deliver at-home care and developing mail delivery systems for medications. Nurses should also pay special attention to the increased stress and fear that adolescents face during a public health crisis, especially those living with chronic illnesses. Multidisciplinary teams may also involve therapists and psychiatrists to help patients address these challenges. Taking these steps would ensure that nurses are caring for every aspect of their patients’ lives, since this study demonstrated that fear and financial struggles are two significant issues that Ugandan adolescents with HIV faced during the pandemic and continue to face today.
Future research should include qualitative interviews with patients about their experienced interruptions in care during the COVID-19 pandemic. This could allow researchers to understand impacts in a more comprehensive way, leading to policies that better address the most important factors. Multiple factors that were not addressed in this quantitative study could be addressed in a future qualitative study, including extended family and social support, understanding of HIV and the consequences of interruptions in care and baseline care quality. In order to understand the impacts on adolescents throughout Uganda, research could also be expanded to other clinics throughout the country, allowing researchers to compare and contrast the impacts of COVID in rural versus urban settings. Longitudinal studies on anxiety and fear related to interruptions in care and other effects of public health crises could offer direction for how to address them. These future research directions could address the currently existing gap identified in our study and build upon its initial contributions.
References
Alsan, M. and Cutler, D. (2013) ‘Girls’ education and HIV risk: Evidence from Uganda’, Journal of Health Economics, 32(5), 863–872, available: https://doi.org/10.1016/j.jhealeco.2013.06.002.
Bwire, G., Sartorius, B., Guerin, P., Tegegne, M. A., Okware, S. I. and Talisuna, A. O. (2023) ‘Sudan Ebola virus (SUDV) outbreak in Uganda, 2022: Lessons learnt and future priorities for sub-Saharan Africa’, BMC Medicine, 21(1), 144–144, available: https://doi.org/10.1186/s12916-023-02847-1.
Çıkrıkçı, Ö., Çıkrıkçı, N. and Griffiths, M. (2022) ‘Fear of COVID‐19, stress and depression: A meta‐analytic test of the mediating role of anxiety’, Psychology and Psychotherapy, 95(4), 853–874, available: https://doi-org.ezp2.lib.umn.edu/10.1111/papt.12406.
Dubrocq, G. and Rakhmanina, N. (2018) ‘Antiretroviral therapy interruptions: Impact on HIV treatment and transmission’, HIV/AIDS (Auckland), 10, 91–101, available: https://doi.org/10.2147/HIV.S141965.
Farago, F., Eggum-Wilkens, N. D. and Zhang, L. (2021) ‘Ugandan adolescents’ descriptive gender stereotypes about domestic and recreational activities, and attitudes about women’, Youth & Society, 53(5), 723–744, available: https://doi.org/10.1177/0044118X19887075.
Ferris, M., Cohen, S., Haberman, C., Javalkar, K., Massengill, S., Mahan, J., Kim, S., Bickford, K., Cantu, G., Medeiros, M., Phillips, A., Ferris, M. and Hooper, S. (2015) ‘Self-management and transition readiness assessment: Development, reliability, and factor structure of the STARx questionnaire’, Journal of Pediatric Nursing, 30(5), 691–699, available: https://doi.org/10.1016/j.pedn.2015.05.009.
Fleischer, B., Olum, R., Nakwagala, F., Nassozi, D., Pitua, I., Paintsil, E., Baluku, J. and Bongomin, F. (2022) ‘Higher intensive care unit consultations for COVID‐19 patients living with HIV compared to those without HIV coinfection in Uganda’, Journal of Medical Virology, 94(9), 4294–4300, available: https://doi-org.ezp1.lib.umn.edu/10.1002/jmv.27887.
Gittings, L., Toska, E., Medley, S., Cluver, L., Logie, C., Ralayo, N., Chen, J. and Mbithi-Dikgole, J. (2021) ‘“Now my life is stuck!”: Experiences of adolescents and young people during COVID-19 lockdown in South Africa’, Global Public Health, 16(6), 947-963, available: https://doi.org/10.1080/17441692.2021.1899262.
Golden, S. and Earp, J. (2012) ‘Social ecological approaches to individuals and their contexts: Twenty years of “health education & behavior” health promotion interventions’, Health Education & Behavior, 39(3), 364–372, available: https://doi-org.ezp1.lib.umn.edu/10.1177/1090198111418634.
Harris, P.A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N. and Conde, J.G. (2009) ‘Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support’, Journal of Biomedical Informatics, 42(2), 377–381, available: https://doi.org/10.1016/j.jbi.2008.08.010.
Himmelstein, M. S. and Sanchez, D. T. (2016) ‘Masculinity impediments: Internalized masculinity contributes to healthcare avoidance in men and women’, Journal of Health Psychology, 21(7), 1283–1292, available: https://doi.org/10.1177/1359105314551623.
Huang, Y., Wang, H., Diaz-Gonzalez de Ferris, M. and Qin, J. (2022) ‘Translation and validation of the STARx questionnaire in transitioning Chinese adolescents and young adults with chronic health conditions’, Journal of Pediatric Nursing, 71(1), 111–119, available https://doi.org/10.1016/j.pedn.2022.11.003.
International Labour Organization. (2020) COVID-19 and the world of work: A focus on people living with HIV, available: https://www.ilo.org/global/topics/hiv-aids/publications/WCMS_747263/lang--en/index.htm.
Joint United Nations Programme on HIV/AIDS. (2022) UNAIDS Data 2022, available: https://www.unaids.org/sites/default/files/media_asset/data-book-2022_en.pdf
Linnemayr, S., Jennings Mayo-Wilson, L., Saya, U., Wagner, Z., MacCarthy, S., Walukaga, S., Nakubulwa, S. and Karamagi, Y. (2021) ‘HIV care experiences during the COVID-19 pandemic: Mixed-methods telephone interviews with clinic-enrolled HIV-infected adults in Uganda’, AIDS and Behavior, 25(1), 28–39, available: https://doi-org.ezp2.lib.umn.edu/10.1007/s10461-020-03032-8.
Magson, N., Freeman, J., Rapee, R., Richardson, C., Oar, E. and Fardouly, J. (2021) ‘Risk and protective factors for prospective changes in adolescent mental health during the COVID-19 pandemic’, Journal of Youth and Adolescence, 50(1), 44–57, available: https://doi-org.ezp2.lib.umn.edu/10.1007/s10964-020-01332-9.
McElroy‐Heltzel, S., Shannonhouse, L., Davis, E., Lemke, A., Mize, M., Aten, J., Fullen, M., Hook, J., Van Tongeren, D., Davis, D. and Miskis, C. (2022) ‘Resource loss and mental health during COVID‐19: Psychosocial protective factors among U.S. older adults and those with chronic disease’, International Journal of Psychology, 57(1), 127–135, available: https://doi-org.ezp2.lib.umn.edu/10.1002/ijop.12798.
Mirzaei, H., McFarland, W., Karamouzian, M. and Sharifi, H. (2021) ‘COVID-19 among people living with HIV: A systematic review’, AIDS and Behavior, 25(1), 85–92, available: https://doi-org.ezp2.lib.umn.edu/10.1007/s10461-020-02983-2.
Moen, P., Elder, G., Lüscher, K. and Bronfenbrenner, U. (1995) Examining lives in context: Perspectives on the ecology of human development. Washington: American Psychological Association.
Nitpolprasert, C., Anand, T., Phanuphak, N., Reiss, P., Ananworanich, J. and Peay, H. L. (2022) ‘A qualitative study of the impact of coronavirus disease (COVID-19) on psychological and financial wellbeing and engagement in care among men who have sex with men living with HIV in Thailand’, HIV Medicine, 23(3), 227–236, available: https://doi.org/10.1111/hiv.13190.
Onwuegbuzie, A., Collins, K. and Frels, R. (2013) ‘Using Bronfenbrenner's ecological systems theory to frame quantitative, qualitative, and mixed research’, International Journal of Multiple Research Approaches, 7(1), 2–8, available: https://doi-org.ezp2.lib.umn.edu/10.5172/mra.2013.7.1.2.
Penedo, F.J., Cohen, L., Bower, J. and Antoni, M.H. (2020) [COVID-19: Impact of the Pandemic and HRQOL in Cancer Patients and Survivors], unpublished.
Pettinicchio, D., Maroto, M., Chai, L. and Lukk, M. (2021) ‘Findings from an online survey on the mental health effects of COVID-19 on Canadians with disabilities and chronic health conditions’, Disability and Health Journal, 14(3), available: https://doi.org/10.1016/j.dhjo.2021.101085.
Sapnas, K. G. and Zeller, R. A. (2002). ‘Minimizing sample size when using exploratory factor analysis for measurement’. Journal of Nursing Measurement, 10(2), 135–154. https://doi-org.ezp2.lib.umn.edu/10.1891/jnum.10.2.135.52552
Tang, M., Gaufin, T., Anson, R., Zhu, W., Mathews, W. and Cachay, E. (2022) ‘People with HIV have a higher risk of COVID‐19 diagnosis but similar outcomes to the general population’, HIV Medicine, 23(10), 1069–1077, available: https://doi-org.ezp3.lib.umn.edu/10.1111/hiv.13312.
Taylor, S., Landry, C., Paluszek, M., Fergus, T., McKay, D. and Asmundson, G. (2020) ‘COVID stress syndrome: Concept, structure, and correlates’, Depression and Anxiety, 37(8), 706–714, available: https://doi-org.ezp3.lib.umn.edu/10.1002/da.23071.
Staden, Q., Laurenzi, C. and Toska, E. (2022) ‘Two years after lockdown: Reviewing the effects of COVID‐19 on health services and support for adolescents living with HIV in South Africa’, Journal of the International AIDS Society, 25(4) available: https://doi.org/10.1002/jia2.25904.
Uganda Driver Licensing System (2023) Requirements for a new driving license, available: https://udls.co.ug/get-a-new-driver-licence.
UNAIDS (2022) Country Factsheets, Uganda, available: https://www.unaids.org/en/regionscountries/countries/uganda.
UNICEF (2023) HIV and AIDS, available: https://www.unicef.org/uganda/what-we-do/hiv-aids.
U.S. Embassy in Uganda (2017) Determined to reduce HIV infections in northern Uganda, available: https://ug.usembassy.gov/education-culture/cultural-exchange-programs/alumni/dreams/determined-reduce-hiv-infections-northern-uganda/.
Vrazo, A., Golin, R., Fernando, N., Killam, W., Sharifi, S., Phelps, B., Gleason, M., Wolf, H., Siberry, G. and Srivastava, M. (2020) ‘Adapting HIV services for pregnant and breastfeeding women, infants, children, adolescents and families in resource‐constrained settings during the COVID‐19 pandemic’, Journal of the International AIDS Society, 23(9), available: https://doi.org/10.1002/jia2.25622.
Wagner, Z., Mukasa, B., Nakakande, J., Stecher, C., Saya, U. and Linnemayr, S. (2021) ‘Impact of the COVID-19 pandemic on use of HIV care, antiretroviral therapy adherence, and viral suppression: An observational cohort study from Uganda’, Journal of Acquired Immune Deficiency Syndromes, 88(5), 448–456, available: https://doi.org/10.1097/QAI.0000000000002811.
Webling Library (2023) Nursing Resources: Validity Threats, available: https://researchguides.library.wisc.edu/c.php?g=861013&p=6170094.
Zikusooka, C. M., Kyomuhang, R., Orem, J. N. and Tumwine, M. (2009) ‘Is health care financing in Uganda equitable?’, PubMed [Preprint], available: https://pubmed.ncbi.nlm.nih.gov/20589107.
Acknowledgements
The authors gratefully acknowledge the help of Barbara J. McMorris, PhD and Michelle A. Mathiason in the development of this paper. Thank you to the UMN School of Nursing Foundation for funding this study and the healthcare providers and staff at Nsambya Home Care for their partnership.