People aging with HIV – protecting a population vulnerable to effects of COVID-19 and its control measures

ABSTRACT

Certain comorbidities known to increase the risk of poor outcomes in COVID-19 exist at higher rates in people with HIV; people aging with HIV (PAWH) face additional risk due to the association of advanced age with COVID-19 mortality. Cognitive and functional deficits and social barriers have been identified in cohorts of people aging with HIV. It is postulated that the COVID-19 pandemic potentially threatens PAWH disproportionately to the general population, both in mortality risk due to age and comorbidities, and in potential deleterious effects of policies that seek to drastically limit in-person interaction and access to healthcare systems. A description of and preliminary data from a demonstration project to improve geriatric assessments of people with HIV over age 50 in an urban HIV clinic are presented, in support of this theory. Advice is offered on key strategies utilized to continue to provide care to PAWH during the COVID-19 pandemic, including transition to telemedicine, vaccination, revision of staff roles, repurposing of funding, and a new reliance on available local resources.

KEYWORDS:

• Older people with HIV
• people aging with HIV
• COVID-19
• SARS CoV-2
• social isolation
• social distancing

Introduction

The global spread of severe acute respiratory syndrome coronavirus 2 (SARS CoV-2) has led to a pandemic of Coronavirus Disease 2019 (COVID-19), with highest mortality rates observed in African Americans, males, those of advanced age, those living in congregate settings, and those with certain comorbidities including but not limited to coronary artery disease, hypertension, type 2 diabetes mellitus, cerebrovascular disease, chronic kidney disease, liver disease, asthma and chronic obstructive pulmonary disease, and tobacco use (Centers for Disease Control and Prevention, 2021, October 11; Jin et al., 2020; Simonnet et al., 2020; Yancy, 2020; Zhou et al., 2020).

People aging with HIV (PAWH) have above average rates of age-related comorbidities, including low bone mineral density, cardiovascular disease, renal disease, neurocognitive deficits, and certain cancers (Dickinson & Fantry, 2012; Negredo et al., 2017; Wing, 2016). Increased risk of COVID-19 hospitalization, ICU admission, and death in PLHIV found in multiple studies is greatly diminished when age and comorbidities are adjusted for (Bertagnolio et al., 2021; Bhaskaran et al., 2021; Braunstein et al., 2021; Hadi et al., 2020; Mellor et al., 2021; Tesoriero et al., 2021; Wang et al., 2021; Western Cape Department of Health in collaboration with the National Institute for Communicable Disease, South Africa, 2021). However, CD4 cell count <200 cells/mm³ is an independent risk factor for poorer outcomes, including disease severity, hospitalization, ICU admission, and death (Braunstein et al., 2021; Dandachi et al., 2020; Hoffman et al., 2020; Tesoriero et al., 2021).

In addition to medical comorbidities, loneliness, poor social support, cognitive impairment, and difficulties with activities of daily living (ADL) have also been identified in PAWH (John et al., 2016). As the population of people living with HIV (PLHIV) ages, HIV clinics are finding a need to incorporate geriatric principles into the comprehensive care of PAWH (Davis et al., 2021).

Herein we describe the initiation and early findings of a demonstration project utilizing a new care model to improve geriatric care for PAWH at an urban US HIV clinic, which subsequently informed our approach to care of all PLHIV during the COVID-19 pandemic. This population of PAWH is found to have multiple medical factors that put them at high risk for poor health outcomes from COVID-19. High rates of baseline psychosocial vulnerability, including loneliness and social isolation, are also identified. Therefore, this pandemic potentially threatens PAWH disproportionately to the general population, both in mortality risk due to age and comorbidities, and in potential deleterious effects of policies that seek to drastically limit in-person interaction and access to healthcare systems.

Methods

Patients and setting

The THRIVE program (Together Healing, Reaching, Inspiring, to achieve Victory over Illness and Embrace life) is an HIV primary and specialty care clinic serving approximately 2500 PLHIV in Baltimore, Maryland. THRIVE patients have access to extensive wrap-around services (Table 1). The majority of clients are African American (88%) and male (59%) with 63% over the age of 50. Over a third of our patients report prior or current substance abuse and over half live below the federal poverty level.

Table 1. THRIVE program services.

Medical services	Wrap-around psychosocial support services
Primary Care and HIV Specialty Care	Social worker assigned to each patient Home based case management Employment counseling Housing coordination Emergency financial assistance Transportation assistance Nutritional counseling, nutritional supplements, grocery store vouchers Mental health counseling Substance abuse counseling Peer support coaches Support groups
Vaccinations STI testing and treatment Cancer screenings: cervical and anal Papinocolou smear, colposcopy, high resolution anoscopy, referrals for others On-site laboratory Mental health care Buprenorphine maintenance therapy DAART pharmacy Clinical HIV pharmacists
HIV Prevention
nPEP PrEP
HCV Specialty Care
HCV evaluation and treatment Dedicated HCV pharmacist Fibroscan

Key: STI, sexually transmitted infection; DAART, directly administered antiretroviral therapy; nPEP, non-occupational post-exposure prophylaxis; PrEP, pre-exposure prophylaxis; HCV, hepatitis C virus.

In March through June 2019, patient listening sessions were conducted to identify experiences and needs of PAWH. This feedback informed the development of the “Strengthening Therapeutic Resources for Older patients Aging with HIV” (STRONG) demonstration project. The project aimed to further characterize areas of concern for older adults with HIV identified in prior studies and to evaluate for additional possible vulnerabilities in our clinic population.

Starting in November 2019, PLHIV over the age of 50 receiving care at THRIVE were recruited to participate in the STRONG project, via fliers posted in the clinic space and patient self-referral. This study was approved by the University of Maryland Baltimore Institutional Review Board on April 10, 2019 (listening session; protocol # HP-00084887) and on October 11, 2019 (aging assessments; protocol # HP-00086173). An informed consent statement was read aloud and recorded for participants at the beginning of patient listening sessions; written consent was not required. Written informed consent was obtained from all participants for the aging assessments.

Study design and flow

Each patient underwent in-person geriatric assessments and completed a socio-demographic questionnaire, with study visits conducted by one of two graduate research assistants. All questions were read aloud regardless of patient-stated reading comprehension. Patients received a US$25 grocery store gift card at the completion of their assessments and were offered follow-up appointments to review results with their HIV specialist and a clinical pharmacist. Retrospective medical and pharmacy chart review was conducted concurrently. The completed assessment results, questionnaire, and chart review were shared with each patient’s HIV specialist, social worker, and clinical pharmacist. All results were entered into the patients’ medical records and recorded in REDcap (Research Electronic Data Capture) research database.

Assessments, questionnaire, and chart review

Patient demographics recorded included age, race, ethnicity, biological sex, sexual orientation, and gender identity. Validated assessments of physical, mental, cognitive, and social function (Cella et al., 2007; Dwyer, 1994; Fillenbaum & Smyer, 1981; Fried et al., 2001; Goff et al., 2014; Guralnik et al., 1994; Kroenke et al., 2001; Nasreddine et al., 2005; Spitzer et al., 2006) were chosen based on THRIVE provider input, gerontologist recommendations, and feasibility testing with patients for duration and comfort with assessments. Additional questions not addressed in other validated assessments were incorporated into a socio-demographic questionnaire in order to address themes identified in patient listening sessions. Topics included HIV history, stigma, loss, HIV disclosure, support systems, relationships, caregiving responsibilities, substance use, housing, employment, financial stability, community engagement, advanced care planning, and healthcare utilization. In addition to the assessments and the socio-demographic questionnaire, a pharmacist and a medical provider reviewed each patient’s medical records to identify opportunities for medication optimization (Goff et al., 2014; Grundy et al., 2019), evaluated for the presence of age-related comorbidities (Aberg et al., 2014; Dickinson & Fantry, 2012), and assessed for completion of age-related guideline-based health screens (Aberg et al., 2014; Oeffinger et al., 2015; Saslow et al., 2012; Wolf et al., 2018) (Table 2).

Table 2. Assessments utilized in STRONG study.

Parameter assessed	Tool used
Depression	Patient Health Questionnaire 9 (PHQ9)
Anxiety	General Anxiety Disorder 7 (GAD7)
Cognition	Montreal Cognitive Assessment (MoCA)
Physical performance	Short physical performance battery (SPPB)
Functional status (activities of daily living)	Older Americans Resources and Services (OARS)
Frailty	Fried Frailty Index
Nutritional risk	DETERMINE
Current HIV status	Most recent CD4 count and HIV RNA values
Cardiovascular risk	Recorded tobacco use status, lipid levels, diagnosis of hypertension or diabetes, and use of anti-hypertensives, diabetes medications, statin drugs, and aspirin; ASCVD risk score and recommendations
Renal disease	Urinalysis, GFR (UA with blood or protein, or GFR <60 defined as abnormal); HIV Primary Care guidelines
Liver disease	Liver function panel (AST, ALT, total bilirubin or alkaline phosphatase > ULN defined as abnormal); HIV Primary Care guidelines
HIV history (medical and personal experience)	socio-demographic questionnaire via patient self-report
Advanced care planning	socio-demographic questionnaire via patient self-report
Substance use, housing, employment, relationships, finances, educational attainment, support system, caregiving, community engagement	socio-demographic questionnaire via patient self-report

Key: AST, aspartate aminotransferase; ALT, alanine aminotransferase; ULN, upper limit of normal; MSM, man who has sex with men

Statistical analysis

Variables were collected as either binary, categorical, or continuous, as appropriate. In all analyses, either frequency distribution or the average was calculated for the individual variables. For binary or categorical data, the frequency distribution was calculated, while for continuous variables, the mean and range were calculated. All descriptive statistics were calculated using Microsoft Excel. Percentages, means, and ranges were evaluated to describe the patient population and the results of their assessments.

COVID-19 pandemic effect on study

On March 5, 2020, the first three cases of COVID-19 were reported in Maryland, and community spread was confirmed on March 11th. Progressive restrictions were implemented in March, with an eventual stay-at-home order announced on March 30th. In early March, THRIVE began postponing routine visits, transitioning to telemedicine, cancelling support groups, and ensuring patients had an adequate stock of their antiretrovirals, opioid replacement therapy, and other medications. The last study participant was enrolled on March 11th, with recruitment halted in order to protect this vulnerable population. We report preliminary results for the first 58 participants, with a focus on factors that warrant particular attention in the midst of the COVID-19 pandemic.

Results and discussion

Risk factors for poor medical outcomes of COVID-19 in PAWH

The mean age of the initial 58 participants was 59 years (range 50–73), 95% were African American, and 59% were male; advanced age, African American race, and male sex are each associated with higher COVID-19 mortality. Average CD4 cell count at the time of enrollment was 683 cells/mm³ and 98% had a suppressed HIV RNA. Prevalence of comorbidities associated with poor outcomes from COVID-19 was high, including hypertension (72%), abnormal renal function (59%), overweight (29%), obesity (33%), diabetes mellitus (22%), and abnormal liver function (14%). Calculated 10-year atherosclerotic cardiovascular disease (ASCVD) (Goff et al., 2014) risk was elevated with a mean of 17.7% (range 2.1–57.1) and 57% were current smokers (Table 3). While the percentages of co-morbidities were high, 67% did not have an advanced directive and 66% had not appointed surrogate decision-makers, highlighting a gap in advanced care planning in this group.

Table 3. Risk factors for COVID-19 severity (Centers for Disease Control and Prevention, 2021).

	Prevalence in STRONG cohort
Race
Non-white	95% African American
Gender
Male	59% male
Age
Increased; over 65 years	Mean 59 years Range 50–73 years
Co-morbidities
Obesity, overweight	33% obese, 29% overweight
Diabetes mellitus (type 1, 2)	22% diabetes mellitus
Cardiac disease (coronary artery disease, congestive heart failure, hypertension, cardiomyopathy)	76% hypertension ASCVD risk score average 17.7% ASCVD risk score range 2.1–57.1%
Cerebrovascular disease, neurological conditions, including dementia	MoCA average score 21.8 of 30 MoCA score range 10–29 78% cognitive impairment
Liver disease	14% abnormal liver function
Renal disease	59% abnormal glomerular filtration rate, hematuria, or proteinurea
Smoking, former or current	57% current smokers 80% ever smokers
Substance use	3% current heavy alcohol use 47% ever heavy alcohol use 3% current drug use 71% ever drug use 42% ever injection drug use
Mental illness	34% mild depression 21% moderate or severe depression 22% mild anxiety 22% moderate or severe anxiety
Lung disease (COPD, interstitial lung disease, pulmonary fibrosis, pulmonary hypertension, cystic fibrosis, asthma)	Not assessed
Pregnancy	Not assessed
Solid organ or blood stem cell transplant	Not assessed
Cancer, immunosuppressive medications, immune deficiencies	Not assessed
Sickle cell disease, thalassemia	Not assessed
Down Syndrome	Not assessed

Key: ASCVD, artherosclerotic cardiovascular disease; MoCA, Montreal Cognitive Assessment; COPD, chronic obstructive pulmonary disease.

Risk factors for deleterious effects of COVID-19 pandemic public health measures

Prior to the COVID-19 pandemic, 70% of participants reported struggling financially, 58% were receiving social security disability income, and only 16% had full-time jobs, indicating that baseline structural inequities could further make our PAWH more susceptible to negative outcomes from the COVID-19 pandemic. While critical to stemming the spread of SARS CoV-2, public health measures have also placed financial strain on many Americans, particularly those already impoverished like our population of PAWH.

In our cohort pre-COVID-19 pandemic, 34% met criteria for mild depressive symptoms and 21% for moderate to severe depression. Likewise, 22% had mild anxiety and 19% had moderate or severe anxiety. 50% reported living alone, 68% were single, and 71% reported a history of substance use, with 42% ever using injection drugs, and 3% with current drug use. During patient listening sessions conducted in March 2019, PAWH at THRIVE expressed vulnerabilities regarding loneliness, social isolation, and social support (Table 4). The sizeable proportion of baseline mental illness and substance use in our clinic population and the stated concerns regarding loneliness and social isolation indicate possible vulnerability to worsening of behavioral health issues in the setting of social distancing and quarantines. The mental strain of the ongoing loss of life from COVID-19, compounded with potential personal losses of employment, income, social connections, and even loved ones is profound for all but potentially exaggerated in this already vulnerable group.

Table 4. Patient listening session sample questions and responses.

Sample Questions

“What does it mean to be a long-term survivor?”

“What are you most concerned about during this time in your life?”

“What factors in your life have helped you age well? What factors have made getting older more difficult for you?”

“Do you have the social support that you want/need?”

Sample Responses

Gaps in social network

“For me, I had 5 kids, I'm all alone now. I don't have a love in my life, it's just me. … deep down inside, I don't wanna be alone … I don't wanna die alone … .”

Social support challenges due to life course changes

“I live alone, my kids are adults, you know, the nest is empty, so I'm home alone a lot and I have so many problems … a lot of things I can't really do, they're difficult for me to do at home.”

Social interaction providing purpose

“I think even being out just doing those things would give me purpose and help me … I live alone. Most of the time I am alone, but when I get out amongst the living I feel so much better”

Effect of support groups on well-being

“I really need the support groups to get me out the house, to keep me active and focus on what I need to be doing for myself. It's very important to me.”

At baseline, participants reported having difficulty or needing help with the following activities of daily living (ADLs) [10]: walking (48%), housework (26%), dressing (21%), getting out of bed (21%), bathing (16%), grocery shopping (16%), traveling (16%), preparing meals (12%), grooming (12%), toileting (7%), and taking medications (5%). The pandemic response has led to a forced and rapid restructuring of many aspects of daily routines. Roles in family and community units have changed overnight, with some people now needing to rely on others to obtain basic necessities safely or conversely losing the ability to safely have physical contact with their support system. With so many needing help with daily activities at baseline and with likely increased sedentary behavior during the pandemic, it is likely that COVID-19 alterations will have negative effects on those with baseline functional limitations and/or reduced access to groceries.

The average score on the Montreal Cognitive Assessment was 21.8 of 30 (range 10–29), consistent with mild cognitive impairment, and 26% had not finished high school. Since the majority of the participants are not actively in the work force (82%), they may not have had either a need to learn or access to education on modern technology. Many of THRIVE’s PLHIV and particularly PAWH do not have Internet access, computers, or smartphones and struggle with joining a telemedicine video visit. Their medical providers must make the difficult choice of requesting an in-person visit, which for most patients requires public transportation with potential exposure to SARS CoV-2, or relying on a telephone call alone to manage patients’ complex medical and behavioral health issues. While the necessary shift to telemedicine rather than in-person visits has allowed for the continuation of many critical aspects of medical care of PAWH and for continued engagement of PAWH with their THRIVE team, patients with lower levels of educational attainment, age-related cognitive decline, less technology literacy, and less access to technology may not fully reap the benefits of telemedicine.

Based on the data noted here, PAWH are more vulnerable to the effects of both the COVID-19 pandemic and the public health response. Due to the STRONG demonstration project initiation and early results, THRIVE was uniquely attuned to the vulnerabilities and needs of PAWH when the pandemic struck, which informed the care provided to all THRIVE patients during this difficult period. We were therefore positioned to lend guidance to other HIV care organizations in potential steps to mitigate the risk to this vulnerable population. Transition to telemedicine, revision of THRIVE staff roles, repurposing or obtaining new grant funding, and relying on available local resources were key to provision of care during this pandemic.

Meeting medical needs outside of in-person visits

Once local community spread of COVID-19 was identified, all routine medical and laboratory appointments, support groups, and home visits at THRIVE were suspended, and we shifted to telemedicine. This shift also de-congested our clinic space and allowed for us to temporarily move our smaller in-person practice to another site and use the larger clinic space to run a COVID-19 assessment center, available free of charge to any patient within the University of Maryland System, including THRIVE patients. Exceptions for in-person visits were newly diagnosed or sub-optimally engaged PLHIV, and other patients with urgent needs, including testing and assessment for COVID-19.

Social workers initiated conversations on advanced care planning via telemedicine and partners at the School of Law were available to complete advanced directive documents. Patients were provided with early or 90-day refills of all medications and home delivery if available. Pharmacists conducted telephonic medication reconciliations for patients with polypharmacy, consolidated medications from multiple providers and pharmacies, and synchronized refill dates to reduce patients’ trips to their pharmacies. Current funding mechanisms were redirected to the purchase of home sphygmomanometers for telemedicine visits in hypertensive patients. Funds for pulse oximetry machines and thermometers for any THRIVE patient diagnosed with COVID-19 were also made available. Patients were encouraged to obtain any urgently required blood work at outside private phlebotomy companies, rather than coming to our center (located within a hospital). Peer support coaches began calling all patients with no recent or upcoming appointment to schedule telemedicine visits and trouble shoot technological challenges to telehealth appointments. Grant funding was requested for THRIVE staff to acquire any needed telework equipment to be able to continue to assist patients in completion of online applications (e.g., insurance or unemployment applications) and paper forms. Systems were put into place to provide patients with educational information on COVID-19, information on THRIVE telemedicine capabilities, and a donated facemask and bottle of hand sanitizer.

Once COVID-19 vaccinations became available, an aggressive campaign to link medically vulnerable patients to mass-vaccination sites was initiated. Peer navigators, medical providers, social workers, pharmacists, and nurses called all patients 65 years and older, starting with the oldest patients first, to offer information on vaccination and assist patients in signing up for vaccine appointments. Patients hesitant to receive the vaccination but willing to learn more were scheduled for telemedicine visits with THRIVE clinical pharmacists. A vaccine educational session for clinical and non-clinical staff was held to dispel misinformation, improve staff vaccination rates, and encourage staff to act as vaccine ambassadors. Photos of staff and medical providers receiving their vaccinations, “frequently asked questions” guides, and local vaccination sites were displayed prominently in the clinic waiting room. Once vaccines could be requested for administration at individual sites, THRIVE moved quickly to obtain vaccines and coordinate administration for all eligible interested patients. Patients receiving the vaccine were further celebrated with a vaccine pin, the privilege of ringing THRIVE’s “vaccine bell” and could add a sticker to our “vaccine tracker”.

As the pandemic response progresses and restrictions on in-person interactions evolve, we plan to continue telehealth measures until it is safe for all patients to return in-person. Additionally, we will continue to protect vulnerable patients by implementing spaced-out appointment slots, physical distancing within the clinical space and continue to limit in-person interactions as appropriate. We hope to develop a grant-funded nurse-run mobile clinic for home visits, equipped with laboratory, vaccination, and telemedicine capabilities. As more information on true COVID-19 risk in PLHIV becomes available, preventative measures should be most targeted to those deemed to be the most vulnerable, which currently includes those of advanced age, with certain comorbidities, and with more profound immunosuppression.

Meeting patient resource needs

Through interactions between THRIVE staff and patients early in the pandemic, it became quickly apparent that people were struggling with obtaining needed resources, particularly food. Medical providers were encouraged to enquire about resource needs on telemedicine calls and to utilize social workers to address these needs. THRIVE relies on grant-funded grocery store food vouchers and meal delivery programs to supplement assistance that patients receive through the Supplemental Nutrition Assistance Program; however, soon after COVID-19 struck, the systems to process food vouchers were strained or inaccessible, and reduced grocery store supplies and delivery resources hampered efforts to get food to patients. Because THRIVE was networked with local HIV and HIV/Aging advocacy organizations, we became aware of new resources and forged new partnership that resulted in enhanced food delivery to patients with food insecurity. Additionally, THRIVE “Care Packages” including groceries, toiletries, and sanitizing items were made available to patients through courier service or curb-side pick up at the clinic. We also loosened volume restrictions on the provision of liquid nutritional supplements. In typical times THRIVE also provides public transportation fares to ensure patients can get to their appointments; to avoid the use of public transportation during this time, we expanded our capacity to arrange ride-share services instead. Urban HIV service organizations and clinics are often well equipped with resources; however, COVID-19 has forced immediate re-organization of existing models of care in order to meet patient needs.

Meeting patients mental and behavioral health needs

Aggressive measures to engage with patients in the midst of the COVID-19 pandemic were meant to counter social isolation and loneliness in addition to addressing medical needs. Patients were guided in downloading and using video call applications to connect with their own support systems. Due to national and local shortages of psychiatrists in the US, we had been operating under the “collaborative care model”, in which the social worker and mental health counselor discuss behavioral health needs of each patient with a psychiatrist to develop treatment plans. Subsequently, the HIV specialist prescribes psychotropic medications per the psychiatrist’s recommendation. This model left us well equipped to continue all mental health care with no interruptions. The transition to mental health counselor telephone visits actually increased show rates, with 38% more kept appointments in April than in February. Support groups were re-initiated over video platforms. Restrictions on methadone prescribing in Maryland were loosened under the state of emergency, allowing programs to provide one-month take home supplies of methadone. THRIVE replicated this with our buprenorphine/naloxone program, switching from weekly or bi-weekly urine drug screens, counselor check-ins, and prescriptions, to all monthly prescriptions and limited urine drug screens, but with frequent telephone or video check-ins with the counselor and prescriber.

Limitations

The COVID-19 pandemic remains an evolving situation. As such, strategies employed at one point and one site may not be applicable or advisable at different time points or in varied settings. The perspectives shared here are from a single-center urban US clinic that is well resourced through governmental and industry grants, and therefore may not be applicable to all sites, especially those with less flexibility in funding or staff roles or less well resourced.

The data are also taken from a small cohort of patients over age 50 living with HIV and attending the THRIVE clinic; members of this group elected to participate and completed enrollment, suggesting a level of executive function, availability, and interest in research that may not be representative of all eligible patients. However, this early data obtained does correspond well with known demographics for the clinic population. Data from the small cohort presented here were used to inform the care of a much larger clinic population, including those under age 50, who were not represented in this cohort. If this resulted in over-generalization of vulnerabilities, it is unlikely to have been detrimental to patients at lower risk.

Conclusion

Preliminary data from a cohort of PAWH highlights the disproportionate risk this group faces medically from SARS CoV-2 due to age and comorbidities, and the psychosocial vulnerabilities expected to result from COVID-19 public health policies. Despite these risks, reasonable strategies can be implemented to continue to provide comprehensive medical and mental health care and wrap-around services during this pandemic, as local resources allow. Suggested strategies include transition to telemedicine, vaccination, revision of staff roles, repurposing of funding, and new reliance on available local resources.

Acknowledgements

The THRIVE program and STRONG study group would like to acknowledge the patients participating in the STRONG study, THRIVE staff and providers, local HIV/Aging partners, including the Maryland Coalition on HIV and Aging, and Gilead Sciences.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

The STRONG demonstration project is supported through Gilead Sciences “Aging Positively” grant.