“Undetectable, Now What?” HIV Provider Opinions on Barriers to Healthy Aging for Older People Living with HIV in North America

Background: People living with HIV (PLWH) experience age-associated health conditions earlier than their HIV-uninfected peers and have higher rates of co-occurring conditions that impact aging. Thus, HIV providers frequently confront issues related to HIV and aging. Objective: The objective of this project was to understand provider opinions about the care of older PLWH better. Design: This was accomplished using a quantitative survey. Participants: This study involved 681 physicians treating PLWH in North America. MAIN MEASURES: We collaborated with the Emerging Infections Network (EIN) to administer a ninequestion survey covering practice characteristics, attitudes, and perceived barriers in caring for older PLWH. Key Results: Two hundred and ninety-four (43.2%) responses were collected. Providers estimate that 35% (IQR: 25-50) of their HIV-infected patients were >50 years. The majority (72%) agreed it is difficult to care for older PLWH but had confidence in their ability to do so (85%). Most list a lack of time (55.4%) and insufficient multidisciplinary support (58.5%) as limitations to the effective management of older PLWH. Multi-morbidity was overwhelmingly perceived as the most important barrier to healthy aging (62.2%) followed by tobacco/alcohol use (10%), low income/savings (8.2%), polypharmacy (4.8%) and mental illness (4.4%). Loneliness, frailty, and cognitive difficulties were judged to be less important. In conclusion, HIV providers recognized the complexity of caring for older PLWH, and yet were confident they could care for this population. Conclusion: Multi-morbidity was identified as a major barrier to healthy aging, while syndromes such as frailty and cognitive difficulties were deemed less important despite a growing body of evidence that these geriatric syndromes are common in older PLWH. © 2020 Maile Y Karris. Hosting by Science Repository. All rights reserved


Background
Highly effective and well-tolerated, antiretroviral therapy (ART) has transformed HIV into a chronic disease [1]. The effectiveness of ART has changed the demographics of people living with HIV (PLWH). By 2020, estimates suggest 70% of PLWH in the U.S. will be older than 50 years [1]. The importance of recognizing and planning for this aging population is apparent in part because it appears that PLWH may experience "age-associated" disorders such as frailty, osteopenia, functional deficits, and cognitive decline at chronologically younger ages than HIV-uninfected peers [2][3][4][5]. PLWH are also burdened with high rates of co-occurring psychosocial conditions (i.e., substance use, poverty, social isolation) that may negatively impact aging [2][3][4][5]. On the other hand, older age is associated with improved ART adherence and higher rates of virologic control [6][7][8][9][10]. Thus, as PLWH age, HIV care providers may need to shift from focusing primarily on HIV-linked issues such as optimizing ART regimens to a broader engagement that includes management of issues associated with aging [11].
Recent evidence suggests that, in the United States, as a group HIV specialists may provide suboptimal primary care screening practices compared to their colleges caring for a general population and that this results in poorer clinical outcomes for conditions not directly linked to HIV infection [12]. For example, PLWH with hypertension cared for by HIV specialty care providers were 40% less likely to be prescribed antihypertensive medication compared to persons being seen by primary care providers (HR=1.4, 95% CI 1.016-1.942) [13]. In addition to these issues related to the delivery of competent primary care, the population of older PLWH have also been noted to have high frequencies of geriatric syndromes [14,15].
In one study, at least two geriatric syndromes were identified in 53.6% of 179 PLWH older than 50 years, who underwent a comprehensive geriatric assessment. The most frequent syndromes were pre-frailty (56.1%), difficulty with one or more independent activities of daily living (46.5%), and cognitive impairment (46.5%) [14]. Results such as this have served as the impetus for some centers to integrate geriatric expertise into HIV care, creating what some have termed the birth of geriatric-HIV medicine [16][17][18]. Despite growing enthusiasm for the integration of geriatric expertise into HIV management, it is unclear if such expertise will improve outcomes in older PLWH. It is also not known if HIV specialists value geriatric expertise, a factor critical to the uptake of geriatric consultation and subsequent implementation of geriatric recommendations. In concert with the Emerging Infections Network (EIN), we performed a nationwide survey of HIV specialists that sought out opinions about caring for older PLWH, perceived barriers to care, and perceived value of geriatric expertise. As is customary for EIN queries, to minimize innate questionnaire bias, this survey was vetted by volunteer infectious disease physicians unrelated to the study that provided feedback on sentencing structure and format of ranking questions. Provider opinions on caring for older PLWH were evaluated on a Likert-type scale with four response choices: strongly disagree, somewhat disagree, somewhat agree, strongly agree.

I Study Population and Study Design
Respondents were asked to rank the five most important barriers to healthy aging of 12 proposed. Respondents were also asked to rank the three most valuable resources to assist in the care of older PLWH of six proposed. Respondents could provide additional written comments on barriers to care and available resources for an aging population (Supplementary Table 1).

III Statistical Analyses
Chi-square and Fisher's exact tests were used for univariate analyses comparing demographics between non-respondents and respondents. Data were analyzed using SAS software version 9.3 (SAS Institute, Cary, NC). This study was not designed for formal qualitative analyses. However, respondents did provide comments, and these are provided in an online appendix.

I Characteristics of Respondents Compared to Non-Responders
A total of 345 of 681 eligible physicians (51%) responses were collected across North America (Table 1). This response rate and the difference in demographics are typical of EIN surveys [19][20][21][22]. All regions of North America were well represented, ranging from 46-59% of members in each regional area (divided into New England, Mid Atlantic, East North Central, West North Central, South Atlantic, East South Central, West South Central, Mountain, Pacific, and Canada). A full range of employers and hospital types were represented, and this did not differ from non-responders. However, non-responders were significantly more likely than respondents to have < 25 years of Infectious Diseases experience (p < 0.001).

II HIV Provider Characteristics and Opinions about Caring for PLWH
Of those who responded, 294 (43.1%) treated PLWH in the outpatient setting and proceeded to answer the remainder of the survey. Roughly half (153, 52%) provided primary care to PLWH. Slightly less (138, 47%) provided care in a Ryan White HIV/AIDS Program funded facility, and 168 (57%) practiced in a clinic that provided multidisciplinary (mental health, case management, etc.) support. Providers estimated that 35% (IQR 25-50%) of their population were > 50 years old. Most providers agreed that it is difficult to care for aging persons living with HIV (72.5% somewhat or strongly agreed) yet were confident in their ability to do so (85.3% somewhat or strongly agreed). Less than half reported adequate time to manage the issues that exist in aging persons living with HIV (44.5% somewhat or strongly agreed) and adequate multidisciplinary support (41.3% somewhat or strongly agreed) ( Table  2).

III Perceived Barriers to Healthy Aging in PLWH
Multi-morbidity was most commonly ranked among the top five of twelve barriers to healthy aging, followed by low income/savings, tobacco/alcohol use, mental illness, polypharmacy, isolation/loneliness, cognitive difficulties, frailty/low physical activity, illicit substance use, homelessness, high risk sexual behaviors and end of life planning (Figure 1). Of the listed barriers, multi-morbidity was most commonly ranked number one (n=181, 62%) followed by tobacco/alcohol use (n=30, 10%), low income/savings (n=23, 8%), polypharmacy (n=14,

IV Useful Resources in the Care of Older PLWH
Lastly, respondents were asked to rank the top three of six resources they believed could best assist in the care of older PLWH. Of all potential resources, case management was ranked by the most, followed by access to mental health providers, expanded guidelines, specialty geriatric consultation clinics, access to geriatricians, and access to substance abuse treatment centers (Figure 2). Seventy-eight of 294 (26.5%) viewed access to case management as the most valuable resource in the care of aging PLWH, followed by guidelines 73 (24.8%) and access to mental health services 65 (22.1%). Access to a specialty HIV geriatrics clinic 34 (11.6%) and geriatricians 32 (10.9%) were perceived as less important.

Discussion
In this survey of HIV specialist opinions and perceptions of caring for older PLWH, respondents stated that 35% of their practices are older than 50 years of age. A majority of HIV providers recognized that caring for older PLWH is complex (72% somewhat or strongly agreed) yet remained confident in their ability to care for this population (85% somewhat or strongly agreed). This perception contrasts with other studies of HIV specialists that report lower levels of comfort in caring for non-HIV associated chronic conditions such as hypertension and diabetes [23,24]. This discrepancy may be due to differences in confidence related to the general care of PLWH versus care for specific non-HIV conditions as our study did not specifically ask about  [25,26].
However, HIV specialists may be less effective in managing non-HIV co-morbidities, conditions that have a greater potential to negatively affect the health of most older PLWH than does HIV itself. One study evaluating age-appropriate cancer screening and diabetes management in PLWH found that while PLWH received most HIV-specific health maintenance interventions (such as pneumococcal vaccination and cervical cancer screening), they had low rates of recommended diabetes care (foot examinations, ophthalmologic examinations and microalbuminuria screening) [27]. In our study, respondents noted that lack of time, lack of multidisciplinary support, and insurance barriers all negatively affect the care of older PLWH.
We also found that HIV specialists perceived multi-morbidity as the single major barrier to healthy aging in PLWH, followed by low income/savings and tobacco/alcohol use. Geriatric syndromes like frailty and cognitive difficulties were viewed as less important. When asked what resources would be valuable for caring for aging PLWH, respondents valued case management, specific care guidelines, and mental health providers over geriatric expertise and support. This is not surprising, as most HIV providers in North America are trained in Internal Medicine or Family Medicine, and as such, are familiar with multi-morbidity, but not with geriatric syndromes [11]. Thus, there may be value in the future development of novel approaches to care that introduce geriatric syndrome diagnosis and management into HIV care. Lastly, it should be noted that surveys and focus groups of older PLWH suggest their primary concerns as they age are quite different than what the providers in this survey prioritize. These include their fragile social networks, mental health, and perceptions of cognitive decline [28][29][30].
The increasing medical and psychosocial complexity of older PLWH and projections that there will be an insufficient number of HIV providers to care for PLWH supports the urgency of exploring new approaches to HIV management. Our data suggest that HIV provider "buy-in" is key to implementing and disseminating new care models, such as the integration of geriatric assessments. These findings are support by a recently published paper detailing the development of the "Golden Compass HIV and aging care program" that was designed with patient and clinic staff perspectives [31]. The successful implementation of geriatric concepts into HIV care on a wider scale will likely require a) ongoing education of HIV providers on the changing needs of older PLWH and the potential value of geriatric expertise, b) data from randomized clinical trials demonstrating the effectiveness of geriatric care models, and c).
This study is limited by biases inherent in questionnaire-based work [32]. This study is also likely limited by response bias as most respondents had been in practice for greater than 25 years, and thus, the responses may over-represent views of specialists who trained in a different era of HIV care. Lastly, this survey only included input from physicians, and the opinions and perceptions cannot be extended to allied professionals who also care for older PLWH.

Conclusion
In conclusion, HIV providers recognize the complexity of caring for older PLWH, are confident in their ability to care for this population and tend not to perceive the impact of geriatric conditions on older PLWH nor to value geriatricians. Research designed to evaluate outcomes of comorbidities (including geriatric syndromes) in older PLWH are needed to answer the question "Undetectable, Now what?".