People with HIV and healthcare workers views on screening for cognitive impairment in people with HIV: A qualitative study

People with HIV are an ageing population with an increased risk of cognitive impairment. Although cognitive impairment is dependent upon assessment, the acceptability of screening for cognitive impairment is unclear. This study aimed to explore the views of people with HIV and healthcare workers regarding routine screening for cognitive impairment.


INTRODUCTION
Cognitive impairment (CI) is an increasingly important health concern in the context of an ageing HIV population.In the UK, approximately half of people accessing HIV care are 50 years or over [1].Therefore, the prevalence of age-related illnesses, including CI, is rising.Recent meta-analyses have indicated an overall prevalence of CI in people with HIV (PWH) of around 40% [2,3] (however, this figure includes asymptomatic cases which are of debatable clinical significance).In the last decade, a milder cognitive phenotype has emerged whereby the causes are multifactorial [i.e.HIV, combination antiretroviral therapy (cART) and host factors including cardiovascular and cerebrovascular diseases, co-infections, mental illness and lifestyle factors] and the impairment experienced is relatively stable.Indeed, studies have found that around 60% of PWH do not show deterioration over a 5-year follow-up [4].
Cognitive difficulties impact broad areas of life (including functional, physical, social and mental domains along with employment maintenance [5]).PWH who have CI report lower quality of life than both PWH who do not have CI and HIV-negative individuals with mildto-moderate dementia [6,7].Therefore, identifying issues early is critical for health and quality of life.Screening for CI is the first step of clinical management.It allows clinicians to determine which PWH are most likely to have CI, detect early signs of cognitive dysfunction, support PWH who may be struggling, and manage the modifiable risk factors contributing to the impairment seen [8].
There is discord between HIV guidelines regarding screening for CI, with few recommendations and little agreement on details, such as whether screening should be targeted at specific groups, the frequency of screening and what screening tool should be used.However, the 2018 Standard of Care for PWH released by the British HIV Association (BHIVA) [9] and the European AIDS Clinical Society (EACS) [10] guidelines recommend regular screening (annually and every 12-24 months, respectively) for all PWH, and at a greater frequency for those in high-risk groups (i.e.aged > 50 years, with symptoms of CI and having cardiovascular risk factors).Cognitive screening tools aim to effectively detect CI and use of these tools results in early intervention; however, the only HIV guideline to endorse a specific screening tool is EACS.EACS recommends the use of three questions pertaining to memory, reasoning and attention as an initial screen for CI, with a positive response to one or more of the questions initiating next steps in decision-making, beginning with an assessment of mental health as a possible underlying cause, prior to undertaking any further assessment of cognitive function [10].Despite the endorsements on screening from different HIV guidelines, a recent survey of UK HIV clinics found that only 61% of HIV services ask about cognitive symptoms routinely and there is little consensus on the screening tools that should be used [11].
Studies in the general population suggest that people want to know early if they have CI [12]; however, there are no data on preferences for PWH and the views of healthcare workers on this.While other studies report that PWH are concerned about CI [5,13], their preferences regarding screening are unknown.Moreover, little is known about how it is conducted in practice and perceptions on the benefits and harms of screening.Therefore, the aim of this study was to understand the acceptability of screening for CI in PWH by exploring the concerns of PWH and HIV healthcare workers about CI and their views on routine screening for CI as part of HIV care.

Study design
We conducted an exploratory qualitative study with participants recruited from HIV services in the south-east of England between September 2022 and January 2023.Indepth semi-structured interviews were conducted with PWH participants and focus groups were conducted with HIV healthcare workers.The study was designed based on discussions with our patient and public involvement (PPI) lead (GP), and all documents including topic guides were reviewed by PPI members.Analysis of transcripts and decisions regarding the themes identified were led by an experienced qualitative researcher (KB), and the team included a research assistant (SS), a research fellow in HIV and neurology (KA), and an HIV medical consultant/academic (JV).

Participants
Participants were patients, aged 18 and over, attending specialist HIV services.All had a diagnosis of HIV and were on cART.PWH who were too unwell, lacked capacity or were not able to provide informed consent were not recruited.Participation in the study did not include screening or a diagnosis of CI; however, PWH participants may have experienced screening and/or received a diagnosis for CI previously.HIV healthcare workers were those who worked in HIV services at the study sites in a clinical capacity.

Procedure
Clinicians in the HIV service advised potential PWH participants about the study and referred interested participants to the researchers.All PWH participants gave informed consent prior to participating.Interviews were conducted face to face (n = 12) or over the telephone (n = 8) depending on PWH preference.HIV healthcare workers self-referred following an email advert to HIV staff at the HIV service site.Focus groups were conducted either in person (n = 2) or on Microsoft Teams (n = 1), depending on individual logistical requirements.
All were audio-recorded, transcribed verbatim and checked for accuracy.Interview guides developed by the study team were used to structure the session.The topic guide combined a series of open-ended questions, and more specific prompts and probes.Key areas explored were: understanding of CI, experiences of being asked or told about CI within the HIV service, concerns about cognitive issues, experiences of cognitive issues, knowledge of screening for CI, concerns and benefits of screening for CI, whether screening should be offered and, if so, to whom and by whom (see Table 1 for key questions and probes).

Data analysis
A team-based analysis of interview and focus group transcripts was conducted by the study team to identify themes relating to the experiences of and views on screening for CI in PWH.Data were analysed using reflexive thematic analysis, informed by Braun and Clarke's (2006/2019) [14,15] six-phase process.Interviews and focus groups were analysed concurrently using the same coding frame to allow for exploration of commonalities and differences between the groups.Analysis was conducted by SS, who was supported by KA and KB.Phase 1 required SS to familiarize themselves with the dataset (reading and re-reading, immersive and familiarization with content); phase 2 involved coding [generating succinct labels (codes) that capture and evoke important features of the dataset].SS, KA and KB coded three transcripts independently, then met together to discuss areas of similarity and familiarity.Phase 3 involved generating initial themesexamining codes and collating data to begin to develop broader patterns of meaning (potential themes).This initial framework was developed collaboratively by SS, KA and KB, based on the three coded transcripts and then based on the further reading of two transcripts (SS and KA).Phase 4 required the continued development and reviewing of themes (checking candidate themes against coded data, themes were further refined, developed, split, combined or discarded).Healthcare workers were asked modified versions of the above, in addition to: 12. What prompts you to consider screening?
13. Describe the current process of assessing or screening patients in your service?
14. How could screening be improved?
15. How do you feel about screening for cognitive impairment?
The coding and themes were reviewed regularly by SS and KA, who followed an iterative process, with movement back and forth between different phases.Phase 5 involved the final refining, defining and naming of themes (this involved developing detailed analysis of each theme, deciding the scope and focus and naming themes).The final themes generated were decided in a team meeting between SS, KB and KA, who examined codes within themes independently, explored similarities and differences and decided upon final theme names and content.The last phase involved writing up by weaving together the analytic narrative and data extracts along with contexualising in relation to the literature [14,15].

Study participants
In all, 20 PWH completed interviews and 12 healthcare workers took part in three focus groups.Interviews with PWH participants lasted 18 and 70 min and focus groups lasted 60 and 115 min.The PWH sample consisted of 14 men and six women, with an age range of 30-79 years.
The healthcare workers' sample consisted of four staff nurses, three consultants in HIV and sexual health, two HIV clinical nurse specialist, one clinical professor of HIV medicine, one specialist registrar in HIV and one HIV-specialist clinical psychologist (see Table 2 for full participant characteristics).Three principal themes were identified to understand the views of PWH and healthcare workers on screening for CI in HIV services.These themes are summarized in the following sections and additional supportive quotations are provided in Table 3.

Theme 1: Cognitive impairment as a shared concern for people with HIV
All PWH participants generally understood the term CI to mean a decline in memory function.Some suggested that a diagnosis of CI would mean an individual might have issues with concentration, decision-making, ability to process information and a general 'slowing down of thoughts'.Knowledge of the causes of CI was varied: most participants did not know that as someone living with HIV they were at increased risk of developing CI, while others had some awareness that HIV can affect cognitive health.The majority of participants thought CI was likely to be the result of antiretroviral toxicities or a consequence of ageing.Importantly, several participants thought a diagnosis of CI was a diagnosis of dementia and thought cognitive decline was inevitable (quote 1).Most PWH participants we spoke to stated that they had experienced or had concerns about their cognitive health (previous or current).Several individuals stated that forgetfulness was an issue and described instances whereby they had forgotten where they were or what they were doing.These individuals described fluctuating cognitive problems, such a 'brain fog' and difficulties processing information sometimes, which impacted on confidence, particularly in social situations or when tasks required more effort.Regardless of current symptoms, most PWH participants stated that CI or dementia was a worry for them (quote 2).Interestingly, many individuals described a high threshold of severity when asked what would initiate help-seeking for cognitive concerns (quote 3).Moreover, individuals almost exclusively relied on memory function as the metric for assessing their cognitive health and reported that forgetfulness would need to be persistent and impact on function for them to seek help.PWH participants did, however, state that if they were asked directly by a healthcare worker, they would report any cognitive difficulties they were having.Some participants reported being unsure as to whom they should report cognitive concerns; however, most stated that it would be something they would comfortably bring up with their HIV care team.Interestingly, for these individuals, helpseeking was not necessarily due to their knowledge that cognitive issues and HIV can be linked, but rather because they see their HIV service as holistic, personcentred and one concerned with both HIV and non-HIV impacts on their life (quote 4).Most PWH participants did not recall having previously been asked about their cognitive health or being told about CI, or indeed cognitive health, by anyone in T A B L E 3 Themes with illustrative quotes.

Theme Illustrative quote
Cognitive impairment as a shared concern for PWH (1) 'We saw a lot of people with AIDS-related dementia, it was really scary… I bring that to my experience and think, "Oh god my God!Is that happening to me?"' (P16) (2) '…definitely something that I've worried about… it's not necessarily come up with a doctor (but) it has been something I've worried about a lot".' (P20) (3) 'If I became really forgetful… you think of dementia do not you… (so if I) started really forgetting things, I'd be asking questions.' (P3) (4) 'I've contacted the (HIV service) about three or four times outside of my regular appointments with a concern and I've always been seen and dealt with.' (P10) ( 'My beef with it… to ask a 23-year-old man who's just been diagnosed with HIV, seems pointless when he might be more interested in talking about other things.'(FG2 HCW2) The HIV clinic as a safe space to explore cognitive issues as needed (12) 'If there is evidence it's a risk factor… there's probably evidence that it's a risk factor for particular groups, then that's worth screening… rather than whole population.' (P1) (13) 'I think because they have got such an in-depth record of me, they know me, if I brought something up I'd be in good hands.'(P20) (14) 'You'd be wanting to ask what I can do to help myself, I'm very much about being involved in my own health… I would expect to be given choices about treatments too.' (P11) (15) 'The EACS questions are good, crude, yes, but a quick way for us to identify people who might need a more detailed assessment… it works for us 'cause we do not have a lot of time and we do have a lot to cover.' (FG1 HCW3) Abbreviations: FG, focus group; HCW, healthcare worker; P, participant; PWH, people with HIV.
their HIV care team.Almost all PWH participants had no recollection of discussing their cognitive health with anyone in their HIV care team.Interestingly, during focus group discussions, nurses identified more training as a necessary requirement to improve their confidence to discuss cognitive health and impairment with PWH.They described feeling less knowledgeable about the causes of CI in PWH and about how to advise patients on supporting cognitive health (quote 5), compared to other health conditions they may discuss with patients.Despite this, healthcare workers felt that discussion around cognitive health was particularly relevant given the profile of patients typically seen.
Theme 2: A shared receptivity to screening The majority of healthcare worker participants stated that screening for CI was conducted routinely at a patient's annual health check.This contrasted with reports from almost all PWH participants, who could not recall being screened.Healthcare workers described employing the EACS CI screening questions in an informal, conversational manner which probably accounts for PWH participants' reports (quote 6).Other PWH participants were aware of screening for CI if they had been previously given a Montreal Cognitive Assessment [16] (MoCA; as is standard practice in the clinic if cognitive concerns exist based on the EACS cognitive screening questions) or if they had attended the specialist memory service run by the HIV service.Almost all PWH participants were in favour of regular formal screening for CI.One PWH who did not agree felt that it was not necessary and PWH would tell their healthcare workers if they had an issue.The key advantage expressed by PWH participants was prevention and a sense of 'catching it early'.Individuals described how knowing about an undiagnosed issue early would allow access to treatment which could support and preserve cognitive function (quote 7).Furthermore, identifying a problem early allows for the causes of impairments to be explored and for the potentially nefarious causes to be managed.They felt that regular screening would facilitate an awareness of problems in those who may not otherwise notice or feel able to spontaneously discuss issues with their care team.Many of those we spoke to also discussed how a knowledge of issues would allow them to prepare, both mentally and practically, for possible longer-term consequences of CIs and encourage lifestyle changes to protect cognitive health.Some PWH participants also identified the benefit of having difficulties acknowledged, which can be validating and reassuring and allows for compensatory strategies to be more formally considered to mitigate functional difficulties that may be experienced (quote 8).
Healthcare workers stated that the main benefit of routine screening was that it felt less pressured for patients and, if expected, it would create less concern and hypervigilance in patients than if screening were only conducted based on a patient's or healthcare worker's concerns.Additionally, healthcare workers felt that explicitly telling patients they were being screened for CI would facilitate conversations about cognitive health, encouraging those with issues to open up about difficulties and eliciting discussions about looking after cognitive health (quote 9).
Most PWH participants we spoke to did not see any downside to regular screening for CI.For those who did foresee disadvantages, the main concerns expressed were the potential for false positives, with individuals stating the importance of thorough further investigation.Similar to the concerns of healthcare workers, some individuals described how knowing that they were undergoing CI screening may cause increased stress or pressure, which in turn may skew results.Additionally, two PWH participants expressed that the knowledge that PWH are at increased risk for CI could cause hypervigilance which would have an impact on quality of life (quote 10).Healthcare workers agreed with this perspective and felt that an explicit screen for CI would increase health anxieties in patients and create high levels of 'worried well'.Other concerns described by healthcare workers were around the validity and reliability of screening tools.Specifically, they described how the relative crudeness of the EACS screening questions might create false assurances or concerns in patients.Furthermore, given the selfreport nature of the EACS screening questions, it could miss those with anosognosic presentations.Lastly, a concern voiced by a number of healthcare worker participants was around the increasing number of assessments or 'checks' being required of them and their patients.Healthcare workers felt, particularly in cases where CI is less likely, that screening without apparent need degrades the patient-carer relationship and, importantly, takes time away from addressing issues that may be more pressing for patients (quote 11).
Theme 3: The HIV clinic as a safe space to explore cognitive issues as needed The final section of the interviews asked participants about the practicalities and preferences of screening for CI.All but one PWH participant felt that screening should be routinely offered in some capacity to PWH.Just under half of the PWH participants we spoke to felt everybody should be offered routine CI screening.Several individuals stated that screening and the frequency of screening should be based on evidence: specifically, based on risk in different demographic or clinical profiles (including age, gender, cART type, length of time someone has been living with HIV etc.) (quote 12).This was echoed by many others, who stated that screening should commence from a particular age onwards, if indeed age is a primary risk factor.Lastly, a couple of participants felt that screening would be best suited to those who express concern when asked about cognitive issues by their healthcare workers.Interestingly, a couple of PWH participants further commented that a baseline screen should be conducted as soon as someone enters the HIV service, thereby providing comparative data should someone experience difficulties in the future, regardless of whether screening is conducted routinely or not.
The majority of PWH participants expressed a preference for CI screening to be brief (e.g.under 20 min) and conducted yearly as part of their annual health check.Individuals did not feel a comprehensive assessment should be undertaken routinely; however, they thought a formal neuropsychological assessment should be offered if issues are detected.A brief screening assessment would enable healthcare workers to identify those who may have CI and who could then be signposted for a more comprehensive cognitive assessment.PWH participants felt that offering a choice regarding screening administration would optimize uptake.Most participants stated that they would be happy to complete a screening tool online, particularly if that eased time constraints in the clinic.A smaller minority stated that they would prefer screening to be conducted face to face and described either having difficulties using technology or feeling that, due to the nature of the inquiry, having an healthcare worker on hand would assuage anxieties.Finally, when considering face-to-face screening, while a small number of PWH participants stated having no preference regarding where a CI screening takes place (i.e.GP, memory assessment service or HIV service), the vast majority stated that they would prefer screening to take place at their HIV service and to be conducted by one of the healthcare workers working there.This preference appeared to be driven by individuals feeling particularly comfortable and supported at their HIV service and feeling that their HIV service was best placed to manage or signpost those who are identified as having a cognitive issue (quote 13).PWH participants wanted the results of the screening test to be communicated to them, and in cases where this led to a diagnosis of CI, all stated that they expected this should be communicated to them by a doctor, preferably in person, although some stated the telephone would be acceptable.Participants noted the importance of being able to ask questions pertaining to their diagnosis and to ascertain treatment options and management plans (quote 14).Interestingly, all but one participant stated that they would want to know if assessment suggested CI regardless of whether they had symptoms (e.g.asymptomatic CI).
Healthcare workers who stated that they did conduct routine screening in the HIV service reported using the EACS screening questions, typically in an informal, conversational manner, to elicit whether patients might have a CI.If they were concerned, a MoCA would be administered at a later date and, if this indicated an issue, the patient would be signposted to the in-house specialist HIV memory service.Healthcare workers felt this process worked, and despite concerns regarding the validity and reliability of the EACS screening questions, its use best balanced the capacity constraints of the service with the needs of the patient (quote 15).In practice, healthcare workers felt that employing the MoCA (for example) as a screening tool for CI would be too time-consuming and not relevant to enough patients to warrant this increased time expenditure.

DISCUSSION
We found PWH to be receptive to routine cognitive screening and to perceive screening as relevant and an important part of managing health as they age.Healthcare workers felt that this might present some challenges and expressed concerns regarding the capacity of HIV services to implement routine screening and also questioned the validity of screening measures used.However, PWH felt that screening and subsequent detection of CI, if present, might help them to prepare for future issues and promote active management strategies and care pathways, which would support cognitive health.Our study elicited information on the practical preferences that PWH have with regard to cognitive screening, which included a preference for screening to be conducted by the HIV service using a short tool which can be administered either online or in person, depending on individual preferences.
Our results found that PWH felt routine screening for CI would be a beneficial addition to their HIV care.This aligns with recent work to develop an outcome measure for PWH, to support person-centred care delivery.The new validated measure (Positive Outcomes), informed by the experiences of PWH, includes concerns about CI (memory and concentration) with its items [17,18].Similar findings have been reported in other qualitative studies evaluating undiagnosed CI and dementia in the general population, and studies regarding other ageingrelated morbidities such as frailty among PWH [13].
Palazzo et al. [12] found that older adults broadly support an early diagnosis of CI, perceiving the benefits to include time to adjust and plan for the future and to identify resources to assist in clinical management.Additionally, in their qualitative work, participants emphasized the need for thoughtful communication and that a conversation on CI should include advice on prognosis, treatment and resources if CI or dementia were diagnosed.Participants in our study also voiced a preference for candour, stating that they would want to know if screening indicated CI even if they were not experiencing noticeable symptoms.Furthermore, participants stated that they would want information on treatment choices and care management strategies along with self-management advice which may help to preserve cognitive function and to maintain function.
Overall, PWH had a limited knowledge of the symptoms of CI, outside of general memory loss, and most were not aware that living with HIV places you at increased risk of CI.The finding that some healthcare workers were unsure of the causes of CI and many PWH thought CI was a type of dementia is concerning and highlights the need for accurate information for both PWH and healthcare workers.Loss of cognitive function and dementia was a concern for many PWH.This is in line with previous findings that PWH appear more concerned about cognitive frailty and dementia than physical frailty [13].Age-related differences to concerns were seen whereby some of the younger participants (<50 years old) felt it would unlikely be an issue for them currently.This, however, did not appear to influence views of screening, with all those under 50 in favour of routine screening either globally or after a certain age.Interestingly, healthcare workers tended to report employing the EACS CI screening questions in an informal manner at patients' annual health review.Therefore, it was not surprising that PWH reported limited understanding of and exposure to cognitive screening and a desire to know more about CI in the context of HIV.In the focus groups, healthcare workers discussed concerns regarding usefulness of the EACS questions during consultations.This aligns with studies showing poor sensitivity and specificity of the EACS screening questions [19] and supports the notion that a short validated screening tool for CI that is easily implementable in HIV medical consultation is required.This would address the clear expectation of patients to be screened and improve healthcare workers' confidence in the usefulness and interpretation of findings.
Indeed, along with screening, PWH and healthcare workers stated that they would like educational material on how to support cognitive health in PWH.Healthcare workers identified further training as an important means by which they could become more confident in talking to PWH about their cognitive concerns and offering health and lifestyle advice.Given this finding, an implementation strategy involving an explicit screening process, information on why it is being conducted and information provision for PWH on supporting good cognitive health could be effective and an important avenue for further training.This would align with current public health initiatives in England which involve promoting individual-level interventions and lifestyle changes to support cognition in older adults [20].
The present study used rigorous qualitative methodology and involved an interdisciplinary team with diverse perspectives in all phases of the study, from conceptualisation to design of interview guide, analysis and interpretation of data.Purposive sampling produced a diverse sample of PWH and healthcare workers, albeit from a single HIV service, and all were English speakers, which may limit generalizability of findings.We relied only on PWH-reported experience and did not include information on additional factors that may influence receptivity to screening, such a current CI diagnosis.Furthermore, our findings are collated from those participants willing to take part in this interview study.Those who declined participation may not be as receptive to routine screening for CI.
People with HIV are concerned about CI and would welcome regular screening for this as part of the holistic care provided by the HIV team.Healthcare workers tended to explore cognitive impairment informally and conversationally and had concerns about causing distress or concern.However, most PWH wanted to know if they did have CI, to enable them to access the care and support they need.

T A B L E 2
Abbreviation: cART, combination antiretroviral therapy; MSM, men who have sex with men; PWH, people with HIV. a Median (range).
5) 'The other thing is whether we as clinicians have enough training to understand what the screening means and how we communicate that to our patient… if a screening is negative, it might not be negative negative, it's their lifestyle and whether we have the tools sometimes, to explain what's not healthy.'Ithink it's very relevant… if there is an underlying problem with someone's memory it's really important to catch it early… you do not want it to get worse, maybe there are things you can do to help.' (P2) (8)'From my perspective it would create some recognition of this being an important part of my life, and a realization that thing's need to be monitored.'(P17) (9) 'I think because a lot of the people we see are older, if we had that discussion really transparently… it would let us bring in more around looking after cognitive health, 'cause I do not think people really know much.' (FG2 HCW5) (10) 'It would put that fear into people's head: "There must be something wrong then"… they could misinterpret it and think they must get cognitive impairment if they are HIV-positive.'(P6) studies for, and received honoraria for training content development from, Gilead Sciences.MM receives research support from the National Institute for Health and Care Research (NIHR) Applied Research Collaboration South London (NIHR ARC South London) at King's College Hospital NHS Foundation Trust.The views expressed are those of the authors and not necessarily those of the NIHR or the Department of Health and Social Care.JHV has received honoraria and research grants from and been a consultant or investigator in trials sponsored by Merck, Janssen Cilag, Piramal and Gilead Sciences.He has received sponsorship to attend scientific conferences from Janssen Cilag, Gilead Sciences and AbbVie.DATA AVAILABILITY STATEMENT Anonymized transcripts are available on request.ETHICS STATEMENT This study was approved by the UK Health Research Authority (HRA) and Bromley Research Ethics Committee (REC).ORCID Kate Alford https://orcid.org/0000-0001-5356-5644Shiraaz Sidat https://orcid.org/0000-0001-6435-3444Katherine Bristowe https://orcid.org/0000-0003-1809-217XNatalie St. Clair-Sullivan https://orcid.org/0000-0003-1097-0759Maddocks Matthew https://orcid.org/0000-0002-0189-0952Deokhee Yi https://orcid.org/0000-0003-4894-1689Richard Harding https://orcid.org/0000-0001-9653-8689Tom Levett https://orcid.org/0000-0003-2792-6279Jaime H. Vera https://orcid.org/0000-0002-1165-0573