Study design and recruitment

PACE-DLB is an observational longitudinal cohort study involving five Lewy Body Dementia Association Research (LBDA) Research Centers of Excellence in the United States (University of Florida, University of Michigan, Mayo Clinic Rochester, University of Virginia, University of Miami) and recruitment of a virtual cohort (targeting individuals not receiving subspecialty care). Recruitment for the virtual cohort occurred through the LBDA, Lewy Body Dementia Research Center, clinicaltrials.gov, Alzheimer’s Association Trial Match, the Fox Trial Finder, advertising in caregiver newsletters, support group presentations, and unaffiliated neurologists who learned about the study and offered to share recruitment materials.

Study participants

Inclusion criteria were: 1) person with a clinical diagnosis of DLB (reported by person with DLB, caregiver, or clinician and confirmed with a Lewy Body Composite Risk Score [LBCRS] [7] score ≥3), 2) person with DLB and primary informal caregiver willing to participate as a dyad, 3) U.S. residents, 4) at least moderate severity dementia as assessed by the Quick Dementia Rating System (QDRS, score of >12 suggestive of at least moderate dementia) [8], 5) person with DLB expected to live at least 6 months (by clinician or participant estimation), and 6) caregiver Telephone Interview for Cognitive Status score of >31 [9] to ensure that the caregiver was able to reliably complete study visits. The participating caregiver was the person providing the majority of the informal care for the person with DLB and attending the majority of their clinical visits. The current analysis includes the first 50 dyads with a post-death study visit. Because saturation of themes was reached with this cohort, the interview questions subsequently changed. Thus, the current analysis includes visits relating to the original semi-structured interview. Included post-death visits reflect participants who died after the baseline visit and before the 6-month follow up and participants who had multiple study visits prior to death.

Standard protocol approvals, registrations, and patient consents

This study was first approved by the University of Florida institutional review board (IRB202001438) on 6/23/2020. It was registered on clinicaltrials.gov (NCT04829656). Caregivers provided written informed consent for their own participation and individuals with DLB provided consent or assent with additional consent from a legally authorized representative. The first participant was enrolled on 2/25/2021. The last visit included in the current analysis of the first 50 post-death visits occurred on 7/20/2023. The semi-structured interview changed after this time due to saturation of themes for all interview questions. Study enrollment closed 12/22/2023; follow up visits are ongoing.

Study visits and measures

Study visits were designed for virtual and in-person completion given a priori plans for inclusion of a virtual cohort. Because funding occurred during the COVID pandemic, dyads enrolled at LBDA Research Centers of Excellence were allowed to choose in-person or virtual study completion. Virtual study visits were completed by phone or HIPAA-compliant videoconferencing. Measures were administered verbally by study coordinators to minimize differences in conduct between virtual and in-person visits and because some older caregivers could be uncomfortable with electronic form completion. Coordinators entered data directly into electronic case report forms using REDCap (Research Electronic Data Capture) tools hosted at the University of Florida [10,11]. Visits occurred every 6 months until the death of the person with DLB. A post-death visit was completed with the caregiver approximately 3 months after the death of the person with DLB and this visit formed the basis for the current analysis. This visit included questions about the end of life derived from the prior DLB survey [4], the Last Month of Life Survey from the National Health and Aging Trends Study [12], and a semi-structured interview (S1 File) that was based on the prior interview study [5] but revised for PACE-DLB with input from the study team, including a former caregiver. Interviews were scheduled to last up to 30 minutes. The current analysis focuses on the first research question (end-of-life experiences); interviews for the second research question about post-death experiences are ongoing. Interviews were performed by the research coordinator who had conducted prior study visits to build on established relationships. Coordinators received training on conducting interviews as part of site orientation. The part of the study visit including the Last Month of Life Survey and semi-structured interview was audio recorded with participant consent.

Analysis

Descriptive statistical measures included means, standard deviations, minimum and maximum values of continuous variables (range) and frequency of categorical variables. The current analysis focused on qualitative experiences and no quantitative analyses were performed with the descriptive and qualitative results. For this qualitative analysis, there were two research questions: 1) what were the experiences of individuals with DLB at the end of life (as reported by the caregiver) and 2) what healthcare factors were associated with positive or negative experiences toward the end of life, particularly for caregivers? Thematic analysis was used to analyze and present interview data through an inductive process in which themes emerged from the data, with no theoretical constructs or existing framework used to classify data [13,14]. Braun & Clarkes’ criteria for thematic analysis [13] involves an iterative process beginning with broad codes, then collapsing codes, and continuously refining codes until themes are finalized and contain rich description [15]. This process overlaps with the constant comparative method commonly used in grounded theory. However, thematic analysis does not require theory development [13]. An iterative process ensured rigor [16]. Themes were considered saturated when no new codes emerged, utilizing an inductive thematic approach [17].

Prior qualitative analyses relating to end of life in DLB were reviewed to inform coding [5,18,19] but a new codebook was developed for the current analysis. One coder (ENW, a post-doctoral researcher with experience in qualitative methods) open-coded three transcripts to develop an initial coding scheme. The codebook was then created by two researchers (ENW, MJA) and subsequently refined throughout the process. Codes were collapsed by the primary analysis team (ENW, MJA) into broader categories representing related concepts and overarching themes [13]. After overarching themes were developed, the primary coder (ENW) closed-coded remaining transcripts to further establish thematic descriptions and exemplars. The codebook was then shared with co-authors for further verification. Participant checking was not performed. Qualitative data were managed using ATLAS.ti software. Consolidated criteria for reporting qualitative research guided the reporting of study findings (S2 File) [20].

Experiences in the last month of life

Thirty-nine (78%) caregivers reported that the person with DLB received either very good or excellent care in the last month of life (Table 2). Some caregivers, however, reported fair or poor experiences. When pain, trouble breathing, or anxiety/sadness were present at the end of life, most caregivers reported that these symptoms were adequately treated. Decisions were usually made with input from the person with DLB and their family and were congruent with what the person with DLB would have wanted, though this was not universal (Table 2). People with DLB were typically treated with respect based on caregiver observations. Over 90% of caregivers reported that they were usually or always kept informed about what was happening during the last month of life, though a couple caregivers reported they were not kept informed at all. Health professionals spoke to the person with DLB about his or her religious beliefs less than half the time, but when this occurred, caregivers felt the degree of contact was usually in line with what the person wanted.

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Table 2. Responses to the last month of life survey.

https://doi.org/10.1371/journal.pone.0309530.t002

Interview themes for end-of-life experiences

Worsening symptoms at the end of life.

When relating experiences of the person with DLB towards the end of life, caregivers described both physical and cognitive declines:

“I felt like…his mind was gone several months before his physical self. So, when he really started going downhill physically, not being able to bear his weight, being incontinent, needing help holding a utensil—when those became apparent and got worse, then I felt like we were approaching kind of that last road.” (1927–31, wife)

Caregivers described that when approaching the end of life, the person with DLB was increasingly unable to complete ADLs such as eating, toileting, bathing, and mobility, and also had increased trouble communicating (Table 3). Cognitive, behavioral, and psychiatric symptoms commonly worsened preceding death. Other symptoms included increased sleepiness, loss of appetite, weight loss, and breathing changes (Table 3).

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Table 3. Experiences of individuals with dementia with lewy bodies prior to death: Exemplar quotes.

https://doi.org/10.1371/journal.pone.0309530.t003

End-of-life trajectories

Multiple caregivers described being surprised by a sudden and rapid worsening leading to the death of the person with DLB:

“I just didn’t expect it had to happen so quickly because he was walking and talking, then the next week he wasn’t able to really do anything…” (1923–01, wife)

“I found it shocking and painful that two weeks before his death, he was walking around, and we were doing things together and I would—I was feeding him…and we would sit and watch TV together and things like. That seemed kind of like a normal time. And then two weeks later he was done. It still shocks me that [he] went so quickly.” (1925–06, wife)

“It was a shock to me. And of course, it was shock to the family because we didn’t––my anticipation of his life was going to be that I would end up having to have in home care… [but] he was still eating everything I gave him. He had many falls and of course the neurologist suggested that, ‘this is what we’re going to be going down.’ …none of that happened. Just that quick, he died. So, I don’t know what he died of. I don’t think it was the dementia that caused his death, [or] whether something else happened.” (1926–09, wife)

Other caregivers described variability in the person with DLB’s trajectory prior to death: “he could have a bad couple of weeks and then kind of have a good few days; so that part, I think to me was the unpredictable part” (1927–100, daughter). “And the week before he died, that’s the time when he would rally back and I thought, well, maybe he’s going to come off hospice… then he passed away” (1927–53, daughter).

Healthcare factors associated with positive or negative experiences

Healthcare factors associated with positive or negative experiences when the person with DLB was dying related to (1) having information about DLB and what to expect, (2) access to support, and (3) utilizing hospice care.

Having information about DLB and what to expect. Caregivers wanted to receive DLB-related education, including information about the disease itself, what to expect at the end of life, and how to provide care to someone with DLB. Caregivers often described having to search for this information themselves. Regarding education about DLB, caregivers expressed wanting more information and encouraged others to self-educate: “I say this to even people beginning the journey, especially with Lewy body, is read… read what you can read [from] the LBDA, ask your doctor” (1927–10, wife). However, as the same caregiver pointed out, “Some doctors need to be educated because they don’t know everything, especially primary care” (1927–10, wife). Caregivers particularly desired information about what to expect at the end of life for individuals with DLB, especially since hospice was sometimes unable to provide this information. “I wish that I had knew more about kind of what to expect…I don’t know if all the patients go into delirium like that. I just wished that I had been better prepared to have recognized what was going on. Even hospice didn’t know” (1927–25, wife). Other caregivers, however, felt intimidated when they read about what to expect at the end of life: “When I read about people’s experiences, I was terrified and anticipating the difficulty swallowing and a long period of immobility” (1927–01, ex-wife).

Caregivers also wanted caregiving advice and tips. For example, one caregiver highlighted the helpfulness of recommendations to make dressing easier, such as using Velcro shoes or shirts: “There are little improvements that go a long way and meet him where he’s at” (1927–44, wife). Others discussed information about psychosocial aspects of caregiving: “I was reading an article about the burden on caregivers for LBD. One element of that burden being the sense of being not fully competent. And I was thinking, how would it ever be possible to feel competent when you’re walking into a room and this person that you love is saying, ‘I can’t find my fingers’” (1927–01, ex-wife). Often advice came from internet searches or support groups rather than healthcare teams. “I had a support group for people whose [loved ones] have dementia… They understood and also, they were an incredible resource for material. You know, I got two wheelchairs from, I got two walkers, different walkers, and just information about, ‘well, what kind of diapers did you use? And how did you deal with this?’… just tips on how to deal with the many things” (1927–75, wife).

Access to support. Caregivers discussed the importance of both formal support (e.g. support groups) and support from the community (e.g. family, friends, neighbors, other caregivers). Caregivers recommended attending support groups as way to learn coping techniques, vent frustrations, and “hear the experiences of other people, and then you don’t feel as alone because you find out that there are similarities, and when you find those similarities, it eases the burden” (1926–01, wife). Attending support groups taught caregivers about ways to cope: “People are really creative [with] the ways they find to get through things and handle things” (1923–10, wife). As noted above, support groups were also a place for caregivers to find information that they were not receiving from their medical teams: “I learned more about Lewy body from being on the Facebook support groups for Lewy body caregivers. I learned more about it there than any place else” (1927–77, wife).

Caregivers also described fostering relationships and community as a way to obtain support from family, friends, and neighbors:

“Probably the biggest advice is, you need to surround yourself with friends and family because you can’t go through it alone. You have to have your support–people you can just vent to, people that care for you and what you’re going through… those connections and relationships are so important” (1927–03, husband).

“I think it’s really important to nurture the relationships you have with the people that you have, [so that] you have a support system… A lot of people I know don’t have very many friends or aren’t very involved… or don’t get along with their neighbors. They don’t go out, they’re somewhat isolated, and I think you have to be as involved with as many people as you can” (1923–10, wife).

Sometimes such local support was lacking: “Well, I haven’t [received support]. My son… I mean, he’s wonderful, but he’s far away. I have really no family or friends close by” (1926–06, wife). Caregivers said they needed to learn to ask for and accept help from others. “Asking for help, that’s important. And that’s something it took me a little while to do. I couldn’t ask friends to help. But towards the end, I did” (1927–35, wife). This can involve a change in mindset by caregivers: “One of the problems was, I got it in my head that nobody else could take care of him, I can take care of it. That’s not true” (1926–01, wife).

Caregivers appreciated when others spent time with the individual with DLB and/or caregiver, which provided socialization and also gave caregivers a break. “We had gotten into a good routine with the people I had coming to help me. We really had it down to a system… We had our daughters and their spouses alternating time [and] had friends coming in” (1923–10, wife). Caregivers also noted the value of having company during the individual with DLB’s final days: “My closest friend, my college roommate, flew up here to be with me. I don’t know how I would have done it by myself… If there’s someone who can be there at your side at the end and in the days that follow, make that happen” (1927–01, ex-wife). Caregivers often felt surprised by the willingness of others in their support system to be available, which created a more positive experience: “I did not expect to have as much help and support [as I did]. I did not expect my daughters and their spouses to put so many things on hold to be there” (1923–10, wife). Others emphasized that their children “even came in the middle of the night if we called them” (1924–04, wife).

Caregivers appreciated expressions of empathy and concern provided both verbally (e.g., checking-in with caregivers about their emotional well-being) or through actions (e.g., dropping off meals). This included community/informal support but also empathy and concern from healthcare workers:

I applaud the hospice group, from the pastor right on down to the relief nurses over the weekends, because they were genuinely concerned…. Even now, I get cards from them, I get calls from them. They want to know how I’m doing, is there anything they can do for me. (1923–12, husband)

I would ask for a replica of my experience in terms of a strong support from the hospital community, not only the physicians, but the nurse practitioners and physician’s assistant, down to even the people that came in and cleaned the room; just the whole support, understanding that we needed that love and caring. Also, the nurse practitioner who followed up from neurology every three months. That continuity of support was very valuable. (1925–07, wife)

Utilizing hospice care. Some caregivers recommended trying to start hospice as early as possible, though this also had limitations, such as lacking Medicare coverage and/or losing access to non-hospice clinicians (e.g. neurologists). Multiple caregivers reported that hospice initially declined referrals for individuals with DLB who were felt to be too early in their disease to qualify. Other caregivers reported that the hospice referral came too late and everyone had to scramble. Multiple caregivers described “fabulous” and “amazing” hospice staff who showed concern for both the caregiver and the person with DLB, but experiences were not universally positive. Benefits of hospice included support for the person with DLB and their family, information about home medication administration, and explanations about what to expect.

Both positive and negative experiences with hospice revolved around the themes of communication, care coordination, quality care, and caregiver education. When health care professionals communicated consistently and empathetically, caregivers reported a more positive experience. Lacking communication was a negative experience that made it harder for caregivers to coordinate care. Sometimes hospice helped coordinate care when the person with DLB was in a facility: “Having hospice in, I think that helped us a lot… It felt like we had professionals in there… instead of me just me constantly trying to contact her doctor and stuff, who was only available certain days and whatever” (1927–12, daughter). The degree of help coordinating care at the end of life was a driver of the end-of-life experience, both positively and negatively, with lacking coordination increasing caregiver burden: “the nurses in a way were more of a nuisance because of the constant changing times and days” (1927–59, wife).

In terms of quality care, caregivers reported dissatisfaction when health care professionals at the end of life were unfamiliar with DLB:

I think I was surprised at how little the staff really understood the disease. And how shocked they seemed to be at her behavior. But most people there didn’t have Lewy body… I think normally when people think of dementia, [they] assume somebody is going to be kind of withdrawn or in their own worlds or whatever, but my mom was not. She was hard to handle (1927–12, daughter).

Staff turnover and insufficient staffing also negatively affected end-of-life experiences for individuals with DLB living in facilities and their families. Caregivers described negative experiences with both under- and over-medication of the individual with DLB at the end of life. Caregivers expressed higher satisfaction when they felt hospice was providing resources such as equipment and adequate pain management. Caregivers also appreciated receiving end-of-life education from hospice staff on topics such as practical strategies (e.g. for incontinence), monitoring for medication side effects, and what to expect at the end of life.