“It’s a disease of families”: Neurologists’ insights on how to improve communication and quality of life for families of Parkinson’s disease patients

Abstract

Objectives

Parkinson’s disease presents an evolving challenge for patients and families due to an unpredictable disease trajectory and symptoms that complicate social interactions. In this study, we explore neurologists’ perspectives on the challenges Parkinson’s disease presents for families and the strategies they use to improve communication and quality of life.

Methods

We conducted hour-long semi-structured interviews with 16 neurologists at 4 care delivery institutions in the San Francisco Bay Area, focusing on techniques neurologists use to support families through the Parkinson’s disease journey.

Results

Neurologists identified strategies for addressing caregiver–patient disagreements around symptom accuracy and negotiating driving safety. Family education is needed to contextualize patient symptoms and to identify psychosocial support resources. Unmet caregiver needs remain, particularly in the form of psychosocial support, respite care and support for unequal gender dynamics in the Parkinson’s disease caregiving experience.

Discussion

Family members of Parkinson’s disease patients face unique caregiving and interpersonal challenges due to the nature of the disease. Targeted education and structural support are needed to alleviate current burdens and allow for improved patient- and family-centered care.

Keywords

Caregivers neurodegenerative disease communication gender quality of life

The one thing that I feel strongly about is the disease is not a disease of people, it’s a disease of families. Because it’s not just the patient that gets [Parkinson’s disease. It] doesn’t just affect the patient. It affects everyone, right? (N9, Female Movement Disorder Specialist)

Parkinson’s disease (PD) is a neurodegenerative illness diagnosed primarily by its cardinal motor symptoms of tremor, bradykinesia (slowness of movement), rigidity and postural instability.¹ However, the disease is accompanied by a host of non-motor symptoms that affect psychological and social functioning.² Many patients report that the non-motor symptoms are more disabling than the motor impairments,³ and impact their self-image and sense of independence.^4,5 These physical and psychosocial changes lead people with PD to experience new limitations that progressively circumscribe their activities of daily life.

In addition to the decreased motor abilities, PD patients may experience changes in the way they perceive social cues and express emotion, which may complicate interpersonal communication with their family members. Such changes may include impaired ability to read emotion⁶ or to accurately infer what another person is thinking or feeling,⁷ resulting in “social cognitive impairment.”⁸ PD patients also frequently experience dampened affect across facial and vocal channels.^9,10 Mood disorders, including depression, anxiety and apathy, are common in PD^11–13 and may affect patients’ desire to engage in activities. Taken together, these changes may contribute to interpersonal conflict around perceptions of “reality,” and may be reflected in reports of caregiver–patient disagreement.^14,15 In one such study, people with PD and their caregivers even disagreed on such seemingly objective measures as how frequently patients exercised.¹⁶ Family relationships are affected even at early stages of disease progression due to disease-related changes that call for evolving family roles as patients’ functional abilities change.¹⁷ Given that PD affects family relationships on multiple levels,^5,18 additional work is needed to identify strategies to better support caregivers and families during the PD journey.

Given the heterogeneity of PD’s clinical presentation¹⁹ and its unpredictable progression,²⁰ it can be difficult for patients and families to know how to prepare for the evolving challenges this neurodegenerative disease presents. Neurologists and Movement Disorder Specialists^a have contact with PD patients and their caregivers at all stages of disease progression, making them uniquely positioned to provide insights on how to navigate challenges across the disease trajectory. In this study, we interviewed neurologists to learn about unmet PD patient and family needs, including neurologist-perceived opportunities for education, strategies for symptom management, and approaches to navigating caregiver–patient disagreement that could allow patients and caregivers to navigate the PD journey more successfully.

Methods

Study design

To capture the range of settings in which care for PD patients is delivered, we recruited neurologists from across four sites: one multi-specialty clinic, one specialty care clinic, and two academic medical centers in the San Francisco Bay Area.

Procedures

Neurologists were initially recruited by email through online public and institutional directories. Subsequent participants were referred to the study by colleagues. The study was approved by the local institutional review board. All participants were informed that their participation was voluntary, had no bearing on their employment status, and that their participation or lack thereof would be kept confidential. Participants were informed that they had the option to withdraw from the study at any time without penalty. Inclusion criteria consisted of providing care for at least five PD patients per month and having practiced as a neurology specialist for at least two years. Written informed consent was obtained for the initial participants; however, we subsequently amended the consent process to verbal-only consent in order to provide additional anonymity for study participants. All participants donated their time.

After completing a background demographic questionnaire, neurologists participated in roughly 60-min semi-structured interviews which targeted the following domains: professional training and background; communication strategies used to optimize the clinical encounter; medicating practices and techniques for symptom management; common psychosocial symptoms; caregiver needs; knowledge of PD education and specialist referral resources; systems-level barriers and facilitators to care delivery; and unmet patient needs. The digitally audio-recorded interviews were transcribed and de-identified for analysis.

Participants

A total of 17 providers (8 female, 9 male) took part in the study. It was later determined that one participant did not meet inclusion criteria of having practiced a minimum of two years, and her data were excluded from analyses. The 16 remaining participants included 7 women and 9 men. Six were general neurologists at multispecialty care clinics; six were movement disorder specialists at academic medical centers; and four were movement disorder specialists at a specialty care clinic.

Data analysis

We used a general descriptive qualitative approach^21,22 to analyze interview data. The first author (RS) transcribed the interviews and conducted primary coding. Initial codes were developed based on topical areas and concepts from the interview guide and later refined during the first reading of interview transcripts. To ensure reliability, a subset of codes (20% of the total coded passages) was independently reviewed and coded by a second author (CG).²³ Interrater agreement was slightly over 83%, a score considered to be in the optimal range.²⁴ All discrepancies were resolved by consensus. After establishing reliability, codes were then grouped together around common themes and exemplary quotations selected to illustrate thematic findings.

Results

Participant demographics

The mean age of participants was 49 (SD = 14) and ranged from 35 to 76 years old. Ten neurologists were Caucasian, five were Asian, and one was Middle Eastern. All neurologists had been practicing as neurological specialists for a minimum of 2 years (with an average of 15 years in practice). The general neurologists delivered care to an average of 17 patients per month in clinical practice (SD = 8), while the movement disorder specialists cared for an average of 100 patients per month (SD = 65). Length of patient visits varied according to site resources and also varied according to individual provider within sites (e.g. one site included specific neurologists who engaged in phone and web-based video visits, allowing for more frequent, but shorter visits; some sites had trainees who completed some patient charting before the neurologist arrived, altering the total visit length, etc.). When asked to estimate the disease stage distribution of their patients, newly diagnosed patients composed approximately 13%, early-stage patients were roughly 28%, mid-stage composed 37%, and advanced stage patients made up 22% of the patient panel. This distribution suggests that neurologists in this study had experience navigating the challenges patients and caregivers face across different stages of disease progression.

Emergent themes

Three themes emerged: (1) Neurologists highlighted caregiver–patient disagreements around symptom accuracy and driving safety and identified strategies for addressing discord; (2) Family education is needed to contextualize patient symptoms and to identify psychosocial support resources; (3) Unmet caregiver needs remain, particularly in the form of psychosocial support, respite care and support for unequal gender dynamics in the PD caregiving experience.

Theme 1: Neurologists highlighted caregiver–patient disagreements around symptom accuracy and driving safety and identified strategies for addressing discord

Symptom accuracy

Neurologists reported that caregiver and patient reports of symptoms frequently differ, requiring neurologists to either decide which family member to believe or work with everyone to arrive at a collective understanding. They shared examples of symptoms that were more troublesome to caregivers than to patients, such as dyskinesias, and discussed instances where patients would minimize symptoms despite caregivers’ concerns. When asked whether they relied more upon patient or caregiver report during discrepancies, neurologists’ approaches varied; some tended to believe the caregiver was a more objective reporter, while others believed the patient. Many said this determination of whose report to trust depended on the extent of their relationship with both patient and caregiver, and was complicated by their knowledge that patient and caregiver perspectives often differed. As one neurologist explained,

In real life, family members have their own issues too, so sometimes we can’t trust that either. So, it’s really a case-by-case judgment of impairment and personality issues (N16, Male Movement Disorder Specialist).

Other strategies neurologists used for approaching this interpersonal challenge included reflecting aloud the statements they heard from each side and using humor in the form of understatement (e.g. “it seems there’s a difference of opinion here…”) to diffuse tension while remaining a neutral participant whose goal was to arrive at a collective understanding of families’ experiences.

Neurologists reported that both patients and caregivers tend to minimize mental health issues, such as cognitive decline, hallucinations and delusions, due to the fear and stigma associated with these issues. However, they stressed that the onus was on neurologists to elicit these symptoms during the clinic visits, since some of these symptoms could be relieved by medication adjustments. They spoke to the interpersonal challenges that arose because of disease-related changes that interfered with effective communication, and shared strategies for destigmatizing couple’s counseling by “medicalizing” the mental health symptoms. One neurologist described communication and education strategies to address tension in the relationship:

I try to sort of, not take sides but like, voice what I’m hearing from everybody. Often in those cases I am recommending some sort of counseling…the disease is unmasking whatever relationship difficulties were already there, and then now have just been given this additional stressor… Often [referring to mental health services is about] getting the notion that this is something that you can get specialized help in. And kind of breaking down some of the stigma around counseling and mental health care to begin with. A lot of that is framing it as part of Parkinson’s disease…mood and mental health are related to the disease itself. It’s not just some sort of character flaw or something like that. So trying to medicalize some of the symptoms to some extent. And then also give people resources. Give them access to people who can help them. (N15, Male Movement Disorder Specialist)

Negotiating driving safety

Most neurologists expressed discomfort with family discussions about whether or not patients were safe to continue driving. Multiple neurologists stressed that because PD patients frequently lacked insight into their own motor abilities, neurologists often deferred to family members’ reports when determining whether to assess driver safety. However, some neurologists believed that PD negatively affects driving even at early stages of the disease. As one explained,

Parkinson’s almost really goes at driving. Because if you think about what the main cognitive effects of Parkinson’s are, it’s multi-tasking, which is driving, visuospatial, reaction time and slowness. So those are all like, key, key things for Parkinson’s. You could make arguments that even mildly affected people could be [impaired]. That’s why it’s really tough. (N16, Male Movement Disorder Specialist)

Neurologists offered two main strategies for conscientiously navigating the family tension involved in trading independence for safety: one involved negotiating a “patient-provider pact” that would gradually restrict driving by limiting the radius the patient travels from their home and eliminating freeway driving to mitigate danger. A second strategy, particularly when there was conflict between patients and other family members about patients’ abilities, involved having patients take a driving test. Neurologists shared stories of advising PD patients to take a driving test either through a private driver’s education company or through the Department of Motor Vehicles. The latter tactic was suggested as a high-stakes technique for definitively settling marital conflict on the issue. As one neurologist explained:

Until I figured this out, in the old days, I got in the middle of a horrible fight… now I have a very simple solution. You think you can drive? Then go down, take your driver’s test voluntarily [at the DMV]. You pass, she’ll quiet down! And if you don’t, you shouldn’t be driving. And if they’re willing to do that, fine. And if they’re not, they’re toast, because now she’s in control… (N11, Male Movement Disorder Specialist).

Theme 2: Family education is needed to contextualize patient symptoms and to identify psychosocial support resources

Neurologists highlighted educational opportunities they felt could help families better understand both the cause of patients’ challenging behavior and strategies for bridging the interpersonal “chasms” the disease-related changes can create. As one neurologist summarized,

There’s a lot of frustration on families’ part that I hear. They think the patient is doing it voluntarily, that they’re, that they can’t move fast enough or they just are not motivated enough, and they need to know that it’s the disease. (N6, Female General Neurologist)

The mood disorders associated with PD were frequently cited as an underlying cause of familial discord. Neurologists felt that additional family education could be useful; however, they also noted that in many cases, education alone is not sufficient to solve the problem. One neurologist explained,

[Apathy] has a huge impact on the family because the spouse, they want to go out, they want to have dinner, they want to go to a movie. The patient just wants to sit around. That’s where the real chasm begins to crack the family because the poor spouse is going crazy, they don’t want to just sit. And the patient’s just so apathetic. We don’t have a good treatment. (N11, Male Movement Disorder Specialist)

The changes in facial and vocal expression that PD patients experience were also cited as a contributing factor in marital discord. One description of an educational strategy used to overcome these disease-related expressive changes included encouraging family members to explicitly ask how the patient is feeling instead of relying on perceptual emotional cues. One neurologist explained:

I try and help people understand that there’s a dissociation—like, that someone can have an inner emotional experience and maybe they don’t show it on their face…If you can’t read the unspoken signals, you got to use your words. You got to talk about what you’re feeling because now the shortcuts that used to work basically are not working. (N15, Male Movement Disorder Specialist)

Theme 3: Unmet caregiver needs remain, particularly in the form of psychosocial support, respite care and support for unequal gender dynamics in the PD caregiving experience

Neurologists highlighted that PD is a “different disease” for female than for male patients due to how the disease-induced changes affected their family role. The neurologists attributed this to established gender roles in heterosexual relationships, where women are traditionally the “nurturers.” They also noted that evolving gender roles contributed to different caregiving practices according to generation, with those in their 70s frequently accompanied in clinic by a caregiver, whereas those from younger generations often came alone if the patient was female. Neurologists spoke of female caregivers typically taking on a patient advocacy role, while they reported that caregiving husbands “tend to recede into the background a little bit more” (N16, Male Movement Disorder Specialist). While they were careful to acknowledge there could be counter examples, both male and female neurologists spoke to this pattern.

Neurologists highlighted the guilt and grief associated with both the caregiver and patient roles, sharing anecdotes about family conversations taking place in the clinic when patients were distressed about their impact on other family members. Neurologists had multiple approaches to addressing these issues; one neurologist asked patients to share their concerns with the family members during clinic visits so that the neurologist could facilitate a discussion to make sure all family members understood each other’s perspectives. They discovered that most of the time, patients’ perceptions about what other family members were thinking and feeling were inaccurate, and a more transparent understanding of each person’s perspective alleviated stress for all family members. Another neurologist felt it was the doctor’s responsibility to directly address patients’ feelings of guilt and grief, but noted that neurologists are not equipped with adequate communication training to know how to navigate this well:

I think a lot of what our patients go through is a tremendous amount of guilt and a tremendous amount of grief…I think that we do not do a good job of treating that at all or recognizing that…[Doctors] need to learn how to use communication as a therapy tool, in terms of helping patients feel less grief and less guilt about their diagnosis and about their symptom burden so they can be more at peace with it. (N13, Female Movement Disorder Specialist)

Neurologists expressed concern that many PD caregivers need additional support. They described how the focus during clinical encounters is primarily on the patient, and the time constraints of the clinic visits did not always allow them to check in about how the caregiver was doing. They proposed that additional structural support systems be developed to alleviate caregiver burden, which they felt would lead to improved patient quality of life. As one neurologist explained:

I talked to a spouse a year ago…she was so angry because there was no support system. I always tell patients, look, if your caregiver goes down, you go down! So, it’s self-interest. But [patients] get to a point where they’re not even aware. So, I think that’s a huge social issue. Patients’ day care, respite care would be enormous. But there aren’t many respite care [options] for Parkinson’s patients. There’s a lot [for] Alzheimer’s, but imagine you’re still with it inside and you put them in with 30 Alzheimer’s patients all day. So, I would say respite care or some other way to [help] the caregiver get a break so they can keep functioning [is needed]. (N11, Male Movement Disorder Specialist)

Discussion

Summary of findings

In this study, 16 neurologists across four care delivery institutions identified strategies for improving clinical communication and quality of life for PD patients and their families. The neurologists highlighted core areas where support is needed. These included psychosocial support in the form of destigmatizing mental health issues and referrals to clinicians with training in how to help patients and families address guilt and grief. They proposed educational initiatives that could help families understand the disease-related cause of frustrating PD patient behavior and communication strategies that emphasize the elicitation of patient thoughts and feelings that may be masked by disease-related changes in expressivity. Finally, they discussed a need for systems-level support, in the form of PD-specific respite care, to allow caregivers a chance to recharge in order to have the resources necessary to continue delivering care. Gender differences in the PD patient and caregiving experience were highlighted as an area requiring additional attention in order to improve quality of life.

Study strengths and limitations

While our sample size was modest, each neurologist, and particularly the Movement Disorder Specialists with their larger sample of PD patients, represented a large, synthesized set of PD patient and caregiver experiences. Additional studies with larger sample sizes are needed, as these specialists have a wealth of knowledge that is seldom drawn upon. Feedback from the neurologists suggested they were eager for opportunities to share their insights to usefully inform future research and care practices.

The four care institutions, located within 50 miles of each other in the San Francisco Bay Area, were selected to represent a range of settings in which PD care is delivered. These included institutions that accept government-subsidized health insurance to capture socioeconomic diversity and to gather data on the different challenges more impoverished patients may face. However, the challenges neurologists in our study spoke to may not necessarily be reflective of those from very different practice environments elsewhere in the country. Given the small sample size and limited geographic region, future research is needed to explore the extent to which the results from this study may be generalizable.

Results in the context of existing literature

There is well-established evidence that PD caregivers experience specific challenges, characterized by greater interpersonal conflict, particularly around issues of independence and care decisions.^25,26 There is disagreement in the literature on the extent to which patients with Alzheimer’s disease experience similar caregiver–patient disagreement (see Davis et al.²⁵ and Roland and Chappell²⁶ compared to Burke et al.²⁷). However, difficulty in caregiver–patient communication has been noted across disease conditions in the elderly population²⁸ and effective solutions are needed to bridge perspectives. The cause of the interpersonal tension has not been fully explored and is necessary for developing effective interventions. Exploring the role of cognitive impairment in patient-caregiver discrepancies may be valuable in developing targeted solutions.

In this study, neurologists propose that the disease-related changes affecting patients’ mood and compromising their ability to accurately convey their emotions may be a key source of interpersonal misunderstanding. This is in keeping with evidence suggesting that PD-related changes result in inaccurate perception of patients’ emotional experience;²⁹ however, neurologists in this study emphasized that the next step towards bridging this interpersonal “chasm” requires education for families around disease-related causes of patient behavior. This neurologist-perceived need for family education as a means to alleviating conflict is evident elsewhere in the literature, with PD caregivers reporting frustration with what they perceived as a lack of effort and engagement on the patient’s part.²⁵ Previous PD education programs have been effective in reducing caregiver burden (see Mosley et al.³⁰ for a recent review), but such programs have yet to be integrated as a routine part of PD care delivery. Additional support is needed in the form of a strong referral network of PD nurses and allied health staff who can guide patients and their families in navigating the loss of independence and the identity challenges that come with declining motor and cognitive abilities. Providing caregivers with education around how PD impacts mood, motivation, and emotional expression can pave the way for new communication strategies that better reflect patients’ realities.

Implications for future research and clinical practice

The challenges of PD caregiving are well-documented (see Mosley et al.³⁰ for a comprehensive review); however, there is not yet routine support for PD caregivers in the form of psychosocial resources, respite care, and educational programs that could allow families to better understand the link between PD and patient behavior that creates familial tension. While outside the scope of the current article, future research could beneficially explore the variation in, and barriers to, neurologist referrals to available systems- and community-level PD resources (e.g. national PD foundations and support groups, access to allied health professionals and educational programs) as a means to improving patient and family quality of life during the PD journey. PD care is traditionally monodisciplinary,³¹ and PD patients who could benefit from access to allied health professionals frequently do not receive such referrals.³² PD caregiver education efforts have also yielded positive results,³³ demonstrating improved mood in both patients and caregivers, a reduction in psychosocial problems and less need for help post-intervention in one randomized control trial.³⁴ However, many neurologists in our study reported limited knowledge of, and access to, such resources, suggesting a need for greater understanding of how to facilitate referrals to available resources. Neurologists’ insights have been largely overlooked in PD research to date, despite their unique knowledge of the breadth of experiences PD patients and families navigate over the course of the disease. By partnering with neurologists, we can more effectively identify unmet PD patient and family needs and opportunities to improve quality of life for PD patients and families.

Footnotes

Acknowledgements

RS was previously a postdoctoral fellow at the Palo Alto Medical Foundation Research Institute, where the project originated. We thank the neurologists who took part in this study for being so generous with their time and insights. We would also like to thank the clinical and research staff at each site who provided assistance with physician recruitment.

Authors’ contributions

RS conceptualized and designed the study, carried out the data collection and analyses, and drafted the initial manuscript. DZ provided interpretation of the coded data, critically appraised and revised the manuscript. CG conducted independent parallel coding of the transcripts, provided guidance on the qualitative analysis and contributed to revisions of the manuscript. MKG provided input to the discussion and manuscript revision. RT provided conceptual input, guided data interpretation, and provided primary revisions of the manuscript. All authors approved the final manuscript as submitted.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by an AcademyHealth Delivery System Science Fellowship award to RS. This research did not receive specific grant funding from agencies in the public, commercial, or not-for-profit sectors. RS was also supported by a VA Office of Academic Affairs Advanced Fellowship in Health Services Research. DZ was supported by the VA HSR&D Career Development Award (HSR&D CDA 12–173). The views expressed herein are those of the authors and do not necessarily reflect the views of the Department of Veterans Affairs.

Note

References

Stebbins

Goetz

Burn

. et al. How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord 2013; 28: 668–670.

Bonnet

Jutras

Czernecki

. et al. Nonmotor symptoms in Parkinsons disease in 2012: relevant clinical aspects. Parkinsons Dis 2012; 2012: 1–15.

Witjas

Kaphan

Azulay

. et al. Nonmotor fluctuations in Parkinson’s disease: frequent and disabling. Neurology 2002; 59: 408–413.

Solimeo

Sex and gender in older adults’ experience of Parkinson’s disease. J Gerontol B Psychol Sci Soc Sci 2008; 63: S42–S48.

Roland

Jenkins

Johnson

AM.

An exploration of the burden experienced by spousal caregivers of individuals with Parkinson’s disease. Mov Disord 2010; 25: 189–193.

Saenz

Doé de Maindreville

Henry

. et al. Recognition of facial and musical emotions in Parkinson’s disease. Eur J Neurol 2013; 20: 571–577.

Narme

Mouras

Roussel

. et al. Emotional and cognitive social processes are impaired in Parkinson’s disease and are related to behavioral disorders. Neuropsychology 2013; 27: 182–192.

Kawamura

Koyama

Social cognitive impairment in Parkinson’s disease. J Neurol 2007; 254: 49–53.

Jaywant

Pell

MD.

Listener impressions of speakers with Parkinson’s disease. J Int Neuropsychol Soc 2010; 16: 49–57.

10.

Simons

Pasqualini

MCS

Reddy

. et al. Emotional and nonemotional facial expressions in people with Parkinson’s disease. J Int Neuropsychol Soc 2004; 10: 521–535.

11.

Kaji

Hirata

Apathy and Anhedonia in Parkinson’s disease. ISRN Neurol 2011; 2011: 1–9.

12.

Pontone

Williams

Anderson

. et al. Prevalence of anxiety disorders and anxiety subtypes in patients with Parkinson’s disease. Mov Disord 2009; 24: 1333–1338.

13.

Lachner

Armstrong

Gruber-Baldini

. et al. Discordance between physician assessment and patient-reported depressive symptoms in Parkinson disease. J Geriatr Psychiatry Neurol 2017; 30: 191–195.

14.

Sitek

Sołtan

Wieczorek

. et al. Self-awareness of motor dysfunction in patients with Huntington’s disease in comparison to Parkinson’s disease and cervical dystonia. J Int Neuropsychol Soc 2011; 17: 788–795.

15.

Khlebtovsky

Rigbi

Melamed

. et al. Patient and caregiver perceptions of the social impact of advanced Parkinson’s disease and dyskinesias. J Neural Transm 2012; 119: 1367–1371.

16.

Fleming

Cook

Nelson

. et al. Proxy reports in Parkinson’s disease: caregiver and patient self-reports of quality of life and physical activity. Mov Disord 2005; 20: 1462–1468.

17.

Whetten-Goldstein

Sloan

Kulas

. et al. The burden of Parkinson’s disease on society, family, and the individual. J Am Geriatr Soc 1997; 45: 844–849.

18.

Martin

SC.

Relational issues within couples coping with Parkinson’s disease. J Fam Nurs 2016; 22: 224–251.

19.

Marras

Lang

Parkinson’s disease subtypes: lost in translation?

J Neurol Neurosurg Psychiatry 2013; 84: 409–415.

20.

Hudson

Toye

Kristjanson

LJ.

Would people with Parkinson’s disease benefit from palliative care?

Palliat Med 2006; 20: 87–94.

21.

Sandelowski

What’s in a name? Qualitative description revisited. Res Nurs Health 2010; 33: 77–84.

22.

Sandelowski

Whatever happened to qualitative description?

Res Nurs Health 2000; 23: 334–340.

23.

Thomas

DR.

A general inductive approach for analyzing qualitative evaluation data. Am J Eval 2006; 27: 237–246.

24.

Hruschka

Schwartz

St. John

. et al. Reliability in coding open-ended data: lessons learned from HIV behavioral research. Field Methods 2004; 16: 307–331.

25.

Davis

Gilliss

Deshefy-Longhi

. et al. The nature and scope of stressful spousal caregiving relationships. J Fam Nurs 2011; 17: 224–240.

26.

Roland

Chappell

NL.

Caregiver experiences across three neurodegenerative diseases: Alzheimer’s, Parkinson’s, and Parkinson’s with dementia. J Aging Health. 2019; 31: 256–279.

27.

Burke

Roccaforte

Wengel

. et al. Disagreement in the reporting of depressive symptoms between patients with dementia of the Alzheimer type and their collateral sources. Am J Geriatr Psychiatry 1998; 6: 308–319.

28.

Fried

Bradley

O’Leary

. et al. Unmet desire for caregiver-patient communication and increased caregiver burden. J Am Geriatr Soc 2005; 53: 59–65.

29.

Schwartz

Pell

MD.

When emotion and expression diverge: the social costs of Parkinson’s disease. J Clin Exp Neuropsychol 2017; 39: 211–230.

30.

Mosley

Moodie

Dissanayaka

Caregiver burden in Parkinson Disease: a critical review of recent literature. J Geriatr Psychiatry Neurol 2017; 30: 235–252.

31.

van der Marck

Kalf

Sturkenboom

IHWM

. et al. Multidisciplinary care for patients with Parkinson’s disease. Parkinsonism Relat Disord 2009; 15: S219–S223.

32.

Nijkrake

Keus

SHJ

Oostendorp

RAB

. et al. Allied health care in Parkinson’s disease: referral, consultation and professional expertise. Mov Disord 2009; 24: 282–286.

33.

Simons

Thompson

SBN

Smith Pasqualini

MC.

An innovative education programme for people with Parkinson’s disease and their carers. Parkinsonism Relat Disord 2006; 12: 478–485.

34.

A’Campo

LEI

Wekking

Spliethoff-Kamminga

NGA

. et al. The benefits of a standardized patient education program for patients with Parkinson’s disease and their caregivers. Parkinsonism Relat Disord 2010; 16: 89–95.