A Mixed-Methods Approach to Understanding the Palliative Needs of Parkinson’s Patients

Abstract

Parkinson’s disease (PD) is the second-most common age-related neurodegenerative disorder. Despite recommendations for a palliative approach, little is known about what palliative needs are unmet by standard care. This study aims to (a) identify palliative needs of PD patients, (b) determine the relationship between palliative needs and health-related quality of life (HRQoL), and (c) probe into factors affecting HRQoL. PD patients and neurologists were recruited for a survey on palliative need; a subset of patients was interviewed. Significant differences between physicians and patients were found in Physical, Psychological, Social, Financial, and Spiritual domains. Physical and Psychological needs predicted HRQoL. Primary themes across interviews included (a) lack of healthcare education and (b) need for care coordination. Secondary themes included (a) the importance of support groups, (b) the role of spirituality/religion, and (c) the narrow perceived role of the neurologist. Findings highlight the importance of coordinated individualized care.

Keywords

Parkinson’s disease palliative care mixed methods

Purpose of the Study

Parkinson’s disease (PD) is the second-most common age-related neurodegenerative disease (Langston, 2006; Lees, Hardy, & Revesz, 2009; Tolosa, Wenning, & Poewe, 2006), presenting with numerous motor and non-motor symptoms and requiring integrative care for optimal management. PD incidence increases rapidly as individuals age beyond 60 years, and only 4% of cases are in individuals under the age of 50 (Van Den Eeden et al., 2003). Complications of advancing age, such as complex medication schedules, multiple comorbidities, neuropsychiatric issues, and cognitive impairment, interact negatively with disease-related factors, resulting in additional management obstacles for older patients (Bainbridge & Ruscin, 2009).

Because PD is incurable, treatment is focused on quality of life, and numerous studies promote a palliative approach to the disease (Bunting-Perry, 2006; Hudson, Toye, & Kristjanson, 2006; A. J. Hughes, Daniel, Blankson, & Lees, 1993; Lokk & Fereshtehnejad, 2013). Palliative care is a medical specialty that focuses on improving quality of life (QoL) in a holistic manner by addressing patients’ physical, psychological, social, financial, and spiritual needs (Bunting-Perry, 2006; Meyers & Linder, 2003; National Consensus Project for Quality Palliative Care, 2013). While neurologists may employ basic palliative principles in practice (e.g., focusing on QoL; Institute of Medicine, 2015), most older PD patients do not receive palliative treatment from certified clinicians (e.g., physicians certified by the American Board of Medical Specialties, nurses credentialed through the Hospice and Palliative Credentialing Center, social workers certified through the National Association of Social Workers, etc.) until they are admitted to hospice at the end of life (Centers for Medicare & Medicaid Services, 2009).

While palliative services can be provided at all stages of a serious illness, hospice is a palliative care model reserved for individuals during the last 6 months of life, who are foregoing curative treatment (Giovanni, 2012; National Consensus Project for Quality Palliative Care, 2013). The proportion of patients with neurodegenerative conditions (dementia and PD) in hospice has increased from 16% in 2004 to 19% in 2009, and the average length of stay for these patients is nearly double that of all other diagnoses (101 days vs. 56 days; Centers for Medicare & Medicaid Services, 2009). The National Home and Hospice Care Survey has indicated that individuals with neurological diagnoses are more likely to be discharged live from hospice care than those with cancer diagnoses (Kutner, Blake, & Meyer, 2002). Preliminary research indicates that, particularly advanced PD patients share many symptomatic needs with metastatic cancer patients (e.g., constipation, dysphagia, anxiety, pain, etc.), and current neurology interventions may be insufficient to meet these non-motor needs (Miyasaki et al., 2012). This evidence indicates that PD patients may substantially benefit from receiving palliative services earlier in the course of the disease.

Research also indicates that availability of nonterminal (both outpatient and in-home) palliative care is growing (M. T. Hughes & Smith, 2014). According to the Center to Advance Palliative Care, there was a 148% increase in the number of available palliative teams between 2000 and 2010 (Strand, Mansel, & Swetz, 2014). In response to these trends, and growing empirical evidence showing palliative care is cost-effective and improves QoL, the Center for Medicare and Medicaid Services is pilot testing a program that will support nonterminal palliative care programs for Medicare and Medicaid beneficiaries (Centers for Medicare & Medicaid Services, 2014; Evans, 2015). Because research shows that palliative care treatment is cost-effective (Smith, Brick, O’Hara, & Normand, 2014), private insurance providers also will likely develop policies promoting use of palliative services. To facilitate access and promote timely and appropriate referrals from neurologists, it is important to identify the needs of patients who may benefit from early palliative treatment.

The first aim of this study was to determine the extent to which palliative needs of PD patients are addressed by standard neurological care as reported by patients and physicians. Because neurological care primarily focuses on addressing physical symptoms (Lees et al., 2009; Weernink, van Til, van Vugt, Movig, & Groothuis-Oudshoorn, 2016), we hypothesized that patients and physicians would report more nonphysical needs (i.e., psychological and social needs) than physical needs. A second aim of this study was to determine the relationship between patient-reported palliative needs and health-related quality of life (HRQoL). Health is widely known to affect QoL, a multifactorial concept reflecting subjective satisfaction with life and its circumstances. Therefore, HRQoL aims to assess the physical, mental, social, and spiritual well-being of an individual, particularly as it pertains to health (Marinus, Ramaker, van Hilten, & Stiggelbout, 2002). Because palliative care focuses on improving QoL (Meyers & Linder, 2003; Morrison & Meier, 2004; National Consensus Project for Quality Palliative Care, 2013), we hypothesized that patients with greater levels of palliative need would report poorer HRQoL. The third aim of this study was to use qualitative methods to examine factors hypothesized to affect PD patients’ HRQoL, to explore areas of patient need not captured in the survey, and to explore, in detail, patients’ experiences, expectations, and awareness regarding their own palliative needs and current neurological care.

Data and Method

This mixed-methods study uses an explanatory sequential design in which qualitative interviews with patients were used to provide context and enhanced understanding of quantitative survey findings. Data collection occurred in two phases, first with electronic surveys released in May 2015 and next with interviews commencing the following month. Interview participants were recruited on a rolling basis as surveys were collected, with interested individuals providing their contact information in the final question of the survey. At the end of the study, inferences from both quantitative and qualitative data were triangulated through iterative review of quantitative data followed by verification with qualitative responses, and meta-inferences drawn from these findings are included as part of an overall interpretation of the results presented in sections “Discussion” and “Conclusion” of the article (Creswell & Plano Clark, 2011).

Study Participants and Procedure

It was determined a priori that 50 PD patients and 50 neurologists would be needed to detect a small effect size of .20 between the five symptom groups with an alpha of .05 and a power of .80 (Faul, Erdfelder, Buchner, & Lang, 2009; Faul, Erdfelder, Lang, & Buchner, 2007; Peto, Jenkinson, & Fitzpatrick, 2001).

Quantitative participant sample

Individuals with PD were recruited through the American Parkinson Disease Association Georgia Chapter support group network, neurology clinics, and senior centers throughout Georgia. Purposive sampling strategies are recommended in PD participant recruitment, because of the relatively low population prevalence of PD (Picillo, Kou, Barone, & Fasano, 2015). With the expectation that most participants would be older adults, any adult with a PD diagnosis was included in the study to allow for the possibility of exploring differences in palliative need between older and younger cohorts. Additional eligibility criteria included having a diagnosis of PD and being fluent in English, and patients self-screened into the study.

Quantitative physician sample

Neurologists were recruited through the National Parkinson Foundation and the Medical Association of Georgia, as well as through neurology clinics identified through the American Academy of Neurology’s Georgia clinician database. Eligibility for the physician survey included being currently employed as a general neurologist or movement disorders specialist.

Qualitative patient sample

Patient survey participants were invited to provide contact information if interested in participating in the qualitative component of the study. A total of 38 (77.6%) survey respondents consented to be contacted for a potential follow-up qualitative interview, and ultimately 23 (46.9%) survey participants participated in the qualitative component of the study. Sample size for the qualitative component is consistent with recent suggestions for sampling designs in mixed-methods research and for qualitative studies that employ thematic analysis (Braun & Clarke, 2006; Onwuegbuzie & Collins, 2007).

Data Collection Procedures

Data were collected between May and November of 2015. All surveys were conducted electronically through the university Qualtrics software program. Contact information for interview participants was stored separately from data files, and participants were assigned unique identifiers to link interviews with surveys while maintaining participant confidentiality. Follow-up qualitative interviews were conducted face-to-face in private locations and at times convenient to each participant (most frequently the participant’s home). Interviews were digitally recorded and transcribed verbatim. Study procedures were approved by the university Institutional Review Board prior to data collection.

Measures

As per the National Consensus Project for Quality Palliative Care (2013), palliative care was operationalized as

patient and family-centered care that optimizes quality of life by anticipating, preventing, and treating suffering. Palliative care throughout the continuum of illness involves addressing physical, intellectual, emotional, social, and spiritual needs and to facilitate patient autonomy, access to information, and choice. (p. 12)

Patient quantitative measures

To measure palliative need consistent with authors’ operationalization of the term, a 31-item survey was adapted from the 12-item Palliative Outcome Scale for Parkinson’s and expanded to include early and moderate-stage palliative PD needs based on previous literature (Bunting-Perry, 2006; Hearn & Higginson, 1999; Hudson et al., 2006). Palliative needs were categorized into five domains (physical, psychological, social, financial, and spiritual) and were assessed through a 4-point Likert-type scale (with anchors from Very Well to Poorly). Not Applicable was an option for those not experiencing a symptom. Content validity of the measure was assessed by a five-person panel of experts in palliative care and PD. Cronbach’s alphas were calculated for all patient symptom categories with more than one item (Physical α = .88, Psychological α = .93, Social α = .94, and Financial α = .88), indicating good to excellent reliability of the items in the measure.

PD participants also completed the Parkinson’s Disease Questionnaire (PDQ)-39, the most commonly used HRQoL measure for individuals with PD (Bushnell & Martin, 1999). Subscales, which were assessed via a 5-point Likert-type scale (with anchors of Never and Always), include mobility (10 items), activities of daily living (6 items), emotional well-being (6 items), stigma (4 items), social support (3 items), cognition (4 items), communication (3 items), and bodily discomfort (3 items). A Summary Index Score was calculated for each participant, with lower scores reflecting better HRQoL. Research examining the validity and reliability of the scale have found acceptable internal consistency for most domains (Bushnell & Martin, 1999).

Patient qualitative interview guide

The semi-structured interview guide addressed the following four broad domains: (a) general background information about the study participant, including length of time living in the current city, educational and employment history, and availability of social support; (b) access to formal care, including community health resources; (c) individual’s diagnosis of PD, including events leading up to the diagnosis and the diagnosis itself; and (d) current PD stage and symptoms, including any perceived needs related to these symptoms. The physical symptoms section of the semi-structured interview guide was developed based on domains included in the Needs at the End-of-Life Screening Tool (NEST; Emanuel, Alpert, & Emanuel, 2001) and the PDQ-39 (Peto, Jenkinson, & Fitzpatrick, 1998). The NEST is a measure commonly used in palliative care to examine the subjective experiences of patients through multiple dimensions including physical, psychological, social, financial, and spiritual domains (Emanuel et al., 2001). Interviews also included follow-up probes to gather additional information based on individual quantitative survey responses. For example, in one interview with an 83-year-old male, the interviewer stated, “You noted some memory and swallowing issues [in your survey] and you said that they were being pretty well taken care of. Can you talk a little about them?” These probes revealed information about symptoms and disease management that were not apparent based on survey results, discussed further in sections “Results” and “Discussion.”

Physician measures

Physicians completed a survey complementary to the patient survey that measured their perceived ability to address each symptom for a majority of their patients. Cronbach’s alphas were calculated for all symptom categories with more than one item (Physical α = .89, Psychological α = .84, Social α = .85, and Financial α = .67). The alpha for the financial category items was slightly below the threshold for an acceptable value. Because consistency was good in the patient survey and removal of items did not improve reliability, all items in the financial category were retained for analysis.

Analyses

Quantitative analysis

SAS 9.3 (Cary, North Carolina) was used for quantitative analyses. To retain as many participants as possible from the dataset, for each symptom category, if 25% or fewer items were missing for a participant, scores for those missing items were imputed from the average of remaining items in that category. The means and standard deviations (SD) for each category were calculated for each sample to determine the extent to which each category was reported as addressed or unaddressed by current care. Higher scores indicate greater unmet need for each symptom.

A MANOVA analysis was run to assess differences in reported palliative need between patients and physicians. A multiple regression analysis was run to determine the relationship between patient-reported palliative need and patient HRQoL. Based on the literature, covariates selected for initial analysis included sex, age, race, income, duration of PD, and number of nonphysician clinicians seen (De Lau et al., 2004; Lang & Lozano, 1998; Prizer & Browner, 2012). Covariates for a final reduced model were chosen through a backward selection process.

Qualitative analysis

A book of preset codes was developed prior to data collection, to assist with tagging, sorting, and organizing data for higher-level analysis (Guest, MacQueen, & Namey, 2012). A priori codes were based on the study aims as well as domains found in the NEST (Emanuel et al., 2001). As analysis progressed, emergent codes were added to the codebook. All transcription and coding were performed by the first author. Codes and emerging themes were discussed, refined, and verified through regular meetings with coauthors. The NVivo 10 software package was used for data management and to facilitate analysis.

Thematic analysis was used to identify patterns and recurrent themes in these data (Braun & Clarke, 2006; Fereday & Muir-Cochrane, 2008). The method adopted an inductive and deductive approach, where initial codes were developed based on previously established palliative care domains and other literature used to inform the aims (Bunting-Perry, 2006; Hudson et al., 2006; Lokk & Fereshtehnejad, 2013). Consistent with guidelines established by Braun & Clarke, 2006, analysis involved six recursive phases: (a) immersion in the data through repeated rereading of interview transcripts, (b) refinement of the initial codebook, (c) searching for themes among and across codes, (d) reviewing themes and linking these with relevant themes in the literature, (e) refining and naming the final overarching and secondary themes, and (f) writing the results. Analysis was considered complete when themes were refined and fully developed with consensus from the research team, and upon reaching saturation where no new themes or relevant data were identified in the interview transcripts.

Results

Participant Characteristics

In total, 75 patients with PD were recruited for the survey; however, only 49 cases (65.3%) were complete and retained for analysis. A total of 23 participants participated in the qualitative interviews, and the interview sample was representative of the quantitative sample. Interview participants were not excluded based on geographic location, and all were located within a 75-mile radius of metro Atlanta, Georgia. At the time of the project, no outpatient palliative care program designated for PD patients was available in the study area. Table 1 outlines patient participant demographic statistics. A total of 62 (81.6%) out of the 76 physicians enrolled had complete data and were included in the analysis reported in this article. Studies on web survey data collection indicate these completion rates are adequate based on the longer length of the surveys and lack of available incentives (Galesic & Bosnjak, 2009; Granello & Wheaton, 2004). Table 2 outlines their demographic statistics.

Table 1.

Demographic Characteristics of Patient Participants (Survey N = 49; Interview N = 23).

Characteristic	Survey participants		Interview participants
Characteristic	M	SD	M	SD
Age (years)	66.4	10.4	66.2	10.1
Duration of PD (years)	8.2	5.1	8.1	3.9
Quality of Life Index Score	28.9	17.8	21.7	13.1
Allied Health Clinician Referrals	2.2	1.7	2.23	1.52
	N	%	N	%
Sex^a
Male	28	58	13	57
Female	19	40	10	43
Annual Household Income^b
$0-19,999	1	2.1	1	4
$20,000-29,999	4	8.5	1	4
$30,000-39,999	6	12.8	2	11
$40,000-49,999	4	8.5	2	11
$50,000-59,999	3	6.4	2	11
$60,000-69,999	0	0	0	0
$70,000-79,999	2	4.4	1	4
$80,000+	19	40.4	10	53
Race
Black or African American	1	2.1	1	4
White or European American	45	93.8	22	96
Asian or Asian American	1	2.1	0	0
American Indian	0	0	0	0
Mixed or Multiple Races	0	0	0	0
Other	1	2.1	0	0
Referrals to Nonterminal Palliative Care^a	2	4.26	1	4

Note. PD = Parkinson’s disease.

Two missing values.

10 missing values.

Table 2.

Demographic Characteristics of Physician Survey Participants (N = 62).

Characteristic	M	SD
Age (years)	45.8	10.4
Length of time as physician (years)	15.4	10.3
Length of time working with PD patients	14.3	9.3
Complementary clinicians in practice	2.2	1.7
	N	%
Sex
Male	36	60
Female	24	40
Movement Disorders Specialist
Yes	55	91.7
No	5	8.3
Refer to Nonterminal Palliative Care
Yes	32	54.2
No	27	45.8

Note. PD = Parkinson’s disease.

Quantitative Results

On the PDQ-39 100-point index scale for HRQoL, the mean index score for participants was 28.9 (SD = 17.8), with higher scores indicating greater impairment in HRQoL. Participants reported seeing an average of 2.2 (SD = 1.7) nonphysician clinicians (e.g., nurse, social work, physical therapy, occupational therapy, speech therapy, and chaplain) in their Parkinson’s care. Only two respondents (4.3%) stated that they had been treated by a non-hospice palliative care team. Patients and physicians differed in how they ranked the level of need between groups. Patients reported psychological needs as being the least met, followed by physical, social, spiritual, and financial need. Physicians ranked spiritual need as being most unmet, followed by physical, financial, psychological, and social (Table 3). While physical needs were ranked as the second-most unmet need by both participant groups, our hypothesis was supported to the extent that nonphysical need categories were identified as having the most unmet need.

Table 3.

PD Patient and Physician Mean Scores and Standard Deviations on Palliative Need by Category.

Need category	Patient			Physician
Need category	M	SD	Rank	M	SD	Rank
Physical	1.38	0.76	2	2.25	0.54	2
Psychological	1.48	0.99	1	1.88	0.43	4
Social	1.19	1.03	3	2.11	0.43	5
Financial	0.98	1.19	5	2.31	0.35	3
Spiritual	1.06	1.39	4	2.73	0.98	1

Note. PD = Parkinson’s disease.

The MANOVA analysis indicated that patients and physicians reported significantly different levels of patient need in all five palliative symptom groups: Physical F(1) = 48.91, p < .0001; Psychological F(1) = 21.82, p < .0001; Social F(1) = 40.16, p < .0001; Financial F(1) = 52.01, p < .0001; and Spiritual F(1) = 44.06, p < .0001. In all need domains, physicians perceived that their patients have greater unmet palliative need than patients reported experiencing (Tables 3 and 4).

Table 4.

Multivariate Analysis of Variance of Palliative Need as Indicated by PD Patients and Physicians.

Source	Df	SS	MS	F	p	r ²
Physical	1	20.65	20.65	48.91	<.0001	.31
Psychological	1	12.55	12.55	21.82	<.0001	.16
Social	1	23.67	23.67	40.16	<.0001	.26
Financial	1	41.79	41.79	52.01	<.0001	.32
Spiritual	1	60.97	60.97	44.06	<.0001	.28

Note. Df = Degrees of freedom; SS = Sums of squares; MS = Mean squares.

A multiple linear regression was calculated to predict HRQoL from the Physical, Psychological, Social, Financial, and Spiritual symptom categories. Of the five groups, Physical (F = 85.21, p < .0001) and Psychological (F = 17.9, p = .0001) symptom categories were found to significantly predict HRQoL, as hypothesized, with greater unmet need in those categories predicting poorer HRQoL. The full model was then run, including age, sex, race, years since diagnosis, income, and number of nonphysician clinicians seen. After the backward selection process, only Physical needs (F = 20.84, p < .0001) and Psychological needs (F = 9.02, p = .005) significantly predicted patient HRQoL (Table 5).

Table 5.

Summary of Multiple Regression Analysis to Predict Quality of Life.

Variable	Full model				Reduced model
Variable	B	SE B	F	p	B	SE B	F	p
Physical	12.38	2.76	20.09	<.0001	12.02	2.63	20.84	<.0001*
Psychological	7.90	2.80	7.97	.008	8.06	2.68	9.02	.005*
Social	−0.89	2.51	0.13	.72	−0.20	2.44	0.01	.94
Financial	−2.21	2.19	1.02	.32	−2.22	1.82	1.49	.23
Spiritual	0.82	1.31	0.39	.54	1.15	1.21	0.89	.35
Race			3.15	.04			3.42	.03*
White or European American	0	0			0	0
Black or African American	−9.94	9.41			−9.68	9.38
Asian or Asian American	13.39	12.60			8.70	11.09
Other	33.40	11.57			29.82	9.87
Age	−0.20	0.17	1.32	.26
Complementary Clinicians	0.66	1.02	0.42	.52
Years Since Diagnosis	0.16	0.30	0.29	.59
R ²		.80				.78

p < .05.

Qualitative Results

Qualitative interviews with patients ranged in length from 29 min to 83 min, with a mean length of 55 min. Interviews aimed to explore, in detail, patients’ experiences, expectations, and awareness regarding their own palliative needs and current neurological care and to examine areas of patient need not captured in the survey. Thematic analysis identified two overarching themes regarding gaps in care not captured by the patient survey: (a) need for more effective care coordination and (b) lack of healthcare education. Three prominent secondary themes also were identified that have important implications for patients’ HRQoL and ability to successfully manage and cope with their illness: (a) the importance of support groups, (b) the vital role of spirituality and religion, and (c) the narrow perceived role of the neurologist in PD care.

Need for more effective care coordination

A prominent theme throughout interviews was the need for more effective care coordination. This theme includes two subthemes: (a) limited communication among providers and (b) challenges managing and integrating care (i.e., coordinating multiple treatments, resources, and specialists).

Limited communication among providers

Several participants did not believe that their physicians ever communicated with one another. One 65-year-old man stated, “It’d be nice if they had a conference call once in a while.” Another 73-year-old male patient accepted the lack of communication among his providers, based on his perception that his physicians were too busy to communicate with one another: “I wish that would happen, but I think they’re both so busy that I understand that they don’t.” A 65-year-old woman noted that she encouraged her doctors to talk with each other to no avail,

I said, “why don’t you two talk to each other?” . . . And [the nurse] sent me an email and said that he never answered. So I just let it go . . . So . . . communication there? No.

Others indicated that they felt responsible for communicating healthcare information among their providers.

I don’t really know that there’s a procedure that my notes from one place to go another unless I get them there. (45-year-old male)

I have to do it . . . by pushing each one to send the information to the other. (70-year-old male)

I do a lot more work with trying to pull everybody together . . . I doubt that they ever communicate [unless I convey the information]. (73-year-old female)

I know that when I see the neurologist and I see the internist, I tell the internist what the neurologist is doing and vice versa. So I try to keep them up to date. (70-year-old female)

Some patients assumed that their providers communicated but had no evidence:

I don’t know if they speak, but their offices probably fax things back and forth in this day and age. (62-year-old female)

I’m almost certain they document everything in the system. (65-year-old female)

A majority of participants interviewed noted that they had several conditions for which they were receiving treatment, but very few of them knew or believed that their clinicians communicated among one another. For some patients, this resulted in frequent changes in medications between neurology visits with different practitioners, and one 70-year-old woman noted that she received contradictory diets from two of her physicians who were not communicating about their treatment recommendations.

Challenges managing and integrating care

A common perception among patients was that care is not well integrated across the healthcare system. Many indicated that coordinating care was a burden that primarily fell on them or a family member and was not a role that they were well equipped to manage. One patient expressed a common frustration:

My main complaint about the current medical system is that we’ve really taken away the medical manager, the HMO [Health Maintenance Organization], and I have to be my own HMO. I have to go find the physician, interview the physician, and sit down with them. Make sure that they’re giving us the right care. Ask if there’s somewhere else we should go. And all of that falls on my shoulders now. (70-year-old male)

Similarly, another stated,

In today’s medical system . . . the biggest challenge is to know who’s in charge. And there’s really no one in charge of it but me, and I gotta get all these people that don’t speak each other’s language or talk to each other to coordinate and make sure they’re all thinking holistically. It is hard. (45-year-old male)

One patient noted that this problem is exacerbated for people with PD and those with other complicated chronic conditions that require coordination among multiple treatments, providers, and resources:

My endocrinologist . . . can’t tell me anything about my foot. I have to go to a podiatrist or the podiatrist has to send me to the ear, nose, and throat guy. The ear, nose, and throat guy sends me to the general surgeon. The general surgeon sends me back to my primary care physician. And I have to coordinate all of that. (70-year-old male)

Lack of healthcare education

Narrative data also indicated that patients received minimal instruction or educational resources from their neurologists to assist them in managing their care. In many cases, patients reported that they did not remember receiving such information and concluded that the information either was not provided nor was not memorable or useful enough to make an imprint. The following statements were in response to a question regarding whether patients’ neurologists provided information and resources on PD at diagnosis:

I don’t remember. So that means there wasn’t much. (65-year-old female)

I really don’t remember what all the first person [neurologist] might have given me. I know the second one didn’t give me anything. (73-year-old female)

Several patients indicated that information they learned on their own was more useful than that provided by their neurologist, making statements such as, “It’s been more on my own, picking things up” (73-year-old female).

Some patients reported that neurologists placed too much emphasis regarding education about medications and neglected other important aspects of care. One 54-year-old man stated, “I think they [neurologists] need to take a bigger role in making people aware of things that can help them besides medications” and “I think they [physicians] are terrible about making you aware of support groups, the value of physical therapy, exercise, [etc.].” A 72-year-old woman who indicated only receiving educational information related to medications said, “She [the neurologist] gave me a list of medications that I can’t take, but I have a file folder full of information that I’ve gotten from the Parkinson’s Foundation and various other organizations.”

Importance of support groups

The importance of support groups was one of three secondary themes identified in this study. Support groups have important implications for PD patients’ HRQoL and ability to successfully cope with their illness. Key insights from the current analysis include the importance of support groups in providing needed education and referrals not typically offered by healthcare providers, especially in the area of psychosocial support, and evidence of the critical role that these groups play in helping patients cope with their illness. A 55-year-old woman discussed numerous PD exercise programs she was informed of through her support group peers. Regarding peer support, one 76-year-old man stated, “There’s a sense of sharing and you’re not in it alone,” and that there was a “healing power” in attending the group. Unfortunately, data from this study showed that few patients were connected to this important resource through their physicians.

Vital role of religion and spirituality

Another key finding was the importance of religion and spirituality in helping patients manage and cope with their illness. Although patients indicated relatively low levels of unmet spiritual need in the survey, as well as in the qualitative interview, many discussed at length the importance of spirituality and religion in their health management. The following statements are reflective of many participants:

I think faith gets us through whatever it is we have to do. God’s given me this challenge for a reason. (72-year-old woman)

I pray for [God] to give me emotional, mental, and physical strength to get through things. (65-year-old male)

I think it’s important to use your relationship with God to help you get through these kinds of times. (62-year-old female)

A majority of participants interviewed noted that spirituality plays an important role in how they manage and cope with health challenges; however, no participant reported being asked about spiritual needs at appointments, with the exception of one patient who thought he may have been asked if he had any religious beliefs that might limit possible treatments. Although the level of importance of spirituality and religiosity varied among participants, most said that they would appreciate having their providers ask about their spiritual needs. However, as one 65-year-old man noted, “Everybody is afraid to talk about it.”

The limited perceived role of the neurologist in PD care

A third secondary theme related to patients’ perceptions regarding the role of their neurologist. Although all participants recognized the importance of having their psychosocial needs met, most did not view their neurologist as a resource for addressing them. When asked what role they expected their neurologist to play in their PD care, one 76-year-old man said, “I expect them to put their primary interest in . . . what I’m medically and what they might do with pills or surgery.” Similarly, another 65-year-old man stated, “I guess just keep prescribing my medications.” As indicated in these data presented above, some patients believed that neurologists should adopt a more holistic approach to care and address needs other than just medications. The majority had a more narrow view of the neurologist as a medications specialist, however—someone who “really specializes [in] their knowledge of the medications” (54-year-old male). This finding may provide some insight into the relatively low reports of palliative need in the quantitative surveys, as most patients may not perceive their neurologist as a resource to address issues outside of strictly physical needs, regardless of the ability of the neurologist to manage those needs.

These qualitative findings provide a richer understanding of the quantitative results, and highlight areas in which the survey could be further refined to more thoroughly capture palliative need in this population. There was a significant discordance between survey and interview results pertaining to social needs of PD patients, such as assistive technology, caregiver support, educational needs, and so forth. Although many patients do not expect assistance from their neurologist for nonphysical needs, survey results and interview narratives indicate that they often are able to address some of these issues by seeking resources independently. Despite their reported self-advocacy, numerous participants expressed frustration with the current system, indicating a desire for more concrete resources and support from their healthcare professionals. Qualitative findings also highlighted the importance of many of these nonphysical needs in disease management, which may point to potential care disparities for patients who are unaware of such resources, who have limited access to them, or who do not engage in self-advocacy in their care. This mixed-methods approach allowed for the comprehensive study of this topic and revealed complex relationships between available care and patient needs. These results are discussed more in depth below.

Discussion

While previous research has examined potential palliative needs of older PD patients, no known study has focused on measuring the level of palliative need of PD patients as reported by both patients and neurologists. The results of this study suggest that PD patients experience palliative need throughout the course of the disease, and numerous symptoms, particularly nonphysical needs, may be more challenging for neurologists alone to identify and address. While patients may seek resources to address nonphysical needs beyond their neurology appointments, they express a desire for improved integration of care. Highlighting the individuality and complexity of symptom presentation, findings emphasize the need for comprehensive care programs, such as palliative care, as well as for better healthcare coordination overall in the long-term management of PD.

Physical symptoms are the most obvious hallmark of PD, and because of the progressive and changing nature of the disease, it is unsurprising that both patients and neurologists ranked these needs as being relatively difficult to address. While they did not emerge as an independent theme in interviews, the physical symptoms of the disease were often noted to pervasively affect other domains of care, for instance, requiring coordination of additional providers (social domain) or incurring financial costs due to treatment (financial domain). Physical needs were also significantly related to HRQoL, further stressing the importance of managing this domain. Physical symptoms of PD can range from balance issues, to various manifestations of pain (Beiske, Loge, & Svensson, 2009), to nausea as a treatment side effect (Rao, Hofmann, & Shakil, 2006). Symptom management requires a multitude of approaches, and because pharmacologic and surgical treatment effectiveness wanes as symptoms progress over time, interdisciplinary strategies of management become increasingly vital to addressing these needs (Prizer & Browner, 2012). Care coordination is a core tenet of palliative care. Palliative teams actively facilitate communication between providers, even using conference call functions during family meetings with other physicians. The holistic nature of the interdisciplinary palliative care team encourages appropriate referrals for a wide variety of biopsychosocial needs. In this manner, outpatient palliative care clinics may provide optimal opportunities for enhanced care coordination to better target changing physical needs over time (National Consensus Project for Quality Palliative Care, 2013).

Survey respondents reported the greatest amount of need was psychological, and the psychological domain of need was also significantly associated with HRQoL. Interestingly, although psychological reactions to the diagnosis were discussed in interviews, this domain was not a prominent qualitative theme. Survey findings, however, support previous research indicating that emotional support related to ongoing coping with the illness, as well as psychological symptoms, such as depression, are commonly unmet needs in PD care, which strongly relate to HRQoL (Cubo et al., 2002; van der Eijk, Faber, Shamma, Munneke, & Bloem, 2011). While some neurology clinics are able to address psychological needs through the support of a psychiatrist, psychologist, or clinical social worker, this support may not be available for all neurologists. The common psychiatric complications and comorbidities of PD necessitate the inclusion of a mental health professional in an interdisciplinary healthcare team setting, and collaboration with outpatient palliative care would ensure PD patients receive counseling and psychiatric care.

The greatest discordance between survey and interview results pertained to social needs of PD patients, including, but not limited to, assistive technology, community resource, advance care planning, and caregiver support needs. Both patients and physicians reported low levels of social need in the surveys; however, two of the primary themes that emerged in qualitative interviews included the need for more effective care coordination and healthcare education. Because of the increasing prevalence of both PD and of multiple chronic conditions as individuals age, effective care coordination is crucial for older adults (Ward & Schiller, 2013). The importance of care coordination in PD treatment specifically has been emphasized in previous research as one of the highest-ranked indicators of the quality of care (Cheng et al., 2004). This theme, in particular, underscores the weight of other findings, as improved care coordination—through referrals for non-motor symptoms, assistance accessing social and financial resources, and chaplaincy access—for PD patients could potentially impact all five domains of need. In addition, because neurology clinics vary in size and clinical resources, this may be another opportunity for palliative care intervention in PD treatment.

Despite indicating low levels of educational need in surveys, numerous participants noted in interviews that they received very little educational information directly from neurologists. Most patients located information on the disease, treatments, and resources from the Internet or support groups, with little to no help from their neurologists. Several expressed frustrations that when neurologists did provide information, they focused on medications and neglected the nonphysical aspects of disease management. This finding highlights the importance of results from another recent qualitative study where PD patients expressed the need for tailored information from their physicians regarding education, treatment options, and programs and therapies to manage symptoms (van der Eijk et al., 2011). Interview narratives regarding education also underscore the need for sufficient information and guidance to manage nonphysical aspects of PD.

The role of spirituality and religion in healthcare is a growing field of interest (Idler, 2014). Although survey patients indicated low levels of spiritual need, physician respondents acknowledged that this domain was the most difficult to address in practice. While most interview participants noted the importance of spirituality in their health, only one had ever been asked about religion or spirituality at an appointment. A study on family physicians’ views of spirituality in clinical practice noted that doctors differ in their views on and comfort in discussing these matters with patients; however, they understand the integral role that spirituality plays for many patients (Ellis, Campbell, Detwiler-Breidenbach, & Hubbard, 2002). A separate study found that, although patients do not necessarily expect physicians to discuss spirituality, they want to be asked about coping and support strategies, including those related to spiritual health (Hebert, Jenckes, Ford, O’Connor, & Cooper, 2001). This research highlights the need for chaplaincy in clinical practice, and palliative care teams may be promising options to address this need (Prizer & Browner, 2012).

One possible explanation for the discordance between the survey results and these qualitative themes is that patients do not seem to view their neurologists as being responsible for addressing nonphysical care needs. Revised American Academy of Neurology Quality Indicators promote a broad scope of practice for neurologists, including assessment of psychiatric symptoms, cognitive impairment, sleep disturbances, exercise, advance care planning, and so on (Factor, Bennett, Hohler, Wang, & Miyasaki, 2016). However, in interviews, most patients reported that they viewed the primary responsibility of their neurologists as managing medications. As a result, many patients indicated that they seek information and resources independently of their medical appointments. A separate branch of this study examined neurologist perceptions of outpatient palliative care in PD and found that many neurologists believe that they sufficiently address these patient needs, including those not belonging to the Physical domain of care (Prizer et al., 2017). The perceptions of both patients and neurologists, as indicated by these studies, highlight an important gap in patient and provider communication that needs to be addressed in future interventional studies.

Although the study makes an important contribution to the literature regarding previously unexplored gaps in the palliative treatment of PD patients, several limitations need to be acknowledged. Because some patients were recruited from support groups and neurologists were recruited primarily from specialist organizations, sampling bias may be an issue. Specifically, some patients may be better informed of resources than the general PD population or they may be more robust than participants who have stopped attending such programs or cannot participate in research. Despite this potential bias, patients still identified unmet needs in treatment. Patient participants were also recruited exclusively from Georgia, potentially limiting the generalizability and transferability of the findings to other geographic locations. The physician participants come primarily from National Parkinson Foundation (NPF) Centers of Excellence, which, because of the clinical focus and expertise of the NPF, may provide participating neurologists with enhanced access to interdisciplinary team care compared with most neurologists. This potential sampling bias may have resulted in more conservative estimates of palliative needs than would be found in PD patients outside of support groups and without access to neurologist specialist care.

The self-report nature of the survey may lead to inaccuracies due to recall bias; however, similar surveys exist and have been used in research to assess patient symptoms and physician referrals to palliative care (Ahluwalia & Fried, 2009; Jenkinson, Fitzpatrick, Peto, Greenhall, & Hyman, 1997). No standardized measures were available to measure the longitudinal palliative need of PD patients in the five primary domains of palliative care; therefore, one was developed for the study. Additional adjustments to the measure as well as validity and reliability testing are needed, however, to develop a standardized scale to better measure this need in this population. The limited scope of the study precluded clinical confirmation of disease severity and stage for patients, and follow-up studies should work to address this limitation. Future measures should also include methods to examine more organizational characteristics of provider practices to better understand factors affecting physician referrals to palliative services. Because of the limited prior research on this subject, this study focused on a cross-sectional assessment of palliative need, and, as a result, was exploratory in design.

Future studies should also use more racially and socioeconomically diverse samples to better understand palliative need and potential disparities in care within the PD patient population. Additional research is also needed to examine the most effective implementation of palliative care consultations in the long-term treatment of PD.

Conclusion

While patient palliative needs and preferences for care vary significantly among individuals with PD, nonphysical aspects of care (e.g., educational information and care coordination) may be commonly deficient in standard neurological care. Neurologists need to provide clarity to patients during their initial appointments regarding their role in care and, when appropriate, their clinic’s interdisciplinary resources to address potential patient misconceptions. These conversations could set a precedent for enhanced patient and provider communications through the course of illness, more broadly focused on the variety of factors that may influence quality of life. Although patient self-advocacy is encouraged in health maintenance, practitioners may want to consider working to guide patients collaboratively in locating information and developing a plan of care tailored to their needs.

While patients are encouraged to advocate for themselves, the ideal care model is a compromise of patient advocacy and physician treatment and recommendations (van der Eijk et al, 2013). Patients should work with their physicians to receive tailored information, recommendations, and referrals for resources. Needs should be prioritized based on consensus between the patient and neurologist, and the healthcare team should provide support to patients in accessing services and coordinating care. These results corroborate the findings of van der Eijk et al. (2011), who noted the need for a collaborative patient-centered model of care for individuals with PD. This approach is patient-centered, focusing on the symptoms and needs affecting individual HRQoL and providing treatment based on patient preferences (van der Eijk, Nijhuis, Faber, & Bloem, 2013). Palliative care teams currently use this participatory model in practice to work with patients and their families in coordinating their care throughout chronic disease, and these palliative programs may be well suited to assist in the ongoing needs of PD patients.

Despite the range of needs of older PD patients, not all neurologists have access to interdisciplinary teams or feel comfortable managing issues in psychological, social, financial, or spiritual care domains. The reported levels of need in these nonphysical symptom categories highlight the importance of palliative care involvement throughout the course of the illness. The interdisciplinary team involvement of palliative care may provide complementary services to standard neurology care in PD and improve patient outcomes.

Footnotes

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 research was supported by a grant from the College of Public Health at The University of Georgia.

References

Ahluwalia

S. C.

Fried

T. R.

(2009). Physician factors associated with outpatient palliative care referral. Palliative Medicine, 23, 608-615.

Bainbridge

J. L.

Ruscin

J. M.

(2009). Challenges of treatment adherence in older patients with Parkinson’s disease. Drugs & Aging, 26, 145-155.

Beiske

A. G.

Loge

J. H.

Svensson

(2009). Pain in Parkinson’s disease: Prevalence and characteristics. Pain, 141, 173-177.

Braun

Clarke

(2006). Using thematic analysis in psychology. Qualitative Research in Psychology, 3, 77-101.

Bunting-Perry

L. K.

(2006). Palliative care in Parkinson’s disease: Implications for neuroscience nursing. Journal of Neuroscience Nursing, 38, 106-113.

Bushnell

D. M.

Martin

M. L.

(1999). Quality of life and Parkinson’s disease: Translation and validation of the US Parkinson’s Disease Questionnaire (PDQ-39). Quality of Life Research, 8, 345-350.

Centers for Medicare & Medicaid Services (2009). Department of Health and Human Services. Hospice data 1998-2009. Baltimore, MD: Author.

Centers for Medicare & Medicaid Services. (2014). Medicare care choices model. Retrieved from http://innovation.cms.gov/initiatives/Medicare-Care-Choices/

Cheng

E. M.

Siderowf

Swarztrauber

Eisa

Lee

Vickrey

B. G.

(2004). Development of quality care indicators for Parkinson’s disease. Movement Disorders, 19, 136-150.

10.

Creswell

J. W.

Plano Clark

V. L.

(Eds.). (2011). Designing and conducting mixed methods research (2nd ed.). Thousand Oaks, CA: SAGE.

11.

Cubo

Rojo

Ramos

Quintana

Gonzalez

Kompoliti

Aguilar

(2002). The importance of educational and psychological factors in Parkinson’s disease quality of life. European Journal of Neurology, 9, 589-593.

12.

De Lau

Giesbergen

De Rijk

Hofman

Koudstaal

Breteler

. (2004). Incidence of Parkinsonism and Parkinson disease in a general population: The Rotterdam Study. Neurology, 63, 1240-1244.

13.

Emanuel

L. L.

Alpert

H. R.

Emanuel

E. E.

(2001). Concise screening questions for clinical assessments of terminal care: The needs near the end-of-life care screening tool. Journal of Palliative Medicine, 4, 465-474.

14.

Evans

(2015, July 20). CMS to test concurrent coverage of hospice and curative care. Modern Healthcare, 45(30), 10.

15.

Ellis

M. R.

Campbell

J. D.

Detwiler-Breidenbach

Hubbard

D. K.

(2002). What do family physiicans think about spirituality in clinical practice? The Journal of Family Practice, 51(3), 249-254.

16.

Factor

S. A.

Bennett

Hohler

A. D.

Wang

Miyasaki

J. M.

(2016). Quality improvement in neurology: Parkinson disease update quality measurement set. Neurology, 86, 2278-2283.

17.

Faul

Erdfelder

Buchner

Lang

A.-G.

(2009). Statistical power analyses using G8Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41, 1149-1160.

18.

Faul

Erdfelder

Lang

A.-G.

Buchner

(2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39, 175-191.

19.

Fereday

Muir-Cochrane

(2008). Demonstrating rigor using thematic analysis: A hybrid approach of inductive and deductive coding and theme development. International Journal of Qualitative Methods, 5(1), 80-92.

20.

Galesic

Bosnjak

(2009). Effects of questionnaire length on participation and indicators of response quality in a web survey. Public Opinion Quarterly, 73, 349-360.

21.

Giovanni

L. A.

(2012). End-of-life care in the United States: Current reality and future promise—A policy review. Nursing Economics, 30(3), 127-135.

22.

Granello

D. H.

Wheaton

J. E.

(2004). Online data collection: Strategies for research. Journal of Counseling and Development, 82, 387-394.

23.

Guest

MacQueen

K. M.

Namey

E. E.

(2012). Applied thematic analysis. Thousand Oaks, CA: SAGE.

24.

Hearn

Higginson

(1999). Development and validation of a core outcome measure for palliative care: The palliative care outcome scale. Palliative Care Core Audit Project Advisory Group. Quality in Health Care, 8, 219-227.

25.

Hebert

R. S.

Jenckes

M. W.

Ford

D. E.

O’Connor

D. R.

Cooper

L. A.

(2001). Patient perspectives on spirituality and the patient-physician relationship, Journal of General Internal Medicine, 16(10), 685-692.

26.

Hudson

P. L.

Toye

Kristjanson

L. J.

(2006). Would people with Parkinson’s disease benefit from palliative care? Palliative Medicine, 20, 87-94.

27.

Hughes

A. J.

Daniel

S. E.

Blankson

Lees

A. J.

(1993). A clinicopathologic study of 100 cases of Parkinson’s disease. Archives of Neurology, 50(2), 140-148.

28.

Hughes

M. T.

Smith

T. J.

(2014). The growth of palliative care in the United States. Annual Review of Public Health, 35, 459-475.

29.

Idler

E. L.

(Ed.). (2014). Religion as a social determinant of public health. New York: Oxford University Press.

30.

Institute of Medicine. (2015). Dying in America: Improving quality and honoring individual preferences near the end of life. Washington, DC: The National Academy Press.

31.

Jenkinson

Fitzpatrick

Peto

Greenhall

Hyman

(1997). The Parkinson’s Disease Questionnaire (PDQ-39): Development and validation of a Parkinson’s disease summary index score. Age and Ageing, 26, 353-357.

32.

Kutner

J. S.

Blake

Meyer

S. A.

(2002). Predictors of live hospice discharge: Data from the National Home and Hospice Care Survey (NHHCS). American Journal of Hospice & Palliative Care, 19, 331-337.

33.

Lang

A. E.

Lozano

A. M.

(1998). Parkinson’s disease. New England Journal of Medicine, 339, 1044-1053. doi:10.1056/nejm199810083391506

34.

Langston

J. W.

(2006). The Parkinson’s complex: Parkinsonism is just the tip of the iceberg. Annals of Neurology, 59, 591-596.

35.

Lees

A. J.

Hardy

Revesz

(2009). Parkinson’s disease. Lancet Neurology, 373, 2055-2066.

36.

Lokk

Fereshtehnejad

S. M.

(2013). Managing palliative care in Parkinson’s disease from diagnosis to end-stage disease: What the clinician should know. Neurodegenerative Disease Management, 3(2), 169-183.

37.

Marinus

Ramaker

van Hilten

J. J.

Stiggelbout

A. M.

(2002). Health related quality of life in Parkinson’s disease: A systematic review of disease specific instruments. Journal of Neurology, Neurosurgery & Psychiatry, 72, 241-248.

38.

Meyers

F. J.

Linder

(2003). Simultaneous care: Disease treatment and palliative care throughout illness. Journal of Clinical Oncology, 21, 1412-1415.

39.

Miyasaki

Long

Mancini

Moro

Fox

Lang

. . .Hui

(2012). Palliative care for advanced Parkinson disease: An interdisciplinary clinic and new scale, the ESAS-PD. Parkinsonism & Related Disorders, (Suppl. 3), S6-S9.

40.

Morrison

R. S.

Meier

D. E.

(2004). Palliative care. New England Journal of Medicine, 350, 2582-2590.

41.

National Consensus Project for Quality Palliative Care. (2013). Clinical Practice Guidelines for Quality Palliative Care. 3rd Ed. Pittsburg, PA: National Consensus Project for Quality Palliative Care. Retrieved from https://www.hpna.org/multimedia/NCP_Clinical_Practice_Guidelines_3rd_Edition.pdf

42.

Onwuegbuzie

A. J.

Collins

K. M.

(2007). A typology of mixed methods sampling designs in social science research. Qualitative Report, 12, 281-316.

43.

Peto

Jenkinson

Fitzpatrick

(1998). PDQ-39: A review of the development, validation and application of a Parkinson’s disease quality of life questionnaire and its associated measures. Journal of Neurology, 245(1), S10-S14.

44.

Peto

Jenkinson

Fitzpatrick

(2001). Determining minimally important differences for the PDQ-39 Parkinson’s disease questionnaire. Age and Ageing, 30, 299-302.

45.

Picillo

Kou

Barone

Fasano

(2015). Recruitment strategies and patient selection in clinical trials for Parkinson’s disease: Going viral and keeping science and ethics at the highest standards. Parkinsonism & Related Disorders, 21, 1041-1048.

46.

Prizer

L. P.

Browner

(2012). The integrative care of Parkinson’s disease: A systematic review. Journal of Parkinson’s Disease, 2(2), 79-86.

47.

Prizer

L. P.

Gay

J. L.

Perkins

M. M.

Wilson

M. G.

Emerson

K. G.

Glass

A. P.

Miyasaki

J. M.

(2017). Using social exchange theory to understand non-terminal palliative care referral practices for Parkinson’s disease patients. Palliative Medicine, 31, 861-867. doi:10.1177/0269216317701383

48.

Rao

S. S.

Hofmann

L. A.

Shakil

(2006). Parkinson’s disease: Diagnosis and treatment. American Family Physician, 74, 2047-2054.

49.

Smith

Brick

O’Hara

Normand

(2014). Evidence on the cost and cost-effectiveness of palliative care: A literature review. Palliative Medicine, 28(2), 130-150.

50.

Strand

J. J.

Mansel

J. K.

Swetz

K. M.

(2014). The growth of palliative care. Minnesota Medicine, 97(6), 39-43.

51.

Tolosa

Wenning

Poewe

(2006). The diagnosis of Parkinson’s disease. The Lancet Neurology, 5(1), 75-86.

52.

Van Den Eeden

S. K.

Tanner

C. M.

Bernstein

A. L.

Fross

R. D.

Leimpeter

Bloch

D. A.

Nelson

L. M

. (2003). Incidence of Parkinson’s disease: Variation by age, gender, and race/ethnicity. American Journal of Epidemiology, 157, 1015-1022.

53.

van der Eijk

Faber

M. J.

Shamma

S. A.

Munneke

Bloem

B. R

. (2011). Moving towards patient-centered healthcare for patients with Parkinson’s disease. Parkinsonism & Related Disorders, 17, 360-364.

54.

van der Eijk

Nijhuis

F. A. P.

Faber

M. J.

Bloem

B. R

. (2013). Moving from physician-centered care towards patient-centered care for Parkinson’s disease patients. Parkinsonism & Related Disorders, 19, 923-927.

55.

Ward

B. W.

Schiller

J. S.

(2013). Prevalence of multiple chronic conditions among US adults: Estimates from the National Health Interview Survey, 2010. Preventive Chronic Disease, 10, Article E65. doi:10.5888/pcd10.120203

56.

Weernink

M. G. M.

van Til

J. A.

van Vugt

J. P. P.

Movig

K. L. L.

Groothuis-Oudshoorn

C. G. M.

(2016). Involving patients in weighting benefits and harms of treatment in Parkinson’s disease. PLoS ONE, 11(8), e0160771.