Improving patient‐centred care for persons with Parkinson's: Qualitative interviews with care partners about their engagement in discussions of “off” periods

Abstract Objective This study explored how care partners (CPs) of persons with Parkinson's (PwP) are engaged in discussions of “off” symptoms. Methods During qualitative interviews, CPs of PwP sampled by convenience through the Michael J Fox Foundation online clinical trial matching service were asked to describe their familiarity with “off” symptoms, how “off” symptoms were discussed with clinicians, and the impact of “off” symptoms on them. Data were analysed using constant comparative technique by all members of the research team. Results A total of 20 CPs were interviewed. Compared with PwP, they were more likely to describe “off” symptoms to clinicians. CPs identified important aspects of patient‐centred care for PD: establishing a therapeutic relationship, soliciting and actively listening to information about symptoms, and providing self‐management support to both PwP and CPs. CPs said that clinicians did not always engage CPs, ask about “off” symptoms or provide self‐management guidance, limiting their ability to function as caregivers. Conclusion By not engaging and educating CPs, “off” symptoms may not be identified or addressed, leading to suboptimal medical management and quality of life for PwP. These findings must be confirmed on a broader scale through ongoing research but suggest the potential need for interventions targeted at clinicians and at CPs to promote patient‐centred care for PwP.

sweating, light-headedness, urinary urgency, pain and restlessness. 3 PD is a progressive and incurable disease so therapy goals are to relieve symptoms and preserve functional capacity. 1 Pharmacologic treatment largely relies on dopaminergic medication; non-pharmacologic therapies include exercise, and physical, speech and/or occupational therapy. 2 In later disease stages, PwP who are successfully treated with medications may experience periods when motor and non-motor symptoms worsen based on medication timing, with symptoms appearing or worsening at the end of the medication dose and then improving in response to PD therapy. 3 Prevalence estimates for these periods, termed "off" periods, vary; as many as 25%-50% of PwP experience symptom fluctuations as medication wears off. 3 "Off" periods are variable in timing, severity and predominant symptoms both between and within individuals. This necessitates regular and thorough assessment by clinicians to modulate medication and provide education, which is essential to help PwP anticipate and manage motor and non-motor symptoms, reduce potential adverse events and minimize symptom impact on quality of life. 1 Providing PwP with self-management knowledge, skills and confidence to monitor progress and solve problems is important to PwP. 4 In a prior study, the majority of 492 PwP surveyed thought that self-monitoring would improve their understanding of the condition, well-being and ability to cope, and communication with their healthcare team. 5 Hence, patient-centred care (PCC), which involves communication and partnership with patients to support involvement in their own health and health care, is essential for optimal PD management. 6 Patient-centred care is defined as care that considers the values, beliefs, desires, lifestyle and family and social circumstances to inform, educate and engage patients consistent with their needs and values. 7,8 Patient-centred care is considered a fundamental element of high-quality care because it has been shown to improve patient (ie, experience, satisfaction, clinical outcomes) and health system outcomes (ie, cost-effective service delivery and use) across multiple conditions and settings of care. 9,10 Considerable research has characterized PCC as a multidimensional approach to care that involves fostering clinician-patient relationships, involving family or caregivers/care partners, exchanging information, recognizing and responding to patient emotions, managing uncertainty, making decisions and enabling patient self-management. 11 Unfortunately, PCC for PD does not appear to be prevalent.In the United States, 20 Parkinson Centers of Excellence asked 50 consecutive patients to complete the patient centredness questionnaire for PD (PCQ-PD). 12 Significant differences between centres were found for all subscales (rated from 0 to 3); the information subscale (mean 1.62 SD 0.62) and involvement in decisionmaking subscale (mean 2.03 SD 0.58) received the lowest ratings.
In 30 European countries, among 1546 respondents, 34.2% said they were not involved in treatment decision making, and 17.2% said they felt rushed to make a decision. 13 Of those, 200 were care partners (CPs), 59.0% said they helped the PwP to prepare a list of questions, and 46.5% helped to prepare a list of symptom changes prior to consultations, underscoring the role of CPs, including spouses, family members or informal caregivers, in PCC. 14 With respect to PD, a six-psychiatrist panel rated information provided during interviews with 223 PwP and separately by their CPs and judged that 71 (31.4%) CPs were critical for determining a psychiatric diagnosis. 15 Without a CP, 81.3% of those with impulse control disorders and 43.8% of those with anxiety disorders would not have been diagnosed. Hence, the insight and input of CPs is essential to "off" symptom identification and control, which influences the safety, independence and quality of life of PwP, and the ability of CPs to support PwP.
Most studies on the role of CPs in PD have focused on the psychosocial, physical and financial burden on CPs of caring for PwP. 16,17 In contrast, little research has explored the role of CPs in PCC. 13,15 This is germane to the context of PD where CPs can provide clinicians with important information about "off" symptoms and symptom changes, knowledge needed by clinicians to optimize medication and symptom management. The purpose of this study was to explore how CPs of PwP are engaged by clinicians in discussions of "off" periods, including if and how CPs interact with health-care professionals, their role in discussions about symptoms, and their potential impact on the therapeutic relationship and the care received by the PwP they represent. This knowledge may reveal whether there is a need to better engage and support CPs in PCC for PD.

| Approach
This study involved secondary analysis of data collected in a multi-method study to investigate the impact on PwP and CPs of motor and non-motor fluctuations ("off" periods) and communication about these symptoms with clinicians. Given the lack of prior research on the role of CPs in PCC for PD, the study was based on an exploratory research design involving qualitative interviews with PwP, CPs and neurologists to thoroughly identify and describe communication experiences and preferences. 18 Interviews were conducted and analysed using a basic descriptive qualitative approach, which is neither based on nor generates theory, but instead explicitly reports experiences. 19 In this context, it was useful to gather straightforward accounts of CP experiences and recommendations, which could provide insight on how to improve PCC for PwP. All participants provided informed consent prior to being interviewed, and the investigators did not have any relationship with participants. To optimize rigour, we complied with all 32 items of the COREQ reporting standards for qualitative research, which includes providing details about the research team and reflexivity, study design, and analysis and reporting of the findings. 20 To enhance rigour, we analysed responses inductively so that findings emerged from the data, compared independently derived analyses and interpretations to establish saturation and enhance trustworthiness of the findings, reviewed findings with collaborators from the Michael J Fox Foundation to further ensure credibility of the findings, and reported exemplar quotes with anonymous identifiers to illustrate the views and experiences of a variety of participants. 21  This study focuses on CPs; findings of interviews with PwP will be reported elsewhere.

| Data collection
All interviews were conducted by TR, a neurologist, who was trained and mentored by ARG, a PhD-trained researcher with expertise in qualitative methods. Interviews were conducted by telephone from April 5, 2018, to October 30, 2018. Care partners were interviewed separately from PwP, and the mean duration of CP interviews was 33 minutes. Participants were asked three questions: describe your familiarity with "off" symptoms (prompts: which are most common, when and how frequently do they occur), how are you involved in communication with clinicians about "off" symptoms (prompts: attend appointments, ask questions, offer information, barriers, facilitators) and the impact of "off" symptoms on them (prompts: well-being, relationship, usual activities).
Questions were purposefully broad so that themes pertaining to their experiences would emerge from the data. As is customary in qualitative research, additional prompts were deployed if needed to elicit additional information for each question. Interviews were audio-recorded and transcribed verbatim by a professional transcription service.

| Data analysis
TR identified and organized themes in Microsoft Word using inductive qualitative methods with guidance from ARG. 18,19 TR read all transcripts to identify and define themes (firstlevel coding). TR developed a codebook to organize themes and sample quotes. TR re-reviewed coding (constant comparative technique) to assess whether and how to expand or merge themes (second-level coding). Each of first-and second-level coding was independently reviewed by ARG, and by MJA and CM, both neurologists with movement disorder specialization. Saturation was determined by discussion and consensus among the research team following the completion of 20 interviews. Data were reviewed by collaborators at the Michael J Fox Foundation to further ensure credibility. Data, including themes and exemplar quotes, were tabulated and summarized.

| Participants
A total of 20 CPs were interviewed. They provided support to PwP with a mean age of 65.1 years (SD 8.3, range 49-77) whose PD diagnosis was established a mean of 7.8 (SD 4.7, range 1-20) years ago. Just over half of CPs were female (11, 55.0%). Most CPs were spouses (17, 85.0%); others were a son, brother-in-law and close friend.

| Themes
Five main themes were identified: CPs familiar with "off" symptoms, CPs more likely to report and discuss "off" symptoms than PwP, CPs did not experience PCC, CPs not actively engaged in "off" discussions by clinicians, and CPs profoundly impacted by "off" periods. Overall, CPs revealed that without their input, clinicians cannot competently manage PD, potentially exposing PwP and CPs to the risk of adverse outcomes associated with poor symptom control. Individual themes with exemplar quotes are further described here.

| CPs familiar with "off" symptoms
CPs were keenly aware of PwP "off" symptoms and associated behaviour and impact because they were involved in many aspects of the lives of PwP (Table 1). For example, they assist with administering medication, activities of daily living, monitoring for symptoms, and scheduling and planning activities. They are always with or vigilant of the PwP, while at the same time promoting some independence where possible.
We only travel together now…I'm never too far away (CP2) Care partners spoke about recognizing symptoms such as irritability or lack of attention, and carefully timing discussions and activities with PwP to accommodate "off" periods.
I need to be conscious of the time required to do things (CP12)

| CPs more likely to report and discuss "off" symptoms than PwP
Care partners said they prepared for and accompanied PwP to consultations ( Table 2). In particular, CPs said they were more likely to report "off" symptoms to physicians than PwP, who are not aware of, or may deny or hide the extent of their symptoms. A tremor, mostly in his right hand. Sometimes when I see that and I will ask, you know, did he remember to take his meds (CP16) I take emergency medicine with me in case he leaves his pills at home and we'll need them. And I always have them in my purse, so you just plan ahead (CP17) Helps with activities of daily living I usually offer to pick up all the slack, so I'll be cooking dinner and just take over… I just take her in stride and, you know, say, I've got this, and just kind of let her be (CP2) You be very attentive, you know, be there to assist the movement, try to prevent a fall especially when she's using stairs (CP10) There have been times I've had to cook for her (CP16) Understands nuances of symptom timing It's almost like he becomes a person with Asperger's; he has no eye contact, he stoops even more, he'll fix his gaze on a spot in front of him on the floor (CP1) We've tried really meticulously to correlate things like diet, frequency of medication, dose of medication, should she take one whole pill every two hours or a half pill every hour, that kind of stuff. We have experimented with that stuff six ways from Sunday, diet, sleep, exercise (CP2) She tends to feel, most of the time, very good in the morning, then at around 11 o'clock she usually has a period where she gets tired and she -if she forgets her medicine it becomes quite apparent. (CP6) She gets a little low on medication, then she gets some stiffness, especially with walking. It's typically for a period almost ever morning (CP9) She has trouble with movement, moving her feet, particularly going backwards or sideways, a little bit of trouble getting started going forward but not so much going forward (CP10) She's a little less patient, a little more irritable (CP14) The daytime one is mainly really just the shaking on the left side (CP15) It seems like the off periods are worse when he is fatigued, but definitely slower walking, and sometimes slight agitation, either later in the late afternoon or early evening (CP16) It usually entails stiffness and difficulty standing up we attribute to the medication wearing off (CP19) Undertakes scheduling and planning of activities with and for PwP We have had to adjust our schedules to when we do things (CP5) Instead of trying to do a whole bunch, we try to pace things out more (CP6) I need to be conscious of the time required to do things, whether it's travel or prepare a meal, and how that will impact the schedule (CP12) Plans timing of discussions with PwP If we need to discuss something where a decision has to be made, more than likely I'll do it in the morning, because if it's too close to the OFF time and he hasn't taken his medication and it's been in his system for maybe about an hour, I know that whatever we've talked about he either forgets or gets confused (CP5)

Is always with or vigilant of PwP
We only travel together now, she wouldn't travel alone anymore. I'm never too far away…she will frequently drive to a nearby gym or grocery store, and I'll have to pretend this is normal, but also double-checking that she's okay to drive right now (CP2) Also attempts to support some independence

| CPs did not experience PCC
Care partners reported variable PCC practices among physicians.

| CPs not actively engaged in "off" discussions by clinicians
Care partners that described good communication also noted that physicians were open to talking to both the PwP and CP. In contrast, several CPs described suboptimal CP engagement in PCC.
Some physicians did not give or receive information to/from CPs: They're not going to treat her, they're just going to follow her. And that's what it feels like, they're like following, but it doesn't feel like an advocacy for us as we kind of thought they would be more interested or something (CP2) I think she's a good doctor but she said something the other day that sure bothered me: "You're not the only person in the world with Parkinson's, you know?". It really pissed me off (CP8) Ignore symptoms or issues considered important by CP They have no skill for his cognitive issues and they don't seem particularly interested in dealing with it (CP1) Do not actively prompt for information about symptoms or issues It certainly would help for the physician to ask open-ended questions and be patient to listen to the responses (CP1) Her doctors have been -aloof isn't quite the right word -but we only them once every six to nine months, and they're not too keen on getting the scoop…they're certainly not asking the level of questions, like what is the impact and extent and severity of these "off" periods (CP2)

| CPs profoundly impacted by "off" periods
Care partners described numerous detrimental sequelae and profound impacts associated with their roles as caregivers and as care partners (Table 4). These included anxiety, stress, helplessness, I think there was a lot of frustration and I would find myself getting short tempered over certain things like, "Why aren't you remembering this, why are you doing that sort of thing?" (CP12) It's frustrating when you really cannot do a whole lot, where she is dependent upon certain physical activities and medication to try to snap out of the "off" time (CP13) Sadness I feel very sorry for him to tell you the truth (CP17) Fear I feel horrid, I really do. I'm afraid that he's going to hurt himself, depending on the freezing position that he's in. I worry about him falling, which he has done a few times (CP3) It's like her feet don't respond anymore and she went head first into a rock and severely cut her forehead. We were out in the middle of nowhere. I was terrified. I've always been pretty good when there's an emergency but I was absolutely paralyzed, I didn't know what to do (CP18)

Reduced couple activities
It's hard to plan anything in the evening anymore because that seems to be his worst time (CP3) We won't go on a trip where we have to do a whole bunch of hiking. The levels of our activities have changed (CP6) She wants to travel and we can't do that. We haven't been able to do much of anything socially for the last couple of years because of this. It had a pretty severe effect on our social lives and her ability to function in a wider society. That really is limiting (CP7) If it has to do with crowds, like going to a fair or going to a shopping mall or going to a concert venue, we won't do (CP9) He felt less able to do things which made us both feel less able to do things (CP12) We don't go to the movies. We don't go to the theatre. We don't go to the Philharmonic, which was a favourite of ours (CP15) Reduced individual activities I was doing a fair amount of traveling and that has been curtailed because it's not good to leave her (CP2) I have a lot of friends that I like to go to lunch and shopping and things with, and it's hard because all I do is worry about him because he's alone (CP3) I find myself not doing as many things as I used to (CP5) Impact on career There's no way I could consider a fulltime position right now…so I work from home and I take coaching calls…I was doing a fair amount of traveling but that has been curtailed because it's not good to leave her (CP2) distress, uncertainty about the future, frustration, sadness and fear.
"Off" symptoms also limited CP personal and professional activity, and limited joint activities of PwP and CPs.
Helplessness, like you can't do anything to help (CP4) I can see what I think is fear…and that makes me feel anxious because she's not in control (CP7) He felt less able to do things which made us both feel less able to do things (CP12) Hence, further research is needed to understand how to overcome system-level barriers of access to high-quality PCC for PwP.

| D ISCUSS I ON
Recent reviews highlighted the burden of PD on CPs in their caregiving role. 16,17 Our study also identified the profound impact of caregiving that results in anxiety, stress, helplessness, distress, frustration, sadness and fear among CPs of PwP. Our study also revealed the confusion and concern experienced by CPs in consultations when they were uncertain about whether and how to contribute while simultaneously being alarmed that key details that only they could contribute were being missed. This underscores the need to provide CPs of PwP with support for their role as care partners in health-care planning. Numerous instruments are available to assess caregiver burden, 17 but not to assess CP interest and capacity to be involved in PCC for PD. [34][35][36] Thus, further research is needed to specifically investigate how to best engage CPs of PwP in health-care planning, and the best type of intervention to support CPs.
Strengths of this study included the use of rigorous methods for data collection and analysis including independent review by multiple authors to establish and interpret themes, sampling to thematic saturation and compliance with standards for the conduct and reporting of qualitative research. 20,21 Still, the interpretation and application of these findings may be limited by several issues. Sampling was convenience rather than purposive, and we did not collect data on race/ethnicity, education or stage of disease, so we were not able to explore possible differences in views and experiences among  PwP and CP to solicit information and actively listen to information about symptoms and other concerns, and provide education and self-management support. CPs said that clinicians did not always ask about or address symptoms when raised, and did not always engage CPs in discussions. As a result, important information about "off" symptoms was not considered, and CPs were not provided with strategies for dealing with "off" symptoms, further adding to CP burden and potentially resulting in suboptimal management of PD. As a qualitative study, these findings must be confirmed on a broader scale through ongoing research. However, the findings suggest the need for interventions targeted at clinicians and at CPs to promote PCC for PD.

CO N FLI C T O F I NTE R E S T
The authors declare no conflicts of interest.