Patient and care partner views on exercise and structured physical activity for people with Progressive Supranuclear Palsy

Introduction Progressive Supranuclear Palsy (PSP) is a debilitating form of atypical Parkinsonism. People living with PSP experience movement disorders affecting walking, balance and eye movements. The role of exercise in optimising movement remains unclear. Aims To identify beliefs about exercise and structured physical activity through the experience of people with PSP. Methods Using a phenomenological theoretical framework, qualitative methods were employed to obtain the views of people living with PSP, and their care partners, by in-depth interviews. Questions derived from a systematic review and expert opinions guided the interviews which were audio-recorded, transcribed and de-identified. Two researchers independently conducted thematic analysis and reached consensus on emerging themes. Results There were 16 participants. Four themes were identified: (i) there are beliefs and preferences about exercise and physical activity that can impact on engagement; (ii) difficulty coping with disease progression impacts activities; (iii) facilitators to exercise include individual preferences, access to facilities and expert advice; and (iv) perceived barriers include beliefs about limited exercise options, falls risk, cost, transport and access to credible information. Discussion People living with PSP want early guidance about the condition and the role of exercise. It is important to quickly enable people to have access to evidence and resources supporting exercise and structured physical activities. Consideration of individual preferences and access to expert advice facilitate engagement. Individual barriers need to be identified and solutions found. Conclusion People living with PSP are amenable to exercise, especially early in the disease process. Clear guidelines are warranted to document which exercises, and physical activities are most beneficial.


Introduction
Consideration of consumer preferences is therefore a priority for developing programs that are tailored to the individual [38,39]. There remains a need to identify facilitators and barriers to participation and engagement as well as optimal content, dosage and scheduling of exercises for people living with PSP [12].
The present study explores the potential benefits and perceived challenges of exercise through the experiences of people directly affected by this rare, chronic and progressive disease. We aim to identify beliefs about, and facilitators and barriers to, exercise and physical activity. We defined exercise as planned, structured, repetitive and intentional movement intended to improve or maintain strength and fitness [40]. We sought the views of people living with PSP, care partners and family members and developed the following research question: What is the lived experience of exercise and structured physical activity for people living with PSP?

Theoretical framework
Understanding people's beliefs about facilitators and barriers to exercise and physical activity is well suited to a qualitative method of enquiry [41][42][43]. In qualitative research, a phenomenological approach aims to explore personal lived experiences to help understand how people make sense of the world in which they live [44][45][46]. It provides a deep level of understanding that may not always be revealed through randomised controlled trials or responses in questionnaires and surveys [44][45][46]. This framework was applied in the current study to gain a deeper understanding of the perceptions of people diagnosed with PSP, and their caregivers and/or family members, about exercise and physical activity.

Design overview
Individual interviews were conducted at home for people living with PSP, caregivers and family members. We did not conduct focus groups because of the burden of travelling to one location, communication difficulties amplified in a group setting and the sensitive nature of some personal disclosures. The study was reported according to the Consolidated Criteria for Reporting Qualitative studies (COREQ) checklist [47].

Ethics considerations
The study was approved by the La Trobe University Human Research Ethics Committee (Project: HEC18333). All participants provided written informed consent prior to data collection. Participants were assured of confidentiality and anonymity and were assigned an identification number. All data within the transcribed recordings were de-identified for person and place. The participants were given the opportunity to speak freely and openly.

Research team
Three members of the study team trained as physiotherapists and had a range of research and clinical expertise. SCS (PhD) had expertise in physiotherapy, exercise prescription and qualitative research methods. MEM (PhD) and JMG (PhD) had expertise in neurological physiotherapy, movement disorders, quantitative research, project management and supervision. CB (PhD) qualified as an occupational therapist and had expertise in neurological rehabilitation, evidence-based practice and data analysis. BRB (PhD) is an international expert neurologist specialising in movement disorders and Parkinson's research. None of the research team members were known to any of the participants.

Participant eligibility and recruitment
Recruitment of people with PSP, care partners and family members, was via purposive sampling in Australia and continued until data adequacy and saturation were reached. An advertisement and information summary were placed in the state-wide Parkinson's association newsletter and distributed at atypical Parkinson's support groups. Advertisements were also placed in the reception areas of movement disorders neurology and physiotherapy clinics. People living with PSP had to have received a provisional or final diagnosis of PSP from a medical practitioner and have verbal capability for audio-recording. There was no requirement of experience with exercise and there were no cognitive criteria, All patients, family members, and caregivers who contacted the researcher by email or phone were provided with an explanation of the study. The researcher answered any questions and provided potential participants with a consent form. The interviews followed completion of written informed consent and, for people living with PSP, provision of a signed doctor's ethics approved screening form confirming a diagnosis of PSP and medical suitability to participate in an interview. Interviews were scheduled at a time convenient to each of the participants and were either in the home or via videoconferencing.

Data collection
An experienced facilitator (SCS), unknown to any of the participants, conducted audiorecorded interviews. A set of interview questions was informed by a systematic review [12] and expert opinions from the research team as well as consulting with the Parkinson's association representatives ( Table 1). Members of the research team are international experts on movement disorders, PD and atypical parkinsonism, including PSP. There was no participant input or pilot testing due to the possibility of introducing bias in a very small potential participant pool. Questions guided conversation about the diagnostic experience, exercise preferences and practices (such as walking, aquatic, dance, strengthening), movement strategies and information needs. Demographic data such as age, time since diagnosis, medication, co-morbidities, falls incidence, exercise activity and beliefs/preferences and utilisation of allied health services were collected from participants. Care partners provided data such as age, exercise beliefs and practices, co-morbidities. Field notes were made immediately after each interview to provide a record of observations and impressions. These notes included non-verbal or emotional responses, observations and possible patterns emerging from the collected data. Data collection took place from January 2019 until December 2019.

Data storage and confidentiality
Participants were de-identified by number and all hard copy data (master list, informed consent, demographic data and doctor's screening forms) were stored securely in a locked filing cabinet in a locked office. Audio recordings and electronic de-identified verbatim transcriptions were stored on a secure university research drive.

Data analysis
Two researchers (SCS and CB) independently conducted an iterative, step-by-step thematic analysis of the de-identified transcripts by using an inductive method [41,43,44,48]. Transcripts were read several times to ensure familiarity. Data were coded and compared, categorized into clusters of meaning according to similarities. Each researcher independently developed preliminary themes by using descriptive content analysis and conducted documented video-conferencing and face-to-face meetings, followed by confirmation emails, until consensus was reached for the final set of themes and sub-themes. Representative quotations for each theme were selected and pooled together to support the identified themes. A codingtree is available from SCS on request. The research team were available for consultation throughout the analysis process. MEM was consulted for content expertise and consensus.

Bias control and method quality
Steps were taken to enhance the rigour of the study design [49]. These steps included: (1) a priori eligibility; (2) recruitment of participants who had the experiences to address the research questions and were also likely to bring different experiences based on stage of the condition; (3) documented and replicable data collection and data analysis steps; (4) audio-recording and verbatim transcription; (5) independent data analysis by two researchers and (5) results linked to participant data.

Results
In-depth individual interviews were conducted with 16 participants (eight care partners and eight people living with a diagnosis of probable PSP; there were six couples, one mother-son, one widowed care-partner and one individual with PSP). Interviews were conducted by SCS either in the home or in the residential care facility. There were ideas and experiences common to all the interviewees and no dissonant reports. Repeat interviews and member checking of transcripts were not required as, for the former, data saturation was reached, and, for the latter, there was a risk of recall bias. There were no dropouts or refusals to participate.
The mean age of people living with PSP was 71.4 years (SD: 7.7) and of carers was 66.4 years (SD: 10.4) years. The mean time since diagnosis was 3.4 years (SD: 1.1) although cognitive deficits and falls existed for several years prior to provisional diagnosis in all people living with PSP. The mean interview time was 61.0 minutes. Two participants with PSP lived alone in residential care and six participants with PSP lived at home with a care partner/spouse. Falls were frequent and ranged from daily to once a month. Health comorbidities included type 2 diabetes, hypertension, cardiovascular disease, osteoarthritis, vision and speech impairments, sleep apnoea, Meniere's disease, frontal lobe dementia, meningioma and back and neck pain ( Table 2).
An overall finding arising from analysis of the interview data was that people living with a diagnosis of PSP and their care partners perceived that a range of intrinsic and extrinsic factors influence engagement in exercise and structured physical activity. Four main themes were identified: (i) there are beliefs and preferences about exercise and physical activity that impact on engagement; (ii) difficulty coping with disease progression impacts physical activity levels; (iii) there are facilitators to exercise participation in PSP; and (iv) there are perceived physical, psychological and economic barriers to engagement. The themes and sub-themes are presented in the following text, supported by quotations linked to the participants by code and transcription line numbers.

Theme 1: There are beliefs and preferences about exercise that influence engagement a) Engagement in exercise and structured physical activity is influenced by life experience with exercise.
Participants reported that the extent to which they engaged in exercise and physical activity. This was related to their life-long practices in varied exercise activities and environments. Their past history of exercise participation and their capacity for daily physical activity influenced views about participating in structured physical activities after being diagnosed with PSP. (Box 1).

b) Engagement in exercise and structured physical activity is influenced by exercise preferences.
Participants reported different preferences about types of exercise, and this influenced their choices and participation after PSP diagnosis. Many reported the importance of enjoyment and flexibility (Box 2). Theme 2: Difficulty coping with the disease progression impacts activity a) changes in ability affect activity engagement. Participants diagnosed with PSP reported difficulties with loss of mobility, independence and social connectedness. These deficits were associated with rapid disease progression, movement disorders and non-motor symptoms such as cognitive impairment, sleep difficulties, anxiety and depression. The most challenging symptoms included: falls, reduced mobility, vision, speech and swallowing impairments. These symptoms negatively affected participation in activities of daily living, exercises and physical activities (Box 3). b) Care partner strain and relationship changes impact on ability to assist with activity engagement. Care partners articulated elements of carer strain, a sense of social isolation and feelings of guilt, burden and frustration. There was acknowledgment of a transition in roles within the family as the disease progressed. Changes in roles were most often reported by the spouse, partner, child or sibling of the care-recipient. Changing roles, especially later in life, were sometimes associated with emotional tensions, including conflict and feelings of guilt. Care partners and family members often felt frustrated due to a lack of education available for community members, general practitioners and allied health clinicians about PSP (Box 4).

Theme 3: Facilitators to exercise participation in PSP
a) Access to facilities and community groups enabled engagement. Participants reported that local facilities, for example swimming pools, and social connectedness in their local community helped them to keep active. For people living at home, the availability of local facilities such as gymnasiums, swimming pools, dance halls, bike tracks, walking paths and sports facilities was an important factor. Routines in daily living such as dog walking or participation in local groups such as bowls, dancing or bicycle riding were important. For those who lived in residential care, the availability of an in-house space for exercise classes, equipment and staffing support were enabling. Transport to and from the exercise room and supportive, actively involved staff, partners or other caregivers were key (Box 5).
b) Expert advice from health professionals was valued. Participants diagnosed with PSP, and the significant others in their lives, frequently sought guidance about safe exercises and general activities. Guidance was frequently sought from clinicians with experience working with people diagnosed with PSP and clinicians working in movement disorders clinics. Access to advice and therapy was frequently reported to be difficult, yet once attained, the services helped to improve understanding about PSP, mobility and falls prevention. People frequently sought this expert advice because they were unsure whether exercise would aggravate their PSP symptoms (Box 6).   and limited independent engagement in activity. Barriers such as falls risk and reduced balance, strength and fitness may be overcome by exercise (Box 8).

c) Access to facilities is limited by cost, financial resources and transport.
All of the participants talked about their financial position and concerns about the costs of care, including exercise therapies. Movement disorders clinics had long wait times and private care incurred out of pocket expenses. Some people living with PSP became unable to drive or unsafe to use public transport alone and relied on others to access therapies (Box 9).

d) Lack of credible information and limited access to experts.
Participants wanted reliable and credible information about the range of available therapies, such as educational materials and links to support groups and organisation websites. All participants reported this to be difficult to find. Many participants experienced a difficult pathway to finding experienced and expert clinicians and movement disorders clinics (Box 10).

Discussion
Our investigations reflect the difficulty in diagnosing PSP, with often lengthy delays in patients receiving treatments that target the presenting symptoms [18]. People living with PSP reported seldom being referred for exercise therapy by their medical specialist. They reported navigating their own way to exercise by trial and error or by previous life experience of exercise. The participants also reported they did not know which forms of exercise and physical activity were helpful for people with PSP, echoing the findings of a recent systematic review [12]. Where there was a past history of exercise people understood the potential value of exercise. Where there was not a past history of exercise people were unclear about type and dosage.
Participants diagnosed with PSP and the care partners we interviewed were generally positive about exercising, and also reported several facilitators and barriers to participation in physical activities. The facilitators included: (i) being provided with information about the benefits of exercise and movement rehabilitation for PSP early on in the disease process or before provisional diagnosis but at a time when treatable symptoms are already manifest; (ii) having access to accurate information about PSP and its progression; (iii) access to healthcare providers, including medical, nursing and allied health, supportive of the role of exercise in PSP; (iv) having prior exercise experience and (v) having easy access to exercise facilities, groups and programs. Some of the barriers included: (i) perceptions of long delays in reaching a PSP diagnosis; (ii) lack of information about the benefits and contraindications to exercise and physical activity in PSP; (iii) fear of falling during physical activity; (iv) financial and transport constraints in getting to an exercise venue and (v) limited access to movement disorders specialists and PSP experts. These findings concur with the limited available published literature in atypical Parkinsonism [12,13,40] and the more extensive body of work in PD [22,23,50,51].
All of the people with PSP that we interviewed experienced long delays in reaching a provisional diagnosis and often consulted multiple specialists. Moore et al (2014) reported similar findings and noted that a common misconception is that no treatment is available for PSP [52]. The participants also highlighted the need to develop a concise overview of symptoms and care options. Our respondents reported a lack of advice regarding management options and delays in referral to other healthcare providers, such as physiotherapists, podiatrists, occupational therapists and community-based exercise trainers. Arguably, the provision of early accurate information and referrals to movement disorders healthcare providers, who have experience with PSP, might enable the provision of comprehensive care in the period of diagnostic uncertainty and before major cognitive and physical decline. This approach is well established for PD [50,53] and may also be suitable for PSP.
Care partner burden was a recurring theme in our sample of participants and is in agreement with recent international research in PSP and PD [54,[55][56][57]. The care partners were often older and reported high levels of strain and fatigue associated with their carer roles and the time spent seeking out resources, services and providing transportation. Caregiver burden is a recognised phenomenon with families and care partners finding themselves educating healthcare providers, advocating for the needs of people with PSP and attempting to navigating complex health and social care systems [52].
A history of exercise participation and an interest in structured physical activities facilitated exercise engagement. Participants in the present study believed that provision of exercise and activity facilities within the local community was important. For example, sport and activity participation in local facilities such as parks, bicycle paths, walking tracks and gyms [58,59]. Community engagement and connection to others through hobbies, social groups and peer-Box 6. Advice from health professionals is valued "I made up a ramp. The physio said-helped me design and make up a ramp. Walk [37,52,60].
All of the participants reported that fear of falling, consequences of falls and physical limitations influenced their beliefs about the safety of structured physical activities. All reported an increased incidence of falls and near-misses in the period when they were awaiting a definitive diagnosis. These self-reports may be useful for obtaining an earlier diagnosis of PSP [18]. Furthermore, limiting participation in the presence of communication difficulties and cognitive impairment were reported to hamper interactions with others and to increase social isolation. Similar findings were noted by Moore (2014) and Wiblin (2017) [52,60].
Results of this study need to be interpreted with caution in light of several limitations. Although we reached saturation of data for key themes, the results reflected the views of 16 people and might not represent all people living with PSP. Diagnostic uncertainty and the Box 9. Financial resources and access to transport were barriers to exercise participation "A few years ago, I was trying taxis and things, and that doesn't work anymore. . . I had a couple of taxi drivers who wouldn't load the wheelie into the vehicle. And they wouldn't help me in and out of the car" P8, line 713 heterogeneity of the disease itself also could have limited generalisability. Specificity of findings to the people involved and their context with respect to access to community services, health systems, and financial constraints might also limit generalisability. Bias of the researchers may have influenced interpretation, although measures were taken to control bias in the research design.
To conclude, people with PSP and their care-partners were receptive to the value of therapeutic exercises and structured physical activities. Care recipients and healthcare professionals generally did understand that exercise is important for strength, endurance and participation in ADL. Not all of them had access to specific guidance about the optimal type and dosage of exercises and physical activities for people living with atypical Parkinsonism. There was no prior evidence on the potential disease-specific benefits of exercise for people with PSP. After being diagnosed with PSP there was often a prolonged period of inactivity at a time when exercise appears to have the greatest potential to mitigate disability.

Highlights
• People with PSP and their care partners seek early and reliable information about the benefits, and precautions for, different types of exercise and physical activity • Individual exercise preferences and capabilities need to be considered when designing therapeutic exercise programs for people living with PSP • Access to home, healthcare and community facilities for safe exercises and physical activity is needed • User-friendly evidence-based information is needed on the potential benefits of exercise and structured physical activities for movement disorders, falls prevention and social participation