Remote exercise classes are associated with better quality of life in people with Parkinson’s during the Covid-19 pandemic.

Introduction

Parkinson’s disease (PD) is a chronic neurological disease which affects about 8.5 million people worldwide.¹ Its incidence is steadily increasing due to the ageing global population and increased life expectancy; it is estimated that PD incidence will double by 2040.¹ PD is a debilitating disease which can have devastating impacts on patients’ quality of life (QOL), and for which there is yet no cure. The characteristic motor symptoms of PD are tremor, stiffness, and slow movements²; however, patients also suffer from an array of diverse and debilitating non-motor symptoms. For example, many people with Parkinson’s (PwP) have problems with sleep, depression, and motivation, which have huge negative impacts on their overall well-being, as well as on the lives of those around them.^3,4 Previous studies have shown that non-motor symptoms in PwP can also contribute to higher rates of burden on their caregivers.⁵ The overall impact of caring for PwP on their caregivers has been less well documented, particularly in Ireland, and understanding the role of carers can help to inform strategies to support them.

Simple lifestyle strategies such as activity and exercise can have specific positive effects on PD symptoms, thereby contributing meaningfully to the QOL of PwP in numerous ways.⁶ Classical face-to-face exercise programs and regimes have been shown to reduce the burden of progressive PD symptoms,^7–9 improve non-motor symptoms¹⁰ and enhance overall QOL in PwP.¹¹ Furthermore, exercise has been shown to confer positive effects on symptoms in newly-diagnosed PD patients,⁸ and long-term studies have shown that regular activity and exercise levels can also reduce a person’s lifetime risk of developing PD.¹² These studies illustrate the importance of exercise for both management and prevention of PD. The positive effects of exercise can be seen across multiple exercise types in in-person class settings.¹³ Recently, the benefits of exercise conducted via remote web-based settings for PwP have been shown,⁹ including the positive impact of treadmill exercise¹⁴ and balance training.¹⁴ However, these online exercise studies largely focused on just one specific exercise type, and did not compare different modalities or activities. A recent large-scale review has highlighted that different types of exercises and activities may be beneficial in PwP, concluding that a one-size-fits-all approach to exercise may not provide optimal benefits in this particular cohort.¹³

In this study, we assessed the benefits of online exercise classes in Ireland on non-motor symptoms in PwP. This is the first web-based study to assess the benefits of remote exercise programmes in PwP. We carried out this study during the highly-restrictive COVID-19 lockdowns in Ireland. The COVID-19 pandemic caused unimaginable stress on PwP and those who care for them. These lockdowns forced people to isolate from society for long periods of time, which had a large impact on people’s mental and physical health. There was a reduction in physical activity due to the restriction of people’s movement to within a 5 km radius of their home. To overcome this restriction on physical movement, many groups established online support groups, communities, and exercise classes. Stress associated with the spread of COVID-19 has been found to worsen PD symptoms.¹⁵ This may be due to the fact that adaptation to change is constantly required to cope with stress caused by events such as the COVID-19 pandemic, and it is known that PD is associated with cognitive and motor inflexibility, as these functions are dopamine-dependent.^16,17 We wanted to explore if there were simple strategies that could help to alleviate stress levels and improve wellbeing during the COVID-19 pandemic, and furthermore if such strategies could be easily maintained by PwP afterwards. One positive outcome of the pandemic lockdowns and isolation was that this allowed a test phase of online exercise classes for PwP in Ireland. It is known that PwP can struggle with motivation, and experience specific barriers to the completion of exercise programs.⁶ These barriers were recently reviewed and found to include items such as lack of accessibility, wariness of crowded spaces, lack of time, and feeling discomfort in group settings.⁶ Such barriers could be overcome for many PwP through the use of online remote exercise classes, thus helping them to maintain an exercise regime, which can have important positive impact on the long-term management of their disease symptoms.^6,18 The daily QOL of PwP is often adversely impacted by the wide range of debilitating symptoms that are associated with PD. This results in a high degree of reliance on caregivers, both formal (individuals paid to provide care, for example nurses) and informal (family members, spouses, or close friends).^4,19 It has been estimated that approximately 88% of men and 79% of women with PD report that they need caregivers in order to help them to manage their disease.^19,20 The largest proportion of these caregivers are female- mainly wives, daughters, daughter in-laws or granddaughters.^19,20 Studies have suggested that a diagnosis of PD negatively impacts caregivers as well as patients, resulting in caregiver strain.^4,21,22 Identifying areas of struggle for caregivers, via the PDQ-Carers questionnaire, is of high importance in order to allow the provision of the highest available quality of care to PwP, to improve patient outcomes.²³

Methods

Participant recruitment

Ethical approval was obtained from University College Cork’s Social Research Ethics Committee (Log no. 2020-178; 30^th Nov 2020). Written Informed consent was obtained electronically from all participants. All participants were recruited through online study advertisements. Inclusion criteria included age of over 18 years and diagnosis of PD, as information was gathered anonymously through online surveys. We gathered data through remote online surveys to assess participants’ QOL. Participants were asked to provide information on demographics, on COVID-19 virus testing and vaccination, and on lockdowns as well as completing several clinically-validated questionnaires: The Parkinson’s Disease Questionnaire (PDQ-39), The Parkinson’s Disease Questionnaire - Carer (PDQ-C), The Pittsburgh Sleep Quality Index (PSQI), The Hospital Anxiety and Depression Scale (HADS) and Beck’s Depression Inventory (BDI). Individuals were assessed during the first quarter of 2021, during which time Ireland was under Level 5 lockdown (Figure 1), wherein people were instructed to stay at home with movement restricted to a 5 km radius of their home. PwP in our study were participating in a variety of online exercise programmes, including PD Rebels, Corrib Physiotherapy Group Classes, Rock Steady Boxing, Music Movement Therapy and PD Warriors.

Figure 1. Lockdown levels and timelines in Ireland (From National Audit of Clinical Outcomes ICU-BIS Background and Timelines).

Adapted from: https://www.noca.ie/audits/icu-bis-background-and-timelines.

Results

Remote online exercise had an impact on QOL in PwP during lockdowns

During the highly restrictive lockdowns in Ireland, individuals that exercised every day had better (lower) scores on the PDQ-39 (45.67 ± 4.34) compared to individuals who exercised once a week or less (123.50 ± 14.56; p<0.001; Table 2, Figure 2A). The association between exercise and QOL was significant across all domains of the PDQ-39 (p<0.05; Table 2). PwP who exercised daily also scored lower on the BDI depression scale (9.37 ± 1.68) compared to PwP who exercised once a week or less (23.50 ± 3.65; p=0.013; Table 2, Figure 2D). There was no significant difference in scores on the HADS questionnaire between the ‘daily’ (7.59 ± 1.00) and the ‘few times per week’ groups (10.11 ± 1.33; p=0.327); Table 2, Figure 2C). Sleep scores of PwP in the ‘daily’ (7.44 ± 5.92) and ‘once a week or less’ groups (9.5 ± 2.05) were not significantly different (p=0.534; Table 2, Figure 2B).

Table 2. Associations between scores on PDQ-39 elements, HADS, BDI, PSQI and frequency of exercise.

Questionnaire	Exercise daily # (Mean ± SEM)	Every 2 Days	Few times a week	Once a week or less	Once a week or less (Mean ± SEM)	P value
		Effect size
PDQ-39-Mobility	11.88 ± 1.42***	2.12 ± 3.26	1.93 ± 2.63	29.37 ± 5.27***	41.25 ± 5.08	0.00000724
PDQ-39-Activities of daily living	6.69 ± 0.82***	1.40 ± 1.89	1.79 ± 1.52	15.31 ± 3.05***	22.00 ± 2.94	0.0000554
PDQ-39-Emotional well-being	7.10 ± 0.77***	0.99 ± 1.75	0.28 ± 1.42	9.40 ± 2.84**	16.50 ± 2.73	0.0148
PDQ-39-Stigma	2.96 ± 0.42***	-0.38 ± 0.96	-1.06 ± 0.78	5.04 ± 1.55**	8.00 ± 1.49	0.00436
PDQ-39-Social support	2.12 ± 0.36***	0.22 ± 0.80	-0.36 ± 0.65	3.38 ± 1.30*	5.50 ± 1.25	0.0605
PDQ-39-Cognition	5.00 ± 0.47***	1.42 ± 1.08	0.29 ± 0.88	7.25 ± 1.75***	12.25 ± 1.69	0.000935
PDQ-39-Communication	2.92 ± 0.42***	0.25 ± 0.98	0.03 ± 0.79	5.32 ± 1.58**	8.25 ± 1.52	0.0121
PDQ-39-Bodily discomfort	5.24 ± 0.46***	1.02 ± 1.05	-0.47 ± 0.85	4.52 ± 1.71**	9.75 ± 1.64	0.0396
PDQ-39 Total	45.67 ± 4.34***	7.15 ± 9.79	1.27 ± 8.47	77.83 ± 15.19 ***	123.50 ± 14.56	0.0000435
PDQ-39 Summary Index	27.82 ± 2.7***	4.25 ± 5.65	0.25 ± 4.56	45.43 ± 9.14***	73.24 ± 8.80	0.0000587
HADS (n=58)	7.59 ± 1.00***	1.03 ± 2.24	2.52 ± 1.67	-	-	0.327
BDI (n=30)	9.37 ± 1.68***	3.13 ± 4.02	7.13 ± 5.43	14.13 ± 4.02**	23.50 ± 3.65	0.0132
PSQI Total	7.44 ± 5.92***	-1.44 ± 1.43	6.35 ± 1.18	2.06 ± 2.14	9.50 ± 2.05	0.534

# ”Daily exercise” is the reference group and values represent the mean (± SEM). Values for the other groups are effects sizes and represent the difference from the reference group (± SE of the difference). Mean ± SEM values for clinical questionnaires for groups comparing PDQ-39, HADS, BDI, PSQI “daily exercise” group to the “less than once a week” exercise group. N=91 unless otherwise stated.

* p<0.05.

** p<0.01.

*** p<0001 “daily exercise” group compared to the “less than once a week” exercise group.

Figure 2. Associations between scores on PDQ-39, HADS, BDI, PSQI and frequency of exercise.

(A) PwP who exercised daily had better (lower) scores on the PDQ-39 (45.67 ± 4.34) compared to those who exercised once a week or less (123.50 ± 14.56) ***p<0.001. (B, C) There were no significant differences between the groups on PSQI or HADS scores. (D) PwP who exercised daily had better (lower) scores on BDI (9.37 ± 1.68 vs. 23.50 ± 3,65; **p=0.013). Data are shown as mean ± SEM. Data were analysed with a linear model (one-way ANOVA). **p<0.05, ***p<0.001.

PwP who exercised daily during lockdowns had better QOL scores than those who exercised less frequently

Our data show that PwP who exercised with the same or greater frequency during the restrictive lockdowns than beforehand had lower PDQ-39 scores (44.64 ± 5.57) than those who exercised less frequently (76.81 ± 7.75; p=0.0016; Table 3, Figure 3A). This difference was significant for all domains of the PDQ-39 (p<0.05; Table 3), except for the domain ‘bodily discomfort’ in the “same” group (4.97 ± 0.56) compared to the “less” exercise group (1.44 ± 0.99) p=0.351. Those PwP who maintained the same level of exercise during lockdown as beforehand also had lower BDI scores (9.30 ± 2.51) than those who exercised less frequently during lockdowns than they had before (17.00 ± 2.39; p=0.058; Table 3, Figure 3D). The “same” group had lower HADS scores (6.63 ± 1.05) than the “more” exercise group (9.88 ± 1.09; p=0.049; Table 3, Figure 3C). Sleep scores across groups were not found to be significantly different in the “same” group (6.90 ± 0.75) compared to the “less” exercise group (1.04 ± 1.28) p=0.697 (Table 3, and Figure 3B).

Table 3. Associations between scores on PDQ-39 elements, HADS, BDI, PSQI and frequency of exercise change over time.

Questionnaire	Less (Mean ± SEM)	Less (Effect size)	Same # (Mean ± SEM)	More (Effect size)	More (Mean ± SEM)	P Value
PDQ-39-Mobility	22.94 ± 2.65	11.13 ± 3.20***	11.81 ± 1.80 ***	0.013 ± 2.60	11.82 ± 1.87	0.00141
PDQ-39-Activities of daily living	13.06 ± 1.49	6.55 ± 1.81***	6.51 ± 1.01***	0.58 ± 1.46	7.09 ± 1.06	0.00132
PDQ-39-Emotional well-being	11.65 ± 1.31	5.62 ± 1.58***	6.03± 0.89***	1.59 ± 1.28	7.62 ± 0.93	0.00274
PDQ-39-Stigma	4.88 ± 0.74	2.23 ± 0.89*	2.65 ± 0.50***	-0.50 ± 0.72	2.15 ± 0.52	0.0109
PDQ-39-Social support	4.06 ± 0.59	2.49 ± 0.71***	1.57 ± 0.40***	0.43 ± 0.58	2.00 ± 0.42	0.00266
PDQ-39-Cognition	8.24 ± 0.83	3.64 ± 1.01***	4.60 ± 0.57***	0.76 ± 0.82	5.35 ± 0.59	0.00206
PDQ-39-Communication	5.12 ± 0.75	2.41 ± 0.90**	2.70 ± 0.51***	0.09 ± 0.73	2.79 ± 0.53	0.0205
PDQ-39-Bodily discomfort	6.41 ± 0.82	1.44 ± 0.99	4.97 ± 0.56***	0.56 ± 0.81	5.53 ± 0.58	0.351
PDQ-39 Total	76.81 ± 7.75	32.17 ± 9.54**	44.64 ± 5.57***	-0.92 ± 8.01	43.72 ± 5.76	0.00166
PDQ-39 Summary Index	46.52 ± 4.43	21.01 ± 5.35***	25.51 ± 3.00***	2.46 ± 4.34	27.97 ± 3.13	0.000532
HADS (n=58)	11.33 ± 2.23	4.70 ± 2.47	6.63 ± 1.05***	3.25 ± 1.52*	9.88 ± 1.09	0.0494
BDI (n=30)	17.00 ± 2.39	7.70 ± 3.46*	9.30 ± 2.51***	0.075 ± 3.76	9.37 ± 2.80	0.0575
PSQI Total	7.94 ± 1.03	1.04 ± 1.28	6.90 ± 0.75***	0.60 ± 1.05	7.50 ± 0.73	0.697

# The “Same” group is the reference group and values represent the mean (± SEM). Values for the other groups are effects sizes and represent the difference from the reference group (± SE of the difference). N=91 unless otherwise stated.

* p<0.05.

** p<0.01.

*** p<0.001 “same” exercise group compared to “less” exercise group for all variables except HADS same group compared to the more exercise group *p <0.05. Mean ± SEM values for clinical questionnaires for groups comparing PDQ-39, HADS, BDI, PSQI ‘less” group and the “more” exercise group also presented.

Figure 3. Correlation analysis between scores on PDQ-39, HADS, BDI, PSQI and frequency of exercise change over time.

(A) PwP who exercised the same amount (44.64 ± 5.57) or more frequently (43.72 ± 5.76) during restrictive lockdowns had lower PDQ-39 scores compared to those who exercised less frequently (76.81 ± 7.75; **p<0.01). (B) There was no significant difference between the groups on PSQI scores. (C) PwP who exercised the same amount had lower HADS scores compared to those who exercised more frequently (6.63 ± 1.05; *p<0.05) and compared to those who exercised less frequently (11.33 ± 2.23; *p<0.05). (D) PwP who maintained the same level of exercise had lower score on BDI (9.30 ± 2.51) than those who exercised less (17.00 ± 2.39; p<0.035). Data shown as mean ± SEM. Data analysed with a linear model (one-way ANOVA).

Discussion

Here we report the findings of a remote survey which assessed the effects of online exercise programmes on non-motor symptoms in a cohort of people with early-stage PD. We found that PwP who exercised daily during the Level 5 lockdown periods had better overall QOL scores on the PDQ-39 and better scores on depression and anxiety scales. The effects of exercising daily were particularly significant in the mobility, activity, and cognitive domains of the PDQ-39. This is the first study of its kind to take place in Ireland, and the first web-based study to assess the effect of web-based exercise classes on PD symptoms. We also found that PwP who reduced the amount they exercised during the restrictive lockdown periods had worse QOL, sleep and depression than those who maintained the same frequency of exercise as before the lockdowns. During the period of this study, Level 5 lockdowns in Ireland were highly restrictive and stressful on individuals who were vulnerable and who had long-term health conditions. Our survey found that PwP and their caregivers were taking the lockdowns very seriously. The vaccination roll-out programmes were just beginning in nursing home facilities at the time of our study, and PwP may have suffered more than other people as it is known that they have less adaptability to stressful periods of change.¹⁵ This lockdown period was a testing phase for remote exercise classes, and these were generally set up by PD local communities, associations, and support groups in Ireland. These local and national groups provided an online community for PwP and enabled them to overcome technology barriers and therefore to maintain social contact as well as to exercise regularly, which was very valuable to PwP. Recent studies have highlighted the benefits of exercise in PD, reducing the overall clinical burden²⁴ and positively impacting non-motor symptoms such as sleep.¹⁰ Exercise programmes such as online treadmill programmes were found to be safe for PwP.¹⁴ Recently, there have been trials examining the intervention of high-intensity exercise in early stages of PD.⁸ A recent large scale review has highlighted that the benefits of exercise in PD are not limited to high-intensity exercise,¹³ but rather that many types of physical exercise can improve movement and overall QOL, and that there was no evidence for one type of exercise working better than others.¹³ In our study, our classes included a range of different classes such as physiotherapy-led exercise programmes, Irish set-dancing, boxing classes, and yoga classes. This is consistent with the current literature on in-person exercise classes, where a range of exercise types has been shown to confer positive effects on PD symptoms. Our study is the first to show an association between a range of remote exercise types and PD symptoms.

In our study, we also assessed the wellbeing and QOL of caregivers during the period of the Covid-19 lockdowns in Ireland. Providing care for PwP can be challenging, and those who live with and care for PwP provide invaluable support. It was previously shown that the burden of symptoms for patients with PD can impact not only the PwP themselves, but also those around them; the management of chronic PD symptoms has been reported to confer a similar burden to that experienced by people with metastatic cancer.²⁵ With regards to symptom management, non-motor symptoms and disease severity are the biggest contributors to burden on caregivers.²⁶ Long-term follow-up studies need to be conducted on the effects of the management of PD symptoms on the PwP-caregiver unit, and to determine characteristics and interventions that may be applied in order to prevent caregiver burnout. In our study, we found that QOL measures in caregivers were within the normal range. This could reflect the fact that these caregivers and PwP were isolating and so did not feel very stressed about COVID-19, or could be indicative of the fact that the PwP in this cohort were at an early disease stage. Previous studies have shown that those PwP who have the support of a caregiver experience a higher QOL than those without a caregiver, highlighting the importance and positive impacts of caregivers on the wellbeing of PwP.^22,23

Future studies may compare in-person with online exercise classes, as well as assess the impacts of exercise classes on various aspects of non-motor symptoms. More detailed examination of the PwP-caregiver unit is also warranted. One positive effect of the severe lockdowns was the increased use of telemedicine and of remote exercise programmes. These types of programmes could be used for the care of people with potential prodromal PD, or with early-stage PD, as they are low-cost and low-burden on individuals, and they can be tailored to a personalised approach to symptom management. Care and instruction must also be taken, and advice from physiotherapists and neurologists must be sought before any exercise class is taken by individuals, to assess risks of falls and injury. The anxiety scoring was found to increase significantly in the group that were exercising more during lockdowns. This may be due to the nature of the severity of the lockdown situation and capturing a group that may be more anxious due to lockdowns, and exercising more in order to combat this. During our remote study, we switched from using the BDI to the HADS questionnaire to assess depression and anxiety. This was due to feedback from the PD community. The BDI questions can be more sensitive in nature compared to the HADS, so therefore in future remote studies, the HADS should be used instead of the BDI.²⁷ The support unit of PwP needs to be taken into consideration when managing PD symptoms, and it is very important to support and consult with caregivers, as well as with the individuals with PD, to tailor specific programmes to meet individual needs.

Author contributions

LMC performed data collection and analysis. RR and MH performed data analysis and data cleaning. SEL performed the data analysis. AMS, LMC and EC designed the study. AMS supervised all aspects of the study. All authors reviewed the manuscript.