Abstract

Background

The COVID-19 pandemic has been declared as a global emergency by the World Health Organization. Unprecedented restrictions have been implemented to control the viral spread, including a complete lockdown of quarantine isolation in certain countries including Italy [1]. Concerns about the severe restrictions in mobility and the subsequent sedentary lifestyle have been raised when dealing with chronic neurological conditions, such as Parkinson’s disease (PD) [2–5]. Falls are more common (up to 40–70% per year) in advanced PD and their frequency and severity increase with physical inactivity [6]. Overall, people with PD are twice more likely to experience falls than healthy elderly population [7]. Sedentary time was significantly related to several aspects of quality of life, including perceived deficits in mobility, cognitive processing (e.g., memory, concentration), and communication (e.g., difficulty with speech) [8]. Moreover, it is well-known that social deprivation affects cognition, mood and quality of life [9, 10].

Since, physical exercise programs are essential components in the management of motor and non-motor symptoms in PD patients [11–13], the main objective of this pre-post interventional study was to explore the effects of COVID-19 related social and physical restrictions on this population.

Methods

Participants and ethics statement

Twelve PD participants from our Movement Disorders and Parkinson Unit of the University Hospital of Padua (Italy) were tested before and after the 2-months lockdown period in Italy.

All participants had at screening (max 1 week before the baseline visit): (i) diagnosis of idiopathic PD [14]; (ii) Hoehn and Yahr (H&Y) score range 2-3 in the “OFF” state [15]; (iii) Mini Mental State Examination (MMSE) [16], score > 24; and (iv) stable pharmacological treatment for the last 3 months. We excluded participants who: (i) changed pharmacological treatment between baseline and follow-up visits (i.e., during the 8 weeks of lockdown); (ii) were demented based on MMSE score and iADL and ADL or unable to understand and sign the consent form; (iii) had deep brain stimulation and infusion therapies; (iv) suffered from diabetes; (v) reported pathologies of the musculoskeletal system; (vi) had history of brain stroke, myocardial infarction or suffered from uncontrolled hypertension; (vii) reported urinary incontinence considering that the rehabilitation program was planned in thermal water; and (viii) reported relevant brain comorbidities or cerebrovascular disease, as assessed with clinical T1w3D and FLAIR MRI protocol. All patients were part of a larger cohort that previously underwent thermal water rehabilitation. The whole group underwent an extensive evaluation assessing clinical, motor and cognitive aspects, which was administered two weeks prior (pre-isolation: before March 11, 2020) and following the lockdown in Italy (post-isolation: after May 4, 2020). The two evaluation sessions were carried out at the same day time during patients ON phase (see Fig. ​Fig.11).

Open in a separate window

Fig. 1

Pre- and post-isolation evaluation protocol

In order to be sure that participants had no close contact with potential COVID-positive people or became COVID-positive themselves between the two evaluation sessions, a triage questionnaire was administered both by telephone and in person at post-isolation visit. Namely it was checked whether i) their body temperature was lower than 37.5 °C, ii) they experienced COVID-19 symptoms; iii) their family members or close contacts (less than 1 meter in the same room for at least 15 min without protective equipment) confirmed or suspected to have contracted COVID-19 in the 20 days prior the evaluation; iv) they have ever been tested for COVID-19, especially in the 20 days prior the evaluation; and eventually if v) they have ever been positive to COVID-19 tests. None of the patients included in this study had history of positive COVID-19 or had contact with positive people.

Participants were evaluated in the context of a project that aimed to study the effect of rehabilitation in thermal water on people with PD. This rehabilitation program was interrupted due to the COVID-19 lockdown, but all clinical assessments at baseline were successfully performed the 2-weeks before lockdown. Participants were evaluated by the multidisciplinary team in our clinic, which includes a nurse case manager, neurologists, psychologists, physiotherapists and bioengineers working in collaboration with the rehabilitation unit and a study coordinator. Our approach to patients’ management includes education and training according to current recommendations [17, 18]. Assistance via phone calls and emails to those patients who asked for it was granted during the lockdown period and included training about low-intensity physical exercises aimed to relieve immobility-associated pain (i.e., stretching exercises for neck, trunk and lower limbs) and drugs administration. Although being of help, it is worth noting that this intervention is far from the concept of delivering a proper telemedicine where patients can actively interact with clinicians.

The study was carried out according to the Declaration of Helsinki and ethical approval to data collection was granted by the local review board. Participants read and signed an informed written consent form before participating to the study.

Results

Participants’ sociodemographic and clinical characteristics at the screening visit (pre-isolation period) are shown in Table ​Table1.1. Throughout the whole quarantine period, there were no changes in drug therapy. Four individuals reported more than one fall during this period, whereas only one reported falls prior the baseline visit. Six participants reported drug-controlled hypertension, and two of them had suffered from ischemic heart disease. None of our participants was on acetylcholinesterase inhibitors (AChE).

Discussion

To the best of our knowledge, this is the first study assessing the consequences of the COVID-19 related restrictions on both motor and non-motor symptoms of people with PD who had never contracted COVID-19. Considering that our subjects had been assessed just before the implementation of strict lockdown, we had the unique opportunity to test the impact of isolation without any treatment change and through a systematic and complete evaluation.

Our findings showed that no significant worsening in clinical measures and quality of life were detected for this cohort of PD patients in the mild and moderate stages of the disease. These findings should be interpreted considering that PD participants were followed regularly at our clinic and attended several educational activities at our local Parkinson lay association. We suggest that these results further point to the importance of multidisciplinary care interventions for PD patients to hand and learn self-management strategies [17, 18].

The only worsening item we detected was the Mini-BESTest total score. This finding could indicate that, if the lockdown period had continued, we could have possibly observed a clinically significant deterioration in balance performance of these individuals. The Mini-BESTest has proven to be a significant predictor of falls and detector of balance problems in PD [22, 23], and our result indicate that drastic mobility restrictions have a negative impact on balance. Indeed, the clinical cutoff to consider an individual as a faller via the Mini-BESTest is a total score equal to 17.5/28 points [24]. Contrarily to what observed before the lockdown (only 1 participant with Mini-BESTest total score < 17.5, who reported falls prior the baseline visit), six out of 12 participants did not pass such a threshold at the post-isolation visit, with four of them reporting falls during the 2-months lockdown. Four of them showed a decline in the APAs Mini-BESTest sub-items. Anticipatory Postural Adjustments (APA) are the necessary weight shift mechanism that occur prior to an internal or external postural challenge, such as step initiation and postural transfers (e.g. sit-to-stand task). Thus, this neural processing is required to achieve good control of center of mass transition in order to avoid a loss of balance and a subsequent fall [49, 50]. Remarkably, the rest of participants did not show clinical changes.

MDS-UPDRS motor examination total score highlighted only a modest median worsening. However, considering the minimal threshold of +4.63 points for detecting clinically meaningful worsening changes in the score of the MDS-UPDRS part III, this variation was clinically relevant for six of these participants [42]. The fact that only half of these participants showed a clinically negative effect, and that the 6MWT did not differ, could be explained with these participants and their caregivers having received an extensive training and education strategies for managing PD symptoms over the years at our clinic. Moreover, our multidisciplinary interventions were not substantially interrupted during this period thanks to remote-technology solutions. We succeeded in driving technology-based assistance for any requirement and promoting physical activity solutions in any case. This is consistent with the results of a recent survey for an Italian PD patients’ cohort about how the lockdown impacted on physical activity. This resulted in successful self-management patient’s strategies to continue physical activity at home. Moreover, education and awareness on the importance of physical activity were identified as main factors for the preservation of health in PD patients [51]. The body mass index experienced an increase, suggesting that this profound change in daily routine and regular physical activity had resulted in increased body weight, although this may not be specific of PD.

Finally, it should be noticed that baseline clinical, cognitive and functional status was relatively mild for this cohort and PDQ-39 score confirmed that patients were stable, and symptoms were well controlled with pharmacological treatment. Emotional wellbeing was the only domain showing a trend for worsening most likely due to prolonged social isolation [52]. Overall, it should be considered the relative shortness of the isolation period (8 weeks) together with the good baseline values of these patients and the uninterrupted remote assistance have possibly softened negative impacts of strict lockdown.

Conclusion

Our study provides the unique opportunity to test, with the same clinical measurements, in real life and in unprecedented mobility restrictions, the effects of isolation in PD. Even if the overall changes were modest, we observed an increased risk of falls in selected individuals which is nonetheless potentially relevant. The potentially negative effects of lockdown may have been softened by previous participation of these patients to educational activities and continued availability of our multidisciplinary team.

Acknowledgements

Abbreviations

Authors’ contributions

The authors’ contributions were follows: RL conceived and designed the clinical evaluation protocol and rehabilitation program in thermal water. RDM, VC and FP provided advice on the whole study design. RL, RDM, VC, CT, FP and AB conducted all the clinical assessments and collected the data. LW collaborated to the analysis and interpretation of the results. RL was responsible for the drafting the manuscript. AA collaborated in the interpretation of the results and reviewed the manuscript. RDM, RB, MC, CT and LW reviewed the manuscript. AA in collaboration with the principal investigator of the thermal water study, SM, supervised the whole study. All the authors have contributed and approved to the periodic multidisciplinary evaluations in the clinic and reported the data.

Funding

The research study of thermal water rehabilitation is completely funded by the FoRST - Thermal Scientific Research Foundation, the PD_Pal Project (EU-H2020 Program, Grant Agreement n.825785). Cariparo Foundation (Grant: COVID19-CNS: Understanding neurotropism and long-term brain damage from COVID-19) will support the dissemination of the findings.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

Declarations

Footnotes

References