Review Article

Vulnerability of Parkinson’s Patients to COVID-19 and Its Consequences and Effects on Them: A Systematic Review

Table 3

Key results of papers (study population = persons with PD).

ContributionYearCountryAim of the studyStudy designPD durationSample sizeSurvey toolAssessment timeOutcomes: Self-reported changes on symptoms in patients without COVID-19Main resultsLimitations

Fabbri et al. [27]2021-JulyFranceTo explore the outcomes of the first COVID-19 lockdown on motor and nonmotor symptoms in a cohort with Parkinson’s diseaseCross-sectionalMean = 8.67 yrsN = 2563,
EG1 (PEC group) = 441(242 M, 199 F), AgeM = 66.84 yrs,
EG2 (community-based group) = 2212 (1271 M, 941 F), and AgeM = 68.37 yrs
(i) PGI-I
(ii) PDQ-8
(i) Survey after lockdown: 20th April to 16th May 2020(i) Worsened clinical symptoms 40.9%,
(ii) worsened pain (9.2%), rigidity (9.0%), tremor (8.4%),
(iii) walking troubles (6.9%), Akinesia (6.8%), anxiety (6.1%), fatigue (5.4%), and
(iv) balance disturbances (4.5%) and sleep disorders (4.1%)
The first COVID-19 lockdown harmed the motor and nonmotor symptoms in patients with PD, and actions should be created to prevent interruptions in care, including physiotherapy, physical activity, and telemedicine(i) Failure to conduct face-to-face polls
(ii) Missing data on follow-up by patients
(iii) Absence of patients with severe Parkinson’s in the study
Beatrice Ana-Maria Anghelescu et al. [8]2021-AugCanadaComprehending the consequences of COVID-19 on patients’ clinical symptoms of PD in both motor and nonmotor aspects and learning from the unpretentious experiences of virtual therapy from PD patients could supportQualitative researchNot mentionedN = 22 (16 M, 6 F) and AgeM = 70.5 yrs(i) Interview (qualitative analysis)During pandemic: 28th April to 13th May 2020(i) Activities of daily living; attitudes and perceptions,
(ii) worsening in motor including increased OFF-times, tremors/shaking, and stuttering, and
(iii) worsening in nonmotor symptoms
This study provides an overview of the experiences of PD patients during COVID-19 with an emphasis on the clinical and remote care aspects. The three main issues reported by patients with PD as a result of the epidemic were the effects on clinical care, personal life, and changes in attitudes and perceptions(i) Used a preselected sample (selection bias) and
(ii) due to the restrictions and suspension of in-person clinical visits, they were not able to perform any clinical assessments such as MDS-UPDRS at the time
Marika Falla et al. [28]2021-JulyItalyTo acquire data on the consequences of lockdown efforts on motor and nonmotor symptoms of PD enrolled in a research project and to evaluate the feasibility of a remote, web-based video evaluation for PD patients during the COVID-19 pandemicQuasiexperimentalMean = 5.7 yrsN = 14 (7 M, 7 F) and AgeM = 64.9 yrs(i) MDS- UPDRS;
(ii) UPDRS;
(iii) AES-S, AES-I;
(iv) LSNS-R;
(v) PDQ-39-SI;
(vi) FES-I;
(vii) ABCs-I
Baseline: February 2020
Follow-up: 24th April to 1st May 2020
(i) Worsened nonmotor aspects (MDS-UPDRS part I) (),
(ii) worsened motor and nonmotor symptoms (MDS-UPDRS total score) (),
(iii) worsened OR-PAS (Parkinson anxiety scale) avoidance behaviour (), and
(iv) worsened OR-PAS total (Parkinson anxiety scale) ()
The findings indicate impaired nonmotor symptoms in patients with PD and recommend the feasibility and use of telemedicine in monitoring patients with PD during the COVID-19 epidemic(i) Limited number of patients and
(ii) MDSUPDRS, which is derived from UPDRS, has not yet been validated remotely and/or used for comparison between incline and telemedicine visit scores
Alessandra Dodich et al. [29]2021-MarchItalyTo consider the role of social-cognitive capacities in the perceived effect of COVID-19 emergency and the consequences of lockdown measures on patients’ social networks and caregivers’ commitmentQuasiexperimentalMean = 5.7 yrsN = 14 (7 M, 7 F) and AgeM = 55.5 yrs(i) MDS-UPDRS;
(ii) IRI;
(iii) LSNS-R
(iv) CBI
Baseline: February 2020
follow-up: 20th April to 3rd May 2020
(i) Patients showed high levels of IRI personal distress,
(ii) patients felt the disease went faster in the 2 months of lockdown,
(iii) patients reported increased memory difficulties,
(iv) increased anxiety was reported, and
(v) worsened motor functioning
Patients with social cognition disorders displayed a remarkably lower apprehension about the possible effects of COVID-19 on their health. During the lockdown, the burden on caregivers and patients' social networks remained constant. These results suggest that PD sociocognitive disorders may affect patients' ability to estimate the effects of COVID-19 infection. The lack of significant growth in caregiver burden and social isolation(i) Small sample size and the lack of a control group and
(ii) inability to carefully assess the effects of individual sociodemographic and psychological factors
Delfina Janiri et al. [30]2020-NovItalyTo determine risk/protective factors associated with subjective worsening of psychiatric symptomatology during COVID-19Cross-sectionalNot mentionedN = 101 (43 M, 58 F) and AgeM = 71.86 yrs(i) MDS-UPDRS;
(ii) H and Y stage;
(iii) subjective worsening of neurological symptoms during the COVID-19 outbreak
During pandemic: 1st to 15th April 2020(i) Worsening of psychiatric symptomatology 23 subjects,
(ii) the most frequent symptom was depression, followed by insomnia, and
(iii) worsening of neurological symptoms () and lifetime irritability
The results demonstrated that the stress of COVID-19 outbreaks might have a more significant impact on people with PD and people with a history of lifelong psychiatric symptoms. Interventions desired to reduce mood irritability can indirectly influence the health of patients with PD
Roberta Baschi et al. [10]2020-DecItalyTo consider the motor, cognitive, and behavioral changes during the COVID-19 lockdown in patients with Parkinson’s disease (PD) with and without mild cognitive impairmentCross-sectionalNot mentionedN = 96 (58 M, 38 F), AgeM = 67.3 yrs
PD-NC = 34(23 M, 11 F), AgeM = 65.4 yrs
PD-MCI = 31(20 M, 11 F), AgeM = 66.7 yrs
MCInoPD = 31(15 M, 16 F), AgeM = 70 yrs
(i) NPI
(ii) MDS-UPDRS
10 weeks after the COVID-19 lockdown: 20th to 30th May 2020(i) Worsening of cognitive, pre-existing, and new behavioral symptoms, and motor symptoms.
(ii) A significantly higher frequency of cognitive impairment (), fatigue (), and speech () than PD-NC.
(iii) PD-MCI showed significantly higher frequencies in several MDS-UPDRS items compared to MCInoPD, particularly regarding pain (), turning in bed (), getting out of bed (), and walking and balance ()
COVID-19 lockdown will worsen cognitive, behavioral, and motor symptoms in people with PD and MCI, especially PD-MCI(i) Small sample size
Birgul Balci et al. [9]2021-JuneTurkeyTo reach the physical activity and anxiety-depression levels between Parkinson’s disease patients and controls during the lockdownCross-sectionalMean = 8 yrsN = 88,
PD = 45 (30 M, 15 F), AgeM = 67 yrs,
Control = 43 (24 M, 19 F), and AgeM = 66 yrs
(i) PASE
(ii) HADS via telephone interview
After lockdown: 15th to 20th June 2020(i) Worsened motor and nonmotor symptoms: tremor 11 out 45, dyskinesia 7 out 45, bradykinesia (slowness of movements such as turning in bed and rising of chair) 22 out 45, rigidity 18 out 45, gait impairments (height of foot lift, stride length/speed, arm swing) 18 out 45, freezing of gait 7 out 45, balance problem 15 out 45, cognitive impairment (paying attention, following conversations) 7 out 45, sleep problems 9 out 45, daytime sleepiness 7 out 45, pain and other sensations (such as aches, cramps, and tingling) 15 out 45Lockdown may increase the motor and nonmotor symptoms of Parkinson’s disease associated with physical inactivity(i) The information was obtained with self-reported questionnaires, which might increase the risk of bias and insufficient recall
Fukiko Kitani-Morii et al. [31]2021-JanJapanTo elucidate the effect of social restrictions imposed due to the COVID-19 pandemic on neuropsychiatric symptoms in PD patients and to identify risk factors associated with these signsCross-sectionalMean = 5 yrsN = 71,
PD = 39 (25 M, 14 F), AgeM = 74.7 yrs,
CG = 32 (5 M, 27 F), and AgeM = 71.56 yrs
(i) MDS-UPDRSDuring pandemic: 22th April to 15th May 2020(i) Clinical depression (PHQ-9 score) were more in PD patients (39%) than controls (6%) ().
(ii) MDS-UPDRS part 2 score was correlated with the presence of clinical depression (PHQ-9 score) () and clinical anxiety ()
Patients with Parkinson’s are more likely to develop depression than others in social stress, such as an epidemic(i) Absence of information about depression, anxiety, and insomnia of participants before the COVID-19 pandemic and a female bias in sex ratio in the control group
Elisa Montanaro et al. [32]2021-MayItalyTo investigate the psychological impact of the COVID-19 outbreak on APD patients and their caregivers by assessing distress, worries, depressive, and anxious symptoms; also, hypothesized an increasing influence of the COVID-19 outbreak on PD patients and their caregiversQuasiexperimentalMean = 13.4 yrsN = 100 (60 M, 40 F) and AgeM = 62.4 yrs(i) Telephone interview: HADS-A; HADS-DDuring lockdown (T0): April to May 2020
After the end of the lockdown in Italy (T1): June to August 2020
(i) Depression was observed in 35% of APD patients and anxiety in 39%, with a significant reduction of the latter after the lockdown ()
(ii) patients’ main worries were: a possible higher risk of COVID-19 infection (25%), interruption of nonpharmacological treatments (35%), interruption of outpatient clinics (38%), PD complications related to COVID-19 (47%)
The findings show that anxiety, worry, and special needs are more prevalent in Parkinson’s patients during the epidemic(i) Lack of baseline evaluations of anxiety and depression before the COVID-19 outbreak
(ii) Our cohort focused mostly on APD patients treated with DAT
Galit Yogev-Seligmann et al. [33]2021-JulyIsraelTo characterize the effects of COVID-19 social distancing on the function, health, and well-being of people with Parkinson’s disease (PD) and test the association of these effectsCross-sectionalMean = 10.6 yrsN = 142 (83 M, 59 F) and AgeM = 70.6 yrs(i) Web-based survey: Part 1 : 27 multiples-choice questions regarding changes in function, health, medical care, and well-being; Part 2 consisted of the PAM-13After lockdown: 10th May to 1st June 2020(i) Deteriorated walking ability 37%, increased need for assistance with ADL 24%. Only 4.3% reported falling more often than before the lockdown,
(ii) worsened of disease symptoms 53%, while 33.8% reported weight gain. 83.2% were able to control other comorbidities; 34.5% reported an overall worsening of their disease condition, and
(iii) feeling more tired 43%, and 42.1% increases in at least one of the following: depression, anxiety, loneliness, or worry about the future. 26.1% reported a lack of spousal support during the lockdown
Respondents reported a decline in various functions, health, and well-being. Rehabilitation stopped for more than 60% of people. Among those who reported deteriorating health, the majority attributed this to stopping rehabilitation treatments or reducing physical activity(i) Lack of generalization of findings to the whole community for reasons such as spouses' support of patients, regular participation in physical activities, and computer literacy
Megan Feeney et al. [5]2021-JanUSATo experiment with the social and emotional effect of the pandemic and social distancing on PwPD and to examine the factors contributing to accessing alternative health care mechanismsCross-sectionalMean = 7.0 yrsN = 1342 (656 M, 679 F, other 1, missing 6) and AgeM = 70.9 yrs(i) Online questionnaireDuring pandemic: 13th May to 11 June 2020(i) Approximately half of respondents reported a negative change in PD symptoms, with 45–66% reporting mood disturbances.
(ii) Almost half of PwPD reported reduced hours of exercise, and a majority of respondents reported a reduction in activities outside of their residence
Symptoms of PD and its management practices were significantly affected by COVID-19. Finally, it is essential to expand the use of telehealth, especially to reach disadvantaged and low-income populations
Anouk van der Heide et al. [34]2020-AugNetherlandsThe main aim is to test the hypothesis that COVID-19 pandemic has led to an increased psychological distress in PD, worsening PD symptomsCross-sectionalMean = 3.9 yrsN = 358 (220 M, 138 F) and
AgeM = 62.8 yrs
(i) MDS-UPDRS-I and MDS-UPDRS-IIBaseline and end of study:
assessment at the last PPP visit: 7.5 months prior to COVID-19 survey
Assessment during COVID-19 survey: on average 1.4 months COVID-19
Worsened in frigidity: 42.6%
Worsened in fatigue: 41.5%
Worsened in tremor: 40.7%:
Worsened in pain: 33.8%
Worsened in concentration: 32.5%
Worsened in memory problems: 31.9%
Worsened in depressed mood: 31.6%
Worsened in gait and freezing = 31.5%
The main results show that stress caused by the COVID-19 epidemic leads to worsening of PD symptoms by provoking psychological distress as well as lifestyle changes(i) The impact of COVID-19 might well be even more dramatic for patients with late-stage PD;
(ii) due to the retrospective nature of the survey, responses might be less accurate, since for most questions they had no baseline data
Keisuke Suzuki et al. [35]2021-MarJapanResearchers investigated changes in motor symptoms, cognition, mood, sleep, and stress as well as determinants of QOL in PD patients during the COVID-19 outbreakCross-sectionalMean = 5.8 yrsN = 100 (45 M, 55 F) and AgeM = 72.2 yrs(i) HADS-A; HADS-D
(ii) PCS
(iii) MCS scores of the SF-8
Assessment during COVID-19 surveyWorsened in tremor: 34.1%
Worsened in rigidity: 40.4%
Worsened in bradykinesia: 20.2%
Worsened in gait: 55.0%
Worsened in postural stability: 43.0%
Worsened in cognition: 34.0%
Worsened in mood: 36.0%
Worsened in sleep:34.0%
In PD patients, gait disturbance, rigidity, disease severity, smoking, levodopa equivalent dose, weight loss, anxiety, depression, female sex, stress, and disease duration worsened(i) Selection bias cannot be ruled out.
(ii) No baseline data from the period before the COVID-19 pandemic.
(iii) Motor symptoms after the outbreak of COVID-19 were not assessed a clinical examination
Tommaso Schirinzi et al. [36]2020-AugItalyThis study aimed to examine the changes in physical activity in PD patients due to COVID-19Cross-sectionalMean = 6.5 yrsN = 74 (37 M, 37 F) and AgeM = 61.3 yrs(i) IPAQ-SF
(ii) PWBM
(iii) BDI
Assessment during COVID-19 survey: April 20, 2020 and May 2, 2020Patients with PD worsened, 55.5% in motor and nonmotor symptoms, 11.3% in depression, lower total MET (1714) min/weekThe majority of patients reported that their condition had worsened during lockdown, which was mainly due to reduced physical activity(i) The lack of objective and accurate measurement of clinical features.
(ii) The clinical outcome consisted just in the individual perception of patients
Rosa De Micco et al. [37]2020- NovItalyResearch team assessed the psychological impact of the 40-day lockdown in a large cohort of patients with Parkinson’s diseaseCross-sectionalMean = 3.26 yrsN = 94 (62 M, 32 F), AgeM = 63.98 yrs(i) Event scale-revised;
(ii) Kessler psychological distress scale;
(iii) NMSS
(iv) PDQ-39
Assessment at the last PPP visit: 6 months prior to COVID-19 survey
Assessment during COVID-19 survey: a mean of 40 days of lockdown
Worsened in sleep/fatigue: 33%
Worsened in mood/cognition: 40%
Worsened in attention/memory: 46%
Worsened in perceptual problems: 21%
They recognized specific PD motor and nonmotor characteristics predisposing them to the higher psychological impact of stressful circumstances(i) Other factors may have affected the psychological
well-being of PD cohort during the lockdown
period.
(ii) More solid conclusions about the pathophysiological processes potentially
underlying our results
Aline Nogueira Haas et al. [38]2022-JanBrazil(1) To assess mental health symptoms in people with Parkinson’s (PwP) in self-isolation, before and during the COVID-19 pandemic; (2) to investigate associations between mental health and physical activity levelsCross-sectionalMean = 7.29 yrsN = 156 (78 M, 78 F) and AgeM = 64 yrs(i) An online self-administered and validated questionnaire2 months after the pandemic: 12th to 21st of May 2020(i) Worsened mental health symptoms over the time: anxiety (), fear (], and thoughts of death (].
(ii) A lower physical activity level during the pandemic is related to increased probability of thoughts of death.
(iii) Anxiety, fear and depression were not associated with physical activity levels
Anxiety, fear, and thoughts of death worsened during the COVID-19 pandemic. Lower physical activity level during the pandemic was related to an increased probability of thoughts of death(i) The small number of responses obtained from the midwest and northeast Brazilian regions;
(ii) all data were self-reported potentially suffering from social desirability bias;
(iii) prepandemic variables were assessed retrospectively and could suffer from recall bias
Guo et al. [39]2020-OctChinaTo examine the effect of lockdown during the COVID-19 pandemicQuasiexperimentalMean = 6.05 yrsN = 113 (66 M, 47 F) and AgeM = 69.5 yrs(i) COVID-19 Questionnaire
(ii) PDQ-39
(i) During: 1st February to 31th March, 2020
(ii) After: 1st April to 30th April, 2020
(i) Worsening of PD symptoms;
(ii) increased tremor (39.8%), increased stiffness (60.2%), increased slowness (60.2%), newly appearing or worsening of dyskinesia (39.8%), newly appearing or worsening of fluctuation of symptoms (40.7%), excessive fatigue (29.6%), feeling/appear stressed or anxious (79.6%), feeling/appear depressed (50.0%), sleep disorders (39.8%), reduced appetite (10.2%), and increased aches and pains (29.6%)
Quality of life for patients during the period of epidemic prevention and control was worse than that after epidemic prevention and control