|Year : 2022 | Volume
| Issue : 2 | Page : 102-109
Dose-response characteristics of exercise training in individuals with Parkinson's disease: an exploratory study
Xia Shen1, Jia Hu2, Margaret K Y. Mak3
1 Rehabilitation Medicine Research Center, Shanghai Yangzhi Rehabilitation Hospital (Shanghai Sunshine Rehabilitation Center); Department of Rehabilitation Sciences, Tongji University School of Medicine, Shanghai, China
2 Department of Rehabilitation Sciences; Department of Medical Education, Shanghai Yangzhi Rehabilitation Hospital (Shanghai Sunshine Rehabilitation Center), Tongji University School of Medicine, Shanghai, China
3 Department of Rehabilitation Sciences, Hong Kong Polytechnic University, Hong Kong Special Administrative Region, China
|Date of Submission||06-Jun-2022|
|Date of Decision||14-Jun-2022|
|Date of Acceptance||18-Jun-2022|
|Date of Web Publication||29-Jun-2022|
Rehabilitation Medicine Research Center, Shanghai Yangzhi Rehabilitation Hospital (Shanghai Sunshine Rehabilitation Center); Department of Rehabilitation Sciences, Tongji University School of Medicine, Shanghai
Source of Support: None, Conflict of Interest: None
Exercise training is often prescribed as an adjunct to medication to improve postural instability in individuals with Parkinson’s disease. As the association between exercise dose and the corresponding effects on postural stability has not been established in this population, we aimed to explore this topic in the present study. This is an exploratory study conducted in the Gait and Balance Laboratory at the Hong Kong Polytechnic University in a period from June 2011 to June 2013. Eligible participants with Parkinson’s disease (n = 51) were randomly assigned to either a balance and gait training group or a strength training group. The 12-week training period included two 4-week phases of physiotherapist-supervised laboratory-based training separated by a 4-week phase of self-supervised home-based training. Blinded testers examined postural stability using the limit of stability test, single-leg-stance test, walking test, and the activities-specific balance confidence scale, at baseline and after each training phase. Baseline evaluations revealed no significant difference between the balance and gait training and strength training groups. In the balance and gait training group, the first 4-week training phase led to significant improvement in most measures of balance and gait performance (P < 0.025), and the 12-week training phase yielded further improvements in gait velocity and activities-specific balance confidence scale score. In the strength training group, the first 4-week training phase led to significant improvement in the endpoint excursion in the limit of stability test and gait velocity, and the 12-week training phase resulted in an improvement in the single-leg-stance time and stride length in the walking test. All improvements occurred during the laboratory-based training sessions. Therefore, in individuals with Parkinson’s disease, a 4-week period of balance and gait training could improve postural stability, whereas longer durations of strength training are required to gain comparable improvements.
Keywords: balance; dose-response relationship; Parkinson’s disease; rehabilitation; strength
|How to cite this article:|
Shen X, Hu J, Y. Mak MK. Dose-response characteristics of exercise training in individuals with Parkinson's disease: an exploratory study. Brain Netw Modulation 2022;1:102-9
|How to cite this URL:|
Shen X, Hu J, Y. Mak MK. Dose-response characteristics of exercise training in individuals with Parkinson's disease: an exploratory study. Brain Netw Modulation [serial online] 2022 [cited 2022 Dec 8];1:102-9. Available from: http://www.bnmjournal.com/text.asp?2022/1/2/102/348255
Funding: The study was supported by National Natural Science Foundation of China, No. 81802240 (to XS), S. K. Yee Medical Foundation, No. 5-ZH61 (to MKYM) and Hong Kong Parkinson’s Disease Foundation, No. 5-ZH76 (to MKYM).
| Introduction|| |
Parkinson’s disease (PD) occurs frequently in elderly individuals, and the prevalence rate increases with age, especially above 60 years (Pringsheim et al., 2014). Although postural instability is a cardinal motor feature of PD, it has not been directly related to dopaminergic loss (Crouse et al., 2016). Accordingly, it is significantly less responsive to levodopa compared with other typical PD symptoms (Vu et al., 2012). Exercise training is often prescribed as an adjunct to medication to improve postural instability and prevent falls in PD patients (Kim et al., 2013; Shen and Mak, 2015; Shen et al., 2016; Debû et al., 2018).
Various studies have examined the benefits of exercise training on postural instability in people with PD, measured via balance and functional mobility tests, PD-specific impairment, and disability status (Tomlinson et al., 2013; Shen et al., 2016; Mak et al., 2017). Balance and gait training, as well as muscle strength training, are core components of exercises that are beneficial for postural stability and preventing falls in persons with PD (Tomlinson et al., 2013; Shen et al., 2016; Mak et al., 2017). However, the optimal dosage of exercise required to improve postural stability in persons with PD remains unclear. The training periods applied in previous studies have varied largely, from 10 days to 24 months (Lehman et al., 2005; Allen et al., 2010; Prodoehl et al., 2015; Schenkman et al., 2018; Capecci et al., 2019; Gaßner et al., 2019; Leal et al., 2019; Steib et al., 2019; van der Kolk et al., 2019; Zhu et al., 2020; Cherup et al., 2021; Çoban et al., 2021; Granziera et al., 2021; Mak and Wong-Yu, 2021; Soke et al., 2021). However, the length of the training period was not positively associated with the training effects and even negatively influenced the training effects on comfortable gait velocity in previous studies (Lehman et al., 2005; Allen et al., 2010; Ni et al., 2018). For instance, walking performance in persons with PD improved after 10 days of cued walking training (Lehman et al., 2005) but not after 6 months of combined balance, gait, and strength exercise training (van der Kolk et al., 2019). Previous meta-analyses of the effects of exercise training on postural stability reported no association between the total number of training hours and the effects in terms of balance outcomes (Allen et al., 2011; Shen et al., 2016). Given the differences in training components among the previous studies, it is difficult to ascertain the association between exercise dose and the effects on balance and functional mobility.
It is important to clarify the dose-response relationship of exercise interventions within studies (Capecci et al., 2019; Leal et al., 2019; Zhu et al., 2020; Çoban et al., 2021; Granziera et al., 2021; Mak and Wong-Yu, 2021; Soke et al., 2021; Oguz et al., 2022) with different doses and similar exercise training components. Few studies exploring the effects of exercise training on balance in persons with PD have measured the training effects in the middle and at the end of the training period (Lehman et al., 2005; Mak and Hui-Chan, 2008; Esculier et al., 2012; Schenkman et al., 2012; Cheng et al., 2013; Corcos et al., 2013). Improvements between the initial training phase and the end of the training period were comparable for cue-augmented balance (4 weeks) and gait training (10 days) (Lehman et al., 2005; Mak and Hui-Chan, 2008), and for aerobic exercise (4 months) and treadmill walking (12 weeks) in individuals with PD (Schenkman et al., 2012; Cheng et al., 2013). In contrast, gains continuously increased from the first phase to the end of the training period for resistance training (24 months) and home-based balance training (6 weeks) (Esculier et al., 2012; Corcos et al., 2013). These findings could be useful in determining the training duration with the highest time-effectiveness. However, insufficient evidences with a large variance in training duration and inconsistence in some findings would hinder their application.
This study aimed to explore the dose-response relationship of the two main exercise training components, balance and gait training as well as muscle strength training for enhancing postural stability in persons with PD. We examined three different training durations (4, 8, and 12 weeks), considering that previous studies frequently used a 12-week duration (Shen et al., 2016). We hypothesized that for both types of exercise training, a longer duration would lead to better improvement in balance and gait outcomes in individuals with PD.
| Subjects and Methods|| |
This was an exploratory study exploring the dose-response relationship within two parallel exercise training groups (Additional file 1[Additional file 1]). It was registered at clinicaltrials.gov (registration No. NCT01427062) on September 1, 2011. The study conformed to the guidelines of the Helsinki Declaration and was approved by the Ethics Committees of the Hong Kong Polytechnic University (Additional file 2[Additional file 2]) at which experimental implementation took place (from June 2011 to June 2013). Subjects were recruited by poster advertisements and/or recruitment talks at the University campus, the Movement Disorders Clinic at Tung Wah Hospital in Hong Kong, and the Hong Kong Parkinson’s Disease Association, a patient self-help group. Community-dwelling persons with PD were included when they met the inclusion criteria: 1) a diagnosis of idiopathic PD (Hughes et al., 1992), 2) stable anti-Parkinsonian medication regimen, 3) ability to walk independently for at least 10 minutes, and 4) a Mini-Mental State Examination score of 24 or higher (Folstein et al., 1975). Volunteers were excluded if they had neurological conditions other than PD, uncompensated cardiovascular disease, visual problems, or recent musculoskeletal injuries that could interfere with balance and locomotion (Shen and Mak, 2014, 2015). 
Eligible participants were enrolled after providing informed consent (Additional file 3)[Additional file 3]. They were randomized into either a balance and gait training (BAL) group or a strength training (STR) group by drawing lots. Randomization was conducted by a researcher who was not involved in any other study component. The examiners were blinded regarding group assignment. A total of 12 weeks of training was provided to the participants in each group, including two 4-week phases of physiotherapist-supervised laboratory-based training separated by a 4-week phase of self-supervised home-based training. The 8-week laboratory-based training was conducted at a frequency of three sessions per week. The home-based training was performed at a frequency of five sessions per week [Figure 1].
|Figure 1: A flow diagram showing the participants who participated in the study.|
Note: BAL: Balance and gait training group; STR: strength training group.
Click here to view
To emphasize postural control strategies under self-destabilizing conditions during the laboratory-based training phases, participants in the BAL group were asked to stably perform step and reaching movements according to visual cues with a large amplitude, fast speed, and high performance accuracy. Two computerized systems were used for training: a commercially available dancing system (KSD Technology Co. Ltd., Shenzhen, China) and the Smart-Equitest Balance Master system (NeuroCom International Inc., Clackamas, OR, USA). The two systems presented visual cues on a computer screen to guide the movements of the subjects, and simultaneously detected the central pressure of the foot and hand positions of participants, enabling the calculation of performance accuracy scores. The participants received feedback on performance accuracy after each task. The difficulty level, rated by the amplitude and speed of movements, increased when the subject reached 80% performance accuracy. The postural control training included step and reaching movements and lasted 30 minutes. To emphasize postural control strategies that could be used under externally destabilizing conditions, participants in the BAL group were required to take a big step in time when they encountered a sudden external perturbation during walking on a treadmill or on the ground. The perturbation was caused by the sudden starting and stopping of the treadmill belt or by a manual interruption of walking by a physiotherapist. Verbal feedback regarding the response quality and walking performance was given after each task. The difficulty level, which was rated in terms of the walking amplitude, speed, frequency of the perturbations, and gait velocity was increased if the subjects responded rapidly to the perturbation with a large step, good stability, and a good gait pattern. The training sessions for postural control during walking lasted for 30 minutes. Each laboratory-based training session was 60 minutes in total. To emphasize postural control strategies during the home-based training phase, participants in the BAL group were asked to perform sit-to-stand movements in a sequenced and stable manner as well as walking activities with a good gait pattern in all directions. Each home-based training session lasted for 20 minutes. Participants in the STR group underwent strength training targeting the lower limb muscles. During laboratory-based training, dynamometers were used to increase the strength of the hip (flexion, extension, abduction) and knee (flexion, extension) muscles at 60% of one repetition maximum, and participants used a rowing machine to perform rowing exercises as quickly as possible for a 3-minute period. The repetition maximum was measured before training and every 2 weeks within the training period. In addition to exercises using machines, the participants stepped on and off a 6-inch curb and walked on the ground with 0.5–1.5 kg sandbags strapped to each lower extremity. These movements were performed as quickly as possible in a 3-minute period to improve the strength of the hip, knee, and ankle muscles. The duration of each laboratory-based STR training session was 60 minutes. During the home-based training phase, participants in the STR group were required to perform weighted stepping up and down and walking exercises as in the laboratory-based phase. Supervision by their family members was suggested for safety. Each home-based STR training session lasted 20 minutes. Exercise compliance was recorded by the physiotherapists during laboratory-based training and by the subjects during home-based training. More detail information about the intervention has been described in our previous articles (Shen and Mak, 2014, 2015).
We used a series of balance and gait outcomes as primary outcomes and PD-specific impairment scales as secondary outcomes. For balance and gait outcomes, we used the limit of stability (LOS) test, single-leg-stance (SLS) test, and a walking test to examine balance and gait performance and the activities-specific balance confidence (ABC) scale to reflect balance confidence. During the LOS test, the movement velocity and the endpoint excursion of the center of gravity were recorded. A higher movement velocity and a longer endpoint excursion indicate better LOS performance (Jessop et al., 2006). In the SLS test, a longer SLS time indicates better balance performance (Michikawa et al., 2009). During the walking test, we measured self-selected gait velocity (cm/s) and stride length (cm), with higher values indicating better gait performance. As for the ABC scale, we used the average score of 16 daily activities rated from 0 (no confidence) to 100 (full confidence) (Mak and Hui-Chan, 2008). The measurement procedures of these balance and gait outcomes were based on previous studies (Shen and Mak, 2014, 2015). Regarding the secondary outcomes of PD-specific impairment, an examiner scored motor impairment using 14-item motor subscale of the Unified Parkinson’s disease rating scale (UPDRS-III) (Richards et al., 1994). Each item was scored from 0 to 4, with 0 denoting the absence of impairment and 4 denoting severe impairment. The total score of the UPDRS-III was used for data analysis.
All assessments were conducted before and after each phase of training for the subjects with PD in the “on” stage of medication (Pre, Mid4wk, Mid8wk, Post) by examiners who were not aware of group assignments. During the first assessment, we collected demographic data including sex, age, body weight and height, fall history, PD duration, the modified Hoehn and Yahr staging score (to indicate severity of PD) (Hoehn and Yahr, 1967), level of physical activity as determined by a metabolic equivalent questionnaire (Friedenreich et al., 1998), and the Mini-Mental State Examination score as a measure of cognitive status (Folstein et al., 1975). In addition, participant daily levodopa dosages were recorded at each assessment interval.
Sample size calculation
Based on the results of Cheng et al. (2013) regarding changes in gait velocity during 12 weeks of walking training, we required 10 participants in each group to detect differences in improvement in the first 4-week versus the later 8-week period, with an assumption of 95% power. However, this was a sub-study of a fall prevention project that required a much larger number of subjects in each group (BAL: n = 26, STR: n = 25) (Shen and Mak, 2015).
Data were analyzed using SPSS version 17.0 (SPSS, Chicago, IL, USA). Data normality was examined using the Shapiro-Wilk test. Group differences in participant characteristics and baseline measures were analyzed using independent t-tests for variables with normal distribution and chi-square tests for nominal variables. For outcome measurements, dose-response relationships across different time intervals of each group were analyzed using a one-way repeated measures analysis of variance for normally distributed variables (Pre, Mid4wk, Mid8wk, Post) and Friedman for non-normally distributed variables. Post-hoc paired t-tests and Wilcoxon tests were further adopted to analyze dose-response relationships within each time interval and the whole interval (Pre versus Mid4wk, Mid4wk versus Mid8wk, Mid8wk versus Post, Pre versus Post). The significance level was set at P < 0.05 for all tests except for post-hoc tests with P < 0.025.
| Results|| |
Four subjects in the BAL group and two in the STR group dropped out during the study period. The reasons for each drop-out are presented in [Figure 1]. Data from the 45 participants who completed the three phases of training and all assessments were included in data analysis (BAL: n = 22, STR: n = 23).
As shown in [Table 1], we found no significant differences in demographic and clinical characteristics of subjects between the BAL and STR groups. The daily levodopa dosage was comparable between the two groups at each assessment interval. For exercise compliance, participants in the BAL group completed 0.4 more treatment sessions than those in the STR group during each laboratory-based training phase. No between-group difference was found in exercise compliance during the home-based training phase (P > 0.05).
The results of dose-response relationships across different time intervals of each training are shown in [Table 2]. In the BAL group, the time-based effects across the 12 weeks were significant for SLS time, endpoint excursion, and movement velocity in the LOS test, and stride length in the walking test (P < 0.05). The time-based effects were nearly significant for the UPDRS-III score (P = 0.083), but not significant for the gait velocity in the walking test and the ABC score. During the first 4 weeks (Pre versus Mid4wk), the SLS time, endpoint excursion, movement velocity, and stride length significantly improved (P < 0.025), and the increase in UPDRS-III score nearly reached significance (P = 0.098). During the middle 4-week period (Mid4wk versus Mid8wk), no measures showed significant change. During the final 4-week period (Mid8wk versus Post), movement velocity component of the LOS test (P = 0.098), ABC score (P = 0.085), and UPDRS-III score (P = 0.038) demonstrated a nearly significant increase. Finally, compared with the baseline, all measures including the gait velocity and ABC (not yet significant at the first 4 weeks), displayed significant or near-to-significant improvement at the end of the 12-week training period (P < 0.05).
|Table 2: Effects of training with different training durations on balance and gait outcomes and PD-specific impairments|
Click here to view
In the STR group, the time-based effects across the 12-week period were significant for the endpoint excursion in the LOS test and gait velocity in the walking test (P < 0.05), nearly significant for the UPDRS-III score (P = 0.057), and non-significant for the other measures. During the first 4 weeks, only the endpoint excursion and gait velocity significantly improved (P < 0.025). During the second 4-week period, no measures showed significant change except for the UPDRS-III score, which near-to-significantly decreased (P = 0.049). During the final 4-week period, the endpoint excursion and the UPDRS-III score displayed further significant improvement (P < 0.025), whilst gait velocity demonstrated a nearly significant increase (P = 0.092). Finally, at the end of the 12-week training period, we observed a significant improvement in the endpoint excursion, and gait velocity (P < 0.025), and nearly significant increases in the SLS time (P = 0.042) and stride length (P = 0.083), compared with the baseline.
| Discussion|| |
The findings of the present study indicate that 12 weeks of training led to greater improvements in balance and gait outcomes than 4 weeks of training in both exercise groups. These data support our hypothesis that a longer training duration would produce greater improvements in balance and gait outcomes in individuals with PD. Regarding balance and gait performance, 4 weeks of training was sufficient to improve most measures of balance and gait performance in the BAL group, but improvements were only seen in the endpoint excursion and gait velocity in the STR group. Rapid tapering of training effects after initial improvement is a common element of dose-response relationships between training and performance (Busso, 2003). Thus, training duration should be considered to optimize the effects of exercise programs, as well as save time and money. Based on our results, a 4-week BAL training program is likely to be the most cost-effective choice for improving balance and gait performance in individuals with PD, as STR training programs must be longer to elicit comparable improvements in balance and gait performance. To improve balance confidence, we recommend BAL training for at least 12 weeks.
The higher efficiency in the BAL group versus the STR group in terms of improving balance and gait performance could result from the specific training emphasis. Postural instability and muscle weakness both contribute to poor functional balance performance in elderly populations (Orr, 2010). In individuals with PD, postural instability is a hallmark impairment that directly results from PD-related neurological degeneration. However, muscle weakness associated with muscle atrophy might be caused by decreased mobility (Dibble et al., 2006). Thus, postural instability could play a more direct and a larger contributing role in poor functional balance performance than muscle weakness in individuals with PD. Therefore, BAL training with a specific emphasis on postural control could lead to faster improvements in balance and gait performance compared with STR training. Besides the specific training emphasis on postural control, the higher degree of similarity between the BAL training tasks and the tests of balance and gait performance could be another factor contributing to faster improvement in the BAL group compared with the STR group.
During the second training phase, we observed a decrease in the UPDRS-III score in the STR group and no further improvement in other variables. This limited gain during the home-based phase could be attributable to low exercise dose and intensity, as well as self-supervision. We positioned the home-based training sessions between the two laboratory-based training sessions to encourage the participants to apply their learned postural control strategies and exercises into their daily functional activities and to independently form exercise habits. We set the exercise duration to 20 minutes per session and the exercise intensity to a much lower level during the home-based phase to make it easier for the participants to complete the tasks at home. Accordingly, we observed a high compliance rate (> 85%) in both groups. Our finding of reduced benefits from low-intensity exercise were consistent with those of Allen et al. (2011) and Schenkman et al. (2018), who found that more challenging balance and gait exercises had better effects on balance outcomes. Furthermore, people may be less motivated to complete self-supervised training sessions, leading to lower compliance rates and lower completion quality compared with physiotherapist-supervised training. This could lead to decreased gains during home-based training versus laboratory-based training. However, given the comparable compliance rates, completion quality, and other dose and intensity parameters, supervision from a physiotherapist might not have caused the difference in training effects. This speculation is supported by a previous study in which physiotherapist-supervised and self-supervised training groups with the same compliance rate achieved similar training effects in terms of balance and gait (Lun et al., 2005). In summary, a lower exercise dose resulting from a lower exercise intensity, duration, and compliance rate could be the main factor contributing to the decreased gains during home-based training compared with laboratory-based training in both groups.
There were several limitations to this study. First, there was no control group that did not perform exercise, so it is difficult to clearly differentiate the training effects from the time effects. Second, we did not examine the long-term effects of training programs with different durations. In our previous studies, we reported that the BAL group showed excellent long-term effects in terms of balance and gait outcomes at 1 year after completion of the 12-week treatment program (Shen and Mak, 2014, 2015). However, given the design of the present study, we could not determine the long-term effects of the 4-week training phase. To examine the relationship between training dose and short- and long-terms effects, further studies should include two groups that undergo training programs with different durations and a control group that does not complete training. A long interval with no exercise would be helpful to identify the long-term impact of exercise dose. Furthermore, our participants were community-dwelling individuals with a mild-to-moderate disease level. Thus, we are unable to generalize our results to individuals with advanced-stage PD or those who have been institutionalized.
In conclusion, balance and gait performance improved following 4 weeks of balance and gait training, but an additional 8 weeks of training was required to elicit a further increase in self-perceived balance confidence level. A longer duration of muscle strength training was required to gain comparable improvements in balance and gait performances. Our findings may guide clinical physiotherapists in developing exercise programs for persons with PD.
XS conceived and designed the study, performed data acquisition, and drafted the manuscript. JH performed data analysis. MKYM conceived and designed the study. All authors read, revised the paper, and approved the final manuscript.
Conflicts of interest
Authors declared no conflicts of interests.
Editor note: XS is an Editorial Board member of Brain Network and Modulation. She was blinded from reviewing or making decisions on the manuscript. The article was subject to the journal’s standard procedures, with peer review handled independently of this Editorial Board member and her research group.
Availability of data and materials
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Open access statement
This is an open access journal, and articles are distributed under the terms of the Creative Commons AttributionNonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Additional file 1: STROBE checklist.
Additional file 2: Hospital ethics approval.
Additional file 3: Informed consent template.
| References|| |
Allen NE, Sherrington C, Paul SS, Canning CG (2011) Balance and falls in Parkinson’s disease: a meta-analysis of the effect of exercise and motor training. Mov Disord 26:1605-1615.
Allen NE, Canning CG, Sherrington C, Lord SR, Latt MD, Close JC, O’Rourke SD, Murray SM, Fung VS (2010) The effects of an exercise program on fall risk factors in people with Parkinson’s disease: a randomized controlled trial. Mov Disord 25:1217-1225.
Busso T (2003) Variable dose-response relationship between exercise training and performance. Med Sci Sports Exerc 35:1188-1195.
Capecci M, Pournajaf S, Galafate D, Sale P, Le Pera D, Goffredo M, De Pandis MF, Andrenelli E, Pennacchioni M, Ceravolo MG, Franceschini M (2019) Clinical effects of robot-assisted gait training and treadmill training for Parkinson’s disease. A randomized controlled trial. Ann Phys Rehabil Med 62:303-312.
Cheng SP, Yang CY, Tang FI, Chen IJ (2013) Training effects of a 12-week walking program on Parkinson disease patients and community-dwelling older adults. NeuroRehabilitation 32:967-976.
Cherup NP, Strand KL, Lucchi L, Wooten SV, Luca C, Signorile JF (2021) Yoga meditation enhances proprioception and balance in individuals diagnosed With Parkinson’s disease. Percept Mot Skills 128:304-323.
Çoban F, Belgen Kaygısız B, Selcuk F (2021) Effect of clinical Pilates training on balance and postural control in patients with Parkinson’s disease: a randomized controlled trial. J Comp Eff Res 10:1373-1383.
Corcos DM, Robichaud JA, David FJ, Leurgans SE, Vaillancourt DE, Poon C, Rafferty MR, Kohrt WM, Comella CL (2013) A two-year randomized controlled trial of progressive resistance exercise for Parkinson’s disease. Mov Disord 28:1230-1240.
Crouse JJ, Phillips JR, Jahanshahi M, Moustafa AA (2016) Postural instability and falls in Parkinson’s disease. Rev Neurosci 27:549-555.
Debû B, De Oliveira Godeiro C, Lino JC, Moro E (2018) Managing gait, balance, and posture in Parkinson’s disease. Curr Neurol Neurosci Rep 18:23.
Dibble LE, Hale TF, Marcus RL, Droge J, Gerber JP, LaStayo PC (2006) High-intensity resistance training amplifies muscle hypertrophy and functional gains in persons with Parkinson’s disease. Mov Disord 21:1444-1452.
Esculier JF, Vaudrin J, Bériault P, Gagnon K, Tremblay LE (2012) Home-based balance training programme using Wii Fit with balance board for Parkinsons’s disease: a pilot study. J Rehabil Med 44:144-150.
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198.
Friedenreich CM, Courneya KS, Bryant HE (1998) The lifetime total physical activity questionnaire: development and reliability. Med Sci Sports Exerc 30:266-274.
Gaßner H, Steib S, Klamroth S, Pasluosta CF, Adler W, Eskofier BM, Pfeifer K, Winkler J, Klucken J (2019) Perturbation treadmill training improves clinical characteristics of gait and balance in Parkinson’s disease. J Parkinsons Dis 9:413-426.
Granziera S, Alessandri A, Lazzaro A, Zara D, Scarpa A (2021) Nordic walking and walking in Parkinson’s disease: a randomized single-blind controlled trial. Aging Clin Exp Res 33:965-971.
Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427-442.
Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181-184.
Jessop RT, Horowicz C, Dibble LE (2006) Motor learning and Parkinson disease: refinement of movement velocity and endpoint excursion in a limits of stability balance task. Neurorehabil Neural Repair 20:459-467.
Kim SD, Allen NE, Canning CG, Fung VS (2013) Postural instability in patients with Parkinson’s disease. Epidemiology, pathophysiology and management. CNS Drugs 27:97-112.
Leal LC, Abrahin O, Rodrigues RP, da Silva MC, Araújo AP, de Sousa EC, Pimentel CP, Cortinhas-Alves EA (2019) Low-volume resistance training improves the functional capacity of older individuals with Parkinson’s disease. Geriatr Gerontol Int 19:635-640.
Lehman DA, Toole T, Lofald D, Hirsch MA (2005) Training with verbal instructional cues results in near-term improvement of gait in people with Parkinson disease. J Neurol Phys Ther 29:2-8.
Lun V, Pullan N, Labelle N, Adams C, Suchowersky O (2005) Comparison of the effects of a self-supervised home exercise program with a physiotherapist-supervised exercise program on the motor symptoms of Parkinson’s disease. Mov Disord 20:971-975.
Mak MK, Hui-Chan CW (2008) Cued task-specific training is better than exercise in improving sit-to-stand in patients with Parkinson’s disease: A randomized controlled trial. Mov Disord 23:501-509.
Mak MK, Wong-Yu IS, Shen X, Chung CL (2017) Long-term effects of exercise and physical therapy in people with Parkinson disease. Nat Rev Neurol 13:689-703.
Mak MKY, Wong-Yu ISK (2021) Six-month community-based brisk walking and balance exercise alleviates motor symptoms and promotes functions in people with Parkinson’s disease: a randomized controlled trial. J Parkinsons Dis 11:1431-1441.
Michikawa T, Nishiwaki Y, Takebayashi T, Toyama Y (2009) One-leg standing test for elderly populations. J Orthop Sci 14:675-685.
Ni M, Hazzard JB, Signorile JF, Luca C (2018) Exercise guidelines for gait function in parkinson’s disease: a systematic review and meta-analysis. Neurorehabil Neural Repair 32:872-886.
Oguz S, Gurses HN, Kuran Aslan G, Demir R, Ozyilmaz S, Karantay Mutluay F, Apaydin H (2022) Walking training augments the effects of expiratory muscle training in Parkinson’s disease. Acta Neurol Scand 145:79-86.
Orr R (2010) Contribution of muscle weakness to postural instability in the elderly. A systematic review. Eur J Phys Rehabil Med 46:183-220.
Pringsheim T, Jette N, Frolkis A, Steeves TD (2014) The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 29:1583-1590.
Prodoehl J, Rafferty MR, David FJ, Poon C, Vaillancourt DE, Comella CL, Leurgans SE, Kohrt WM, Corcos DM, Robichaud JA (2015) Two-year exercise program improves physical function in Parkinson’s disease: the PRET-PD randomized clinical trial. Neurorehabil Neural Repair 29:112-122.
Richards M, Marder K, Cote L, Mayeux R (1994) Interrater reliability of the Unified Parkinson’s Disease Rating Scale motor examination. Mov Disord 9:89-91.
Schenkman M, Hall DA, Barón AE, Schwartz RS, Mettler P, Kohrt WM (2012) Exercise for people in early- or mid-stage Parkinson disease: a 16-month randomized controlled trial. Phys Ther 92:1395-1410.
Schenkman M, Moore CG, Kohrt WM, Hall DA, Delitto A, Comella CL, Josbeno DA, Christiansen CL, Berman BD, Kluger BM, Melanson EL, Jain S, Robichaud JA, Poon C, Corcos DM (2018) Effect of high-intensity treadmill exercise on motor symptoms in patients with de novo Parkinson disease: a phase 2 randomized clinical trial. JAMA Neurol 75:219-226.
Shen X, Mak MK (2014) Balance and gait training with augmented feedback improves balance confidence in people with Parkinson’s disease: a randomized controlled trial. Neurorehabil Neural Repair 28:524-535.
Shen X, Mak MK (2015) Technology-assisted balance and gait training reduces falls in patients with Parkinson’s disease: a randomized controlled trial with 12-month follow-up. Neurorehabil Neural Repair 29:103-111.
Shen X, Wong-Yu IS, Mak MK (2016) Effects of exercise on falls, balance, and gait ability in Parkinson’s disease: a meta-analysis. Neurorehabil Neural Repair 30:512-527.
Soke F, Guclu-Gunduz A, Kocer B, Fidan I, Keskinoglu P (2021) Task-oriented circuit training combined with aerobic training improves motor performance and balance in people with Parkinson’s disease. Acta Neurol Belg 121:535-543.
Steib S, Klamroth S, Gaßner H, Pasluosta C, Eskofier B, Winkler J, Klucken J, Pfeifer K (2019) Exploring gait adaptations to perturbed and conventional treadmill training in Parkinson’s disease: Time-course, sustainability, and transfer. Hum Mov Sci 64:123-132.
Tomlinson CL, Patel S, Meek C, Herd CP, Clarke CE, Stowe R, Shah L, Sackley CM, Deane KH, Wheatley K, Ives N (2013) Physiotherapy versus placebo or no intervention in Parkinson’s disease. Cochrane Database Syst Rev 2013:CD002817.
van der Kolk NM, de Vries NM, Kessels RPC, Joosten H, Zwinderman AH, Post B, Bloem BR (2019) Effectiveness of home-based and remotely supervised aerobic exercise in Parkinson’s disease: a double-blind, randomised controlled trial. Lancet Neurol 18:998-1008.
Vu TC, Nutt JG, Holford NH (2012) Progression of motor and nonmotor features of Parkinson’s disease and their response to treatment. Br J Clin Pharmacol 74:267-283.
Zhu M, Zhang Y, Pan J, Fu C, Wang Y (2020) Effect of simplified Tai Chi exercise on relieving symptoms of patients with mild to moderate Parkinson’s disease. J Sports Med Phys Fitness 60:282-288.
[Table 1], [Table 2]