Abstract
Background:
Posture instability and unsteady gait disorders in Parkinson’s Disease (PD) usually contribute to fall-related fractures. Fall-related trauma in PD is the most common reason for injury. Despite providing modern care for PD patients (PP) in the recent years, anti-PD drugs have no effect on falling. There is an urgent need to administer exercise interventions to reduce falls and related injuries in the rehabilitation program of PP.
Objectives:
To explore the effect of a selective 10-week corrective exercise with an emphasis on gait training activities (GTA) on the number of falls (NOFs), fear of falling, functional balance, timed up and go (TUG) test among PD patients.
Patients and Methods:
A purposeful sampling was performed on PP who had fallen or were at risk of falling in 2014. The study intervention consisted of a 10-week (3 sessions each week, each lasting 60 min) corrective exercise program. Participants were randomly allocated to control and two exercise groups; the exercise group with balance pad (EGBP) or exercise group with no balance pad (EGNBP). The analysis of variance (ANOVA) and paired t-test were used for comparison between the groups (P ≤ 0.05).
Results:
Administrating a selective corrective exercise in exercise group with balance pad (EGBP) showed a significant difference in number of falls (NOF), Fall Efficacy Scale-international (FES-I), Berg balance scale (BBS) (and timed up and go) TUG (P = 0.001); while administrating the same exercise in exercise group with no balance pad (EGNBP) showed no significant difference in NOF (P = 0.225) and a significant difference in FES-I (P = 0.031), BBS (P = 0.047) and TUG (P = 0.012). The control group showed no significant difference in each of the dependent variables.
Conclusions:
Performing a selective corrective exercise on balance pad improves falling and functional balance in idiopathic PD.
Keywords: PD, Falling, Postural Balance, Exercise Therapy
1. Background
Falling-related trauma in elderly patients is the most common reason for injury and mortality (1). Falling is considered as the main concern in Parkinson’s Disease (PD). Reportedly near two-thirds of PD patients (PP) have a yearly history of falling with half of them with a repeated history of falling (2). Injury and falling-related fears as the outcomes of PD (3-6) are common in sedentary lifestyles (6, 7) aggravating the tension in caring of such patients (8, 9). An estimated number of 5 million patients have PD in only ten populated countries, which may be doubled for next three decades (10). In spite of providing modern caring system in the recent years, anti-PD drugs had no effect on falling (11, 12). Hence, falling due to PD imposes a heavy cost of caring and rehabilitation in the following years.
Considering scarcity of literature, the effects of exercise on falling in PP were evaluated (12, 13). Ashburn et al. (2007) on their short-term exercise protocol reported an improvement in falling (12).
In general, significant effects of exercise are assessed in chronic exercise protocols (tens of hours to months) (14, 15).
The established risk factors for falling in PD are lower extremity muscular weakness, poor balance and gait freezing (16), all of which improve in PD following some exercise (12, 17-21). According to Latt (22) a series of factors are considered as risk factors for falling in PP (e.g., bradykinesia, poor balance, freezing of gait, cognitive impairment as well as age-related impairments, such as reduced lower limb muscle strength). For this reason, designing a corrective exercise to reduce falling to some extent would be targeted to partially recover the balance and lower limb muscle strength. Accordingly, an exercise program for improving falling in PD may be of benefit.
2. Objectives
Given beneficial effects of exercise in alleviating locomotor problems of PD and that performing corrective exercise may be effective we sought to assess the effects of exercise to see whether performing a selective 10-week corrective exercise with an emphasis on gait training activities (GTA) lessens the number of falls (NOFs) and fear of falling using the Fall Efficacy Scale-international (FES-I), functional balance in Berg balance scale (BBS), and the Timed Up and Go (TUG) test among PP.
3. Patients and Methods
3.1. Study Design
The sampling was made based on a purposeful method. Participants were voluntarily recruited from university affiliated neurology clinics and private neurology offices in Kashan. This study consisted of a 10-week (3 sessions per week, each lasting 60 min) corrective exercise for PP who had fallen or were at risk of falling conducted in 2014. After baseline assessment, participants were randomly allocated to control and two exercise groups. The sample size for participants in each group was based on similar studies (23).
The exercise groups were exercise group with balance pad (Exercise Group with Balance Pad [EGBP (no: 15)]) or without a balance pad (Exercise Group with no Balance Pad [EGNBP (no: 15)]). One participant of the EGNBP group dropped out of the study.
The control group (no: 17) received their usual care by a neurologist. Two participants in the control group dropped out of the study.
Cognitive function assessment with Mini-Mental State Examination (MMSE) was conducted one hour after participant's last dose of anti-PD drug.
3.2. Participants
At the start of study, all participants were sequentially screened by a neurologist. Medical assessment was performed to assess whether he or she is able to participate in moderate-intensity wholly-supervised exercise (an MMSE score of > 24) before enrollment in the study. A total of 47 (33 M, 14 F) participants in the second and third stages of the disease were selected based on Hoehn and Yahr criteria (24).
Participants were included in the study if had a diagnosis of idiopathic PD for three years and were able to walk independently, aged between 50 and 70 years, consumed the same anti-PD medication for past 2 weeks and had a history of falling in the past year. Participants were excluded from the study if had significant cognitive impairment (MMSE < 24 (25) or other neurological/musculoskeletal/cardiopulmonary/metabolic conditions that would interfere with safe conduction of training or exercise program.
Background information, including medical history, prescribed medications, age, height, weight, body mass index (BMI), falling history, FES-I, BBS and TUG test were recorded for all participants (Table 1).
Table 1. Participants’ Demographic Dataa.
| Variable | Cont (n = 15) | EGBP (n = 15) | EGNBP (n = 14) | P Value b |
|---|---|---|---|---|
| Age, y | 57.22 ± 6.87 | 59.13 ± 8.37 | 58.77 ± 8.06 | .786 |
| Gender | .870 | |||
| Male | 11 | 10 | 9 | |
| Female | 4 | 5 | 5 | |
| Height, cm | 163 ± 7.9 | 164.8 ± 8.8 | 162 ± 7.5 | .647 |
| Weight, kg | 71.24 ± 11.45 | 68.20 ± 10.59 | 69.89 ± 7.64 | .711 |
| BMI, kg/m 2 | 26.18 ± 4.3 | 24.86 ± 2.6 | 25.52 ± 1.4 | .503 |
| MMSE (range, 0 to 30) | 26.4 ± 0.9 | 27.0 ± 1.0 | 26.7 ± 1.1 | .375 |
| H and Y score (range, 1 to 5) | 2.6 ± 0.5 | 2.53 ± 0.5 | 2.57 ± 0.5 | .938 |
| DD, y | 4.9 ± 1.8 | 4.9 ± 1.9 | 5.2 ± 2.0 | .847 |
| NOF | 1.2 ± 0.8 | 1.3 ± 0.8 | 1.2 ± 1.0 | .957 |
| FES-I | 41.4 ± 7.6 | 42 ± 6.4 | 43.2 ± 5.6 | .772 |
| BBS | 38.00 ± 4.94 | 38.73 ± 5.02 | 40.36 ± 6.77 | .520 |
| TUG | 13.26 ± 2.88 | 13.58 ± 2.58 | 14.23 ± 2.23 | .593 |
Abbreviations: BBS, Berg balance scale; BMI, body mass index; DD, disease duration; EGBP, exercise group with balance pad; EGNBP, exercise group with no balance pad; FES-I, falls efficacy scale- international; H&Y, Hahn & Yard; MMSE, mini-mental state examination; NOF, number of falling; TUG, timed up and go.
aData are presented as mean ± SD.
bBased on ANOVA test.
All participants underwent two measurements namely one on entry to the study (pre-test) and one after a 10-week follow-up intervention (post-test).
3.3. Patient Assessment
All participants were evaluated for the following measurements in both pre-test and post-test.
i) Falls measured as the primary outcome of the disease assessed by comparing the number of falls (NOFs) between the study and control groups. The NOFs were recorded by direct questioning. ii) FES-I: a fall efficacy questionnaire denoting the fear of falling (26). iii) The BBS used for assessing functional balance of participants (27), consisted of 14 items assessing the capability to keep balance in different positions/postures. Scoring was based on participant’s ability to do the tasks on a four-score system from 0 (inability in performing) to 4 (normal performance). The higher the acquired scores, the better the participant's balance. BBS was used for routine clinical and research applications as a balance measure, especially in PD (28, 29). iv) The TUG test used for assessment of balance and falling was defined as the time taken for performing a complex task (e.g. a sequential action: standing up from a chair with no arms and 45 cm height from the ground, walking 3 m, turning 180°, returning and sitting down (30). Three practice trials for each test were performed of which the mean of the recorded time was recorded as TUG.
3.4. Exercise Protocol
The exercise protocol undertaken for balance included a 60-min program of progressive balance and GTA 3 times a week for 10 weeks (31).
All exercise sessions included 5 minutes warm-up exercises followed by the main exercises for 50 minutes. The warm-up consisted of lower extremity stretch muscle groups, which act to prevent collapse of the lower limb (hip and knee extensors and ankle plantar flexors) targeted with exercises designed to enhance posture control (i.e. balance) with an emphasis on GTA. The balance exercises were included standing with a decreased base of support, forwards, backwards and sideway leg raise, and graded reaching activities in standing sit-to-stand, forward or lateral step-ups, semi squats and heel raises in standing as well. GTA included forwards, backwards and sideways stepping/walking, static and dynamic marching and tandem walking. Standard principles governing frequency, volume, duration, intensity and progression of exercises were applied (32). The exercise sessions were terminated with 5 minutes cool-down exercise. In both exercise groups, the same training protocol was performed. While, in EGBP all exercises were performed for 4 weeks and then for another 6 weeks using different balance pad sizes (6, 10 cm thickness, AIREX mat, Switzerland [(L) 93 cm × (B) 41 cm × (H) 10 cm); (L) 98 cm × (B) 41 cm × (H) 6 cm], respectively. The control group performed no training during the study period.
3.5. Ethical Considerations
This study was registered in the Iranian Registry for Clinical Trial (IRCT) as 2013032712865N1. They were briefed on the study aims and signed a written informed consent before enrollment. For safety purposes, the participants were instructed how to perform exercises safely with stable supports (such as a table) located nearby for additional support if required.
3.6. Data Analysis
The analysis of variance (ANOVA) was used for comparison of differences in personal characteristics, NOF, FES-I, BBS, TUG, between the three groups. Paired t-test was used for NOF, FES-I, BBS and TUG measures in all the three groups. Data analysis was performed using SPSS software version 16. A P-value less than 0.05 was assumed to be significant.
4. Results
4.1. Demographic Data of the Participants
Table 1 shows no significant difference regarding demographic variables between the groups.
4.2. The Effect of a Selective Corrective Exercise on NOF in EGBP and EGNBP Compared to Control Group
A selective corrective exercise on a balance pad in EGBP showed a significant difference in NOF between pre-test and post-test (P < 0.001). However, administrating the same exercise without a balance pad in EGNBP showed no significant difference; it caused a 33.3% decrease in falling rate. No significant change was seen in the control group (Table 2).
Table 2. Differences Between the Groups (Control vs. EGBP / EGNBP) for the Secondary Outcome Measures Related to Number of Falling, Falls Efficacy Scale-International, Berg Balance Scale and Timed Up and Goa.
| Pre-test | Post-test (> 10 Weeks) | P Value b | |
|---|---|---|---|
| NOF | |||
| EGBP | 1.3 ± 0.8 | 0.2 ± 0.4 | .000 c |
| EGNBP | 1.2 ± 1.0 | 0.8 ± 0.7 | .225 |
| Cont | 1.2 ± 0.8 | 1.5 ± 1.0 | .487 |
| FES-I | |||
| EGBP | 42 ± 6.4 | 26.8 ± 6.4 | .000 c |
| EGNBP | 43.2 ± 5.6 | 39.8 ± 3.9 | .031 b |
| Cont | 41.4 ± 7.6 | 42.7 ± 6.3 | .165 |
| BBS | |||
| EGBP | 38.73 ± 5.02 | 46.20 ± 3.50 | .000 c |
| EGNBP | 40.36 ± 6.77 | 44.29 ± 4.14 | .047 b |
| Cont | 38.00 ± 4.94 | 38.20 ± 4.60 | .582 |
| TUG | |||
| EGBP | 13.58 ± 2.58 | 11.92 ± 2.70 | .000 c |
| EGNBP | 14.23 ± 2.23 | 12.97 ± 2.17 | .012 b |
| Cont | 13.26 ± 2.88 | 13.34 ± 2.83 | .669 |
Abbreviations: BBS, Berg balance scale; Cont, control; EGBP, exercise group with balance pad; EGNBP, exercise group with no balance pad; FES-I, fall efficacy scale; NOF, number of falling; TUG, timed up and go.
aData are presented as mean ± SD.
bBased on paired t-Test; P < 0.05.
cBased on paired t-Test; P < 0.001.
4.3. The Effect of a Selective Corrective Exercise on FES-I in EGBP and EGNBP Compared to Control Group
A selective corrective exercise in both EGBP and EGNBP (Table 2) showed a significant improvement in the FES-I (P < 0.001 and P < 0.05, respectively).
4.4. The Effect of a Selective Corrective Exercise on BBS in EGBP and EGNBP Compared to Control Group
A selective corrective exercise in both EGBP and EGNBP (Table 2) showed a significant improvement in BBS (P < 0.001 and P < 0.05, respectively).
4.5. The Effect of a Selective Corrective Exercise on the TUG in the EGBP and EGNBP Compared to Control Group
A selective corrective exercise on both EGBP and EGNBP (Table 2) showed a significant improvement in TUG (P < 0.001 and P <0.05, respectively).
5. Discussion
Our study on idiopathic PP revealed that administrating a selective corrective exercise on a balance pad in EGBP group showed a significant difference in NOF, while without a balance pad in EGNBP group showed no significant difference. In addition, administrating the same exercise on both EGBP and EGNBP groups showed a significant improvement in FES-I, BBS and TUG.
Alzheimer’s disease and PD are primary and secondary causes of neurodegeneration worldwide (33). Fall-related injuries are the cause of disability (70 - 87%) (34, 35)and higher rates of fractures in PD surviving for decades after PD onset (36).
The core medical management of PD is drug therapy to enhance decreased dopamine secretion. Anti-PD drugs are routinely used in the first stages of PD; their use in advance stages of the disease has no beneficial effect (37). Nevertheless, even with administration of best selective drugs, PP has repeated falls with destructive outcomes. Reportedly more than 68% of PP have a history of falling and up to 46% of people with PD disease would experience frequent falls annually (6, 22), which is two times more than normal individuals (6). Consistent with this finding, a one-year length study reported a yearly 27% falling rate among PP.
In addition, as reported by most PD researchers, falling etiology is multifactorial. Independent factors involved in higher falling risk are chronic nature of PD, having a sedentary lifestyle, multiple locomotor disorders, abnormal posture, freezing of gait, frontal impairment, impaired balance and reduced knee extensor strength (2, 12). Furthermore, osteoporosis and osteopenia are very common findings in patients with PD. Multiple mechanisms are involved in the occurrence of osteoporosis in PP including sedentary life, endocrine (i.e., lower vitamin D level), malnutrition and iatrogenic reasons, female sex, stages III and IV of Hoehn and Yahr criteria (24), aging and lower BMI (38). As PD usually occurs late in life, postural instability and unsteady gait disorders usually contribute to fall-related fractures.
Considering significance of fall-related injuries and fractures among this group, there is an urgent need to identify and use effective exercise interventions to reduce falls and related injuries in patients with PD. To date, only few clinical studies investigated corrective exercise interventions to reduce falls in patients with PD. In our study, we showed that administrating a selective corrective exercise in EGBP resulted in a significant difference in NOF between pre-test and post-test, while administrating the same exercise in EGNBP led to no significant difference between pre-test and post-test and only caused a 33.3% decrease in falling rate.
Reviewing the literature in senile group demonstrated the benefits and preventive role of exercise interventions on balance and lower extremity muscle strength in falling (14, 39). Moreover, a significant correlation between lower extremity muscle strength in PD and physical parameters has been reported (40, 41), which emphasizes the effect of exercise as an appropriate intervention in this group.
Reportedly posture instability is the main characteristic of late PD (2), which causes falling (42). It is well established that impaired balance is the probable psychological outcome of FOF. FOF is considered as immediate outcome preceding falls, which can result in severe immobility (6).
A series of studies (12, 17, 43-46) using some specific tools such as Berg Balance Scale, Functional reach test and Sensory Orientation Test (SOT) indicated balance as an outcome of PD and reported a significant improvement in balance. Nevertheless, Toole et al. (46) noticed an encouraging improvement on SOT, but not on the Berg Balance Scale. Cakit et al. (47) and Hackney et al. (48) showed an improvement in BBS in incremental speed-dependent treadmill training and progressive Tango lessons, respectively.
Caglar et al. using a home-based exercise (49) and Tamir et al. using a physiotherapy technique plus imagery (50) found the same findings and reported the efficient role of corrective exercise on TUG.
Acknowledgments
The authors would like to thank academic members of Kish International Campus of Tehran University and the authorities of Shahid Beheshti Hospital of Kashan for their kind cooperation during the project.
Footnotes
Authors’ Contribution:Hassan Daneshmandi, supervised the project. Noureddin Karimi and Amir-Hossein Barati, provided the advisory supervision. Parisa Sedaghati, performed the project, statistical analysis and prepared the first draft.
References
- 1.Blake AJ, Morgan K, Bendall MJ, Dallosso H, Ebrahim SB, Arie TH, et al. Falls by elderly people at home: prevalence and associated factors. Age Ageing. 1988;17(6):365–72. doi: 10.1093/ageing/17.6.365. [DOI] [PubMed] [Google Scholar]
- 2.Wood BH, Bilclough JA, Bowron A, Walker RW. Incidence and prediction of falls in Parkinson's disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry. 2002;72(6):721–5. doi: 10.1136/jnnp.72.6.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Temlett JA, Thompson PD. Reasons for admission to hospital for Parkinson's disease. Intern Med J. 2006;36(8):524–6. doi: 10.1111/j.1445-5994.2006.01123.x. [DOI] [PubMed] [Google Scholar]
- 4.Pressley JC, Louis ED, Tang MX, Cote L, Cohen PD, Glied S, et al. The impact of comorbid disease and injuries on resource use and expenditures in parkinsonism. Neurology. 2003;60(1):87–93. doi: 10.1212/wnl.60.1.87. [DOI] [PubMed] [Google Scholar]
- 5.Adkin AL, Frank JS, Jog MS. Fear of falling and postural control in Parkinson's disease. Mov Disord. 2003;18(5):496–502. doi: 10.1002/mds.10396. [DOI] [PubMed] [Google Scholar]
- 6.Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH. Prospective assessment of falls in Parkinson's disease. J Neurol. 2001;248(11):950–8. doi: 10.1007/s004150170047. [DOI] [PubMed] [Google Scholar]
- 7.Franchignoni F, Martignoni E, Ferriero G, Pasetti C. Balance and fear of falling in Parkinson's disease. Parkinsonism Relat Disord. 2005;11(7):427–33. doi: 10.1016/j.parkreldis.2005.05.005. [DOI] [PubMed] [Google Scholar]
- 8.Davey C, Wiles R, Ashburn A, Murphy C. Falling in Parkinson's disease: the impact on informal caregivers. Disabil Rehabil. 2004;26(23):1360–6. doi: 10.1080/09638280400000195. [DOI] [PubMed] [Google Scholar]
- 9.Schrag A, Hovris A, Morley D, Quinn N, Jahanshahi M. Caregiver-burden in parkinson's disease is closely associated with psychiatric symptoms, falls, and disability. Parkinsonism Relat Disord. 2006;12(1):35–41. doi: 10.1016/j.parkreldis.2005.06.011. [DOI] [PubMed] [Google Scholar]
- 10.Dorsey ER, Constantinescu R, Thompson JP, Biglan KM, Holloway RG, Kieburtz K, et al. Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology. 2007;68(5):384–6. doi: 10.1212/01.wnl.0000247740.47667.03. [DOI] [PubMed] [Google Scholar]
- 11.Grimbergen YA, Munneke M, Bloem BR. Falls in Parkinson's disease. Curr Opin Neurol. 2004;17(4):405–15. doi: 10.1097/01.wco.0000137530.68867.93. [DOI] [PubMed] [Google Scholar]
- 12.Ashburn A, Fazakarley L, Ballinger C, Pickering R, McLellan LD, Fitton C. A randomised controlled trial of a home based exercise programme to reduce the risk of falling among people with Parkinson's disease. J Neurol Neurosurg Psychiatry. 2007;78(7):678–84. doi: 10.1136/jnnp.2006.099333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Protas EJ, Mitchell K, Williams A, Qureshy H, Caroline K, Lai EC. Gait and step training to reduce falls in Parkinson's disease. NeuroRehabilitation. 2005;20(3):183–90. [PubMed] [Google Scholar]
- 14.Sherrington C, Whitney JC, Lord SR, Herbert RD, Cumming RG, Close JC. Effective exercise for the prevention of falls: a systematic review and meta-analysis. J Am Geriatr Soc. 2008;56(12):2234–43. doi: 10.1111/j.1532-5415.2008.02014.x. [DOI] [PubMed] [Google Scholar]
- 15.Robertson MC, Campbell AJ, Gardner MM, Devlin N. Preventing injuries in older people by preventing falls: a meta-analysis of individual-level data. J Am Geriatr Soc. 2002;50(5):905–11. doi: 10.1046/j.1532-5415.2002.50218.x. [DOI] [PubMed] [Google Scholar]
- 16.Latt MD, Lord SR, Morris JG, Fung VS. Clinical and physiological assessments for elucidating falls risk in Parkinson's disease. Mov Disord. 2009;24(9):1280–9. doi: 10.1002/mds.22561. [DOI] [PubMed] [Google Scholar]
- 17.Hirsch MA, Toole T, Maitland CG, Rider RA. The effects of balance training and high-intensity resistance training on persons with idiopathic Parkinson's disease. Arch Phys Med Rehabil. 2003;84(8):1109–17. doi: 10.1016/s0003-9993(03)00046-7. [DOI] [PubMed] [Google Scholar]
- 18.Dibble LE, Hale TF, Marcus RL, Droge J, Gerber JP, LaStayo PC. High-intensity resistance training amplifies muscle hypertrophy and functional gains in persons with Parkinson's disease. Mov Disord. 2006;21(9):1444–52. doi: 10.1002/mds.20997. [DOI] [PubMed] [Google Scholar]
- 19.Nieuwboer A, Kwakkel G, Rochester L, Jones D, van Wegen E, Willems AM, et al. Cueing training in the home improves gait-related mobility in Parkinson's disease: the RESCUE trial. J Neurol Neurosurg Psychiatry. 2007;78(2):134–40. doi: 10.1136/jnnp.200X.097923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Morris ME, Iansek R, Kirkwood B. A randomized controlled trial of movement strategies compared with exercise for people with Parkinson's disease. Mov Disord. 2009;24(1):64–71. doi: 10.1002/mds.22295. [DOI] [PubMed] [Google Scholar]
- 21.Dibble LE, Addison O, Papa E. The effects of exercise on balance in persons with Parkinson's disease: a systematic review across the disability spectrum. J Neurol Phys Ther. 2009;33(1):14–26. doi: 10.1097/NPT.0b013e3181990fcc. [DOI] [PubMed] [Google Scholar]
- 22.Latt MD. "Why do people with ParkinsonPD's disease fall? Sydney: Sydney; 2006. [Google Scholar]
- 23.Robertson G, Caldwell G, Hamill J, Kamen G, Whittlesey S. Research Methods in Biomechanics. 2 ed. Champaign: Human Kinetics; 2013. [Google Scholar]
- 24.Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. 1967. Neurology. 2001;57(10 Suppl 3):S11–26. [PubMed] [Google Scholar]
- 25.Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189–98. doi: 10.1016/0022-3956(75)90026-6. [DOI] [PubMed] [Google Scholar]
- 26.Yardley L, Beyer N, Hauer K, Kempen G, Piot-Ziegler C, Todd C. Development and initial validation of the Falls Efficacy Scale-International (FES-I). Age Ageing. 2005;34(6):614–9. doi: 10.1093/ageing/afi196. [DOI] [PubMed] [Google Scholar]
- 27.Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: validation of an instrument. Can J Public Health. 1992;83 Suppl 2:S7–11. [PubMed] [Google Scholar]
- 28.Brusse KJ, Zimdars S, Zalewski KR, Steffen TM. Testing functional performance in people with Parkinson disease. Phys Ther. 2005;85(2):134–41. [PubMed] [Google Scholar]
- 29.Lim LI, van Wegen EE, de Goede CJ, Jones D, Rochester L, Hetherington V, et al. Measuring gait and gait-related activities in Parkinson's patients own home environment: a reliability, responsiveness and feasibility study. Parkinsonism Relat Disord. 2005;11(1):19–24. doi: 10.1016/j.parkreldis.2004.06.003. [DOI] [PubMed] [Google Scholar]
- 30.Morris S, Morris ME, Iansek R. Reliability of measurements obtained with the Timed "Up & Go" test in people with Parkinson disease. Phys Ther. 2001;81(2):810–8. doi: 10.1093/ptj/81.2.810. [DOI] [PubMed] [Google Scholar]
- 31.ParkinsonPD Society Canada. Exercises for people with ParkinsonPD. 1965. Available from: http://www.parkinsonPD.ca/atf/cf/%7B9ebd08a9-7886-4b2d-a1c4- a131e7096bf8%7D/ http://www.parkinsonPD.ca/atf/cf/%7B9ebd08a9-7886-4b2d-a1c4.
- 32.Vancouver Coastal Health Seniors. Fall and Injury Prevention Initiative, STAY ON YOUR FEET. 2010. Available from: http://fallprevention.vch.ca/media/SOYF_8.5x11_Book_v5.pdf.
- 33.Van der Schyf CJ, Geldenhuys WJ. Multimodal drugs and their future for Alzheimer's and Parkinson's disease. Int Rev Neurobiol. 2011;100:107–25. doi: 10.1016/B978-0-12-386467-3.00006-6. [DOI] [PubMed] [Google Scholar]
- 34.Pickering RM, Grimbergen YA, Rigney U, Ashburn A, Mazibrada G, Wood B, et al. A meta-analysis of six prospective studies of falling in Parkinson's disease. Mov Disord. 2007;22(13):1892–900. doi: 10.1002/mds.21598. [DOI] [PubMed] [Google Scholar]
- 35.Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG. The Sydney multicenter study of Parkinson's disease: the inevitability of dementia at 20 years. Mov Disord. 2008;23(6):837–44. doi: 10.1002/mds.21956. [DOI] [PubMed] [Google Scholar]
- 36.Melton LJ, Leibson CL, Achenbach SJ, Bower JH, Maraganore DM, Oberg AL, et al. Fracture risk after the diagnosis of Parkinson's disease: Influence of concomitant dementia. Mov Disord. 2006;21(9):1361–7. doi: 10.1002/mds.20946. [DOI] [PubMed] [Google Scholar]
- 37.Alizadeh R, Mehrabi S, Hadjighassem M, Alizadeh. Cell Therapy in Parkinson's Disease. Archives Neuroscience. 2013;1(2):43–50. doi: 10.5812/archneurosci.10279. [DOI] [Google Scholar]
- 38.Invernizzi M, Carda S, Viscontini GS, Cisari C. Osteoporosis in Parkinson's disease. Parkinsonism Relat Disord. 2009;15(5):339–46. doi: 10.1016/j.parkreldis.2009.02.009. [DOI] [PubMed] [Google Scholar]
- 39.Gillespie LD, Gillespie WJ, Robertson MC, Lamb SE, Cumming RG, Rowe BH. WITHDRAWN: Interventions for preventing falls in elderly people. Cochrane Database Syst Rev. 2009;(2):CD000340. doi: 10.1002/14651858.CD000340.pub2. [DOI] [PubMed] [Google Scholar]
- 40.Canning CG, Ada L, Johnson JJ, McWhirter S. Walking capacity in mild to moderate Parkinson's disease. Arch Phys Med Rehabil. 2006;87(3):371–5. doi: 10.1016/j.apmr.2005.11.021. [DOI] [PubMed] [Google Scholar]
- 41.Paasuke M, Ereline J, Gapeyeva H, Joost K, Mottus K, Taba P. Leg-extension strength and chair-rise performance in elderly women with Parkinson's disease. J Aging Phys Act. 2004;12(4):511–24. doi: 10.1123/japa.12.4.511. [DOI] [PubMed] [Google Scholar]
- 42.Bloem BR, van Vugt JP, Beckley DJ. Postural instability and falls in Parkinson's disease. Adv Neurol. 2001;87:209–23. [PubMed] [Google Scholar]
- 43.Murphy SL, Williams CS, Gill TM. Characteristics associated with fear of falling and activity restriction in community-living older persons. J Am Geriatr Soc. 2002;50(3):516–20. doi: 10.1046/j.1532-5415.2002.50119.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Schenkman M, Cutson TM, Kuchibhatla M, Chandler J, Pieper CF, Ray L, et al. Exercise to improve spinal flexibility and function for people with Parkinson's disease: a randomized, controlled trial. J Am Geriatr Soc. 1998;46(10):1207–16. doi: 10.1111/j.1532-5415.1998.tb04535.x. [DOI] [PubMed] [Google Scholar]
- 45.Toole T, Hirsch MA, Forkink A, Lehman DA, Maitland CG. The effects of a balance and strength training program on equilibrium in Parkinsonism: A preliminary study. NeuroRehabilitation. 2000;14(3):165–74. [PubMed] [Google Scholar]
- 46.Toole T, Maitland CG, Warren E, Hubmann MF, Panton L. The effects of loading and unloading treadmill walking on balance, gait, fall risk, and daily function in Parkinsonism. NeuroRehabilitation. 2005;20(4):307–22. [PubMed] [Google Scholar]
- 47.Cakit BD, Saracoglu M, Genc H, Erdem HR, Inan L. The effects of incremental speed-dependent treadmill training on postural instability and fear of falling in Parkinson's disease. Clin Rehabil. 2007;21(8):698–705. doi: 10.1177/0269215507077269. [DOI] [PubMed] [Google Scholar]
- 48.Hackney ME, Kantorovich S, Levin R, Earhart GM. Effects of tango on functional mobility in Parkinson's disease: a preliminary study. J Neurol Phys Ther. 2007;31(4):173–9. doi: 10.1097/NPT.0b013e31815ce78b. [DOI] [PubMed] [Google Scholar]
- 49.Caglar AT, Gurses HN, Mutluay FK, Kiziltan G. Effects of home exercises on motor performance in patients with Parkinson's disease. Clin Rehabil. 2005;19(8):870–7. doi: 10.1191/0269215505cr924oa. [DOI] [PubMed] [Google Scholar]
- 50.Tamir R, Dickstein R, Huberman M. Integration of motor imagery and physical practice in group treatment applied to subjects with Parkinson's disease. Neurorehabil Neural Repair. 2007;21(1):68–75. doi: 10.1177/1545968306292608. [DOI] [PubMed] [Google Scholar]