- freely available
Brain. Sci. 2013, 3(1), 87-100; doi:10.3390/brainsci3010087
Abstract: Parkinson’s disease (PD) is a neurological disorder that is manifested in the form of both motor and non-motor symptoms such as resting tremor, bradykinesia, muscular rigidity, depression, and cognitive impairment. PD is progressive in nature, ultimately leading to debilitating disruption of activities of daily living. Recently, a myriad of research has been focused on non-pharmacological interventions to alleviate the motor and non-motor symptoms of the disease. However, while there is a growing body of evidence supporting exercise as a viable therapy option for the treatment of Parkinson’s disease, there is a lack of literature enumerating a specific exercise sequence for patients with PD. In this literature review, we analyze the success of specific modalities of exercise in order to suggest an optimal exercise regimen for Parkinson’s disease patients.
Parkinson’s Disease (PD) is a debilitating illness affecting between 4.1 and 4.6 million individuals over the age of 50 , making it the second most common neurodegenerative disorder after Alzheimer’s disease. The initial clinical signs appear after the degeneration of about 60% of the dopaminergic neurons of the substantia nigra , resulting in motor dysfunction that manifests with a tetrad of primary symptoms—resting tremors, bradykinesia, muscular rigidity and postural instability. Research has suggested that non-motor symptoms, such as constipation, olfactory dysfunction and depression, also occur, and may precede motor dysfunction by several years . Progressive in nature, PD tends to worsen with time, leading to a general decrease in activity , an increased risk of falling, immobility, and cognitive impairment .
Many aspects of patient’s lives are affected by this progressive disease; over three-quarters of patients complain of difficultly walking, rising from chairs, clumsy movements, a lack of energy and the need to expend extra physical effort to accomplish daily tasks . As such, there is a considerable benefit to identifying supplemental therapies that, in conjunction with pharmacologic and surgical treatments, may increase patient strength and endurance.
History of the Role of Exercise in Parkinson’s
The benefits of exercise in PD have not always been well characterized. Despite the American Academy of Neurology encouraging the use of exercise as an adjunctive therapy for Parkinson’s patients in the 1990s , systemic reviews from the Cochrane collaboration released in 2001 found insufficient evidence to support or refute the efficacy of physiotherapy in PD [8,9]. Although most of the individual trials analyzed in these reviews appeared to find a beneficial effect of physiotherapy, it was determined that many of the studies had methodological flaws and biases that prevented any firm conclusions of the validity of physiotherapy . Interestingly, this led to a situation in which physicians were instructed to encourage regular exercise, despite little evidence of its efficacy in slowing disease progression or improving activities of daily living .
However, more recent studies suggest that there are indeed benefits of physical activity in PD patients. A recent meta-analysis supported exercise as being beneficial with regards to physical functioning, health-related quality of life, strength, balance, and gait speed for PD patients . A large study following 438 PD patients found after four years, that mortality was lower for regularly exercising patients, even for those who could not walk independently . Despite affirming the benefits of exercise, there is little consensus of dosages and types of exercise needed to target the wide range of symptoms that present with PD. This review attempts to highlight the potential benefits of cardiovascular, balance, and resistance training while extracting the most efficacious exercise strategies to mitigate the bradykinesia, muscle weakness, and balance impairment experienced by PD patients.
Furthermore, to apply these findings in a clinical setting to improve the quality of life for Parkinson’s disease patients (taking into account the importance of empowering patients with PD to self-manage their disease to some extent ), we have used the existing literature to develop a high-yield exercise regimen designed to maximize balance, coordination and functional strength for patients with mild to moderate disease. We focus on exercises that can readily be translated into a home-based program, noting that a Cochrane review found older adults are more likely to adhere to home-based programs than center-based programs . Acknowledging that there is no “one size fits all” exercise prescription for such a variable and progressive disease, we advocate this regimen not as a universally applicable exercise plan, but rather as a template to be modified by physicians and physiotherapists to best suit the needs of patients.
2. Exercise in Parkinson’s Disease
2.1. Exercise and Risk of Disease
Exercise appears to have a neuroprotective effect against developing PD. Prospective cohort studies have found that men [15,16,17] and women [16,17] who partake in moderate [16,17] and strenuous [15,16,17] (but not light [16,17]) exercise (including swimming, tennis, basketball, cycling and running) appear to have a significantly decreased incidence in developing PD, although this is not a universal finding . Interestingly, higher levels of activity during 35–39 years of age—decades before the average age of onset of the disease—significantly reduces risk of acquiring the disease . Evidence from animal models support these suggested neuroprotective effects of exercise against developing PD, highlighting the influence of exercise on neuroplasticity and self-repair [19,20].
While the underlying mechanisms for these potential neuroprotective effects are unclear, elevated plasma uric acid levels, seen in vigorous (but not light) exercise , is hypothesized to play a role in the decreased risk and slower progression of the disease (for reviews, see [22,23,24]). It should be noted that these findings could be due to reverse causality—i.e., preclinical PD may lead to a reduction in activity, rather than a reduction in activity leading to an increased risk for the disease. However, this appears unlikely, as animal models suggest decreased physical activity is not a symptom of the disease itself  and human studies have found no noticeable decrease in activity before diagnosis . However, while the benefits of exercise for PD patients have become more widely accepted recently, the most effective exercise sequence has yet to be elucidated.
2.2. Cardiovascular Training for Parkinson’s Patients
Cardiovascular training, as defined as a routine that increases heart rate and oxygen demand, appears to have direct benefits for Parkinson’s patients in a dose-dependent fashion . Interestingly, some of these benefits are evident nearly immediately. After a single session of either speed-dependent treadmill training or limited-progressive treadmill training, patients show improved gait parameters compared to controls and those given only conventional gait training . Similarly, a single session of a high intensity cardiovascular exercise intervention, in the form of assisted cycling, showed reductions in tremor and bradykinesia without excessive fatigue in PD patients . Weeks of treadmill training showed enhanced balance, gait, and improved quality of life [29,30], with the benefits persisting for four weeks . One case study has reported that eight weeks of aerobic exercise improved language and cognition in a PD patient who already had high performance scores in cognitive measures at baseline . In a recent randomized clinical trial, 121 patients with mild to moderate PD who underwent 16 weeks of aerobic endurance exercise (utilizing a treadmill, bicycle, or elliptical trainer) improved overall function, balance, and movement efficiency . Importantly, compared with alternative exercise modalities, this study further suggested aerobic endurance was the most beneficial for walking economy. Case studies of patients (Hoehn and Yahr, H & Y, stages 2–2.5) who underwent still longer training (4 months of cardiovascular training regimens supplemented with an additional 12 months of home exercise) have reported sustained increases in UPDRS, functional performance, and economy of movement during the entire course of training . Coupled with the findings that sedentary, but otherwise healthy adults do not typically increase walking economy with endurance training [34,35], these results suggest that Parkinson’s patients do not simply benefit from exercise to the same extent as healthy individuals , but may gain advantages from exercise above and beyond those available to the general population.
While there is a limited amount of randomized controlled studies confirming the long term benefits of cardiovascular training in PD patients, there is a growing body of data suggesting that this is the case. Patients with mild to moderate PD progression (H & Y stage 1–3) who underwent high intensity treadmill training showed changes in brain plasticity, namely a lengthening of the cortical silent period , a measure of corticomotor excitability typically shortened in Parkinson’s patients . Patients that perform cardiovascular exercise also have an increased longevity in mortality studies , further implicating the existence of long term benefits.
Less conventional therapies, such as body weight-supported treadmill training, have also been attempted in patients with mild to moderate PD (H & Y stages 1–3), and have led to a greater improvement in ambulation speed, number of steps, and short-step gait compared to conventional physical therapy [38,39], with the benefits lasting for about four months . However, the precise differences between treadmill trainings have been difficult to fully assess, as a study attempting to identify the differences between assisted weight bearing, additional weight bearing, and conventional treadmill training in patients (H & Y stages 1–7) found improvements to balance, UPDRS, and gait regardless of the specific type of treadmill training utilized .
2.3. Balance Training for Parkinson’s Patients
Postural instability and balance impairments are common symptoms of PD , contributing to an increased frequency of falls and injuries  which in turn increases morbidity and mortality . The large impact of postural instability on patients is a significant concern, especially considering that dopamine replacement medications are often insufficient to control these deficits .
There have been a number of studies examining the best types of training to improve balance and mitigate falls. Patients who participate in balance training have shown improvements in gait and ambulation . Results from 10 weeks of balance and strength training indicated improvement in equilibrium by two distinct mechanisms: (1) training altered the ability to control the motor system when vestibular cues had to be the primary source of reliable feedback; (2) training helped subjects to override faulty proprioceptive feedback and utilize reliable visual or vestibular cues. A larger study indicated that patients participating in balance training, compared to general physical exercises, showed improvements as determined by the Berg Balance Scale, Activities-based Balance Scale, postural transfer test, and number of falls . Furthermore, these improvements were maintained one month post-treatment.
A meta-analysis found moderate evidence that physical activity and exercise will result in improvements in postural instability and balance task performance, although there was limited evidence to support an improvement in quality of life and falls outcomes in patients with mild to moderate PD . Similarly, another meta-analysis found multifaceted training improved balance-related activity performance, but notes that there was no evidence that the number of falls were impacted . The report also suggests that the inclusion of highly challenging balance training may improve the efficacy of intervention on balance-related activity performance. To significantly address falling, balance training may need to be supplemented with resistance training—a small study suggested that the combination of balance and resistance training improved the balance scores of PD patients significantly more than did balance training alone .
Similar to the limitations of the studies examining the benefits of cardiovascular exercise, the long term effects of balance training is unclear. However, given the progressive nature of PD, it is likely that to maintain efficacy, the balance training would need to be ongoing. Allen et al. (2011)  alludes to the problematic nature this situation, noting the difficulty of sustainably maintaining a challenging training regimen in a home-based program. However, other studies have suggested a number of readily accessible and relatively inexpensive options by which patients can reduce balance impairments at home. These include the use of commercially available motion controlled video games , which could theoretically allow for a home-based, yet monitorable, form of training.
Another suggested option is Tai Chi . In healthy patients, Tai Chi has been shown to be more effective in preventing falls in elderly patients compared to conventional physical therapy . In patients with mild to moderate PD, Tai Chi training appears to improve physical function  and reduce balance impairments in patients . A large randomized clinical trial investigating the impact of a 24 week Tai Chi class, compared to resistance training or low-intensity stretching found that the Tai Chi significantly improved maximum excursion, directional control, gait and strength measures, and is the only large scale trial to demonstrate a significant reduction in falls as a result of exercise . Overall, this suggests that in mild to moderate PD, Tai Chi is more effective than stretching or resistance-training in improving postural stability.
2.4. Resistance Training for Parkinson’s Patients
There is a strong body of evidence that suggests PD not only leads to motor dysfunction, but also adversely affects muscle strength (for review, see ). Studies have demonstrated that Parkinson’s patients have decreased isokinetic muscle strength affecting a number of muscle groups, most notably the flexors and extensors of the hip, knee, and wrist [56,57,58,59,60,61]. Furthermore, numerous studies have suggested Parkinson’s patients demonstrate altered isometric ability in the hands [31,62,63,64,65,66] and core muscles , including longer times to reach peak torque and contraction, lower rates of force development, and irregular force-time curves, although it should be noted that these are not universal findings [57,68]. While the complete mechanism for this weakness is not fully understood, it likely involves decreased activation of motor neurons due to inadequate basal ganglia stimulation of cortical motor centers, as well as incomplete contractions from action tremors caused by the rhythmic and synchronous discharging of motor units during voluntary activity in Parkinson’s patients . Importantly, studies have suggested that muscle weakness is likely inherent to PD and not merely a secondary consequence of aging or inactivity . Coupled with the finding that healthy older adults already expend close to maximal force production capabilities to navigate stairs and rise from chairs , the burden of PD on ADLs from muscle weakness cannot be understated.
To mitigate these strength deficits, resistance training is an accessible modality of exercise for PD patients. A number of small studies have shown improvements in muscle strength [49,72,73,74], muscular endurance [73,75], neuromuscular function [73,75], muscle force production , as well as gait speed and initiation  as well as chair rise function . All of these improvements impact functional mobility. Interestingly, studies have even suggested that patients with mild-to-moderate PD can obtain increases in strength similar to that of normal adults of the same age in a resistance training program .
Resistance training emphasizing both eccentric muscle contractions, which enable high muscle forces with low metabolic requirements , and concentric contractions has been shown to improve muscle hypertrophy, strength, and mobility in persons with PD . A clinical trial measuring the impact of high-force eccentric resistance training on muscle volume, muscle force, and functional status showed improvements in persons with PD, with the eccentric trial group showing significantly improved scores for muscle structure, stair descent, and 6 min walk than those in a standard care group .
There is a limited amount of research determining the volume of such training necessary to yield optimal results, however it is generally agreed that the most advantageous volume of exercise should maximize intensity while minimizing fatigue . Small trials have suggested that in healthy older patients, three sets of strength and endurance training for selected exercises result in greater gains that single sets . More research on the optimal volume is needed for PD patients, as many of the current studies evaluating resistance training in PD employ a single set regimen. Notably, a pilot study measuring the impact of moderate volume (3 sets of 3 exercises), high load weight training on PD patients showed significant strength increases compared to baseline and was well tolerated by participants . This finding suggests a moderate volume of high intensity exercise may be beneficial and manageable for people with PD. However, this notion has been contested. Schenkman et al. . compared home-based exercise to more intensive endurance and balance exercise programs. Initially, the two more intensive regimens yielded higher overall functional gains. However, in the long term, all three programs improved overall function. This finding suggests there is a greater importance in maintaining consistently high levels of physical activity than performing a specific regimen of sets and repetitions.
2.5. LSVT BIG™
Lee Silverman Voice Treatment (LSVT) BIG™, which differs from other forms of physical therapy for PD by focusing on movement amplitude as the sole treatment parameter through high-effort training , is a form of PD therapy growing in popularity in the PD patient community. Given the programs rapid expansion, a brief discussion of the program is warranted, as physicians will likely encounter questions about the benefits of the program from patients. The goal of LSVT BIG™ is to overcome deficient speed-amplitude regulation leading to underscaling of movement amplitude at any given velocity. Continuous feedback on motor performance and training of movement perception is used to counteract reduced gain in motor activities resulting from disturbed sensorimotor processing .
In a noncontrolled study assessing effects of LSVT BIG™ in individuals with PD, after four weeks of training, subjects demonstrated a modest (12%–14%) increase in velocity of walking and reaching movements . In a rater-blinded Berlin study, LSVT BIG™ was found to be more effective than Nordic walking, a type of fitness walking that forces the patient to utilize upper and lower body muscles simultaneously, when delivered as group training . The beneficial outcome was reflected by improvements in assessments including the UPDRS motor score, standard time-up and go task and 10 m walk . Overall, while these results appear promising, these authors express concern about advocating this program for patients until more literature is available.
As suggested above, specific modalities of exercise such as cardiovascular training, resistance training, and balance training are able to relieve patients of debilitating motor and non-motor symptoms and allow for increased functional ability to complete ADLs. The most beneficial exercise regimen likely combines these three modes of exercise to reduce both motor and non-motor symptoms.
Utilizing the evidence available enumerated, we have formulated an exercise regimen tailored to treat the specific symptoms of PD:
(1) Cardiovascular exercise such as high intensity treadmill training or assisted cycling has been shown to reduce bradykinesia as well as improve gait function and ambulation [28,29,30]. Based on these data, and given the lack of evidence suggesting differences between various types of cardiovascular training, we recommend moderate to high intensity cardiovascular exercise in the form of treadmill training or assisted cycling for up to 30 min per session every other day.
(2) To increase muscle strength, we recommend moderate volume (3 sets each) high load resistance training 2–3 times per week. It has been suggested that this volume and modality may optimally increase muscle strength without causing excessive fatigue [75,79]. While both concentric contractions and eccentric contractions to will increase strength gains, we recommend an emphasis on eccentric movements to minimize metabolic demand.
(3) Balance training in the form of Tai Chi should be used to improve postural control and walking ability. A large-scale trial demonstrated that patients performing Tai Chi show improvements in maximum excursion and directional control that were not seen in balance training or strength training . Given that patients can complete Tai Chi at home without the use of clinical equipment, coupled with the benefits to balance and postural control that were not observed with traditional balance training alone, we recommend Tai Chi for 1 h at least twice weekly.
(4) Given the limited number of clinical trials measuring the efficacy of LSVT BIG™, we express caution in recommending LSVT BIG™ as a supplemental therapy at the current time.
(5) For patients who present with a more advanced stage of PD or cannot adhere to an intensive exercise regimen at home, we recommend physical therapy sessions with a licensed Physical Therapist specialized in PD rehabilitation.
In a clinical setting, patients who undergo physical therapy consisting on strength exercises, balance and gait training in addition to medication therapy show short and long term increases in quality of life, mobility, walking speed, and activities of daily living (ADLs) compared to patients who only receive medication . Physical therapy appears to bestow short term gains for patients which persist for weeks after training, and while cessation of structured therapy sessions lead to a return to baseline strength within months , the benefits to walking speed, activities of daily living, and the Unified Parkinson’s Disease Rating Scale continue to persist . Similar goals should be expected for home-based programs. While there has been some success in employing home-exercise regimen consisting of muscle strengthening, balance exercises, and cardiovascular training to lower rates of falling , more research is needed to determine whether other home-based programs can mirror this success.
Notably, many of the studies referenced in this review were of short duration, highly supervised, facility based, and included a limited amount of participants with mild to moderate disease severity, all of which attest to a need to further research. Since PD is a long-term degenerative disorder, studies with longer durations are essential to evaluate how long a patient should be encouraged to continue on an exercise regimen. Highly supervised programs, such as nearly all of the referenced trials, are less likely to give information about effectiveness of the intervention when put into clinical practice [87,88]. Larger randomized controlled studies are needed to confirm many of the findings highlighted in this review, and to determine whether the exercise regimen presented herein is an appropriate guideline for patients with increased disease severity.
Conflict of Interest
The authors declare no conflict of interest.
- Dorsey, E.R.; Constantinescu, R.; Thompson, J.P.; Biglan, K.M.; Holloway, R.G.; Kieburtz, K.; Marshall, F.J.; Ravina, B.M.; Schifitto, G.; Siderowf, A.; Tanner, C.M. Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 2007, 68, 384–386. [Google Scholar] [CrossRef]
- Hornykiewicz, O. The discovery of dopamine deficiency in the parkinsonian brain. J. Neural Transm. Suppl. 2006, 70, 9–15. [Google Scholar] [CrossRef]
- Tolosa, E.; Pont-Sunyer, C. Progress in defining the premotor phase of Parkinson’s disease. J. Neurol. Sci. 2011, 310, 4–8. [Google Scholar] [CrossRef]
- Fertl, E.; Doppelbauer, A.; Auff, E. Physical activity and sports in patients suffering from Parkinson’s disease in comparison with healthy seniors. J. Neural Transm. Park. Dis. Dement. Sect. 1993, 5, 157–161. [Google Scholar] [CrossRef]
- Leroi, L.; Pantula, H.; McDonald, K.; Harbishettar, V. Neuropsychiatric symptoms in Parkinson’s disease with mild cognitive impairments and dementia. Park. Dis. 2012, 2012. [Google Scholar] [CrossRef]
- Brod, M.; Mendelsohn, G.A.; Roberts, B. Patients’ experiences of Parkinson’s disease. J. Gerontol. B Psychol. Sci. Soc. Sci. 1998, 53, 213–222. [Google Scholar]
- Koller, W.C.; Silver, D.E.; Lieberman, A. An algorithm for the management of Parkinson’s disease. Neurology 1994, 44, S1–S52. [Google Scholar] [CrossRef]
- Deane, K.H.; Jones, D.; Playford, E.D.; Ben-Shlomo, Y.; Clarke, C.E. Physiotherapy for patients with Parkinson’s Disease: A comparison of techniques. Cochrane Database Syst. Rev. 2001. [Google Scholar] [CrossRef]
- Deane, K.H.; Jones, D.; Ellis-Hill, C.; Clarke, C.E.; Playford, E.D.; Ben-Shlomo, Y. A comparison of physiotherapy techniques for patients with Parkinson’s disease. Cochrane Database Syst. Rev. 2001. [Google Scholar] [CrossRef]
- Nutt, J.G.; Wooten, G.F. Diagnosis and initial management of Parkinson’s disease. N. Engl. J. Med. 2005, 353, 1021–1027. [Google Scholar] [CrossRef]
- Goodwin, V.A.; Richards, S.H.; Taylor, R.S.; Taylor, A.H.; Campbell, J.L. The effectiveness of exercise interventions for people with Parkinson’s disease: A systematic review and meta-analysis. Mov. Disord. 2008, 23, 631–640. [Google Scholar] [CrossRef]
- Kuroda, K.; Tatara, K.; Takatorige, T.; Shinsho, F. Effect of physical exercise on mortality in patients with Parkinson’s disease. Acta Neurol. Scand. 1992, 86, 55–59. [Google Scholar]
- Allen, N.E.; Sherrington, C.; Suriyarachchi, G.D.; Paul, S.S.; Song, J.; Canning, C.G. Exercise and motor training in people with Parkinson’s disease: A systematic review of participant characteristics, intervention delivery, retention rates, adherence, and adverse events in clinical trials. Parkinsons Dis. 2012, 2012. [Google Scholar] [CrossRef]
- Ashworth, N.L.; Chad, K.E.; Harrison, E.L.; Reeder, B.A.; Marshall, S.C. Home versus center based physical activity programs in older adults. Cochrane Database Syst. Rev. 2005. [Google Scholar] [CrossRef]
- Chen, H.; Zhang, S.M.; Schwarzschild, M.A.; Hernán, M.A.; Ascherio, A. Physical activity and the risk of Parkinson disease. Neurology 2005, 64, 664–669. [Google Scholar] [CrossRef]
- Thacker, E.L.; Chen, H.; Patel, A.V.; McCullough, M.L.; Calle, E.E.; Thun, M.J.; Schwarzchild, M.A.; Ascherio, A. Recreational physical activity and risk of Parkinson’s disease. Mov. Disord. 2008, 23, 69–74. [Google Scholar] [CrossRef]
- Xu, Q.; Park, Y.; Huang, X.; Hollenbeck, A.; Blair, A.; Schatzkin, A.; Chen, H. Physical activities and future risk of Parkinson disease. Neurology 2010, 75, 341–348. [Google Scholar] [CrossRef]
- Logroscino, G.; Sesso, H.D.; Paffenbarger, R.S., Jr.; Lee, I.M. Physical activity and risk of Parkinson’s disease: A prospective cohort study. J. Neurol. Neurosurg. Psychiatr. 2006, 77, 1318–1322. [Google Scholar] [CrossRef]
- Smith, A.D.; Zigmond, M.J. Can the brain be protected through exercise? Lessons from animal model of Parkinsonism. Exp. Neurol. 2003, 184, 31–39. [Google Scholar] [CrossRef]
- Faherty, C.J.; Sheperd, K.R.; Herasimtschuk, A.; Smeyne, R.J. Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res. Mol. Brain Res. 2005, 134, 170–179. [Google Scholar]
- Green, H.J.; Fraser, I.G. Differential effects of exercise intensity on serum uric acid concentration. Med. Sci. Sports Exerc. 1988, 20, 55–59. [Google Scholar] [CrossRef]
- Constantinescu, R.; Zetterberg, H. Urate as a marker of development and progression in Parkinson’s disease. Drugs Today 2011, 47, 369–380. [Google Scholar]
- Cipriani, S.; Chen, X.; Schwarzschild, M.A. Urate: A novel biomarker of Parkinson’s disease risk, diagnosis and prognosis. Biomark. Med. 2010, 4, 701–712. [Google Scholar]
- Schlesinger, I.; Schlesinger, N. Uric acid in Parkinson’s disease. Mov. Disord. 2008, 23, 1653–1657. [Google Scholar] [CrossRef]
- Tillerson, J.L.; Cohen, A.D.; Caudle, W.M.; Zigmond, M.J.; Schallert, T.; Miller, G.W. Forced nonuse in unilateral parkinsonian rats exacerbates injury. J. Neurosci. 2002, 22, 6790–6799. [Google Scholar]
- Fisher, B.E.; Wu, A.D.; Salem, G.J.; Song, J.; Lin, C.H.; Yip, J.; Cen, S.; Gordon, J.; Jakowec, M.; Petzinger, G. The effect of exercise training in improving motor performance and corticomotor excitability in people with early Parkinson’s disease. Arch. Phys. Med. Rehabil. 2008, 89, 1221–1229. [Google Scholar] [CrossRef]
- Pohl, M.; Rockstroh, G.; Rückriem, S.; Mrass, G.; Mehrholz, J. Immediate effects of speed-dependent treadmill training on gait parameters in early Parkinson’s disease. Arch. Phys. Med. Rehabil. 2003, 84, 1760–1766. [Google Scholar] [CrossRef]
- Ridgel, A.L.; Peacock, C.A.; Fickes, E.J.; Kim, C.H. Active-assisted cycling improves tremor and bradykinesia in Parkinson’s disease. Arch. Phys. Med. Rehabil. 2012, 93, 2049–2054. [Google Scholar] [CrossRef]
- Herman, T.; Giladi, N.; Gruendlinger, L.; Hausdorff, J.M. Six weeks of intensive treadmill training improves gait and quality of life in patients with Parkinson’s disease: A pilot study. Arch. Phys. Med. Rehabil. 2007, 88, 1154–1158. [Google Scholar] [CrossRef]
- Cakit, B.D.; Saracoglu, M.; Genc, H.; Erdem, H.R.; 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, 698–705. [Google Scholar] [CrossRef]
- Park, J.; Wu, Y.H.; Lewis, M.M.; Huang, X.; Latash, M.L. Changes in multifinger interaction and coordination in Parkinson’s disease. J. Neurophysiol. 2012, 108, 915–924. [Google Scholar] [CrossRef]
- Nocera, J.R.; Altmann, L.J.P.; Sapienza, C.; Okun, M.S.; Hass, C.J. Can exercise improve language and cognition in Parkinson’s disease? A case report. Neurocase 2010, 16, 301–306. [Google Scholar] [CrossRef]
- Schenkman, M.; Hall, D.; Kumar, R.; Kohrt, W.M. Endurance exercise training to improve economy of movement of people with Parkinson Disease: Three case reports. Phys. Ther. 2008, 88, 63–76. [Google Scholar] [CrossRef]
- Spina, R.J.; Ogawa, T.; Kohrt, W.M.; Martin, W.H.; Holloszy, J.O.; Ehsani, A.A. Differences in cardiovascular adaptations to endurance exercise training between older men and women. J. Appl. Physiol. 1993, 75, 849–855. [Google Scholar]
- Poulin, M.J.; Paterson, D.H.; Govindasamy, D.; Cunningham, D.A. Endurance training of older men: Responses to submaximal exercise. J. Appl. Physiol. 1992, 73, 452–457. [Google Scholar]
- Bergen, J.L.; Toole, T.; Elliott, R.G., III; Wallace, B.; Robinson, K.; Maitland, C.G. Aerobic exercise intervention improves aerobic capacity and movement initiation in Parkinson’s disease patients. NeuroRehabilitation 2002, 17, 161–168. [Google Scholar]
- Cantello, R.; Tarletti, R.; Civardi, C. Transcranial magnetic stimulation and Parkinson’s disease. Brain Res. Rev. 2002, 38, 309–327. [Google Scholar] [CrossRef]
- Miyai, I.; Fujimoto, Y.; Ueda, Y.; Yamamoto, H.; Nozaki, S.; Saito, T.; Kang, J. Treadmill training with body weight support: Its effect on Parkinson’s disease. Arch. Phys. Med. Rehabil. 2000, 81, 849–852. [Google Scholar] [CrossRef]
- Miyai, I.; Fujimoto, Y.; Yamamoto, H.; Ueda, Y.; Saito, T.; Nozaki, S.; Kang, J. Long-term effect of body weight-supported treadmill training in Parkinson’s disease: A randomized controlled trial. Arch. Phys. Med. Rehabil. 2002, 83, 1370–1373. [Google Scholar] [CrossRef]
- Toole, T.; Maitland, C.G.; Warren, E.; Hubmann, M.F.; Panton, L. The effects of loading and unloading treadmill walking on balance, gait, fall risk, and daily function in Parkinsonism. NeuroRehabilitation 2005, 20, 307–322. [Google Scholar]
- Paul, S.S.; Sherington, C.; Fung, V.S.; Canning, C.G. Motor and cognitive impairments in Parkinson’s disease: Relationships with specific balance and mobility tasks. Neurorehabil. Neural Repair 2013, 27, 63–71. [Google Scholar] [CrossRef]
- Ashburn, A.; Stack, E.; Pickering, R.M.; Ward, C.D. Predicting fallers in a community-based sample of people with Parkinson’s disease. Gerontology 2001, 47, 277–281. [Google Scholar] [CrossRef]
- Ashburn, A.; Fazakarley, L.; Ballinger, C.; Pickering, R.; McLellan, L.D.; 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. Psychiatr. 2007, 78, 678–684. [Google Scholar]
- Bloem, B.R.; Beckley, D.J.; van Dijk, J.G.; Zwinderman, A.H.; Remler, M.P.; Roos, R.A. Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov. Disord. 1996, 11, 509–521. [Google Scholar] [CrossRef]
- Toole, T.; Hirsch, M.A.; Forkink, A.; Lehman, D.A.; Maitland, C.G. The effects of a balance and strength training program on equilibrium in Parkinsonism: A preliminary study. NeuroRehabilitation 2000, 14, 165–174. [Google Scholar]
- Smania, N.; Corato, E.; Tinazzi, M.; Stanzani, C.; Fiaschi, A.; Girardi, P.; Gandolfi, M. Effect of balance training on postural instability in patients with idiopathic Parkinson’s disease. Neurorehabil. Neural Repair 2010, 24, 826–834. [Google Scholar] [CrossRef]
- Dibble, L.E.; 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, 14–26. [Google Scholar]
- Allen, N.E.; Sherrington, C.; Paul, S.S.; Canning, C.G. Balance and falls in Parkinson’s disease: A meta-analysis of the effect of exercise and motor training. Mov. Disord. 2011, 26, 1605–1615. [Google Scholar] [CrossRef]
- Hirsch, M.A.; Toole, T.; Maitland, C.G.; Rider, R.A. The effects of balance training and high-intensity resistance training on persons with idiopathic Parkinson’s disease. Arch. Phys. Med. Rehabil. 2003, 84, 1109–1117. [Google Scholar] [CrossRef]
- Pompeu, J.E.; Mendes, F.A.; Silva, K.G.; Lobo, A.M.; Oliveira Tde, P.; Zomignani, A.P.; Piemonte, M.E. Effect of Nintendo Wii™-based motor and cognitive training on activities of daily living in patients with Parkinson’s disease: A randomised clinical trial. Physiotherapy 2012, 98, 196–204. [Google Scholar] [CrossRef]
- Li, F.; Harmer, P.; Fitzgerald, K.; Eckstrom, E.; Stock, R.; Galver, J.; Maddalozzo, G.; Batya, S.S. Tai Chi and postural stability in patients with Parkinson’s disease. N. Engl. J. Med. 2012, 366, 511–519. [Google Scholar] [CrossRef]
- Tousignant, M.; Corriveau, H.; Roy, P.M.; Desrosiers, J.; Dubuc, N.; Hebert, R. Efficacy of supervised Tai Chi exercises versus conventional physical therapy exercises in fall prevention for frail older adults: A randomized controlled trial. Disabil. Rehabil. 2012. [Google Scholar] [CrossRef]
- Li, F.; Harmer, P.; Fisher, K.J.; Xu, J.; Fitzgerald, K.; Vongjaturapat, N. Tai Chi-based exercise for older adults with Parkinson’s disease: A pilot-program evaluation. J. Aging Phys. Act. 2007, 15, 139–151. [Google Scholar]
- Hackney, M.E.; Earhart, G.M. Tai Chi improves balance and mobility in people with Parkinson disease. Gait Posture 2008, 28, 456–460. [Google Scholar] [CrossRef]
- Cano-de-la-Cuerda, R.; Pérez-de-Heredia, M.; Miangolarra-Page, J.C.; Muñoz-Hellín, E.; Fernández-de-las-Peñas, C. Is there muscular weakness in Parkinson’s disease? Am. J. Phys. Med. Rehabil. 2010, 89, 70–76. [Google Scholar] [CrossRef]
- Durmus, B.; Baysal, O.; Altinayar, S.; Altay, Z.; Ersoy, Y.; Ozcan, C. Lower extremity isokinetic muscle strength in patients with Parkinson’s disease. J. Clin. Neurosci. 2010, 17, 893–896. [Google Scholar] [CrossRef]
- Koller, W.; Kase, S. Muscle strength testing in Parkinson’s disease. Eur. Neurol. 1986, 25, 130–133. [Google Scholar] [CrossRef]
- Nogaki, S.H.; Fukusako, T.; Sasabe, F.; Negoro, K.; Morimatsu, M. Muscle strength in early Parkinson’s disease. Mov. Disord. 1995, 10, 225–226. [Google Scholar] [CrossRef]
- Nogaki, H.; Kakinuma, S.; Morimatsu, M. Movement velocity dependent muscle strength in Parkinson’s disease. Acta Neurol. Scand. 1999, 99, 152–157. [Google Scholar] [CrossRef]
- Stevens-Lapsley, J.; Kluger, B.M.; Schenkman, M. Quadriceps muscle weakness, activation deficits, and fatigue with Parkinson disease. Neurorehabil. Neural Repair 2012, 26, 533–541. [Google Scholar]
- Schilling, B.K.; Karlage, R.E.; LeDoux, M.S.; Pfeiffer, R.F.; Weiss, L.W.; Falvo, M.J. Impaired leg extensor strength in individuals with Parkinson disease and relatedness to functional mobility. Parkinsonism Relat. Disord. 2009, 15, 776–780. [Google Scholar]
- Stelmach, G.E.; Worringham, C.J. The preparation and production of isometric force in Parkinson’s disease. Neuropsychologia 1988, 26, 93–103. [Google Scholar] [CrossRef]
- Robichaud, J.A.; Pfann, K.D.; Vaillancourt, D.E.; Comella, C.L.; Corcos, D.M. Force control and disease severity in Parkinson’s disease. Mov. Disord. 2005, 20, 441–450. [Google Scholar] [CrossRef]
- Kunesch, E.; Schnitzler, A.; Tyercha, C.; Knecht, S.; Stelmach, G. Altered force release control in Parkinson’s disease. Behav. Brain Res. 1995, 67, 43–49. [Google Scholar] [CrossRef]
- Pedersen, S.W.; Oberg, B.; Larsson, L.E.; Lindval, B. Gait analysis, isokinetic muscle strength measurement in patients with Parkinson’s disease. Scand. J. Rehabil. Med. 1997, 29, 67–74. [Google Scholar]
- Reck, C.; Florin, E.; Wojtecki, L.; Groiss, S.; Voges, J.; Sturm, V.; Schnitzler, A.; Timmermann, L. Differential distribution of coherence between beta-band subthalamic oscillations and forearm muscles in Parkinson’s disease during isometric contraction. Clin. Neurophysiol. 2009, 120, 1601–1609. [Google Scholar]
- Bridgewater, K.J.; Sharpe, M.H. Trunk muscle performance in early Parkinson’s disease. Phys. Ther. 1998, 78, 566–576. [Google Scholar]
- Jordan, N.; Sagar, H.J.; Cooper, J.A. A component analysis of the generation and release of isometric force in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 1992, 55, 572–576. [Google Scholar] [CrossRef]
- Brown, P.; Corcos, D.M.; Rothwell, J.C. Does parkinsonian action tremor contribute to muscle weakness in Parkinson’s disease? Brain 1997, 120, 401–408. [Google Scholar]
- Kakinuma, S.; Nogaki, H.; Pramanik, B. Morimatsu M. Muscle weakness in Parkinson’s disease: Isokinetic study of the lower limbs. Eur. Neurol. 1998, 39, 218–222. [Google Scholar]
- Hortobágyi, T.; Mizelle, C.; Beam, S.; DeVita, P. Old adults perform activities of daily living near their maximal capabilities. J. Gerontol. A Biol. Sci. Med. Sci. 2003, 58, M453–M460. [Google Scholar] [CrossRef]
- Dibble, L.E.; Hale, T.F.; Marcus, R.L.; Droge, J.; Gerber, J.P.; LaStayo, P.C. High-intensity resistance training amplifies muscle hypertrophy and functional gains in persons with Parkinson’s disease. Mov. Disord. 2006, 21, 1444–1452. [Google Scholar] [CrossRef]
- Hass, C.J.; Collins, M.A.; Juncos, J.L. Resistance training with creatine monohydrate improves upper body strength in patients with Parkinson’s disease. Neurorehabil. Neural Repair 2007, 21, 107–115. [Google Scholar] [CrossRef]
- Shulman, L.M.; Katzel, L.I.; Ivey, F.M.; Sorkin, J.D.; Favors, K.; Anderson, K.E.; Smith, B.A.; Reich, S.G.; Weiner, W.J.; Macko, R.F. Randomized clinical trial of 3 types of physical exercise for patients with Parkinson’s disease. Arch. Neurol. 2012. [Google Scholar] [CrossRef]
- Scandalis, T.A.; Bosak, A.; Berlinder, J.C.; Helman, L.L.; Wells, M.R. Resistance training and gait function in patients with Parkinson’s disease. Am. J. Phys. Med. Rehabil. 2001, 80, 38–43. [Google Scholar] [CrossRef]
- Dibble, L.E.; Hale, T.F.; Marcus, R.L.; Gerber, J.P.; Lasayo, P.C. High intensity eccentric resistance training decreases bradykinesia and improves quality of life in persons with Parkinson’s disease: A preliminary study. Parkinsonism Relat. Disord. 2009, 15, 752–757. [Google Scholar] [CrossRef]
- Hass, C.J.; Buckley, T.A.; Pitsikoulis, C.; Barthelemy, E.J. Progressive resistance training improves gait initiation in individuals with Parkinson’s disease. Gait Posture 2012, 35, 669–673. [Google Scholar] [CrossRef]
- Galvão, D.A.; Taaffe, D.R. Resistance exercise dosage in older adults: Single- versus multiset effects on physical performance and body composition. J. Am. Geriatr. Soc. 2005, 53, 2090–2097. [Google Scholar] [CrossRef]
- Schilling, B.K.; Pfeiffer, R.F.; LeDoux, M.S.; Karlage, R.E.; Bloomer, R.J.; Falvo, M.J. Effects of moderate-volume, high-load lower-body resistance training on strength and function in persons with Parkinson’s disease: A pilot study. Parkinsons Dis. 2010, 2010. [Google Scholar] [CrossRef]
- Schenkman, M.; Hall, D.; Baron, A.E.; Schwartz, R.S.; Mettler, P.; Kohrt, W.M. Exercise for people in early- or mid-stage Parkinson disease: A 16-month randomized controlled trial. Phys. Ther. 2012, 92, 1395–1410. [Google Scholar] [CrossRef]
- Behrman, A.L.; Teitelbaum, P.; Cauraugh, J.H. Verbal instructional sets to normalise the temporal and spatial gait variables in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 1998, 65, 580–582. [Google Scholar] [CrossRef]
- Fox, C.; Ebersbach, G.; Ramig, L.; Sapir, S. LSVT LOUD and LSVT BIG: Behavioral treatment programs for speech and body movement in Parkinson’s Disease. Parkinsons Dis. 2012, 2012. [Google Scholar] [CrossRef]
- Farley, B.G.; Koshland, G.F. Training BIG to move faster: The application of the speed amplitude relation as a rehabilitation strategy for people with Parkinson’s disease. Exp. Brain Res. 2005, 167, 462–467. [Google Scholar] [CrossRef]
- Ebersbach, G.; Ebersbach, A.; Edler, D.; Kaufhold, O.; Kusch, M.; Kupsch, A.; Wissel, J. Comparing exercise in Parkinson’s disease—The Berlin LSVT®BIG study. Mov. Disord. 2010, 25, 1902–1908. [Google Scholar] [CrossRef]
- Ellis, T.; de Goede, C.J.; Feldman, R.G.; Wolters, E.C.; Kwakkel, G.; Wagenaar, R.C. Efficacy of a physical therapy program in patients with Parkinson’s disease: A randomized controlled trial. Arch. Phys. Med. Rehabil. 2005, 86, 626–632. [Google Scholar] [CrossRef]
- Comelia, C.L.; Stebbins, G.T.; Brown-Toms, N.; Goetz, C.G. Physical therapy and Parkinson’s disease: A controlled clinical trial. Neurology 1994, 44, 376–376. [Google Scholar] [CrossRef]
- Sheldon, T.A.; Guyatt, G.H.; Haines, A. Getting research findings into practice. When to act on the evidence. BMJ 1998, 317, 139–142. [Google Scholar] [CrossRef]
- Haynes, B.; Haines, A. Barriers and bridges to evidence based clinical practice. BMJ 1998, 317, 273–276. [Google Scholar] [CrossRef]
© 2013 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).