Effects of treadmill training on gait of elders with Parkinson's disease: a literature review

Natália Mariana Silva Luna; Guilherme Carlos Brech; Alexandra Canonica; Rita de Cássia Ernandes; Danilo Sales Bocalini; Julia Maria D’Andréa Greve; Angélica Castilho Alonso

doi:10.31744/einstein_journal/2020RW5233

. 2020 Nov 18;18:eRW5233. doi: 10.31744/einstein_journal/2020RW5233

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Effects of treadmill training on gait of elders with Parkinson's disease: a literature review

Natália Mariana Silva Luna ¹, Guilherme Carlos Brech ^1,^✉, Alexandra Canonica ¹, Rita de Cássia Ernandes ², Danilo Sales Bocalini ³, Julia Maria D’Andréa Greve ¹, Angélica Castilho Alonso ²

PMCID: PMC7687915 PMID: 33263679

ABSTRACT

Parkinson's disease is the second most common neurodegenerative disorder in old age. Aging process for elders with Parkinson's disease can induce gait disturbances with more functional disabilities than for elders without the disease. Treadmill training as a therapy has resulted in notable effects on the gait of patients with Parkinson's disease and may be a resource for geriatric neurological rehabilitation. This review aimed to study the effects on gait after treadmill training in elderly patients with Parkinson's disease. The search was performed in the databases PubMed®, LILACS, PEDro and EMBASE, with the following keywords: “Parkinson's disease”, “elderly”, “treadmill training” and “gait evaluation”. The quality of the studies included was assessed by PEDro Scale. Eleven studies met the inclusion and exclusion criteria. Eight studies were randomized, and only one did a follow-up. One can observe in this review that treadmill training with or without weight support (at least 20 minutes, two to three times a week, with progressive increase of loads, for minimum of 6 weeks) in elderly patients with the Parkinson's disease was effective to improve gait. In addition, both were considered safe (since some studies described the use of belts, even in unsupported training) and can be associated with therapies complementary to gait, such as repetitive transcranial magnetic stimulation, visual cues or anodal transcranial direct current stimulation. Treadmill training in elderly patients with Parkinson's disease is an intervention that improves gait outcomes, but further studies are required for better proofs.

Keywords: Parkinson disease/rehabilitation, Gait, Aged

INTRODUCTION

Idiopathic Parkinson's disease (PD) is a chronic, progressive and degenerative disease of the central nervous system, associated with a depletion in dopaminergic neurons in the nigrostriatal pathway.⁽¹⁾ Clinical symptoms appear when there is a 40% to 60% reduction of nigral neurones and striatal dopamine.⁽²⁾ Parkinson's disease is the second most common degenerative nervous system disease, affecting 1% to 2% of the population older than 65 years.⁽³⁾ The proportion of elderly in the world is increasing, resulting in larger pool of people at risk for PD.⁽⁴⁾

Cardinal symptoms include resting tremor, muscular rigidity, freezing of gait (FOG); bradykinesia and gait and postural instability.⁽³^,⁴⁾ Gait disorders compromise patients’ independence and quality of life, decreasing mobility and increasing the risk of falls and fractures.⁽⁵⁾Parkinson's disease induces gait disturbances, such as reduced velocity, reduced stride and step length, and increased duration of double stance.⁽⁴^–⁸⁾

The reduction in gait speed is explained by slower center of gravity displacement, decreased vertical component of ground reaction force⁽⁹^–¹¹⁾ and greater lateral displacement of the center of pressure at the beginning of gait.⁽¹²⁾ The reduction in step length occurs mainly due to the deficiency in the detachment phase of the foot, in which a smaller electromyography signal in the gastrocnemius muscle is observed and consequently problems to project limb forwards.⁽¹⁰⁾ Increased support phase is related to decreased gait speed and bradykinesia.⁽⁵⁾ This hinders the automatism of the step during the gait and promotes electromyographic signal changes of the lower limbs.⁽¹³^,¹⁴⁾

Similarly, aging also slows gait velocity and step length, which suggests that PD in elders may lead to greater functional disability, making them more susceptible to falls.⁽¹⁵⁾

Concerning physical gait rehabilitation, treadmill training (TT) as a therapy has shown notable effects on the gait of patients with PD, with superior results in gait parameters compared to patients not undergoing this treatment.⁽¹⁶^–²¹⁾ Literature reviews show that the TT can promote a more stable walking pattern in PD patients, and suggest that the intervention is able to restore rhythmicity and reduces gait variability.⁽¹⁸^,²¹^,²²⁾ However, they analyzed various outcomes, but with no emphasis on the elderly. Hence, the objective of this work was to review the effects on gait after TT in elderly PD patients.

OBJETIVE

The objective of this study was to review the effects on gait after treadmill training in elderly Parkinson's disease patients.

METHODS

Search strategy

The search was performed in PubMed®, LILACS, PEDro and EMBASE database; and published articles related to the effects of TT on the gait of elderly patients with PD were found based on the following keywords: “Parkinson's disease”, “elderly”, “treadmill training” and “gait evaluation”.

Study selection

The critical literature review identified the following inclusion criteria: studies in humans, in English, and published in scientific journals during the last 10 years. Articles describing patients aged less than 60 years, or who have not undergone treadmill gait training, and without outcome measures regarding gait were excluded. Articles describing treadmill gait training in patients without PD and treadmill gait training in combination with virtual reality were also excluded. After reading the titles and/or abstracts, articles meeting the inclusion criteria and identified as relevant to the development of this work were selected. A total of 25 references to simple combinations were found in PubMed®, LILACS, PEDro and EMBASE. Eleven articles were finally selected based on the established criteria.

Quality appraisal

The quality of 11 studies included⁽²³^–³³⁾ was assessed by PEDro scale checklist ( Table 1 ), which presents 11 items that consider the following criteria: eligibility criteria and source of participants; random allocation; blind allocation; comparability of baseline; subjects were blind; therapists were blind; evaluators were blind; results with more than 85% of participants; intention-to-treat analysis; statistical comparisons between groups; and point measures and variability measures.

Table 1. PEDro scale of the 11 studies selected.

Authors	Eligibility	Random allocation	Blind allocation	Comparability of baseline	Subjects were blind	Therapists were blind	Evaluators were blind	Results with more than 85% of participants	Intention-to-treat analysis	Statistical comparisons between groups	Point measures and variability measures
Frazzitta et al.⁽²³⁾	Yes	Yes	No	Yes	No	No	Yes	Yes	Yes	Yes	No
Yang et al.⁽²⁴⁾	Yes	No	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Galli et al.⁽²⁵⁾	Yes	No	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	No
Canning et al.⁽²⁶⁾	Yes	No	Yes	Yes	No	No	Yes	Yes	Yes	Yes	Yes
Frazzitta et al.⁽²⁷⁾	Yes	Yes	no	Yes	No	No	Yes	Yes	Yes	Yes	No
Picelli et al.⁽²⁸⁾	Yes	No	Yes	Yes	No	No	Yes	Yes	Yes	Yes	No
Fisher et al.⁽²⁹⁾	Yes	No	Yes	Yes	Yes	No	No	Yes	Yes	Yes	No
Schlick et al.⁽³⁰⁾	Yes	No	Yes	Yes	No	No	No	Yes	Yes	Yes	No
Arcolin et al.⁽³¹⁾	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	No
Herman et al.⁽³²⁾	Yes	No	No	No	No	No	No	Yes	Yes	No	No
Fernández-Lago et al.⁽³³⁾	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	No

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RESULTS

Eleven studies met the inclusion criteria.⁽²³^–³³⁾ Studies that obtained the highest score on the PEDro scale were conducted by Yang et al.,⁽²⁴⁾ and Galli el al.,⁽²⁵⁾ ( Table 1 ).

Of the 11 studies,⁽²³^–³³⁾ eight were randomized.⁽²³^–³⁰⁾ In relation the type of training, five studies analyzed training without body weight support,⁽²³^,²⁴^,²⁶^,²⁷^,³⁰⁾ and three studies evaluated with support system⁽²⁵^,²⁸^,²⁹⁾ ( Table 2 ).

Table 2. Summary of the population, protocols, gait measures and results of these investigations.

Studies	Population	Protocol	Gait measures	Results
Frazzitta et al.⁽²³⁾	30 patients with gait disturbance, but without FOG in “on” stage and 30 patients with FOG in “on” stage	Patients underwent a 4-week rehabilitation treatment using a treadmill with auditory and visual cues	Gait speed, stride length, asymmetry of gait, 6MWT, UPDRS II-III, Berg Balance Scale, TUG, comfortable-fast gait speeds, FOG-Q	Data support a direct involvement of the asymmetry of gait in the development of FOG in PD TT is effective in improving gait and balance in PD FOG patients, and this might be related to a reduction of asymmetric gait
Yang et al.⁽²⁴⁾	20 patients with PD with ability to walk independently	-2 groups: 1. Participants received rTMS (Experimental Group) 2. Participants received sham rTMS (Control Group) Followed by TT (30 minutes) for 12 sessions over 4 weeks (3 sessions a week)	Corticomotor inhibition and walking performance	The findings suggested that combination of rTMS and TT enhances the effect of TT on modulation of corticomotor inhibition and improvement of walking performance in those with PD
Galli et al.⁽²⁵⁾	50 idiopathic PD Ability to walk, unassisted or with little assistance, for a distance of 25 feet	-2 groups 1. Robot-assisted therapy group (n=25) 2. Intensive treadmill therapy group (n=25)	Hoehn and Yahr scaleUPDRS Optoelectronic system (ELITE2002, BTS, Milan, Italy)	In the robot group, differences were found in kinematic variables (pelvic obliquity and hip abduction and adduction). The intensive group showed no statistically significant changes. The end-effector robotic rehabilitation locomotor training improved gait kinematics and seems to be effective for rehabilitation in patients with mild PD
Canning et al.⁽²⁶⁾	20 people with idiopathic PD with <2 hours per week of leisure time physical activity in prior 3 months, and had a stable response to levodopa medications	-2 groups: 1. The Experimental Group undertook a semi-supervised home-based program of 30-40 minutes of treadmill walking, 4 times a week for 6 weeks 2. The Control Group received usual care (i.e. advice to maintain current levels of physical activity)	The primary outcome measure of efficacy was walking capacity (6MWT)	Semi-supervised home-based TT is a feasible and safe form of exercise for cognitively intact people, with mild PD
Frazzita et al.⁽²⁷⁾	40 Parkinsonian patients with freezing were randomly assigned to two groups	2 group: 1. Underwent a rehabilitation program based on treadmill training associated with auditory and visual cues 2. Followed a rehabilitation protocol using cues and not associated with treadmill	Functional evaluation was based on the Unified Parkinson's Disease Rating Scale Motor Section (UPDRS III); Freezing of Gait Questionnaire (FOGQ), 6-minute walking test (6MWT), gait speed, and stride cycle	The results suggest that treadmill training associated with auditory and visual cues might give better results than more conventional treatments. Treadmill training probably acts as a supplementary external cue
Picelli et al.⁽²⁸⁾	60 patients with mild to moderate PD	3 groups: 1. Robotic gait training group (n=20);TT group (n=20) performed equal intensity 2. TT without body-weight support 3. The physical therapy group (n=20) underwent conventional gait therapy45 minutes per session 3 days/week, during four consecutive weeks	10-minute walking test6MWT	No statistically significant difference was found between the robotic gait training group and the TT group in the evaluation after training. Statistically significant improvement was found after treatment in favor of the robotic gait training group and TT group compared to the physical therapy group. Findings were confirmed at the 3-month follow-up evaluation
Fisher et al.⁽²⁹⁾	30 PD patients, within 3 years of diagnosis, with Hoehn and Yahr stages 1 or 2	3 groups: 1. High-intensity (body weight-supported TT) 2. Low-intensity exercise (exercises to range of motion, balance and gait) 3. Zero-intensity (education group)	UPDRS Biomechanical analysis of self-selected and fast walking Sit-to-stand tasks Corticomotor excitability	A small improvement in total and motor UPDRS was observed in all groups. High-intensity group subjects showed post-exercise increases in gait speed, step and stride length, and hip and ankle joint excursion during self-selected and fast gait, besides improved weight distribution during sit-to-stand tasks. Improvements in gait and sit-to-stand measures were not consistently observed in the low- and zero-intensity groups. The high-intensity group showed lengthening in cortical silent period
Schlick et al.⁽³⁰⁾	23 outpatients with PD	Patients received 12 training sessions within 5 weeks of either visual cues combined with TT (n=12) or pure TT (n=11)	Gait speed, stride length and cadence Functional tests included the TUG test, the UPDPRS and the freezing of gait-questionnaire	This pilot study suggests that visual cues combined with TT have more beneficial effects on gait than pure TT, in patients with a moderate stage of PD. A large-scale study with longer follow-up is required
Arcolin et al.⁽³¹⁾	29 patients with the diagnosis of idiopathic PDAbility to walk, unassisted	2 groups (randomized): 1. Treadmill (n=13) 2. Cycle ergometer (n=16) Training for 3 weeks, 1 hour/day	6MWT Spatiotemporal variables of gait assessed by baropodometry TUG test MINIBESTest UPDRS	This pilot study shows that cycle ergometer training improves walking parameters and reduces clinical signs of PD, as much as TT does. Gait velocity is accompanied by step lengthening, making the gait pattern close to that of healthy subjects. Cycle ergometer is a valid alternative to treadmill for improving gait in short-term in patients with PD
Herman et al.⁽³²⁾	9 patients with PD who were able to ambulate independently and were not demented	Patients walked on a treadmill for 30 minutes during each training session, 4 training sessions a week, for 6 weeks	PDQ-39 UPDRS Gait speed, stride time variability, swing time variability SPPB	These results show the potential to enhance gait rhythmicity in patients with PD and suggest that a progressive and intensive TT program can be used to minimize impairments in gait, reduce fall risk, and increase quality of life of these patients
Fernández-Lago et al.⁽³³⁾	18 idiopathic PD patientsAbility to walk, unassisted	18 participants with PD were evaluated under the following three conditions (groups): 1. Treadmill walking alone (treadmill) 2. Treadmill walking combined with anodal tDCS (AtDCS + treadmill) delivered over the motor cortex 3. Treadmill walking combined with sham stimulation (StDCS+treadmill)	Overground walking performance, soleus H-reflex, reciprocal Ia inhibition from the tibialis anterior to the soleus muscle, intracortical facilitation, and short intracortical inhibition of the tibialis anterior muscle	All treadmill conditions improved walking performance and modulated spinal and corticospinal parameters compare with other kind of treatments. However, AtDCS + treadmill lead to a different modulation of reciprocal Ia inhibition in comparison with the other treadmill conditions

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FOG: freezing of gait; 6MWT: 6-Minute Walk Test; UPDPRS: Unified Parkinson Disease Rating Scale; TUG: Timed Up and Go; FOG-Q: Freezing of Gait Questionnaire; TT: treadmill training; PD: Parkinson disease; rTMS: repetitive transcranial magnetic stimulation; MINIBESTest: Balance Evaluation Systems Test; PDQ-39: Parkinson Disease Questionnaire-39; SPPB: Short Physical Performance Battery; tDCS: transcranial direct current stimulation.

DISCUSSION

Some studies on TT in PD patients and literature reviews address the subject. However, the reviews analyzed all age groups and present methodologies with different outcomes: quality of life, balance and gait. Our review aimed to focus only studies with groups of PD patients older than 60 years, as well as outcomes related gait specificities; and in according with check list of PEDro scale, the articles included were considered adequate for scientific publication.

The Hoehn and Yarh scale ranged from 1 to 3, with the most⁽²³^,²⁵^–²⁷^,²⁹^,³²^,³³⁾ addressed patients between 1 and 2, a score that represents discrete balance impairment. In four studies⁽²⁴^,²⁸^,³⁰^,³¹⁾ the stage was between 2 to 3, a score in which the disease is necessarily bilateral and exists some postural instability, but the patient is physically independent.

The Hoehn and Yarh scale characterizes the patient's functional status through observation.⁽³⁴⁾ Other studies with patients younger than 60 years or mixing different age groups also showed this Hoehn and Yarh scale score. Thus, the moderate Hoehn and Yarh score could suggest aging did not interfere in the disease.

The duration of disease was another demographic variable that was different among the studies. In eight studies,⁽¹⁵^–¹⁷^,¹⁹^,²¹^–²⁴⁾ the duration was between 5 and 10 years and, in two, the duration was more than 10 years.⁽²⁷^,²⁹⁾ Only one did not mention this data.⁽²³⁾ Studies showed that, with the evolution of the disease (5 to 7 years), there is worsening of motor condition and onset of dyskinesias.⁽¹⁵⁾ Seventy percent of patients taking levodopa for 6 or more years have motor complications and need to discontinue use temporarily (“off”).⁽³⁵⁾

The gait evaluations used in studies of review were computerized or functional. Both are important for the explanations of results, but some are more specific than others and thus may help more for the answers on clinical practice.⁽¹¹⁾

The motor score of Unified Scale for Parkinson's Disease (UPDRS) was used in most articles.⁽²³^,²⁹^–³²⁾It is a very reliable (r=0.96) and valid scale, a suitable method for evaluating PD.⁽³⁶⁾ The motor exploration section consists of 14 items (numbers ranging from 18 to 31), but the item that evaluates gait is observational and does not allow accurate analysis.

The Timed Up and Go test (TUG) was also used in five studies.⁽²³^,²⁷^,³⁰^–³²⁾ The TUG measures the time ofmotor task of to get up from chair, to walk 3m, to return and to sit.⁽³⁷⁾ Isles et al.,⁽³⁸⁾ define the test as sensitive and specific to discriminate between fallers and non-faller. It is possible to observe that the test is considered for balance and mobility,⁽³⁹⁾ without, however, analyzing gait specific characteristics.

Another evaluation tool used was the 6-minute walk test (6MWT).⁽¹⁴^,¹⁶^–¹⁹⁾ It is used to evaluate physical response and provides comprehensive analysis of respiratory, cardiac and metabolic systems.⁽⁴⁰⁾ The test reflects limitations of daily life activities, such as gait, but according to the American Thoracic Society (ATS),⁽⁴¹⁾ the accurate indication of 6MWT is the presence of pulmonary disease or mild to moderate heart disease, so that the test is used to measure response to treatment and to predict morbidity and mortality.

Spatial parameters (velocity, step length and cadence) are considered significant for gait clinical evaluation. They can be calculated qualitatively, without cameras and software, or computerized by kinematic and kinetic analyses. Five studies investigated these parameters through qualitative approach⁽²⁷^,²⁹^–³²⁾ and only two by computerized means.⁽²⁵^,²⁹⁾ The use of three-dimensional gait analysis is scarce in studies about PD, but is considered as gold standard method to better biomechanical understanding, providing reproducible and reliable data.⁽¹³⁾

The TT was studied with and without body weight support. Eight studies analyzed training without body weight support,⁽¹⁴^–¹⁸^,²²^–²⁴⁾ and three studies assessed with support system.⁽¹⁹^–²¹⁾ All showed improvements in gait variables after training, but there were differences between the methodologies.

Only Herman et al.,⁽³²⁾ did a follow-up study. They performed 6 weeks of TT (four times a week, 30 minutes each session), followed by 1 month of TT with progressive increase of intensity in nine patients with PD. There was improvement of UPDRS regarding velocity and step length, as well as gait variability after training period and follow-up of 6 weeks. These results suggested that a progressive and intensive TT program can be used to minimize impairments in gait, reduce fall risk, and increase quality of life in these patients.

Frazzitta et al.,⁽²³⁾ recruited Parkinson's patients with and without FOG, who underwent the same protocol, TT without support associated with visual and auditory cues. Subjects received TT for 30 minutes every day for 5 days a week, during 4 weeks (20 sessions in total). Treadmill training is effective in improving gait and balance in PD patients and this asymmetry in gait may be related to an increased chance of FOG.

The others compared the traditional TT with other type of TT. Frazzitta et al.,⁽²⁷⁾ compared TT without support associated with visual and auditory cues with gait training without treadmill, also associated with visual and auditory cues. The results suggest that TT associated with auditory and visual cues might give better results than more conventional treatments. Subjects received training for 20 minutes every day, for 4 weeks (28 sessions in all). Treadmill training probably acts as a supplementary external cue.

Schlick et al.,⁽³⁰⁾ analyzed 20 patients with PD, who were divided into two interventions: TT group with visual cues and TT group no cues. This pilot study suggests that visual cues combined with TT have more beneficial effects on gait than traditional TT. The visual cue acts as a stimulus to visual receptors, generating repetitive sensory afferent stimuli to the central nervous system. In PD patients these signals may also represent external sensory cues, a trigger for intact circuits unaffected by the disease, such as the lateral pathway of the premotor cortex.⁽²^,⁶⁾

Yang et al.,⁽²⁴⁾ compared TT with and without prior application of repetitive transcranial magnetic stimulation (rTMS). The TT was carried out for 12 sessions (3 sessions a week) over a 4-week period. All participants walked on a motorized treadmill (Biodex, Shirley, New York, USA) after the rTMS. The findings suggested that combination of rTMS and TT enhances the effect of TT on modulation of corticomotor inhibition and improvement of walking performance in PD patients.

Canning et al.,⁽²⁶⁾ observed an Experimental Group undertook a semi-supervised home-based program of 30 to 40 minutes of treadmill walking, four times a week for 6 weeks. The Control Group received usual care ( i.e . advice to maintain current levels of physical activity). Semi-supervised home-based TT is a feasible and safe form of exercise for cognitively intact people with mild PD. The home treatment is an important strategy in geriatric rehabilitation, and it is possible to associate TT as a reinforcement to gait exercises.

Arcolin et al.,⁽³¹⁾ randomized 29 PD inpatients to treadmill (n=13) or cycle ergometer (n=16) training for 3 weeks, 1 hour per day. This pilot study shows that cycle ergometer training improves walking parameters and reduces clinical signs of PD, as much as TT does. Gait velocity is accompanied by step lengthening, making the gait pattern close to that of healthy subjects. Cycle ergometer is a valid alternative to treadmill for improving gait in short term in patients with PD.

Studies not included in review due to sample with no elderly also showed that TT without body weight support in patients with PD, compared to other motor therapies, increased speed and stride length.⁽⁴²^,⁴³⁾

Three studies included used TT with body weight support⁽¹⁸^–²⁰⁾ and two⁽¹⁹^,²¹⁾ showed superiority of supported training compared to other therapy, and one did not observe a difference.⁽²⁸⁾ Fisher et al.,⁽²⁹⁾ recruited 30 PD patients (stage Hoehn and Yarh I to II) who were randomized into three groups: high-intensity therapy (supported training), low-intensity physical therapy (passive and active range of motion, balance, gait, muscular endurance and daily functions exercises) and non-intensive therapy, characterized by therapeutic education (six classes during a 8-week period about quality of life). The interventions lasted 8 weeks, totaling 24 sessions (three times a week with 1-hour sessions). The TT started with 10% of suspended body weight, however if the patient could not perform the gait, this percentage was increased, so that the goal of each session was for the patient to reach and maintain a level higher than 3 METS, while respecting rest, whenever necessary. The results showed improvement in UPDRS in all groups. The supported training group showed increase in gait velocity, step and stride length, and excursions of hip and ankle in sagittal plane, as well as improved weight distribution during exercise and raise of cortical silent period.

Gali et al.,⁽²⁵⁾ and Picelli et al.,⁽²⁸⁾ also used training with body weight support, however with robotic assistance. Picelli et al.,⁽²⁸⁾ compared three groups: the robotic gait training group; TT without body-weight support group and physical therapy group. Each training session consisted of three parts, with a 5-minute rest after each. First, we trained patients at 1km/hour of speed for 10 minutes; then, at 1.5km/hour of speed for 10 minutes; finally, at 2.0km/hour of speed for 10 minutes. There were no differences in the spatial and temporal parameters of the 6- and 10-minute walk tests. Gali et al.,⁽²⁵⁾ evaluated 50 PD patients, who were divided into two groups: 25 were assigned to the robot-assisted therapy and 25 to the intensive treadmill therapy group. The end-effector robotic rehabilitation locomotor training improved gait kinematics, and seems to be effective for rehabilitation in patients with mild PD.

Some studies with non-elderly patients also observed similar results. There were no differences in temporal-spatial variables of the 6-minute and 10-minute walk tests and TUGT and UPDRS,⁽⁴⁴⁾ when comparison between TT and Lokomat TT was performed. Other studies have observed the effect of TT with weight support in relation to without weight support,⁽⁴⁵⁾ to ground gait training⁽⁴⁶⁾ and to other motor therapies.⁽¹⁶^,¹⁷⁾

Toole et al.,⁽⁴⁵⁾ reported the effects of TT for 6 weeks, on 23 PD patients randomized into three groups. Two groups trained gait with 25% and 5% of body weight support, and the third group without support. The three groups improved on the UPDRS and Berg scales, with no difference between them. The study by Ganesan et al.,⁽⁴⁶⁾ used computerized posturography to evaluate the effect of a 4-week TT with 20% body weight support, four times a week (30 minutes per day). The authors reported improvements in the limits of stability and medial lateral oscillation of the center of mass with the training with support in relation to the training of conventional gait off the treadmill. Miyai et al.,⁽¹⁶⁾ compared gait training with 20% body weight support versus conventional physiotherapy for 4 weeks in PD patients, and reported that weight-bearing TT improved gait motor performance (10-minute walk test) and in daily life activities, which persisted for 6 months.⁽¹⁷⁾

Fernández-Lago et al.,⁽³³⁾ described that a single session combining treadmill walking and anodal transcranial direct current stimulation (tDCS) delivered over the motor cortex resulted in a specific modulation of the reciprocal a inhibition from the tibialis anterior to the soleus muscle. However, this acute effect did not result in improvements of gait parameters associated with treadmill walking in Parkinson's disease.

Unsupported body weight training seems to be more challenging because it requires greater muscle demand. The main reasons for this evidence are constant velocity; continuous sensory stimulation; external sensory cues; activation of gait neural circuits generating central pattern; visual feedback; constant speed and motor learning.⁽¹⁶^,¹⁷^,⁴⁵^,⁴⁶⁾

Training with body weight support, even if it decreases peripheral stimulation (muscle strength and aerobic effort), may increase proprioceptive stimulation.⁽⁴⁷⁾The partial weight support can also extend the useful training period because it reduces fatigue.⁽⁴⁸⁾ In addition, facilitates movement of lower limbs,⁽⁴⁹⁾ and can therefore be considered a promising intervention for sensorimotor control training by improvement of postural reflexes.⁽¹⁶^,¹⁷⁾ It may also facilitate the use of strategies that use non-dopaminergic pathways and are not affected by disease. Other authors suggested that training with weight support stimulated the gait control in spinal cord.⁽¹⁷^,⁴⁷⁾

It is possible to observe in review that TT with or without weight support (at least 20 minutes, 2 to 3 times a week, with progressive increase of loads, for a minimum of 6 weeks) in elderly PD patients is effective for improving gait. In addition, both are considered safe (since even unsupported training, studies describe the use of belts) and can be associated with therapies complementary to gait, such as rTMS, visual cues or anodal tDCS.

However, it is important to emphasize that assessments used to gait were different. Five studies⁽¹⁷^,¹⁹^,²¹^,²²^,²⁴⁾ were able to evaluate gait clinical characteristics, which can help in evolution of treatment. Only two used gold standard measure, the computerized evaluation.⁽²⁵^,²⁹⁾ Treadmill training with or without weight support can be an intervention to neurological geriatric rehabilitation, but there is a need for more studies with this theme that better characterize the sample of elderly with PD, as well as using more specific gait assessment tools.

There are some limitations in this study. We did not analyze the subgroups of elderly patients among the studies that recruited adults in the sample and, therefore, were excluded. Most of the studies have a relatively small sample, with a total of 300 patients in all studies.

CONCLUSION

Treadmill training with or without weight support (at least 20 minutes, two to three times a week, with progressive increase of loads, for minimum of 6 weeks) is an intervention that improves gait outcomes in elderly Parkinson's disease patients, but further studies are warranted.

ACKNOWLEDGMENTS

This work was carried out with the support of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Financing Code 001.

REFERENCES

1.Pieruccini-Faria F, Menuchi MR, Vitório R, Gobbi LT, Stella F, Gobbi S. Parâmetros cinemáticos da marcha com obstáculos em idosos com Doença de Parkinson, com e sem efeito da levodopa: um estudo piloto. Rev Bras Fisioter. 2006;10(2):233–239. [Google Scholar]; 1. Pieruccini-Faria F, Menuchi MR, Vitório R, Gobbi LT, Stella F, Gobbi S. Parâmetros cinemáticos da marcha com obstáculos em idosos com Doença de Parkinson, com e sem efeito da levodopa: um estudo piloto. Rev Bras Fisioter. 2006;10(2):233-9.
2.de Goede CJ, Keus SH, Kwakkel G, Wagenaar RC. The effects of physical therapy in Parkinson's disease: a research synthesis. Arch Phys Med Rehabil. 2001;82(4):509–515. doi: 10.1053/apmr.2001.22352. [DOI] [PubMed] [Google Scholar]; 2. de Goede CJ, Keus SH, Kwakkel G, Wagenaar RC. The effects of physical therapy in Parkinson's disease: a research synthesis. Arch Phys Med Rehabil. 2001;82(4):509-15. [DOI] [PubMed]
3.Svehlík M, Zwick EB, Steinwender G, Linhart WE, Schwingenschuh P, Katschnig P, et al. Gait analysis in patients with Parkinson's disease off dopaminergic therapy. Arch Phys Med Rehabil. 2009;90(11):1880–1886. doi: 10.1016/j.apmr.2009.06.017. [DOI] [PubMed] [Google Scholar]; 3. Svehlík M, Zwick EB, Steinwender G, Linhart WE, Schwingenschuh P, Katschnig P, et al. Gait analysis in patients with Parkinson's disease off dopaminergic therapy. Arch Phys Med Rehabil. 2009;90(11):1880-6. [DOI] [PubMed]
4.Blin O, Ferrandez AM, Serratrice G. Quantitative analysis of gait in Parkinson patients: increased variability of stride length. J Neurol Sci. 1990;98(1):91–97. doi: 10.1016/0022-510x(90)90184-o. [DOI] [PubMed] [Google Scholar]; 4. Blin O, Ferrandez AM, Serratrice G. Quantitative analysis of gait in Parkinson patients: increased variability of stride length. J Neurol Sci. 1990;98(1):91-7. [DOI] [PubMed]
5.Peppe A, Chiavalon C, Pasqualetti P, Crovato D, Caltagirone C. Does gait analysis quantify motor rehabilitation efficacy in Parkinson's disease patients? Gait Posture. 2007;26(3):452–462. doi: 10.1016/j.gaitpost.2006.11.207. [DOI] [PubMed] [Google Scholar]; 5. Peppe A, Chiavalon C, Pasqualetti P, Crovato D, Caltagirone C. Does gait analysis quantify motor rehabilitation efficacy in Parkinson's disease patients? Gait Posture. 2007;26(3):452-62. [DOI] [PubMed]
6.Morris ME, Iansek R, Matyas TA, Summers JJ. The pathogenesis of gait hypokinesia in Parkinson's disease. Brain. 1994;117(Pt 5):1169–1181. doi: 10.1093/brain/117.5.1169. [DOI] [PubMed] [Google Scholar]; 6. Morris ME, Iansek R, Matyas TA, Summers JJ. The pathogenesis of gait hypokinesia in Parkinson's disease. Brain. 1994;117(Pt 5):1169-81. [DOI] [PubMed]
7.Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson's disease. Normalization strategies and underlying mechanisms. Brain. 1996;119(Pt 2):551–568. doi: 10.1093/brain/119.2.551. [DOI] [PubMed] [Google Scholar]; 7. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson's disease. Normalization strategies and underlying mechanisms. Brain. 1996;119(Pt 2):551-68. [DOI] [PubMed]
8.Camicioli R, Oken BS, Sexton G, Kaye JA, Nutt JG. Verbal fluency task affects gait in Parkinson's disease with motor freezing. J Geriatr Psychiatry Neurol. 1998;11(4):181–185. doi: 10.1177/089198879901100403. [DOI] [PubMed] [Google Scholar]; 8. Camicioli R, Oken BS, Sexton G, Kaye JA, Nutt JG. Verbal fluency task affects gait in Parkinson's disease with motor freezing. J Geriatr Psychiatry Neurol. 1998;11(4):181-5. [DOI] [PubMed]
9.Galletly R, Brauer SG. Does the type of concurrent task affect preferred and cued gait in people with Parkinson's disease? Aust J Physiother. 2005;51(3):175–180. doi: 10.1016/s0004-9514(05)70024-6. [DOI] [PubMed] [Google Scholar]; 9. Galletly R, Brauer SG. Does the type of concurrent task affect preferred and cued gait in people with Parkinson's disease? Aust J Physiother. 2005;51(3):175-80. [DOI] [PubMed]
10.Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson's disease: comparison with a healthy control group. Arch Phys Med Rehabil. 2005;86(5):1007–1013. doi: 10.1016/j.apmr.2004.08.012. [DOI] [PubMed] [Google Scholar]; 10. Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson's disease: comparison with a healthy control group. Arch Phys Med Rehabil. 2005;86(5):1007-13. [DOI] [PubMed]
11.Liu W, McIntire K, Kim SH, Zhang J, Dascalos S, Lyons KE, et al. Bilateral subthalamic stimulation improves gait initiation in patients with Parkinson's disease. Gait Posture. 2006;23(4):492–498. doi: 10.1016/j.gaitpost.2005.06.012. [DOI] [PubMed] [Google Scholar]; 11. Liu W, McIntire K, Kim SH, Zhang J, Dascalos S, Lyons KE, et al. Bilateral subthalamic stimulation improves gait initiation in patients with Parkinson's disease. Gait Posture. 2006;23(4):492-8. [DOI] [PubMed]
12.Gantchev N, Viallet F, Aurenty R, Massion J. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol. 1996;101(2):110–120. doi: 10.1016/0924-980x(95)00253-h. [DOI] [PubMed] [Google Scholar]; 12. Gantchev N, Viallet F, Aurenty R, Massion J. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol. 1996;101(2):110-20. [DOI] [PubMed]
13.Roiz RM, Cacho EW, Pazinatto MM, Reis JG, Cliquet A, Jr, Barasnevicius-Quagliato EM. Gait analysis comparing Parkinson's disease with healthy elderly subjects. Arq Neuropsiquiatr. 2010;68(1):81–86. doi: 10.1590/s0004-282x2010000100018. [DOI] [PubMed] [Google Scholar]; 13. Roiz RM, Cacho EW, Pazinatto MM, Reis JG, Cliquet A Jr, Barasnevicius-Quagliato EM. Gait analysis comparing Parkinson's disease with healthy elderly subjects. Arq Neuropsiquiatr. 2010;68(1):81-6. [DOI] [PubMed]
14.McVey MA, Stylianou AP, Luchies CW, Lyons KE, Pahwa R, Jernigan S, et al. Early biomechanical markers of postural instability in Parkinson's disease. Gait Posture. 2009;30(4):538–542. doi: 10.1016/j.gaitpost.2009.08.232. [DOI] [PubMed] [Google Scholar]; 14. McVey MA, Stylianou AP, Luchies CW, Lyons KE, Pahwa R, Jernigan S, et al. Early biomechanical markers of postural instability in Parkinson's disease. Gait Posture. 2009;30(4):538-42. [DOI] [PubMed]
15.Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. 2003;24(2):197–211. doi: 10.1016/s0197-4580(02)00065-9. [DOI] [PubMed] [Google Scholar]; 15. Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. 2003;24(2):197-211. [DOI] [PubMed]
16.Miyai I, Fujimoto Y, Ueda Y, Yamamoto H, Nozaki S, Saito T, et al. Treadmill training with body weight support: its effect on Parkinson's disease. Arch Phys Med Rehabil. 2000;81(7):849–852. doi: 10.1053/apmr.2000.4439. [DOI] [PubMed] [Google Scholar]; 16. Miyai I, Fujimoto Y, Ueda Y, Yamamoto H, Nozaki S, Saito T, et al. Treadmill training with body weight support: its effect on Parkinson's disease. Arch Phys Med Rehabil. 2000;81(7):849-52. [DOI] [PubMed]
17.Miyai I, Fujimoto Y, Yamamoto H, Ueda Y, Saito T, Nozaki S, et al. Long-term effect of body weight-supported treadmill training in Parkinson's disease: a randomized controlled trial. Arch Phys Med Rehabil. 2002;83(10):1370–1373. doi: 10.1053/apmr.2002.34603. [DOI] [PubMed] [Google Scholar]; 17. Miyai I, Fujimoto Y, Yamamoto H, Ueda Y, Saito T, Nozaki S, et al. Long-term effect of body weight-supported treadmill training in Parkinson's disease: a randomized controlled trial. Arch Phys Med Rehabil. 2002;83(10):1370-3. [DOI] [PubMed]
18.Herman T, Giladi N, Hausdorff JM. Treadmill training for the treatment of gait disturbances in people with Parkinson's disease: a mini-review. J Neural Transm (Vienna) 2009;116(3):307–318. doi: 10.1007/s00702-008-0139-z. Review. [DOI] [PubMed] [Google Scholar]; 18. Herman T, Giladi N, Hausdorff JM. Treadmill training for the treatment of gait disturbances in people with Parkinson's disease: a mini-review. J Neural Transm (Vienna). 2009;116(3):307-18. Review. [DOI] [PubMed]
19.Hottenrott K, Ludyga S, Schulze S. Effects of high intensity training and continuous endurance training on aerobic capacity and body composition in recreationally active runners. J Sport Sci Med. 2012;11(3):483–488. [PMC free article] [PubMed] [Google Scholar]; 19. Hottenrott K, Ludyga S, Schulze S. Effects of high intensity training and continuous endurance training on aerobic capacity and body composition in recreationally active runners. J Sport Sci Med. 2012;11(3):483-8. [PMC free article] [PubMed]
20.Schenkman M, Hall DA, Barón AE, Schwartz RS, Mettler P, Kohrt WM. Exercise for people in early- or mid-stage Parkinson disease: a 16-month randomized controlled trial. Phys Ther. 2012;92(11):1395–1410. doi: 10.2522/ptj.20110472. [DOI] [PMC free article] [PubMed] [Google Scholar]; 20. Schenkman M, Hall DA, Barón AE, Schwartz RS, Mettler P, Kohrt WM. Exercise for people in early- or mid-stage Parkinson disease: a 16-month randomized controlled trial. Phys Ther. 2012;92(11):1395-410. [DOI] [PMC free article] [PubMed]
21.Bello O. Fernandez-Del-Olmo M. How does the treadmill affect gait in Parkinson's disease? Curr Aging Sci. 2012;5(1):28–34. doi: 10.2174/1874609811205010028. Review. [DOI] [PubMed] [Google Scholar]; 21. Bello O, Fernandez-Del-Olmo M. How does the treadmill affect gait in Parkinson's disease? Curr Aging Sci. 2012;5(1):28-34. Review. [DOI] [PubMed]
22.Mehrholz J, Kugler J, Storch A, Pohl M, Hirsch K, Elsner B. Treadmill training for patients with Parkinson's disease. Cochrane Database Syst Rev. 2015;(8):CD007830–CD007830. doi: 10.1002/14651858.CD007830.pub3. Update in: Cochrane Database Syst Rev. 2015; (9):CD007830. [DOI] [PubMed] [Google Scholar]; 22. Mehrholz J, Kugler J, Storch A, Pohl M, Hirsch K, Elsner B. Treadmill training for patients with Parkinson's disease. Cochrane Database Syst Rev. 2015;(8):CD007830. Update in: Cochrane Database Syst Rev. 2015; (9):CD007830. [DOI] [PMC free article] [PubMed]
23.Frazzitta G, Pezzoli G, Bertotti G, Maestri R. Asymmetry and freezing of gait in parkinsonian patients. J Neurol. 2013;260(1):71–76. doi: 10.1007/s00415-012-6585-4. [DOI] [PubMed] [Google Scholar]; 23. Frazzitta G, Pezzoli G, Bertotti G, Maestri R. Asymmetry and freezing of gait in parkinsonian patients. J Neurol. 2013;260(1):71-6. [DOI] [PubMed]
24.Yang YR, Tseng CY, Chiou SY, Liao KK, Cheng SJ, Lai KL, et al. Combination of rTMS and treadmill training modulates corticomotor inhibition and improves walking in Parkinson disease: a randomized trial. Neurorehabil Neural Repair. 2013;27(1):79–86. doi: 10.1177/1545968312451915. [DOI] [PubMed] [Google Scholar]; 24. Yang YR, Tseng CY, Chiou SY, Liao KK, Cheng SJ, Lai KL, et al. Combination of rTMS and treadmill training modulates corticomotor inhibition and improves walking in Parkinson disease: a randomized trial. Neurorehabil Neural Repair. 2013;27(1):79-86. [DOI] [PubMed]
25.Galli M, Cimolin V, De Pandis MF, Le Pera D, Sova I, Albertini G, et al. Robot-assisted gait training versus treadmill training in patients with Parkinson's disease: a kinematic evaluation with gait profile score. Funct Neurol. 2016;31(3):163–170. doi: 10.11138/FNeur/2016.31.3.163. [DOI] [PMC free article] [PubMed] [Google Scholar]; 25. Galli M, Cimolin V, De Pandis MF, Le Pera D, Sova I, Albertini G, et al. Robot-assisted gait training versus treadmill training in patients with Parkinson's disease: a kinematic evaluation with gait profile score. Funct Neurol. 2016;31(3):163-70. [DOI] [PMC free article] [PubMed]
26.Canning CG, Allen NE, Dean CM, Goh L, Fung VS. Home-based treadmill training for individuals with Parkinson's disease: a randomized controlled pilot trial. Clin Rehabil. 2012;26(9):817–826. doi: 10.1177/0269215511432652. [DOI] [PubMed] [Google Scholar]; 26. Canning CG, Allen NE, Dean CM, Goh L, Fung VS. Home-based treadmill training for individuals with Parkinson's disease: a randomized controlled pilot trial. Clin Rehabil. 2012;26(9):817-26. [DOI] [PubMed]
27.Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P. Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord. 2009;24(8):1139–1143. doi: 10.1002/mds.22491. [DOI] [PubMed] [Google Scholar]; 27. Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P. Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord. 2009;24(8):1139-43. [DOI] [PubMed]
28.Picelli A, Melotti C, Origano F, Neri R, Waldner A, Smania N. Robot-assisted gait training versus equal intensity treadmill training in patients with mild to moderate Parkinson's disease: a randomized controlled trial. Parkinsonism Relat Disord. 2013;19(6):605–610. doi: 10.1016/j.parkreldis.2013.02.010. [DOI] [PubMed] [Google Scholar]; 28. Picelli A, Melotti C, Origano F, Neri R, Waldner A, Smania N. Robot-assisted gait training versus equal intensity treadmill training in patients with mild to moderate Parkinson's disease: a randomized controlled trial. Parkinsonism Relat Disord. 2013;19(6):605-10. [DOI] [PubMed]
29.Fisher BE, Wu AD, Salem GJ, Song J, Lin CH, Yip J, et al. 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(7):1221–1229. doi: 10.1016/j.apmr.2008.01.013. [DOI] [PMC free article] [PubMed] [Google Scholar]; 29. Fisher BE, Wu AD, Salem GJ, Song J, Lin CH, Yip J, et al. 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(7):1221-9. [DOI] [PMC free article] [PubMed]
30.Schlick C, Ernst A, Bötzel K, Plate A, Pelykh O, Ilmberger J. Visual cues combined with treadmill training to improve gait performance in Parkinson's disease: a pilot randomized controlled trial. Clin Rehabil. 2016;30(5):463–471. doi: 10.1177/0269215515588836. [DOI] [PubMed] [Google Scholar]; 30. Schlick C, Ernst A, Bötzel K, Plate A, Pelykh O, Ilmberger J. Visual cues combined with treadmill training to improve gait performance in Parkinson's disease: a pilot randomized controlled trial. Clin Rehabil. 2016;30(5):463-71. [DOI] [PubMed]
31.Arcolin I, Pisano F, Delconte C, Godi M, Schieppati M, Mezzani A, et al. Intensive cycle ergometer training improves gait speed and endurance in patients with Parkinson's disease: a comparison with treadmill training. Restor Neurol Neurosci. 2016;34(1):125–138. doi: 10.3233/RNN-150506. [DOI] [PubMed] [Google Scholar]; 31. Arcolin I, Pisano F, Delconte C, Godi M, Schieppati M, Mezzani A, et al. Intensive cycle ergometer training improves gait speed and endurance in patients with Parkinson's disease: a comparison with treadmill training. Restor Neurol Neurosci. 2016;34(1):125-38. [DOI] [PubMed]
32.Herman T, Giladi N, Gruendlinger L, Hausdorff JM. 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(9):1154–1158. doi: 10.1016/j.apmr.2007.05.015. [DOI] [PubMed] [Google Scholar]; 32. Herman T, Giladi N, Gruendlinger L, Hausdorff JM. 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(9):1154-8. [DOI] [PubMed]
33.Fernández-Lago H, Bello O, Mora-Cerdá F, Montero-Cámara J, Fernández-Del-Olmo MÁ. Treadmill walking combined with anodal transcranial direct current stimulation in Parkinson disease: a pilot study of kinematic and neurophysiological effects. Am J Phys Med Rehabil. 2017;96(11):801–808. doi: 10.1097/PHM.0000000000000751. [DOI] [PubMed] [Google Scholar]; 33. Fernández-Lago H, Bello O, Mora-Cerdá F, Montero-Cámara J, Fernández-Del-Olmo MÁ. Treadmill walking combined with anodal transcranial direct current stimulation in Parkinson disease: a pilot study of kinematic and neurophysiological effects. Am J Phys Med Rehabil. 2017;96(11):801-8. [DOI] [PubMed]
34.Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17(5):427–442. doi: 10.1212/wnl.17.5.427. [DOI] [PubMed] [Google Scholar]; 34. Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17(5):427-42. [DOI] [PubMed]
35.Schapira AH, Emre M, Jenner P, Poewe W. Levodopa in the treatment of Parkinson's disease. Eur J Neurol. 2009;16(9):982–989. doi: 10.1111/j.1468-1331.2009.02697.x. Review. [DOI] [PubMed] [Google Scholar]; 35. Schapira AH, Emre M, Jenner P, Poewe W. Levodopa in the treatment of Parkinson's disease. Eur J Neurol. 2009;16(9):982-9. Review. [DOI] [PubMed]
36.Jenkins ME, Johnson AM, Holmes JD, Stephenson FF, Spaulding SJ. Predictive validity of the UPDRS postural stability score and the functional reach test, when compared with ecologically valid reaching tasks. Parkinsonism Relat Disord. 2010;16(6):409–411. doi: 10.1016/j.parkreldis.2010.04.002. [DOI] [PubMed] [Google Scholar]; 36. Jenkins ME, Johnson AM, Holmes JD, Stephenson FF, Spaulding SJ. Predictive validity of the UPDRS postural stability score and the functional reach test, when compared with ecologically valid reaching tasks. Parkinsonism Relat Disord. 2010;16(6):409-11. [DOI] [PubMed]
37.Barry E, Galvin R, Keogh C, Horgan F, Fahey T. Is the Timed Up and Go test a useful predictor of risk of falls in community dwelling older adults: a systematic review and meta-analysis. BMC Geriatr. 2014;14(1):14–14. doi: 10.1186/1471-2318-14-14. Review. [DOI] [PMC free article] [PubMed] [Google Scholar]; 37. Barry E, Galvin R, Keogh C, Horgan F, Fahey T. Is the Timed Up and Go test a useful predictor of risk of falls in community dwelling older adults: a systematic review and meta-analysis. BMC Geriatr. 2014;14(1):14. Review. [DOI] [PMC free article] [PubMed]
38.Isles RC, Choy NL, Steer M, Nitz JC. Normal values of balance tests in women aged 20-80. J Am Geriatr Soc. 2004;52(8):1367–1372. doi: 10.1111/j.1532-5415.2004.52370.x. [DOI] [PubMed] [Google Scholar]; 38. Isles RC, Choy NL, Steer M, Nitz JC. Normal values of balance tests in women aged 20-80. J Am Geriatr Soc. 2004;52(8):1367-72. [DOI] [PubMed]
39.Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the timed up & go test. Phys Ther. 2000;80(9):896–903. [PubMed] [Google Scholar]; 39. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the timed up & go test. Phys Ther. 2000;80(9):896-903. [PubMed]
40.Li AM, Yin J, Yu CC, Tsang T, So HK, Wong E, et al. The six-minute walk test in healthy children: reliability and validity. Eur Respir J. 2005;25(6):1057–1060. doi: 10.1183/09031936.05.00134904. [DOI] [PubMed] [Google Scholar]; 40. Li AM, Yin J, Yu CC, Tsang T, So HK, Wong E, et al. The six-minute walk test in healthy children: reliability and validity. Eur Respir J. 2005;25(6):1057-60. [DOI] [PubMed]
41.American Thoracic Society/European Respiratory Society ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166(4):518–624. doi: 10.1164/rccm.166.4.518. [DOI] [PubMed] [Google Scholar]; 41. American Thoracic Society/European Respiratory Society. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002; 166(4):518-624. [DOI] [PubMed]
42.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(12):1760–1766. doi: 10.1016/s0003-9993(03)00433-7. [DOI] [PubMed] [Google Scholar]; 42. 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(12):1760-6. [DOI] [PubMed]
43.Shulman LM, Katzel LI, Ivey FM, Sorkin JD, Favors K, Anderson KE, et al. Randomized clinical trial of 3 types of physical exercise for patients with Parkinson disease. JAMA Neurol. 2013;70(2):183–190. doi: 10.1001/jamaneurol.2013.646. [DOI] [PMC free article] [PubMed] [Google Scholar]; 43. Shulman LM, Katzel LI, Ivey FM, Sorkin JD, Favors K, Anderson KE, et al. Randomized clinical trial of 3 types of physical exercise for patients with Parkinson disease. JAMA Neurol. 2013;70(2):183-90. [DOI] [PMC free article] [PubMed]
44.Carda S, Invernizzi M, Baricich A, Comi C, Croquelois A, Cisari C. Robotic gait training is not superior to conventional treadmill training in parkinson disease: a single-blind randomized controlled trial. Neurorehabil Neural Repair. 2012;26(9):1027–1034. doi: 10.1177/1545968312446753. [DOI] [PubMed] [Google Scholar]; 44. Carda S, Invernizzi M, Baricich A, Comi C, Croquelois A, Cisari C. Robotic gait training is not superior to conventional treadmill training in parkinson disease: a single-blind randomized controlled trial. Neurorehabil Neural Repair. 2012;26(9):1027-34. [DOI] [PubMed]
45.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):307–322. [PubMed] [Google Scholar]; 45. 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]
46.Ganesan M, Sathyaprabha TN, Gupta A, Pal PK. Effect of partial weight-supported treadmill gait training on balance in patients with Parkinson disease. PM R. 2014;6(1):22–33. doi: 10.1016/j.pmrj.2013.08.604. [DOI] [PubMed] [Google Scholar]; 46. Ganesan M, Sathyaprabha TN, Gupta A, Pal PK. Effect of partial weight-supported treadmill gait training on balance in patients with Parkinson disease. PM R. 2014;6(1):22-33. [DOI] [PubMed]
47.Murray MP, Sepic SB, Gardner GM, Downs WJ. Walking patterns of men with parkinsonism. Am J Phys Med Rehab. 1978;57(6):278–294. [PubMed] [Google Scholar]; 47. Murray MP, Sepic SB, Gardner GM, Downs WJ. Walking patterns of men with parkinsonism. Am J Phys Med Rehab. 1978;57(6):278-94. [PubMed]
48.Mhatre PV, Vilares I, Stibb SM, Albert MV, Pickering L, Marciniak CM, et al. Wii Fit balance board playing improves balance and gait in Parkinson disease. PM R. 2013;5(9):769–777. doi: 10.1016/j.pmrj.2013.05.019. [DOI] [PMC free article] [PubMed] [Google Scholar]; 48. Mhatre PV, Vilares I, Stibb SM, Albert MV, Pickering L, Marciniak CM, et al. Wii Fit balance board playing improves balance and gait in Parkinson disease. PM R. 2013;5(9):769-77. [DOI] [PMC free article] [PubMed]
49.Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov Disord. 2002;17(6):1148–1160. doi: 10.1002/mds.10259. Review. [DOI] [PubMed] [Google Scholar]; 49. Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov Disord. 2002;17(6):1148-60. Review. [DOI] [PubMed]

Einstein (Sao Paulo). 2020 Nov 18;18:eRW5233. [Article in Portuguese]

Efeitos do treinamento de marcha em esteira em idosos com doença de Parkinson: uma revisão da literatura

RESUMO

A doença de Parkinson é o segundo distúrbio neurodegenerativo mais comum na velhice. O processo de envelhecimento de idosos com doença de Parkinson pode levar a distúrbios de marcha com mais incapacidades funcionais do que para idosos sem a doença. O treinamento em esteira como terapia pode resultar em efeitos notáveis na marcha de pacientes com Parkinson e ser um recurso para a reabilitação neurológica geriátrica. Esta revisão teve como objetivo estudar os efeitos da marcha após o treinamento em esteira na doença de Parkinson em idosos. A pesquisa foi realizada nas bases de dados PubMed®, LILACS, PEDro e EMBASE, com os seguintes descritores: “doença de Parkinson”, “idosos”, “treinamento em esteira” e “avaliação da marcha”. A qualidade dos estudos incluídos foi avaliada pela escala de PEDro. Atenderam aos critérios de inclusão e exclusão 11 estudos. Oito estudos foram randomizados, e apenas um fez follow-up . Foi possível observar que treinamento em esteira com ou sem suporte de peso (por pelo menos 20 minutos, duas a três vezes por semana, com aumento progressivo de cargas, por, no mínimo, 6 semanas) em idosos com doença de Parkinson foi efetivo para melhorar a marcha. Além disso, ambos os treinamentos foram considerados seguros (pois alguns estudos relataram o uso de cintos, mesmo no treinamento sem suporte de peso) e podem ser associados a terapias complementares à marcha, como estimulação magnética transcraniana repetitiva, estímulos visuais ou estimulação transcraniana direta anódica. O treinamento em esteira em pacientes idosos com doença de Parkinson é uma intervenção que melhora os resultados da marcha, mas requer mais estudos para melhor comprovação.

Descritores: Doença de Parkinson/reabilitação, Marcha, Idoso

INTRODUÇÃO

A doença de Parkinson (DP) idiopática é crônica, progressiva e degenerativa do sistema nervoso central, estando associada a uma depleção nos neurônios dopaminérgicos na via nigroestriatal.⁽¹⁾Os sintomas clínicos aparecem quando há redução de 40% a 60% dos neurônios nigrais e da dopamina estriatal.⁽²⁾A DP é a segunda doença degenerativa mais comum do sistema nervoso, afetando 1% a 2% da população com mais de 65 anos.⁽³⁾A proporção de idosos no mundo está aumentando, o que resulta em maior número de pessoas em risco de DP.⁽⁴⁾

Os sintomas cardinais incluem tremor em repouso, rigidez muscular, congelamento da marcha (FOG - freezing of gait ), bradicinesia, e instabilidade de marcha e postural.⁽³^,⁴⁾Os distúrbios da marcha comprometem a independência e a qualidade de vida dos pacientes, diminuindo sua mobilidade e aumentando o risco de quedas e fraturas.⁽⁵⁾A DP induz a distúrbios da marcha, como redução da velocidade, redução do comprimento da passada e do passo, e aumento do tempo de apoio duplo.⁽⁴^–⁸⁾

A redução da velocidade de marcha é explicada por um deslocamento mais lento do centro de gravidade, um menor componente vertical da força de reação do solo⁽⁹^–¹¹⁾e um maior deslocamento lateral do centro de pressão no início da marcha.⁽¹²⁾A redução no comprimento do passo ocorre principalmente devido à deficiência na fase de descolamento do pé, na qual se observam menor sinal eletromiográfico do músculo gastrocnêmio e consequente dificuldade para projetar o membro para a frente.⁽¹⁰⁾O aumento da fase de suporte está relacionado à diminuição da velocidade da marcha e à bradicinesia.⁽⁵⁾Isso dificulta o automatismo do passo na marcha e promove alterações no sinal eletromiográfico dos membros inferiores.⁽¹³^,¹⁴⁾

Da mesma forma, o envelhecimento também diminui a velocidade da marcha e o comprimento do passo, o que sugere que a DP, em idosos, pode ocasionar maior incapacidade funcional e torná-los mais suscetíveis a quedas.⁽¹⁵⁾

No tocante à reabilitação física da marcha, o treinamento em esteira (TE) como terapia mostrou efeitos notáveis na marcha de pacientes com DP, com resultados superiores nos parâmetros de marcha em comparação com os pacientes que não são submetidos a esse tratamento.⁽¹⁶^–²¹⁾Revisões da literatura mostram que o TE pode promover padrão de caminhada mais estável em pacientes com DP, sugerindo que a intervenção é capaz de restaurar a ritmicidade e reduzir a variabilidade da marcha.⁽¹⁸^,²¹^,²²⁾No entanto, essas revisões analisam vários desfechos, mas nenhuma enfatiza os idosos.

OBJETIVO

O objetivo deste estudo foi analisar os efeitos na marcha após treinamento em esteira em pacientes idosos com doença de Parkinson.

MÉTODOS

Estratégia de busca

A busca foi realizada nas bases de dados PubMed^®, LILACS, PEDro e EMBASE, tendo encontrado artigos publicados relacionados aos efeitos do TE na marcha de pacientes idosos com DP, com os seguintes descritores: “doença de Parkinson”, “idosos”, “treinamento em esteira” e “avaliação da marcha”.

Seleção de estudos

A revisão crítica da literatura foi realizada considerando os seguintes critérios de inclusão: estudos em humanos, no idioma inglês e publicados em periódicos científicos nos últimos 10 anos. Foram excluídos os artigos que descreviam pacientes com idade inferior a 60 anos, ou que não realizaram treinamento de marcha em esteira, e sem medidas de desfecho em relação à marcha. Os artigos que descreviam treinamento de marcha em esteira em pacientes sem DP e treinamento de marcha em esteira combinados com realidade virtual também foram excluídos. Após a leitura dos títulos e/ou resumos, foram selecionados os artigos que atenderam aos critérios de inclusão e identificados como relevantes para o desenvolvimento deste trabalho. Foram encontradas 25 referências após combinações simples no PubMed^®, LILACS, PEDro e EMBASE. Foram finalmente selecionados 11 artigos com base nos critérios estabelecidos.

Avaliação da qualidade

A qualidade dos 11 estudos incluídos(23-33) foi avaliada pela lista de verificação da escala PEDro ( Tabela 1 ), que apresenta 11 itens que levam em consideração os seguintes critérios: elegibilidade e origem dos participantes; distribuição randômica; distribuição oculta; comparabilidade da linha de base; cegamento de sujeitos; cegamento de terapeutas; cegamento de avaliadores; resultados com mais de 85% dos participantes; análise de intenção de tratamento; comparações estatísticas entre grupos; e medidas de precisão e medidas de variabilidade.

Tabela 1. Escala PEDro de 11 estudos selecionados.

Autores	Elegibilidade	Distribuição randômica	Distribuição oculta	Comparabilidade da linha de base	Cegamento de pacientes	Cegamento de terapeutas	Cegamento de avaliadores	Resultados com mais de 85% dos participantes	Análise de intenção de tratamento	Comparações estatísticas entre os grupos	Medidas de precisão e medidas de avaliação
Frazzitta et al.⁽²³⁾	Sim	Sim	Não	Sim	Não	Não	Sim	Sim	Sim	Sim	Não
Yang et al.⁽²⁴⁾	Sim	Não	Sim	Sim	Sim	Sim	Sim	Sim	Sim	Sim	Sim
Galli et al.⁽²⁵⁾	Sim	Não	Sim	Sim	Sim	Sim	Sim	Sim	Sim	Sim	Não
Canning et al.⁽²⁶⁾	Sim	Não	Sim	Sim	Não	Não	Sim	Sim	Sim	Sim	Sim
Frazzitta et al.⁽²⁷⁾	Sim	Sim	Não	Sim	Não	Não	Sim	Sim	Sim	Sim	Não
Picelli et al.⁽²⁸⁾	Sim	Não	Sim	Sim	Não	Não	Sim	Sim	Sim	Sim	Não
Fisher et al.⁽²⁹⁾	Sim	Não	Sim	Sim	Sim	Não	Não	Sim	Sim	Sim	Não
Schlick et al.⁽³⁰⁾	Sim	Não	Sim	Sim	Não	Não	Não	Sim	Sim	Sim	Não
Arcolin et al.⁽³¹⁾	Sim	Não	Não	Sim	Não	Não	Não	Sim	Sim	Sim	Não
Herman et al.⁽³²⁾	Sim	Não	Não	Não	Não	Não	Não	Sim	Sim	Não	Não
Fernández-Lago et al.⁽³³⁾	Sim	Não	Não	Sim	Não	Não	Não	Sim	Sim	Sim	Não

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RESULTADOS

Onze estudos atenderam aos critérios de inclusão.⁽²³^–³³⁾Os estudos que obtiveram maior pontuação na escala PEDro foram realizados por Yang et al.,⁽²⁴⁾e Galli et al.,⁽²⁵⁾( Tabela 1 ).

Dos 11 estudos,⁽²³^–³³⁾oito foram randomizados.⁽²³^–³⁰⁾Em relação ao tipo de treinamento, cinco estudos analisaram treinamento sem suporte de peso corporal,⁽²³^,²⁴^,²⁶^,²⁷^,³⁰⁾e três avaliaram treinamento com sistema de suporte⁽²⁵^,²⁸^,²⁹⁾( Tabela 2 ).

Tabela 2. Resumo sobre população, protocolos, medidas de marcha e resultados destes estudos.

Estudos	População	Protocolo	Medidas de marcha	Resultados
Frazzitta et al.⁽²³⁾	30 pacientes com distúrbio de marcha, mas sem FOG em estágio on , e 30 pacientes com FOG em estágio on	Os pacientes passaram por tratamento de reabilitação de 4 semanas usando uma esteira com pistas auditivas e visuais	Velocidade da marcha, comprimento da passada, assimetria de marcha, TC6, UPDRS II–III, Escala de Equilíbrio de Berg, TUG, velocidade de marcha confortável, FOG-Q	Os dados apoiam um envolvimento direto da assimetria da marcha no desenvolvimento do FOG na DP. O TE é eficaz para melhoria da marcha e do equilíbrio em pacientes com DP e FOG, e isso pode estar relacionado à redução na assimetria da marcha
Yang et al.⁽²⁴⁾	20 pacientes com DP com capacidade de caminhar de forma independente	2 grupos: 1. Participantes que receberam EMTr (Grupo Experimental) 2. Participantes que receberam EMTr simulada (Grupo Controle) Seguido de TE (30 minutos) por 12 sessões durante 4 semanas (3 sessões por semana)	Inibição corticomotora e desempenho da marcha	Os achados sugerem que a combinação de EMTr com TE aumenta o efeito do TE na modulação da inibição corticomotora e na melhoria do desempenho da marcha nos pacientes com DP
Galli et al.⁽²⁵⁾	50 pacientes com DP idiopáticaCapacidade de caminhar, sem auxílio ou com pouco auxílio, por distância de 25 pés (7,62m)	2 grupos: 1. Grupo de terapia com assistência robótica (n=25) 2. Grupo de terapia intensiva em esteira (n=25)	Escala Hoehn e Yahr;UPDRSSistema optoeletrônico (ELITE2002, BTS, Milão, Itália)	No grupo robótico, foram encontradas diferenças nas variáveis cinemáticas (obliquidade pélvica e abdução e adução do quadril). O grupo intensivo não mostrou alterações estatisticamente significativas. O treinamento locomotor de reabilitação robótica para efetor final melhorou as características cinemáticas da marcha e pareceu ser eficaz na reabilitação de pacientes com DP leve
Canning et al.⁽²⁶⁾	20 pacientes com DP idiopática com <2 horas por semana de atividade física de lazer nos 3 meses anteriores e que tiveram resposta estável à levodopa	2 grupos: 1. O Grupo Experimental foi submetido a um programa semissupervisionado de 30 a 40 minutos de caminhada na esteira, realizado no lar, 4 vezes por semana, durante 6 semanas 2. O Grupo Controle recebeu os cuidados habituais (ou seja, foi aconselhado a manter os níveis atuais de atividade física)	O desfecho primário de eficácia foi a capacidade de caminhar (distância percorrida no TC6)	O TE semissupervisionado no lar é uma forma viável e segura de exercício para pessoas cognitivamente intactas, com DP leve
Frazzita et al.(27)	40 pacientes parkinsonianos com congelamento foram aleatoriamente designados a dois grupos	2 grupos: 1. Foi submetido a um programa de reabilitação baseado em treinamento em esteira associado a pistas auditivas e visuais 2. Seguiu um protocolo de reabilitação usando dicas e não associado a esteira	A avaliação funcional foi baseada na Unified Parkinson's Disease Rating Scale Motor Section (UPDRS III); Freezing of Gait Questionnaire (FOGQ), teste de caminhada de 6 minutos (TC6), velocidade da marcha e ciclo de passada	Os resultados sugerem que o treinamento em esteira associado a pistas auditivas e visuais pode dar melhores resultados do que os tratamentos convencionais. O treinamento em esteira provavelmente atua como uma dica externa complementar
Picelli et al.⁽²⁸⁾	60 pacientes com DP leve a moderada	- 3 grupos: 1. Grupo de treinamento de marcha com assistência robótica (n=20) 2. Grupo de TE (n=20) realizou treinamento em intensidade igual sem apoio de peso corpóreo 3. Grupo de fisioterapia (n=20) foi submetido à terapia convencional da marcha45 minutos por sessão 3 dias por semana, por 4 semanas consecutivas	Teste de caminhada de 10 minutos TC6	Nenhuma diferença estatisticamente significativa foi encontrada entre o grupo de treinamento de marcha com assistência robótica e o grupo de TE na avaliação após o treinamento. Uma melhora estatisticamente significativa foi encontrada após o tratamento, a favor do grupo de treinamento de marcha com assistência robótica e do grupo de TE, em comparação com o grupo de fisioterapia. Os achados foram confirmados na avaliação de acompanhamento de 3 meses
Fisher et al.⁽²⁹⁾	30 pacientes com DP, dentro de 3 anos após o diagnóstico, com estágios 1 ou 2 na escala de Hoehn e Yahr	- 3 grupos: 1. Alta intensidade (TE com apoio de peso corporal) 2. Exercício de baixa intensidade (exercícios para amplitude de movimento, equilíbrio e marcha) 3. Intensidade zero (grupo de orientação)	UPDRS Análise biomecânica da caminhada autosselecionada e da caminhada rápida Tarefas sentado para de pé Excitabilidade corticomotora	Foi observada pequena melhora no UPDRS total e motor em todos os grupos. Os indivíduos do grupo de alta intensidade mostraram aumento pós-exercício na velocidade da marcha, no comprimento do passo e da passada, e na excursão das articulações do quadril e do tornozelo, durante a marcha autosselecionada e a marcha rápida, além de melhor distribuição do peso nas tarefas sentado para de pé. Não foi observada melhora consistente nas medidas da marcha e nas tarefas sentado para de pé nos grupos de baixa intensidade e de intensidade zero. O grupo de alta intensidade apresentou aumento no período de silêncio cortical
Schlick et al.⁽³⁰⁾	23 pacientes ambulatoriais com DP	Os pacientes foram submetidos a 12 sessões de treinamento dentro de 5 semanas com pistas visuais combinadas ao TE (n=12) ou apenas TE (n=11)	Velocidade da marcha, comprimento da passada e cadência; Os testes funcionais incluíram o TUG, UPDRS e o questionário de congelamento da marcha	Este estudo piloto sugere que as pistas visuais combinadas ao TE têm efeitos mais benéficos na marcha do que o TE, em pacientes com estágio moderado da DP. Faz-se necessário um estudo em larga escala com acompanhamento mais longo
Arcolin et al.⁽³¹⁾	29 pacientes com diagnóstico de DP idiopáticaHabilidade para caminhar, sem ajuda	2 grupos (randomizados): 1. Esteira (n=13) 2. Cicloergômetro (n=16) Treinamento por 3 semanas, 1 hora por dia	TC6 Variáveis espaciais e temporais da marcha avaliadas por baropodometria TUG MINIBESTest UPDRS	Este estudo piloto mostra que o treinamento em cicloergômetro melhora os parâmetros de caminhada e reduz os sinais clínicos de DP, tanto quanto o TE. A velocidade da marcha é acompanhada pelo aumento no comprimento do passo, tornando o padrão da marcha próximo ao de indivíduos saudáveis. O cicloergômetro é alternativa válida à esteira para melhorar a marcha em curto prazo em pacientes com DP
Herman et al.⁽³²⁾	9 pacientes com DP que eram capazes de deambular de forma independente e não estavam demenciados	Os pacientes caminharam em esteira por 30 minutos durante cada sessão de treinamento, em 4 sessões de treinamento por semana, durante 6 semanas	PDQ-39, com 39 perguntasUPDRSVelocidade da marcha, variabilidade no tempo da passada, variabilidade no tempo de balançoSPPB	Esses resultados mostram o potencial para aumento da ritmicidade da marcha em pacientes com DP e sugerem que um programa de TE progressivo e intensivo pode ser usado para minimizar défices de marcha, reduzir o risco de queda e aumentar a qualidade de vida desses pacientes
Fernández-Lago et al.⁽³³⁾	18 pacientes com DP idiopática Habilidade de caminhar, sem ajuda	Foram avaliados 18 participantes com DP sob estas três condições (grupos):1. Somente caminhada em esteira (esteira) 2. Caminhada em esteira combinada a ETCC anódica (ETCCa + esteira) aplicada ao córtex motor;3. Caminhada em esteira combinada a estimulação simulada (ETCCs + esteira).	Desempenho de caminhada no solo, reflexo H do músculo sóleo, inibição recíproca da fibra sensorial Ia do músculo tibial anterior para o músculo sóleo, facilitação intracortical e inibição intracortical de curta duração do músculo tibial anterior	Todas as configurações de esteira melhoraram o desempenho da caminhada e modularam os parâmetros espinais e corticospinais comparando-se a outros tipos de tratamento. No entanto, a opção ETCCa + esteira resultou em modulação diferente da inibição recíproca da fibra sensorial Ia, em comparação com as outras configurações de esteira

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FOG: congelamento da marcha; TC6: teste de caminhada de 6 minutos; UPDPRS: Escala Unificada de Avaliação da Doença de Parkinson; TUG: Timed Up and Go; FOG-Q: Questionário de Congelamento da Marcha; TE: treinamento em esteira; DP: doença de Parkinson; EMTr: estimulação magnética transcraniana repetitiva; MINIBESTest: Balance Evaluation Systems Test ; PDQ-39: Parkinson Disease Questionnaire-39; SPPB: Short Physical Performance Battery; ETCC: estimulação transcraniana por corrente contínua.

DISCUSSÃO

Alguns estudos sobre TE em pacientes com DP, assim como revisões da literatura, abordam o assunto. No entanto, as revisões analisam grupos de todas as idades e apresentam metodologias com desfechos primários diferentes: qualidade de vida, equilíbrio e marcha. Nossa revisão teve como objetivo focar apenas estudos com grupos de pacientes com DP com mais de 60 anos, bem como desfechos relacionados a especificidades da marcha. De acordo com a lista de verificação da escala PEDro, os artigos incluídos foram considerados adequados para publicação científica.

A escala Hoehn e Yarh variou de 1 a 3, e a maioria dos pacientes⁽²³^,²⁵^–²⁷^,²⁹^,³²^,³³⁾estudados estava entre 1 e 2 – classificação essa que indica discreto deficit de equilíbrio. Em quatro estudos,⁽²⁴^,²⁸^,³⁰^,³¹⁾o estágio estava entre 2 e 3, uma classificação na qual a doença é obrigatoriamente bilateral e há certa instabilidade postural, mas o paciente é independente em termos físicos.

A escala Hoehn e Yarh caracteriza a condição funcional do paciente por meio de observação.⁽³⁴⁾Outros estudos com pacientes com menos de 60 anos ou que mesclam diferentes grupos etários mostraram essa pontuação da escala Hoehn e Yarh. Assim, a classificação Hoehn e Yarh moderada pode sugerir que o envelhecimento não interferiu na doença.

A duração da doença foi outra variável demográfica que diferiu nos estudos. Em oito estudos,⁽¹⁵^–¹⁷^,¹⁹^,²¹^–²⁴⁾a duração ficava entre 5 e 10 anos e, em dois, a duração foi de mais de 10 anos.⁽²⁷^,²⁹⁾Somente um estudo não mencionou esse dado.⁽²³⁾Os estudos mostraram que, com a evolução da doença (5 a 7 anos), há piora da condição motora e surgimento de discinesias.⁽¹⁵⁾Dentre os pacientes que utilizaram levodopa por 6 anos ou mais, 70% tiveram complicações motoras e precisaram suspender temporariamente seu uso ( off ).⁽³⁵⁾

As avaliações da marcha utilizadas nos estudos de revisão foram computadorizadas ou funcionais. Ambas são importantes para a explicação dos resultados, mas algumas são mais específicas que outras e, portanto, podem ajudar mais na obtenção de respostas para as questões encontradas na prática clínica.⁽¹¹⁾

A avaliação motora da Escala Unificada de Avaliaçãoda Doença de Parkinson (UPDRS) foi utilizada na maioria dos estudos.⁽²³^,²⁹^–³²⁾É uma escala muito confiável (r=0,96) e válida, constituindo método adequado para a avaliação da DP.⁽³⁶⁾A seção de avaliação motora consiste em 14 itens (18 a 31), mas o item que avalia a marcha é de natureza observacional, não permitindo análise precisa.

O teste Timed Up and Go (TUG) também foi utilizado em cinco estudos.⁽²³^,²⁷^,³⁰^–³²⁾O TUG mede o tempo da tarefa motora de se levantar da cadeira, andar 3m, retornar e sentar-se.⁽³⁷⁾Isles et al.,⁽³⁸⁾definem o teste como sensível e específico para discriminar entre caidores e não caidores. É possível observar que o teste é utilizado para avaliar o equilíbrio e a mobilidade⁽³⁹⁾sem, porém, analisar características específicas da marcha.

Outra ferramenta de avaliação utilizada foi o teste de caminhada de 6 minutos (TC6).⁽¹⁴^,¹⁶^–¹⁹⁾Esse teste é utilizado para avaliar a resposta física e fornece análise abrangente dos sistemas respiratório, cardíaco e metabólico.⁽⁴⁰⁾Ele reflete limitações nas atividades cotidianas, como a marcha, mas, de acordo com a American Thoracic Society (ATS),⁽⁴¹⁾a indicação precisa do TC6 é a presença de doença pulmonar ou doença cardíaca leve a moderada, de modo que o teste é usado para medir a resposta ao tratamento e prever a morbimortalidade.

Os parâmetros espaciais (velocidade, comprimento do passo e cadência) são considerados significativos para a avaliação clínica da marcha. Eles podem ser calculados qualitativamente, sem câmeras nem softwares , ou de modo computadorizado, por meio de análises cinemáticas e cinéticas. Cinco estudos investigaram esses parâmetros por abordagem qualitativa⁽²⁷^,²⁹^–³²⁾e apenas dois o fizeram por meios computadorizados.⁽²⁵^,²⁹⁾O uso da análise tridimensional da marcha é escasso nos estudos sobre DP, mas é considerado o método padrão-ouro para melhor compreensão biomecânica, fornecendo dados reproduzíveis e confiáveis.⁽¹³⁾

O TE foi estudado com e sem suporte do peso corporal. Oito estudos analisaram o treinamento sem suporte do peso corporal,⁽¹⁴^–¹⁸^,²²^–²⁴⁾e três avaliaram com sistema de suporte.⁽¹⁹^–²¹⁾Todos apresentaram melhora nas variáveis da marcha após o treinamento, mas houve diferenças entre as metodologias.

Somente Herman et al.,⁽³²⁾realizaram estudo de acompanhamento. Realizaram seis semanas de TE (quatro vezes por semana, 30 minutos cada sessão), seguido de 1 mês de TE com aumento progressivo da intensidade em nove pacientes com DP. Houve melhora do UPDRS no tocante à velocidade e ao comprimento do passo, além de variabilidade da marcha após período de treinamento e acompanhamento de 6 semanas. Esses resultados sugeriram que um programa progressivo e intensivo de TE pode ser usado para minimizar deficiências na marcha, reduzir o risco de queda e aumentar a qualidade de vida desses pacientes.

Frazzitta et al.,⁽²³⁾recrutaram pacientes com Parkinson com e sem FOG, que foram submetidos ao mesmo protocolo de TE sem suporte associado a pistas visuais e auditivas. Os indivíduos receberam TE por 30 minutos todos os dias, 5 dias por semana, durante 4 semanas (20 sessões no total). O TE foi eficaz para melhorar a marcha e o equilíbrio em pacientes com DP, e essa assimetria na marcha pode estar relacionada a uma maior probabilidade de FOG.

Os outros compararam o TE tradicional com outro tipo de TE. Frazzitta et al.,⁽²⁷⁾compararam o TE sem suporte associado a pistas visuais e auditivas com o treinamento de marcha sem esteira, também associado a pistas visuais e auditivas. Os resultados sugerem que o TE associado a pistas auditivas e visuais pode produzir melhores resultados do que os tratamentos mais convencionais. Os indivíduos receberam treinamento por 20 minutos todos os dias, durante 4 semanas (28 sessões no total). O TE provavelmente atua como pista externa suplementar.

Schlick et al.,⁽³⁰⁾analisaram 20 pacientes com DP, que foram divididos em duas intervenções: grupo TE, com pistas visuais, e grupo TE, sem pistas. Esse estudo piloto sugere que as pistas visuais combinadas com o TE têm efeitos mais benéficos na marcha do que o TE tradicional. As pistas visuais atuam como estímulo para os receptores visuais, gerando estímulos aferentes sensoriais repetitivos para o sistema nervoso central. Em pacientes com DP, esses sinais também podem representar pistas sensoriais externas, sendo um gatilho para a ativação de circuitos intactos não afetados pela doença, como a via para o córtex pré-motor lateral.⁽²^,⁶⁾

Yang et al.,⁽²⁴⁾compararam o TE com e sem aplicação prévia de estimulação magnética transcraniana repetitiva (EMTr). O TE foi realizado por 12 sessões (3 sessões por semana) ao longo de um período de 4 semanas. Todos os participantes caminharam em uma esteira motorizada (Biodex, Shirley, New York, USA) após a EMTr. Os resultados sugeriram que a combinação de EMTr e TE aumenta o efeito do TE na modulação da inibição corticomotora e na melhora do desempenho da marcha em pacientes com DP.

Canning et al.,⁽²⁶⁾observaram um Grupo Experimental que foi submetido a um programa semissupervisionado de 30 a 40 minutos de caminhada na esteira, realizado no lar, quatro vezes por semana, durante 6 semanas. O Grupo Controle recebeu os cuidados habituais (ou seja, conselhos para manter o nível de atividade física atual). O TE semissupervisionado em casa foi uma forma viável e segura de exercício para pessoas cognitivamente intactas com DP leve. O tratamento no lar é uma estratégia importante na reabilitação geriátrica, sendo possível associar o TE como reforço aos exercícios de marcha.

Arcolin et al.,⁽³¹⁾randomizaram 29 pacientes com DP internados para TE (n=13) ou com cicloergômetro (n=16) por 3 semanas, 1 hora por dia. Esse estudo piloto mostra que o treinamento com cicloergômetro melhora os parâmetros de marcha e reduz os sinais clínicos de DP, tanto quanto o TE. A velocidade da marcha é acompanhada pelo aumento no comprimento do passo, tornando o padrão da marcha próximo do de indivíduos saudáveis. O cicloergômetro é uma alternativa válida à esteira, para melhorar a marcha a curto prazo em pacientes com DP.

Os estudos que não foram incluídos na revisão porque a amostra não era de idosos também mostraram que o TE sem suporte de peso corporal em pacientes com DP, em comparação com outras terapias motoras, aumentou a velocidade e o comprimento da passada.⁽⁴²^,⁴³⁾

Três estudos incluídos utilizaram TE com suporte de peso,⁽¹⁸^–²⁰⁾sendo que dois⁽¹⁹^,²¹⁾mostraram superioridade do treinamento com suporte em comparação com outras terapias, e um estudo não observou diferença.⁽²⁸⁾Fisher et al.,⁽²⁹⁾recrutaram 30 pacientes com DP (estágio Hoehn e Yarh I a II) que foram randomizados em três grupos: terapia de alta intensidade (treinamento com suporte), fisioterapia de baixa intensidade (amplitude de movimento passiva e ativa, equilíbrio, marcha, resistência muscular e exercícios de funções diárias) e terapia não intensiva, caracterizada por educação terapêutica (seis aulas sobre qualidade de vida durante período de 8 semanas). As intervenções duraram 8 semanas, totalizando 24 sessões (três vezes por semana com sessões de 1 hora). O TE iniciou com 10% do peso corporal suspenso. No entanto, se o paciente não conseguisse realizar a marcha, esse percentual foi aumentado, de modo que o objetivo de cada sessão era o de atingir e manter um nível superior a 3 METs, respeitando o repouso, quando necessário. Os resultados mostraram melhora do UPDRS em todos os grupos. O grupo de treinamento com suporte mostrou aumento na velocidade da marcha, no comprimento do passo e da passada e na excursão do quadril e do tornozelo no plano sagital, além de melhor distribuição do peso durante o exercício e aumento do período de silêncio cortical.

Gali et al.,⁽²⁵⁾e Picelli et al.,⁽²⁸⁾também utilizaram treinamento com suporte do peso corporal, porém com assistência robótica. Picelli et al.,⁽²⁸⁾compararam três grupos: o grupo de treinamento de marcha com assistência robótica, o grupo de TE sem suporte do peso corporal e o grupo de fisioterapia. Cada sessão de treinamento compreendia três partes, com descanso de 5 minutos após cada uma. A princípio, os pacientes foram treinados a uma velocidade de 1km/hora, por 10 minutos; depois, a uma velocidade de 1,5km/hora, por 10 minutos; e, por fim, a uma velocidade de 2,0km/hora, por 10 minutos. Não houve diferenças nos parâmetros espaciais e temporais dos testes de 6 e 10 minutos de caminhada. Gali et al.,⁽²⁵⁾avaliaram 50 pacientes com DP, que foram divididos em dois grupos: 25 foram designados para a terapia com assistência robótica e 25 para o grupo de terapia intensiva em esteira. O treinamento locomotor da reabilitação com assistência robótica do efetor final melhorou a cinemática da marcha, e parece ser eficaz para a reabilitação de pacientes com DP leve.

Alguns estudos com pacientes não idosos também observaram resultados semelhantes. Não houve diferença nas variáveis temporais e espaciais dos testes de caminhada de 6 e 10 minutos e do teste TUG e do UPDRS,⁽⁴⁴⁾quando comparados o TE e o TE Lokomat. Outros estudos observaram o efeito do TE com suporte de peso em relação a sem suporte de peso,⁽⁴⁵⁾ao treinamento de marcha no solo⁽⁴⁶⁾e a outras terapias motoras.⁽¹⁶^,¹⁷⁾

Toole et al.,⁽⁴⁵⁾relataram os efeitos do TE por 6 semanas, em 23 pacientes com DP, randomizados em três grupos. Dois grupos treinaram a marcha com 25% e 5% de suporte do peso corporal, e o terceiro grupo sem suporte. Os três grupos melhoraram nas escalas UPDRS e Berg, sem diferença entre eles. O estudo de Ganesan et al.,⁽⁴⁶⁾utilizou posturografia computadorizada para avaliar o efeito de um TE de 4 semanas com suporte de 20% do peso corporal, quatro vezes por semana (30 minutos por dia). Os autores relataram melhoria nos limites de estabilidade e na oscilação lateral medial do centro de massa com o treinamento com suporte em relação ao treinamento de marcha convencional fora da esteira. Miyai et al.,⁽¹⁶⁾compararam o treinamento de marcha com 20% de suporte do peso corporal em relação à fisioterapia convencional por 4 semanas em pacientes com DP e relataram que o TE com suporte de peso melhorou o desempenho motor da marcha (teste de caminhada de 10 minutos) e as atividades da vida diária, que persistiram por 6 meses.⁽¹⁷⁾

Fernández-Lago et al.,⁽³³⁾descreveram que uma única sessão combinando caminhada na esteira e estimulação transcraniana por corrente contínua (ETCC) aplicada sobre o córtex motor resultou em modulação específica da inibição recíproca da fibra sensorial Ia do músculo tibial anterior ao músculo sóleo. No entanto, esse efeito agudo não resultou em melhora dos parâmetros da marcha associados à caminhada na esteira na DP.

O treinamento sem suporte do peso corporal parece ser mais difícil, pois exige maior demanda muscular. As principais justificativas para essa evidência são velocidade constante; estimulação sensorial contínua; pistas sensoriais externas; ativação de circuitos neurais da marcha gerando padrão central; feedback visual; velocidade constante e aprendizado motor.⁽¹⁶^,¹⁷^,⁴⁵^,⁴⁶⁾

O treinamento com suporte do peso corporal, mesmo que diminua a estimulação periférica (força muscular e esforço aeróbico), pode aumentar a estimulação proprioceptiva.⁽⁴⁷⁾O suporte parcial do peso também pode prolongar o período de treinamento útil, pois reduz a fadiga.⁽⁴⁸⁾Além disso, facilita o movimento dos membros inferiores⁽⁴⁹⁾e, portanto, pode ser considerado uma intervenção promissora para o treinamento do controle sensório-motor por meio da melhoria dos reflexos posturais.⁽¹⁶^,¹⁷⁾Também pode facilitar o uso de estratégias que utilizam vias não dopaminérgicas e não são afetadas pela doença. Outros autores sugerem que o treinamento com suporte de peso estimula o centro medular de controle da marcha.⁽¹⁷^,⁴⁷⁾

É possível observar em revisão que o TE com ou sem suporte de peso (pelo menos 20 minutos, duas a três vezes por semana, com aumento progressivo das cargas, por, no mínimo, 6 semanas) em pacientes idosos com DP foi eficaz para melhorar a marcha. Além disso, ambos são considerados seguros (uma vez que, mesmo no treinamento sem suporte, os estudos descreveram o uso de cintos) e podem ser associados a terapias complementares à marcha, como EMTr, pistas visuais ou estimulação transcraniana por corrente contínua anódica (ETCCa).

Porém, é importante enfatizar que as avaliações utilizadas para a marcha diferiam entre si. Cinco estudos⁽¹⁷^,¹⁹^,²¹^,²²^,²⁴⁾foram capazes de avaliar as características clínicas da marcha, o que pode auxiliar na evolução do tratamento. Apenas dois usaram a medida padrão-ouro: a avaliação computadorizada.⁽²⁵^,²⁹⁾O TE com ou sem suporte de peso pode ser uma intervenção para a reabilitação neurológica geriátrica, mas há necessidade de mais estudos sobre esse tema, que caracterizem melhor a amostra de idosos com DP, além de utilizar ferramentas de avaliação mais específicas da marcha.

Este estudo teve algumas limitações. Não analisamos os subgrupos de pacientes idosos nos estudos que recrutavam adultos na amostra, os quais foram excluídos. A maioria dos estudos tinha amostra relativamente pequena, com total de 300 pacientes em todos os estudos.

CONCLUSÃO

O treinamento em esteira com ou sem suporte do peso corporal (no mínimo 20 minutos, duas a três vezes por semana, com aumento progressivo da carga, por pelo menos 6 semanas) é uma intervenção que melhora os desfechos da marcha em pacientes idosos com doença de Parkinson, porém se faz necessária a realização de mais estudos.

AGRADECIMENTOS

O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Código de Financiamento 001.

[B1] 1.Pieruccini-Faria F, Menuchi MR, Vitório R, Gobbi LT, Stella F, Gobbi S. Parâmetros cinemáticos da marcha com obstáculos em idosos com Doença de Parkinson, com e sem efeito da levodopa: um estudo piloto. Rev Bras Fisioter. 2006;10(2):233–239. [Google Scholar]; 1. Pieruccini-Faria F, Menuchi MR, Vitório R, Gobbi LT, Stella F, Gobbi S. Parâmetros cinemáticos da marcha com obstáculos em idosos com Doença de Parkinson, com e sem efeito da levodopa: um estudo piloto. Rev Bras Fisioter. 2006;10(2):233-9.

[B2] 2.de Goede CJ, Keus SH, Kwakkel G, Wagenaar RC. The effects of physical therapy in Parkinson's disease: a research synthesis. Arch Phys Med Rehabil. 2001;82(4):509–515. doi: 10.1053/apmr.2001.22352. [DOI] [PubMed] [Google Scholar]; 2. de Goede CJ, Keus SH, Kwakkel G, Wagenaar RC. The effects of physical therapy in Parkinson's disease: a research synthesis. Arch Phys Med Rehabil. 2001;82(4):509-15. [DOI] [PubMed]

[B3] 3.Svehlík M, Zwick EB, Steinwender G, Linhart WE, Schwingenschuh P, Katschnig P, et al. Gait analysis in patients with Parkinson's disease off dopaminergic therapy. Arch Phys Med Rehabil. 2009;90(11):1880–1886. doi: 10.1016/j.apmr.2009.06.017. [DOI] [PubMed] [Google Scholar]; 3. Svehlík M, Zwick EB, Steinwender G, Linhart WE, Schwingenschuh P, Katschnig P, et al. Gait analysis in patients with Parkinson's disease off dopaminergic therapy. Arch Phys Med Rehabil. 2009;90(11):1880-6. [DOI] [PubMed]

[B4] 4.Blin O, Ferrandez AM, Serratrice G. Quantitative analysis of gait in Parkinson patients: increased variability of stride length. J Neurol Sci. 1990;98(1):91–97. doi: 10.1016/0022-510x(90)90184-o. [DOI] [PubMed] [Google Scholar]; 4. Blin O, Ferrandez AM, Serratrice G. Quantitative analysis of gait in Parkinson patients: increased variability of stride length. J Neurol Sci. 1990;98(1):91-7. [DOI] [PubMed]

[B5] 5.Peppe A, Chiavalon C, Pasqualetti P, Crovato D, Caltagirone C. Does gait analysis quantify motor rehabilitation efficacy in Parkinson's disease patients? Gait Posture. 2007;26(3):452–462. doi: 10.1016/j.gaitpost.2006.11.207. [DOI] [PubMed] [Google Scholar]; 5. Peppe A, Chiavalon C, Pasqualetti P, Crovato D, Caltagirone C. Does gait analysis quantify motor rehabilitation efficacy in Parkinson's disease patients? Gait Posture. 2007;26(3):452-62. [DOI] [PubMed]

[B6] 6.Morris ME, Iansek R, Matyas TA, Summers JJ. The pathogenesis of gait hypokinesia in Parkinson's disease. Brain. 1994;117(Pt 5):1169–1181. doi: 10.1093/brain/117.5.1169. [DOI] [PubMed] [Google Scholar]; 6. Morris ME, Iansek R, Matyas TA, Summers JJ. The pathogenesis of gait hypokinesia in Parkinson's disease. Brain. 1994;117(Pt 5):1169-81. [DOI] [PubMed]

[B7] 7.Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson's disease. Normalization strategies and underlying mechanisms. Brain. 1996;119(Pt 2):551–568. doi: 10.1093/brain/119.2.551. [DOI] [PubMed] [Google Scholar]; 7. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson's disease. Normalization strategies and underlying mechanisms. Brain. 1996;119(Pt 2):551-68. [DOI] [PubMed]

[B8] 8.Camicioli R, Oken BS, Sexton G, Kaye JA, Nutt JG. Verbal fluency task affects gait in Parkinson's disease with motor freezing. J Geriatr Psychiatry Neurol. 1998;11(4):181–185. doi: 10.1177/089198879901100403. [DOI] [PubMed] [Google Scholar]; 8. Camicioli R, Oken BS, Sexton G, Kaye JA, Nutt JG. Verbal fluency task affects gait in Parkinson's disease with motor freezing. J Geriatr Psychiatry Neurol. 1998;11(4):181-5. [DOI] [PubMed]

[B9] 9.Galletly R, Brauer SG. Does the type of concurrent task affect preferred and cued gait in people with Parkinson's disease? Aust J Physiother. 2005;51(3):175–180. doi: 10.1016/s0004-9514(05)70024-6. [DOI] [PubMed] [Google Scholar]; 9. Galletly R, Brauer SG. Does the type of concurrent task affect preferred and cued gait in people with Parkinson's disease? Aust J Physiother. 2005;51(3):175-80. [DOI] [PubMed]

[B10] 10.Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson's disease: comparison with a healthy control group. Arch Phys Med Rehabil. 2005;86(5):1007–1013. doi: 10.1016/j.apmr.2004.08.012. [DOI] [PubMed] [Google Scholar]; 10. Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson's disease: comparison with a healthy control group. Arch Phys Med Rehabil. 2005;86(5):1007-13. [DOI] [PubMed]

[B11] 11.Liu W, McIntire K, Kim SH, Zhang J, Dascalos S, Lyons KE, et al. Bilateral subthalamic stimulation improves gait initiation in patients with Parkinson's disease. Gait Posture. 2006;23(4):492–498. doi: 10.1016/j.gaitpost.2005.06.012. [DOI] [PubMed] [Google Scholar]; 11. Liu W, McIntire K, Kim SH, Zhang J, Dascalos S, Lyons KE, et al. Bilateral subthalamic stimulation improves gait initiation in patients with Parkinson's disease. Gait Posture. 2006;23(4):492-8. [DOI] [PubMed]

[B12] 12.Gantchev N, Viallet F, Aurenty R, Massion J. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol. 1996;101(2):110–120. doi: 10.1016/0924-980x(95)00253-h. [DOI] [PubMed] [Google Scholar]; 12. Gantchev N, Viallet F, Aurenty R, Massion J. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol. 1996;101(2):110-20. [DOI] [PubMed]

[B13] 13.Roiz RM, Cacho EW, Pazinatto MM, Reis JG, Cliquet A, Jr, Barasnevicius-Quagliato EM. Gait analysis comparing Parkinson's disease with healthy elderly subjects. Arq Neuropsiquiatr. 2010;68(1):81–86. doi: 10.1590/s0004-282x2010000100018. [DOI] [PubMed] [Google Scholar]; 13. Roiz RM, Cacho EW, Pazinatto MM, Reis JG, Cliquet A Jr, Barasnevicius-Quagliato EM. Gait analysis comparing Parkinson's disease with healthy elderly subjects. Arq Neuropsiquiatr. 2010;68(1):81-6. [DOI] [PubMed]

[B14] 14.McVey MA, Stylianou AP, Luchies CW, Lyons KE, Pahwa R, Jernigan S, et al. Early biomechanical markers of postural instability in Parkinson's disease. Gait Posture. 2009;30(4):538–542. doi: 10.1016/j.gaitpost.2009.08.232. [DOI] [PubMed] [Google Scholar]; 14. McVey MA, Stylianou AP, Luchies CW, Lyons KE, Pahwa R, Jernigan S, et al. Early biomechanical markers of postural instability in Parkinson's disease. Gait Posture. 2009;30(4):538-42. [DOI] [PubMed]

[B15] 15.Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. 2003;24(2):197–211. doi: 10.1016/s0197-4580(02)00065-9. [DOI] [PubMed] [Google Scholar]; 15. Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. 2003;24(2):197-211. [DOI] [PubMed]

[B16] 16.Miyai I, Fujimoto Y, Ueda Y, Yamamoto H, Nozaki S, Saito T, et al. Treadmill training with body weight support: its effect on Parkinson's disease. Arch Phys Med Rehabil. 2000;81(7):849–852. doi: 10.1053/apmr.2000.4439. [DOI] [PubMed] [Google Scholar]; 16. Miyai I, Fujimoto Y, Ueda Y, Yamamoto H, Nozaki S, Saito T, et al. Treadmill training with body weight support: its effect on Parkinson's disease. Arch Phys Med Rehabil. 2000;81(7):849-52. [DOI] [PubMed]

[B17] 17.Miyai I, Fujimoto Y, Yamamoto H, Ueda Y, Saito T, Nozaki S, et al. Long-term effect of body weight-supported treadmill training in Parkinson's disease: a randomized controlled trial. Arch Phys Med Rehabil. 2002;83(10):1370–1373. doi: 10.1053/apmr.2002.34603. [DOI] [PubMed] [Google Scholar]; 17. Miyai I, Fujimoto Y, Yamamoto H, Ueda Y, Saito T, Nozaki S, et al. Long-term effect of body weight-supported treadmill training in Parkinson's disease: a randomized controlled trial. Arch Phys Med Rehabil. 2002;83(10):1370-3. [DOI] [PubMed]

[B18] 18.Herman T, Giladi N, Hausdorff JM. Treadmill training for the treatment of gait disturbances in people with Parkinson's disease: a mini-review. J Neural Transm (Vienna) 2009;116(3):307–318. doi: 10.1007/s00702-008-0139-z. Review. [DOI] [PubMed] [Google Scholar]; 18. Herman T, Giladi N, Hausdorff JM. Treadmill training for the treatment of gait disturbances in people with Parkinson's disease: a mini-review. J Neural Transm (Vienna). 2009;116(3):307-18. Review. [DOI] [PubMed]

[B19] 19.Hottenrott K, Ludyga S, Schulze S. Effects of high intensity training and continuous endurance training on aerobic capacity and body composition in recreationally active runners. J Sport Sci Med. 2012;11(3):483–488. [PMC free article] [PubMed] [Google Scholar]; 19. Hottenrott K, Ludyga S, Schulze S. Effects of high intensity training and continuous endurance training on aerobic capacity and body composition in recreationally active runners. J Sport Sci Med. 2012;11(3):483-8. [PMC free article] [PubMed]

[B20] 20.Schenkman M, Hall DA, Barón AE, Schwartz RS, Mettler P, Kohrt WM. Exercise for people in early- or mid-stage Parkinson disease: a 16-month randomized controlled trial. Phys Ther. 2012;92(11):1395–1410. doi: 10.2522/ptj.20110472. [DOI] [PMC free article] [PubMed] [Google Scholar]; 20. Schenkman M, Hall DA, Barón AE, Schwartz RS, Mettler P, Kohrt WM. Exercise for people in early- or mid-stage Parkinson disease: a 16-month randomized controlled trial. Phys Ther. 2012;92(11):1395-410. [DOI] [PMC free article] [PubMed]

[B21] 21.Bello O. Fernandez-Del-Olmo M. How does the treadmill affect gait in Parkinson's disease? Curr Aging Sci. 2012;5(1):28–34. doi: 10.2174/1874609811205010028. Review. [DOI] [PubMed] [Google Scholar]; 21. Bello O, Fernandez-Del-Olmo M. How does the treadmill affect gait in Parkinson's disease? Curr Aging Sci. 2012;5(1):28-34. Review. [DOI] [PubMed]

[B22] 22.Mehrholz J, Kugler J, Storch A, Pohl M, Hirsch K, Elsner B. Treadmill training for patients with Parkinson's disease. Cochrane Database Syst Rev. 2015;(8):CD007830–CD007830. doi: 10.1002/14651858.CD007830.pub3. Update in: Cochrane Database Syst Rev. 2015; (9):CD007830. [DOI] [PubMed] [Google Scholar]; 22. Mehrholz J, Kugler J, Storch A, Pohl M, Hirsch K, Elsner B. Treadmill training for patients with Parkinson's disease. Cochrane Database Syst Rev. 2015;(8):CD007830. Update in: Cochrane Database Syst Rev. 2015; (9):CD007830. [DOI] [PMC free article] [PubMed]

[B23] 23.Frazzitta G, Pezzoli G, Bertotti G, Maestri R. Asymmetry and freezing of gait in parkinsonian patients. J Neurol. 2013;260(1):71–76. doi: 10.1007/s00415-012-6585-4. [DOI] [PubMed] [Google Scholar]; 23. Frazzitta G, Pezzoli G, Bertotti G, Maestri R. Asymmetry and freezing of gait in parkinsonian patients. J Neurol. 2013;260(1):71-6. [DOI] [PubMed]

[B24] 24.Yang YR, Tseng CY, Chiou SY, Liao KK, Cheng SJ, Lai KL, et al. Combination of rTMS and treadmill training modulates corticomotor inhibition and improves walking in Parkinson disease: a randomized trial. Neurorehabil Neural Repair. 2013;27(1):79–86. doi: 10.1177/1545968312451915. [DOI] [PubMed] [Google Scholar]; 24. Yang YR, Tseng CY, Chiou SY, Liao KK, Cheng SJ, Lai KL, et al. Combination of rTMS and treadmill training modulates corticomotor inhibition and improves walking in Parkinson disease: a randomized trial. Neurorehabil Neural Repair. 2013;27(1):79-86. [DOI] [PubMed]

[B25] 25.Galli M, Cimolin V, De Pandis MF, Le Pera D, Sova I, Albertini G, et al. Robot-assisted gait training versus treadmill training in patients with Parkinson's disease: a kinematic evaluation with gait profile score. Funct Neurol. 2016;31(3):163–170. doi: 10.11138/FNeur/2016.31.3.163. [DOI] [PMC free article] [PubMed] [Google Scholar]; 25. Galli M, Cimolin V, De Pandis MF, Le Pera D, Sova I, Albertini G, et al. Robot-assisted gait training versus treadmill training in patients with Parkinson's disease: a kinematic evaluation with gait profile score. Funct Neurol. 2016;31(3):163-70. [DOI] [PMC free article] [PubMed]

[B26] 26.Canning CG, Allen NE, Dean CM, Goh L, Fung VS. Home-based treadmill training for individuals with Parkinson's disease: a randomized controlled pilot trial. Clin Rehabil. 2012;26(9):817–826. doi: 10.1177/0269215511432652. [DOI] [PubMed] [Google Scholar]; 26. Canning CG, Allen NE, Dean CM, Goh L, Fung VS. Home-based treadmill training for individuals with Parkinson's disease: a randomized controlled pilot trial. Clin Rehabil. 2012;26(9):817-26. [DOI] [PubMed]

[B27] 27.Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P. Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord. 2009;24(8):1139–1143. doi: 10.1002/mds.22491. [DOI] [PubMed] [Google Scholar]; 27. Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P. Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord. 2009;24(8):1139-43. [DOI] [PubMed]

[B28] 28.Picelli A, Melotti C, Origano F, Neri R, Waldner A, Smania N. Robot-assisted gait training versus equal intensity treadmill training in patients with mild to moderate Parkinson's disease: a randomized controlled trial. Parkinsonism Relat Disord. 2013;19(6):605–610. doi: 10.1016/j.parkreldis.2013.02.010. [DOI] [PubMed] [Google Scholar]; 28. Picelli A, Melotti C, Origano F, Neri R, Waldner A, Smania N. Robot-assisted gait training versus equal intensity treadmill training in patients with mild to moderate Parkinson's disease: a randomized controlled trial. Parkinsonism Relat Disord. 2013;19(6):605-10. [DOI] [PubMed]

[B29] 29.Fisher BE, Wu AD, Salem GJ, Song J, Lin CH, Yip J, et al. 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(7):1221–1229. doi: 10.1016/j.apmr.2008.01.013. [DOI] [PMC free article] [PubMed] [Google Scholar]; 29. Fisher BE, Wu AD, Salem GJ, Song J, Lin CH, Yip J, et al. 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(7):1221-9. [DOI] [PMC free article] [PubMed]

[B30] 30.Schlick C, Ernst A, Bötzel K, Plate A, Pelykh O, Ilmberger J. Visual cues combined with treadmill training to improve gait performance in Parkinson's disease: a pilot randomized controlled trial. Clin Rehabil. 2016;30(5):463–471. doi: 10.1177/0269215515588836. [DOI] [PubMed] [Google Scholar]; 30. Schlick C, Ernst A, Bötzel K, Plate A, Pelykh O, Ilmberger J. Visual cues combined with treadmill training to improve gait performance in Parkinson's disease: a pilot randomized controlled trial. Clin Rehabil. 2016;30(5):463-71. [DOI] [PubMed]

[B31] 31.Arcolin I, Pisano F, Delconte C, Godi M, Schieppati M, Mezzani A, et al. Intensive cycle ergometer training improves gait speed and endurance in patients with Parkinson's disease: a comparison with treadmill training. Restor Neurol Neurosci. 2016;34(1):125–138. doi: 10.3233/RNN-150506. [DOI] [PubMed] [Google Scholar]; 31. Arcolin I, Pisano F, Delconte C, Godi M, Schieppati M, Mezzani A, et al. Intensive cycle ergometer training improves gait speed and endurance in patients with Parkinson's disease: a comparison with treadmill training. Restor Neurol Neurosci. 2016;34(1):125-38. [DOI] [PubMed]

[B32] 32.Herman T, Giladi N, Gruendlinger L, Hausdorff JM. 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(9):1154–1158. doi: 10.1016/j.apmr.2007.05.015. [DOI] [PubMed] [Google Scholar]; 32. Herman T, Giladi N, Gruendlinger L, Hausdorff JM. 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(9):1154-8. [DOI] [PubMed]

[B33] 33.Fernández-Lago H, Bello O, Mora-Cerdá F, Montero-Cámara J, Fernández-Del-Olmo MÁ. Treadmill walking combined with anodal transcranial direct current stimulation in Parkinson disease: a pilot study of kinematic and neurophysiological effects. Am J Phys Med Rehabil. 2017;96(11):801–808. doi: 10.1097/PHM.0000000000000751. [DOI] [PubMed] [Google Scholar]; 33. Fernández-Lago H, Bello O, Mora-Cerdá F, Montero-Cámara J, Fernández-Del-Olmo MÁ. Treadmill walking combined with anodal transcranial direct current stimulation in Parkinson disease: a pilot study of kinematic and neurophysiological effects. Am J Phys Med Rehabil. 2017;96(11):801-8. [DOI] [PubMed]

[B34] 34.Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17(5):427–442. doi: 10.1212/wnl.17.5.427. [DOI] [PubMed] [Google Scholar]; 34. Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17(5):427-42. [DOI] [PubMed]

[B35] 35.Schapira AH, Emre M, Jenner P, Poewe W. Levodopa in the treatment of Parkinson's disease. Eur J Neurol. 2009;16(9):982–989. doi: 10.1111/j.1468-1331.2009.02697.x. Review. [DOI] [PubMed] [Google Scholar]; 35. Schapira AH, Emre M, Jenner P, Poewe W. Levodopa in the treatment of Parkinson's disease. Eur J Neurol. 2009;16(9):982-9. Review. [DOI] [PubMed]

[B36] 36.Jenkins ME, Johnson AM, Holmes JD, Stephenson FF, Spaulding SJ. Predictive validity of the UPDRS postural stability score and the functional reach test, when compared with ecologically valid reaching tasks. Parkinsonism Relat Disord. 2010;16(6):409–411. doi: 10.1016/j.parkreldis.2010.04.002. [DOI] [PubMed] [Google Scholar]; 36. Jenkins ME, Johnson AM, Holmes JD, Stephenson FF, Spaulding SJ. Predictive validity of the UPDRS postural stability score and the functional reach test, when compared with ecologically valid reaching tasks. Parkinsonism Relat Disord. 2010;16(6):409-11. [DOI] [PubMed]

[B37] 37.Barry E, Galvin R, Keogh C, Horgan F, Fahey T. Is the Timed Up and Go test a useful predictor of risk of falls in community dwelling older adults: a systematic review and meta-analysis. BMC Geriatr. 2014;14(1):14–14. doi: 10.1186/1471-2318-14-14. Review. [DOI] [PMC free article] [PubMed] [Google Scholar]; 37. Barry E, Galvin R, Keogh C, Horgan F, Fahey T. Is the Timed Up and Go test a useful predictor of risk of falls in community dwelling older adults: a systematic review and meta-analysis. BMC Geriatr. 2014;14(1):14. Review. [DOI] [PMC free article] [PubMed]

[B38] 38.Isles RC, Choy NL, Steer M, Nitz JC. Normal values of balance tests in women aged 20-80. J Am Geriatr Soc. 2004;52(8):1367–1372. doi: 10.1111/j.1532-5415.2004.52370.x. [DOI] [PubMed] [Google Scholar]; 38. Isles RC, Choy NL, Steer M, Nitz JC. Normal values of balance tests in women aged 20-80. J Am Geriatr Soc. 2004;52(8):1367-72. [DOI] [PubMed]

[B39] 39.Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the timed up & go test. Phys Ther. 2000;80(9):896–903. [PubMed] [Google Scholar]; 39. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the timed up & go test. Phys Ther. 2000;80(9):896-903. [PubMed]

[B40] 40.Li AM, Yin J, Yu CC, Tsang T, So HK, Wong E, et al. The six-minute walk test in healthy children: reliability and validity. Eur Respir J. 2005;25(6):1057–1060. doi: 10.1183/09031936.05.00134904. [DOI] [PubMed] [Google Scholar]; 40. Li AM, Yin J, Yu CC, Tsang T, So HK, Wong E, et al. The six-minute walk test in healthy children: reliability and validity. Eur Respir J. 2005;25(6):1057-60. [DOI] [PubMed]

[B41] 41.American Thoracic Society/European Respiratory Society ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166(4):518–624. doi: 10.1164/rccm.166.4.518. [DOI] [PubMed] [Google Scholar]; 41. American Thoracic Society/European Respiratory Society. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002; 166(4):518-624. [DOI] [PubMed]

[B42] 42.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(12):1760–1766. doi: 10.1016/s0003-9993(03)00433-7. [DOI] [PubMed] [Google Scholar]; 42. 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(12):1760-6. [DOI] [PubMed]

[B43] 43.Shulman LM, Katzel LI, Ivey FM, Sorkin JD, Favors K, Anderson KE, et al. Randomized clinical trial of 3 types of physical exercise for patients with Parkinson disease. JAMA Neurol. 2013;70(2):183–190. doi: 10.1001/jamaneurol.2013.646. [DOI] [PMC free article] [PubMed] [Google Scholar]; 43. Shulman LM, Katzel LI, Ivey FM, Sorkin JD, Favors K, Anderson KE, et al. Randomized clinical trial of 3 types of physical exercise for patients with Parkinson disease. JAMA Neurol. 2013;70(2):183-90. [DOI] [PMC free article] [PubMed]

[B44] 44.Carda S, Invernizzi M, Baricich A, Comi C, Croquelois A, Cisari C. Robotic gait training is not superior to conventional treadmill training in parkinson disease: a single-blind randomized controlled trial. Neurorehabil Neural Repair. 2012;26(9):1027–1034. doi: 10.1177/1545968312446753. [DOI] [PubMed] [Google Scholar]; 44. Carda S, Invernizzi M, Baricich A, Comi C, Croquelois A, Cisari C. Robotic gait training is not superior to conventional treadmill training in parkinson disease: a single-blind randomized controlled trial. Neurorehabil Neural Repair. 2012;26(9):1027-34. [DOI] [PubMed]

[B45] 45.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):307–322. [PubMed] [Google Scholar]; 45. 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]

[B46] 46.Ganesan M, Sathyaprabha TN, Gupta A, Pal PK. Effect of partial weight-supported treadmill gait training on balance in patients with Parkinson disease. PM R. 2014;6(1):22–33. doi: 10.1016/j.pmrj.2013.08.604. [DOI] [PubMed] [Google Scholar]; 46. Ganesan M, Sathyaprabha TN, Gupta A, Pal PK. Effect of partial weight-supported treadmill gait training on balance in patients with Parkinson disease. PM R. 2014;6(1):22-33. [DOI] [PubMed]

[B47] 47.Murray MP, Sepic SB, Gardner GM, Downs WJ. Walking patterns of men with parkinsonism. Am J Phys Med Rehab. 1978;57(6):278–294. [PubMed] [Google Scholar]; 47. Murray MP, Sepic SB, Gardner GM, Downs WJ. Walking patterns of men with parkinsonism. Am J Phys Med Rehab. 1978;57(6):278-94. [PubMed]

[B48] 48.Mhatre PV, Vilares I, Stibb SM, Albert MV, Pickering L, Marciniak CM, et al. Wii Fit balance board playing improves balance and gait in Parkinson disease. PM R. 2013;5(9):769–777. doi: 10.1016/j.pmrj.2013.05.019. [DOI] [PMC free article] [PubMed] [Google Scholar]; 48. Mhatre PV, Vilares I, Stibb SM, Albert MV, Pickering L, Marciniak CM, et al. Wii Fit balance board playing improves balance and gait in Parkinson disease. PM R. 2013;5(9):769-77. [DOI] [PMC free article] [PubMed]

[B49] 49.Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov Disord. 2002;17(6):1148–1160. doi: 10.1002/mds.10259. Review. [DOI] [PubMed] [Google Scholar]; 49. Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov Disord. 2002;17(6):1148-60. Review. [DOI] [PubMed]

PERMALINK

Effects of treadmill training on gait of elders with Parkinson's disease: a literature review

Natália Mariana Silva Luna

Guilherme Carlos Brech

Alexandra Canonica

Rita de Cássia Ernandes

Danilo Sales Bocalini

Julia Maria D’Andréa Greve

Angélica Castilho Alonso

ABSTRACT

INTRODUCTION

OBJETIVE

METHODS

Search strategy

Study selection

Quality appraisal

Table 1. PEDro scale of the 11 studies selected.

RESULTS

Table 2. Summary of the population, protocols, gait measures and results of these investigations.

DISCUSSION

CONCLUSION

ACKNOWLEDGMENTS

REFERENCES

Efeitos do treinamento de marcha em esteira em idosos com doença de Parkinson: uma revisão da literatura

Natália Mariana Silva Luna

Guilherme Carlos Brech

Alexandra Canonica

Rita de Cássia Ernandes

Danilo Sales Bocalini

Julia Maria D’Andréa Greve

Angélica Castilho Alonso

RESUMO

INTRODUÇÃO

OBJETIVO

MÉTODOS

Estratégia de busca

Seleção de estudos

Avaliação da qualidade

Tabela 1. Escala PEDro de 11 estudos selecionados.

RESULTADOS

Tabela 2. Resumo sobre população, protocolos, medidas de marcha e resultados destes estudos.

DISCUSSÃO

CONCLUSÃO

AGRADECIMENTOS

ACTIONS

PERMALINK

RESOURCES

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