Effects of aerobic physical exercise on neuroplasticity after stroke: systematic review

Penna, Leandro Goursand; Pinheiro, João Pascoa; Ramalho, Sergio Henrique Rodolpho; Ribeiro, Carlos Fontes

doi:10.1590/0004-282X-ANP-2020-0551

Acessibilidade / Reportar erro

Brasil

Arquivos de Neuro-Psiquiatria

Español English

Brasil

Español English

sumário « anterior atual seguinte »

Sumário

View and Review • Arq. Neuro-Psiquiatr. 79 (9) • Sept 2021 • https://doi.org/10.1590/0004-282X-ANP-2020-0551 copy

Effects of aerobic physical exercise on neuroplasticity after stroke: systematic review

Efeitos do exercício físico aeróbico na neuroplasticidade após o acidente vascular cerebral: revisão sistemática de literatura

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Background:

Stroke is among the leading causes of death and disability worldwide. Interventions for stroke rehabilitation aim to minimize sequelae, promote individuals’ independence and potentially recover functional damage. The role of aerobic exercise as a facilitator of post-stroke neuroplasticity in humans is still questionable.

Objective:

To investigate the impact of aerobic exercise on neuroplasticity in patients with stroke sequelae.

Methods:

A systematic review of randomized clinical trials and crossover studies was performed, with searches for human studies in the following databases: PUBMED, EMBASE, LILACS and PeDRO, only in English, following the PRISMA protocol. The keywords used for selecting articles were defined based on the PICO strategy.

Results:

This systematic review evaluated the impacts of aerobic exercise on neuroplasticity through assessment of neural networks and neuronal excitability, neurotrophic factors, or cognitive and functional assessment. Studies that evaluated the effects of aerobic exercise on neuroplasticity after stroke measured through functional resonance (fMRI) or cortical excitability have shown divergent results, but aerobic exercise potentially can modify the neural network, as measured through fMRI. Additionally, aerobic exercise combined with cognitive training improves certain cognitive domains linked to motor learning. Studies that involved analysis of neurotrophic factors to assess neuroplasticity had conflicting results.

Conclusions:

Physical exercise is a therapeutic intervention in rehabilitation programs that, beyond the known benefits relating to physical conditioning, functionality, mood and cardiovascular health, may also potentiate the neuroplasticity process. Neuroplasticity responses seem more robust in moderate to high-intensity exercise training programs, but dose-response heterogeneity and non-uniform neuroplasticity assessments limit generalizability.

Keywords:
Stroke; Stroke Rehabilitation; Exercise; Neuronal Plasticity; Endurance Training; High-Intensity Interval Training; Brain-Derived Neurotrophic Factor; Nerve Growth Factor

Author(s) / year / type of study	Sampling	Experimental intervention	Control	Outcomes	Results
Linder et al., 2019/ Neurorehabilitation and Neural Repair/ randomized clinical trial55. Linder SM, Rosenfeldt AB, Davidson S, Zimmerman N, Penko A, Lee J, et al. Forced, not voluntary, aerobic exercise enhances motor recovery in persons with chronic stroke. Neurorehabil Neural Repair. 2019 Aug;33(8):681-90. https://doi.org/10.1177/1545968319862557 https://doi.org/10.1177/1545968319862557...	N = 40 Patients evaluated: 16 in the “forced exercise group” (FE), 16 in the voluntary exercise group (VE) and 8 in the control group	45 minutes on an exercise bike until reaching 60 to 80% of the reserve heart rate achieved in the cardiopulmonary exercise test	Educational videos and physiotherapy exercises	Change in functional scale (FMA)	The outcomes evaluated were measurements of improvement of motor recovery through functional scales. All three groups improved significantly on FMA: by means of 11, 6 and 9 points for the FE, VE and education groups respectively (p = 0.001).
Ploughman et al., 2019/ Neurorehabilitation and Neural Repair/ randomized clinical trial99. Ploughman M, Austin MW, Glynn L, Corbett D. The effects of poststroke aerobic exercise on neuroplasticity: a systematic review of animal and clinical studies. Transl Stroke Res. 2015 Feb;6(1):13-28. https://doi.org/10.1007/s12975-014-0357-7 https://doi.org/10.1007/s12975-014-0357-...	N = 52 (4 groups): - Aerobic training with cognitive training: 12 - Aerobic training with games: 13 - Physiotherapy activities with cognitive training: 15 - Physiotherapy activities with games: 12	20 to 30 minutes of aerobic physical activity with 20 to 30 minutes of cognitive training. Exercise intensity determined by 60 to 80% of peak VO2 of ergospirometry.	Stretching activity or functional training	Change in RPMT test	Effect of training on intelligent fluidity (RPMT test): difference between groups with p < 0.05 -> Aerobic + COG = 47% increase -> Aerobic + GAMES = 7% increase -> Activity + COG = 20% increase -> Activity + GAMES = 8% reduction
Luft et al., 2008/ Stroke/ randomized clinical trial1111. Luft AR, Macko RF, Forrester LW, Villagra F, Ivey F, Sorkin JD, et al. Treadmill exercise activates subcortical neural networks and improves walking after stroke: a randomized controlled trial. Stroke. 2008 Dec;39(12):3341-50. https://doi.org/10.1161/STROKEAHA.108.527531 https://doi.org/10.1161/STROKEAHA.108.52...	N = 71 (intervention: 37 versus control: 34)	Treadmill training 3 times per week for 40 minutes at the intensity of 60% of the reserve heart rate (RHR).	Stretching with physiotherapist	Cerebral activation on fMRI	The intervention group improved its peak VO₂ by 18% (p < 0.001), test speed by 10 meters and average speed by 19% (p = 0.030) in the walking test. There was cerebral activation measured by fMRI in the posterior lobe of the cerebellum in the intervention group and not in the control group (p = 0.005).
El-Tamawy et al., 2014/ Neurorehabilitation/ randomized clinical trial1919. El-Tamawy MS, Abd-Allah F, Ahmed SM, Darwish MH, Khalifa HA. Aerobic exercises enhance cognitive functions and brain derived neurotrophic factor in ischemic stroke patients. NeuroRehabilitation. 2014;34(1):209-13. https://doi.org/10.3233/NRE-131020 https://doi.org/10.3233/NRE-131020...	N = 30 (intervention: 15 versus control: 15)	30 minutes of physiotherapy + 15 minutes of rest + 40 minutes by bike (30 minutes active and 10 minutes of warm-up and cooldown), 3 times per week for 8 weeks	Stretching, facilitation, strength, postural control, balance and functional training.	Changes in BDNF and ACER score	The mean values of subtest domains (attention, memory, verbal fluency, language and visuospatial ability) in the study group post-treatment were: 16.87, 21.27, 2.6, 25.27 and 15.07 respectively. Comparison of the mean value of each domain with control group revealed a significant increase in all domains in study group (p < 0.005) except verbal fluency. Serum level of BDNF increased in study group after intervention (19.18 to 23.83; p = 0.0001) and was unchanged in control group (p = 0.698) Pearson correlation between the post-treatment changes in ACER total score and BDNF was statistically significant (r = 0.53; p = 0.044), such that cognitive improvement was associated with BDNF improvement.
Shaughnessy et al., 2012/ Journal of Neuroscience Nursing/ randomized clinical trial2323. Shaughnessy M, Michael K, Resnick B. Impact of treadmill exercise on efficacy expectations, physical activity, and stroke recovery. J Neurosci Nurs. 2012 Feb;44(1):27-35. https://doi.org/10.1097/JNN.0b013e31823ae4b5 https://doi.org/10.1097/JNN.0b013e31823a...	N = 71 (intervention: 37 versus control: 34).	6 months of treadmill training: 3 times per week, 40 minutes per session, at the intensity of 60% of RHR. Starting at the individual's capacity, with progression every 2 weeks up to the goal	13 stretching exercises of large muscle groups under physiotherapy supervision	Changes in SIS scale	There was no significant difference between groups. There was an improvement in expectations associated with exercise: this was important because it shows that belief in the benefits of exercise can help in long-term adherence. The results indicated that regardless of group, all study participants experienced increased self-efficacy (F= 2.95; p = 0.09) and outcome expectations for exercise (F = 13.23; p < 0.001) and improvement in activities of daily living as reported in the SIS (F = 10.97; p = 0.002).
Nave et al., 2019/ BMJ/ randomized clinical trial2525. Nave AH, Rackoll T, Grittner U, Bläsing H, Gorsler A, Nabavi DG, et al. Physical fitness training in patients with Subacute Stroke (PHYS-STROKE): multicentre, randomised controlled, endpoint blinded trial. BMJ. 2019 Sep 18;366:l5101. https://doi.org/10.1136/bmj.l5101 https://doi.org/10.1136/bmj.l5101...	N = 200 (intervention: 105 versus control: 95)	50 minutes, 5 times per week, for 4 weeks (20 sessions in total). 25 min doing exercise with a target for the HR reached (50 to 60% of HR max).	25 minutes of relaxation of muscle groups. HR and SPE evaluated during the sessions.	Changes in Barthel index score	Compared with relaxation, aerobic physical fitness training did not result in a significantly higher mean change in maximum walking speed (adjusted treatment effect 0.1 m/s (95% confidence interval 0.0 to 0.2 m/s); p = 0.23) or mean change in Barthel index score (0 (−5 to 5); p = 0.99) at three months after stroke. A higher rate of serious adverse events was observed in the aerobic group, compared with the relaxation group (incidence rate ratio 1.81; 95% confidence interval 0.97 to 3.36).

Author(s) and year/ journal/ type of study	Sampling	Experimental intervention	Control	Outcomes	Results
Nepveu et al., 2017/ Neurorehabilitation and neural repair/ randomized clinical trial1212. Nepveu J-F, Thiel A, Tang A, Fung J, Lundbye-Jensen J, Boyd LA, et al. A single bout of High-Intensity interval training improves motor skill retention in individuals with stroke. Neurorehabil Neural Repair. 2017 Aug;31(8):726-35. https://doi.org/10.1177/1545968317718269 https://doi.org/10.1177/1545968317718269...	N = 22 (intervention: 11 versus control: 11).	Exercise group: 15 minutes of HIIT: 2 min of warm-up at 25% of the peak VO2 (calculated in the ergospirometry test), followed by 3 minutes of high intensity (100% of peak) interspersed with 2 minutes of low intensity at 25% of the peak effort.	Rest group	Changes in Cognitive assessment (MoCA)	Skill retention was significantly better in the HIIT group (unpaired t test, t(19) = 2.20; p = 0.04; effect size d = 0.96), which showed a 9% improvement in skill level, compared with the end of acquisition, while the control group showed a 4% decay. Specifically, 7 out of 11 participants in the HIIT group improved their mean score in the retention block, compared with the best block of training, while only 3 participants in the control group showed improvement.
Abraha et al., 2018/ Frontiers of Physiology/ crossover1313. Abraha B, Chaves AR, Kelly LP, Wallack EM, Wadden KP, McCarthy J, et al. A bout of high intensity interval training lengthened nerve conduction latency to the non-exercised affected limb in chronic stroke. Front Physiol. 2018 Jul 2;9:827. https://doi.org/10.3389/fphys.2018.00827 https://doi.org/10.3389/fphys.2018.00827...	N = 12 (MICE group: 6 and HIIT group: 6)	HIIT group: heating: 80% of VO2 max; maintained 60 to 80 steps per min alternating every 2 min with 40% of VO2 max. Total of 5 HIIT cycles, for 20 minutes	MICE group: Cadence of 60 to 80 passes per minute, at 60% of VO2 max for 20 minutes.	Changes in motor evoked potential (MEP) on electroneuromyography.	MEP latency from the ipsilesional hemisphere was lengthened after HIIT (pre: 24.27 ± 1.8 ms, and post: 25.04 ± 1.8 ms; p = 0.01) but not MICE (pre: 25.49 ± 1.10 ms, and post: 25.28 ± 1.0 ms; p = 0.44). There were no significant changes in motor thresholds, intracortical inhibition or facilitation. Pinch strength of the affected hand decreased after MICE (pre: 8.96 ± 1.9 kg vs. post: 8.40 ± 2.0 kg, p = 0.02) but not after HIIT (pre: 8.83 ± 2.0 kg vs. post: 8.65 ± 2.2 kg, p = 0.29). Regardless of type of aerobic exercise, higher total energy expenditure was associated with greater increases in pinch strength in the affected hand after exercise (p = 0.04) and decreases in pinch strength of the less affected hand (p = 0.02)
Murdoch et al., 2016/ Plos One/ crossover study1515. Murdoch K, Buckley JD, McDonnell MN. The effect of aerobic exercise on neuroplasticity within the motor cortex following stroke. PLoS One. 2016 Mar 28;11(3):e0152377. https://doi.org/10.1371/journal.pone.0152377 https://doi.org/10.1371/journal.pone.015...	N = 12 (intervention: 6 and control: 6)	Cycloergometer at 50 rpm for 30 minutes and with subjective perception of light exertion (11-13/20).	Resting in a seated position for 30 minutes.	Changes in motor evoked potential (MEP) in electroneuromyography.	There was no significant effect on neuronal excitability after a single session of mild-intensity exercise with or without electrical stimulation (iTBs). There was no significant change in MEP amplitude over time with exercise alone (p = 0.661). Mild-intensity aerobic exercise does not result in an improvement in excitability.
Charalambous et al., 2018/ Topics Stroke Rehabilitation/ Randomized clinical trial2020. Charalambous CC, Helm EE, Lau KA, Morton SM, Reisman DS. The feasibility of an acute high-intensity exercise bout to promote locomotor learning after stroke. Top Stroke Rehabil. 2018 Mar;25(2):83-9. https://doi.org/10.1080/10749357.2017.1399527 https://doi.org/10.1080/10749357.2017.13...	N = 34 3 groups: - Control: 11 - Treadmill walk: 13 - Total body exercise: 10	Treadmill walk (TMW): 13 individuals - 15 minutes of high intensity exercise (75 to 80% of HR max. or 13-15 SPE if using BB). - Total Body exercise (TBE): Subjects pedaled at high resistance and fast speed, which we modulated throughout so that the exercise intensity was within the high-intensity range based on either HR or SPE.	Control (CON): 11 individuals - walking on the treadmill at 25% of comfortable speed (low intensity)	Changes in BDNF blood level.	Intensity significantly changed from the beginning to the end of exercise only in the exercise groups (CON: p = 0.104; TMW: p < 0.001; TBE: p < 0.001). Lactate levels were similar between the groups pre-exercise (p > 0.05 in all groups). Only the exercise groups (p < 0.001 in both groups) showed significant changes from pre- to post-exercise (CON: p = 0.592). A significant exercise effect was found for all measurements, except BDNF.
Boyne et al., 2020/ Neurorehabilitation and Neural/ crossover2121. Boyne P, Meyrose C, Westover J, Whitesel D, Hatter K, Reisman DS, et al. Effects of exercise intensity on acute circulating molecular responses poststroke. Neurorehabil Neural Repair. 2020 Mar;34(3):222-34. https://doi.org/10.1177/1545968319899915 https://doi.org/10.1177/1545968319899915...	N = 15 - 3 groups: - HIIT on the treadmill: 5 - Seated stepper HIIT :5 - Continuous exercise (MCT treadmill): 5	- HIIT on the treadmill: 3 min of warm-up + 20 min of HIIT, in which the protocol was 30'' acceleration with 60'' rest and recovery decreasing to 30'' after the first 5 min. The goal was to achieve a RHR of 60%. - Seated stepper HIIT (ergometer cycle): 3 min of warm-up + 20 min of HIIT, in which the protocol was 30'' acceleration with 60'' rest and recovery decreasing to 30'' after the first 5 min. The goal was to achieve a RHR of 60%.	Continuous exercise (MCT treadmill): from moderate intensity to 45% of RHR	Changes in VEGF1, IgF1 and cortisol blood level.	- HIIT elicited significantly (P < 0.05) greater mean responses than MCT for blood lactate (HIT-treadmill, 4.6 mmol/L; HIT-stepper, 6.8 mmol/L; MCT-treadmill, 2.0 mmol/L), mean heart rate (HIT-treadmill, 59.0% of heart rate reserve; HIT-stepper, 67.5%; MCT-treadmill, 43.8%), and peak treadmill speed (HIT-treadmill, 1.30 m/s; MCT-treadmill, 0.68 m/s) - VEGF1 significantly increased in HIIT on the treadmill, with no increase in the other groups - IgF1 increased significantly in both HIIT groups and did not increase in MICE - Cortisol decreased in all 3 groups
Boyne et al., 2019/ Journal of Applied Physiology/ crossover2222. Boyne P, Meyrose C, Westover J, Whitesel D, Hatter K, Reisman DS, et al. Exercise intensity affects acute neurotrophic and neurophysiological responses poststroke. J Appl Physiol (1985). 2019 Feb 1;126(2):431-43. https://doi.org/10.1152/japplphysiol.00594.2018 https://doi.org/10.1152/japplphysiol.005...	N = 15 - 3 groups: - HIIT on the treadmill: 5 - Seated stepper HIIT: 5 - Continuous exercise (MCT treadmill): 5	HIIT on the treadmill: 3 min of warm-up + 20 min of HIIT, in which the protocol was 30'' acceleration with 60'' rest and recovery, decreasing to 30'' after the first 5 min. The goal was to achieve a RHR of 60%. - Seated stepper HIIT (ergometer cycle): Same HIIT protocol on the treadmill.	Continuous exercise: from moderate intensity to 45% of RHR.	Changes in BDNF blood level.	Serum BDNF significantly increased during the treadmill GXT (4.6 ng/ml [95% confidence interval: 0.7-8.4]). The increase was significantly greater for HIT-treadmill, compared with MCT-treadmill (3.9 [0.1-7.8]) but not for HIT-stepper compared with MCT treadmill (2.9 [1.0-6.7]). The increase in BDNF was positively related to lactate, VO2 and HR. The highest BDNF results were with lactate > 4.7, mean VO2 > 67% peak and RHR > 60%.
Morton, 2019/ Topics in Stroke Rehabilitation/ crossover2727. Li X, Charalambous CC, Reisman DS, Morton SM. A short bout of high-intensity exercise alters ipsilesional motor cortical excitability post-stroke. Top Stroke Rehabil. 2019 Sep;26(6):405-11. https://doi.org/10.1080/10749357.2019.1623458 https://doi.org/10.1080/10749357.2019.16...	N = 13 (HIIT and rest)	Two one-week training sessions between them - crossover: - 5 minutes of high intensity on the treadmill - 70 to 80% of HRmax.	Rest	Changes in motor evoked potential (MEP) on electroneuromyography.	All participants were able to reach the target high-intensity exercise level. Blood lactate levels increased significantly after exercise (p < 0.001; d = 2.85). Resting motor evoked potentials from the lesioned hemisphere increased after exercise, compared with the resting condition (p = 0.046; d = 2.76), but this was not the case for the non-lesioned hemisphere (p = 0.406; d = 0.25).

Author and year	Eligibility	Subjects were randomly assigned	Blind distribution	Similar groups	Subjects were blinded	Therapists were blinded	Assessors were blinded	Results measured	Intention-to-treat analysis	Intergroup comparison	Measurement of variability	Total
Linder et al., 201955. Linder SM, Rosenfeldt AB, Davidson S, Zimmerman N, Penko A, Lee J, et al. Forced, not voluntary, aerobic exercise enhances motor recovery in persons with chronic stroke. Neurorehabil Neural Repair. 2019 Aug;33(8):681-90. https://doi.org/10.1177/1545968319862557 https://doi.org/10.1177/1545968319862557...	Yes	Yes	Yes	Yes	No	No	Yes	Yes	No	Yes	Yes	8/11
Ploughman et al., 201999. Ploughman M, Austin MW, Glynn L, Corbett D. The effects of poststroke aerobic exercise on neuroplasticity: a systematic review of animal and clinical studies. Transl Stroke Res. 2015 Feb;6(1):13-28. https://doi.org/10.1007/s12975-014-0357-7 https://doi.org/10.1007/s12975-014-0357-...	Yes	Yes	Yes	Yes	No	No	Yes	Yes	Yes	Yes	Yes	9/11
Luft et al., 20081111. Luft AR, Macko RF, Forrester LW, Villagra F, Ivey F, Sorkin JD, et al. Treadmill exercise activates subcortical neural networks and improves walking after stroke: a randomized controlled trial. Stroke. 2008 Dec;39(12):3341-50. https://doi.org/10.1161/STROKEAHA.108.527531 https://doi.org/10.1161/STROKEAHA.108.52...	Yes	Yes	No	Yes	No	No	Yes	No	No	Yes	Yes	6/11
Nepveu et al., 20171212. Nepveu J-F, Thiel A, Tang A, Fung J, Lundbye-Jensen J, Boyd LA, et al. A single bout of High-Intensity interval training improves motor skill retention in individuals with stroke. Neurorehabil Neural Repair. 2017 Aug;31(8):726-35. https://doi.org/10.1177/1545968317718269 https://doi.org/10.1177/1545968317718269...	No	Yes	No	Yes	No	No	Yes	Yes	Yes	Yes	Yes	7/11
Abraha et al., 20181313. Abraha B, Chaves AR, Kelly LP, Wallack EM, Wadden KP, McCarthy J, et al. A bout of high intensity interval training lengthened nerve conduction latency to the non-exercised affected limb in chronic stroke. Front Physiol. 2018 Jul 2;9:827. https://doi.org/10.3389/fphys.2018.00827 https://doi.org/10.3389/fphys.2018.00827...	No	No	No	No	No	No	No	Yes	Yes	Yes	Yes	4/11
Murdoch et al., 20161515. Murdoch K, Buckley JD, McDonnell MN. The effect of aerobic exercise on neuroplasticity within the motor cortex following stroke. PLoS One. 2016 Mar 28;11(3):e0152377. https://doi.org/10.1371/journal.pone.0152377 https://doi.org/10.1371/journal.pone.015...	Yes	Yes	No	No	No	No	No	No	No	Yes	Yes	4/11
Quaney et al., 20091616. Quaney BM, Boyd LA, McDowd JM, Zahner LH, He J, Mayo MS, et al. Aerobic exercise improves cognition and motor function poststroke. Neurorehabil Neural Repair. 2009 Nov;23(9):879-85. https://doi.org/10.1177/1545968309338193 https://doi.org/10.1177/1545968309338193...	Yes	Yes	No	Yes	No	No	Yes	Yes	No	Yes	Yes	7/11
Yang et al., 20141717. Yang H-C, Lee C-L, Lin R, Hsu M-J, Chen C-H, Lin J-H, et al. Effect of biofeedback cycling training on functional recovery and walking ability of lower extremity in patients with stroke. Kaohsiung J Med Sci. 2014 Jan;30(1):35-42. https://doi.org/10.1016/j.kjms.2013.07.006 https://doi.org/10.1016/j.kjms.2013.07.0...	Yes	Yes	Yes	Yes	No	No	Yes	Yes	No	Yes	Yes	8/11
El-Tamawy et al., 20141919. El-Tamawy MS, Abd-Allah F, Ahmed SM, Darwish MH, Khalifa HA. Aerobic exercises enhance cognitive functions and brain derived neurotrophic factor in ischemic stroke patients. NeuroRehabilitation. 2014;34(1):209-13. https://doi.org/10.3233/NRE-131020 https://doi.org/10.3233/NRE-131020...	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	Yes	6/11
Charalambous et al., 20182020. Charalambous CC, Helm EE, Lau KA, Morton SM, Reisman DS. The feasibility of an acute high-intensity exercise bout to promote locomotor learning after stroke. Top Stroke Rehabil. 2018 Mar;25(2):83-9. https://doi.org/10.1080/10749357.2017.1399527 https://doi.org/10.1080/10749357.2017.13...	Yes	Yes	No	Yes	No	No	No	Yes	Yes	Yes	Yes	7/11
Boyne et al., 20202121. Boyne P, Meyrose C, Westover J, Whitesel D, Hatter K, Reisman DS, et al. Effects of exercise intensity on acute circulating molecular responses poststroke. Neurorehabil Neural Repair. 2020 Mar;34(3):222-34. https://doi.org/10.1177/1545968319899915 https://doi.org/10.1177/1545968319899915...	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	Yes	6/11
Boyne et al., 20192222. Boyne P, Meyrose C, Westover J, Whitesel D, Hatter K, Reisman DS, et al. Exercise intensity affects acute neurotrophic and neurophysiological responses poststroke. J Appl Physiol (1985). 2019 Feb 1;126(2):431-43. https://doi.org/10.1152/japplphysiol.00594.2018 https://doi.org/10.1152/japplphysiol.005...	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	Yes	6/11
Shaughnessy et al., 20122323. Shaughnessy M, Michael K, Resnick B. Impact of treadmill exercise on efficacy expectations, physical activity, and stroke recovery. J Neurosci Nurs. 2012 Feb;44(1):27-35. https://doi.org/10.1097/JNN.0b013e31823ae4b5 https://doi.org/10.1097/JNN.0b013e31823a...	No	Yes	No	Yes	No	No	No	No	No	Yes	Yes	4/11
Sandberg et al., 20162424. Sanderg K, Kleist M, Falk L, Enthoven P. Effects of Twice-Weekly intense aerobic exercise in early subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2016 Aug 1;97(8):1244-53. https://doi.org/10.1016/j.apmr.2016.01.030 https://doi.org/10.1016/j.apmr.2016.01.0...	Yes	Yes	Yes	Yes	No	No	Yes	Yes	No	Yes	Yes	8/11
Nave et al., 20192525. Nave AH, Rackoll T, Grittner U, Bläsing H, Gorsler A, Nabavi DG, et al. Physical fitness training in patients with Subacute Stroke (PHYS-STROKE): multicentre, randomised controlled, endpoint blinded trial. BMJ. 2019 Sep 18;366:l5101. https://doi.org/10.1136/bmj.l5101 https://doi.org/10.1136/bmj.l5101...	Yes	Yes	No	Yes	No	No	Yes	No	Yes	Yes	Yes	7/11
Morton, 20192727. Li X, Charalambous CC, Reisman DS, Morton SM. A short bout of high-intensity exercise alters ipsilesional motor cortical excitability post-stroke. Top Stroke Rehabil. 2019 Sep;26(6):405-11. https://doi.org/10.1080/10749357.2019.1623458 https://doi.org/10.1080/10749357.2019.16...	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	Yes	5/11

Academia Brasileira de Neurologia - ABNEURO R. Vergueiro, 1353 sl.1404 - Ed. Top Towers Offices Torre Norte, 04101-000 São Paulo SP Brazil, Tel.: +55 11 5084-9463 | +55 11 5083-3876 - São Paulo - SP - Brazil
E-mail: revista.arquivos@abneuro.org

Acompanhe os números deste periódico no seu leitor de RSS

[1] Correspondence:
Leandro Goursand Penna; Email: lgpenna@gmail.com.