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Published in: Journal of NeuroEngineering and Rehabilitation 1/2019

Open Access 01-12-2019 | Motor Evoked Potential | Review

Combining transcranial direct-current stimulation with gait training in patients with neurological disorders: a systematic review

Authors: Rubén Hernández de Paz, Diego Serrano-Muñoz, Soraya Pérez-Nombela, Elisabeth Bravo-Esteban, Juan Avendaño-Coy, Julio Gómez-Soriano

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2019

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Abstract

Background

Transcranial direct-current stimulation (tDCS) is an easy-to-apply, cheap, and safe technique capable of affecting cortical brain activity. However, its effectiveness has not been proven for many clinical applications.

Objective

The aim of this systematic review was to determine whether the effect of different strategies for gait training in patients with neurological disorders can be enhanced by the combined application of tDCS compared to sham stimulation. Additionally, we attempted to record and analyze tDCS parameters to optimize its efficacy.

Methods

A search in Pubmed, PEDro, and Cochrane databases was performed to find randomized clinical trials that combined tDCS with gait training. A chronological filter from 2010 to 2018 was applied and only studies with variables that quantified the gait function were included.

Results

A total of 274 studies were found, of which 25 met the inclusion criteria. Of them, 17 were rejected based on exclusion criteria. Finally, 8 trials were evaluated that included 91 subjects with stroke, 57 suffering from Parkinson’s disease, and 39 with spinal cord injury. Four of the eight assessed studies did not report improved outcomes for any of its variables compared to the placebo treatment.

Conclusions

There are no conclusive results that confirm that tDCS can enhance the effect of the different strategies for gait training. Further research for specific pathologies, with larger sample sizes and adequate follow-up periods, are required to optimize the existing protocols for applying tDCS.
Literature
1.
go back to reference Sale P, Franceschini M, Waldner A, Hesse S. Use of the robot assisted gait therapy in rehabilitation of patients with stroke and spinal cord injury. Eur J Phys Rehabil Med. 2012;48:111–21.PubMed Sale P, Franceschini M, Waldner A, Hesse S. Use of the robot assisted gait therapy in rehabilitation of patients with stroke and spinal cord injury. Eur J Phys Rehabil Med. 2012;48:111–21.PubMed
2.
go back to reference Schwartz I, Meiner Z. Robotic-assisted gait training in neurological patients: who may benefit? Ann Biomed Eng. 2015;43:1260–9.CrossRef Schwartz I, Meiner Z. Robotic-assisted gait training in neurological patients: who may benefit? Ann Biomed Eng. 2015;43:1260–9.CrossRef
3.
go back to reference Benito-Penalva J, et al. Gait training in human spinal cord injury using electromechanical systems: effect of device type and patient characteristics. Arch Phys Med Rehabil. 2012;93:404–12.CrossRef Benito-Penalva J, et al. Gait training in human spinal cord injury using electromechanical systems: effect of device type and patient characteristics. Arch Phys Med Rehabil. 2012;93:404–12.CrossRef
4.
go back to reference Esquenazi A, Packel A. Robotic-assisted gait training and restoration. Am. J. Phys. Med. Rehabil. 2012;91:S217–31.CrossRef Esquenazi A, Packel A. Robotic-assisted gait training and restoration. Am. J. Phys. Med. Rehabil. 2012;91:S217–31.CrossRef
5.
go back to reference Louie DR, Eng JJ. Powered robotic exoskeletons in post-stroke rehabilitation of gait: a scoping review. J. Neuroeng. Rehabil. 2016;13:53.CrossRef Louie DR, Eng JJ. Powered robotic exoskeletons in post-stroke rehabilitation of gait: a scoping review. J. Neuroeng. Rehabil. 2016;13:53.CrossRef
6.
go back to reference Tefertiller C, Pharo B, Evans N, Winchester P. Efficacy of rehabilitation robotics for walking training in neurological disorders: a review. J Rehabil Res Dev. 2011;48:387–416.CrossRef Tefertiller C, Pharo B, Evans N, Winchester P. Efficacy of rehabilitation robotics for walking training in neurological disorders: a review. J Rehabil Res Dev. 2011;48:387–416.CrossRef
7.
go back to reference Lam T, Wolfe DL, Domingo A, Eng JJ, Sproule S. Lower Limb Rehabilitation Following Spinal Cord Injury. In: Eng JJ, Teasell RW, Miller WC, Wolfe DL, Townson AF, JTC H, Connolly SJ, Noonan VK, Loh E, McIntyre A, editors. Spinal Cord Injury Rehabilitation Evidence. Version 5.0, 1-73; 2014. Lam T, Wolfe DL, Domingo A, Eng JJ, Sproule S. Lower Limb Rehabilitation Following Spinal Cord Injury. In: Eng JJ, Teasell RW, Miller WC, Wolfe DL, Townson AF, JTC H, Connolly SJ, Noonan VK, Loh E, McIntyre A, editors. Spinal Cord Injury Rehabilitation Evidence. Version 5.0, 1-73; 2014.
8.
go back to reference Hortal E, et al. Using a brain-machine interface to control a hybrid upper limb exoskeleton during rehabilitation of patients with neurological conditions. J Neuroeng Rehabil. 2015;12:92.CrossRef Hortal E, et al. Using a brain-machine interface to control a hybrid upper limb exoskeleton during rehabilitation of patients with neurological conditions. J Neuroeng Rehabil. 2015;12:92.CrossRef
9.
go back to reference Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57:1899–901.CrossRef Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57:1899–901.CrossRef
10.
go back to reference Lefaucheur J-P, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol. 2017;128:56–92.CrossRef Lefaucheur J-P, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol. 2017;128:56–92.CrossRef
11.
go back to reference Nitsche MA, et al. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci. 2003;15:619–26.CrossRef Nitsche MA, et al. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci. 2003;15:619–26.CrossRef
12.
go back to reference Kang N, Summers JJ, Cauraugh JH. Transcranial direct current stimulation facilitates motor learning post-stroke: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2016;87:345–55.CrossRef Kang N, Summers JJ, Cauraugh JH. Transcranial direct current stimulation facilitates motor learning post-stroke: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2016;87:345–55.CrossRef
13.
go back to reference Tedesco Triccas L, et al. Multiple sessions of transcranial direct current stimulation and upper extremity rehabilitation in stroke: a review and meta-analysis. Clin Neurophysiol. 2016;127:946–55.CrossRef Tedesco Triccas L, et al. Multiple sessions of transcranial direct current stimulation and upper extremity rehabilitation in stroke: a review and meta-analysis. Clin Neurophysiol. 2016;127:946–55.CrossRef
14.
go back to reference Elsner B, Kugler J, Pohl M, Mehrholz J. Transcranial direct current stimulation (tDCS) for idiopathic Parkinson’s disease. Cochrane Database Syst Rev. 2016;7:CD010916.PubMed Elsner B, Kugler J, Pohl M, Mehrholz J. Transcranial direct current stimulation (tDCS) for idiopathic Parkinson’s disease. Cochrane Database Syst Rev. 2016;7:CD010916.PubMed
15.
go back to reference Mendonca ME, et al. Transcranial direct current stimulation combined with aerobic exercise to optimize analgesic responses in fibromyalgia: a randomized placebo-controlled clinical trial. Front Hum Neurosci. 2016;10:68.CrossRef Mendonca ME, et al. Transcranial direct current stimulation combined with aerobic exercise to optimize analgesic responses in fibromyalgia: a randomized placebo-controlled clinical trial. Front Hum Neurosci. 2016;10:68.CrossRef
16.
go back to reference Chang W-J, et al. Addition of transcranial direct current stimulation to quadriceps strengthening exercise in knee osteoarthritis: a pilot randomised controlled trial. PLoS One. 2017;12:e0180328.CrossRef Chang W-J, et al. Addition of transcranial direct current stimulation to quadriceps strengthening exercise in knee osteoarthritis: a pilot randomised controlled trial. PLoS One. 2017;12:e0180328.CrossRef
17.
go back to reference Kumru H, Murillo N, Benito-Penalva J, Tormos JM, Vidal J. Transcranial direct current stimulation is not effective in the motor strength and gait recovery following motor incomplete spinal cord injury during Lokomat(®) gait training. Neurosci Lett. 2016;620:143–7.CrossRef Kumru H, Murillo N, Benito-Penalva J, Tormos JM, Vidal J. Transcranial direct current stimulation is not effective in the motor strength and gait recovery following motor incomplete spinal cord injury during Lokomat(®) gait training. Neurosci Lett. 2016;620:143–7.CrossRef
18.
go back to reference Raithatha R, et al. Non-invasive brain stimulation and robot-assisted gait training after incomplete spinal cord injury: a randomized pilot study. NeuroRehabilitation. 2016;38:15–25.CrossRef Raithatha R, et al. Non-invasive brain stimulation and robot-assisted gait training after incomplete spinal cord injury: a randomized pilot study. NeuroRehabilitation. 2016;38:15–25.CrossRef
19.
go back to reference Chang MC, Kim DY, Park DH. Enhancement of cortical excitability and lower limb motor function in patients with stroke by transcranial direct current stimulation. Brain Stimul. 2015;8:561–6.CrossRef Chang MC, Kim DY, Park DH. Enhancement of cortical excitability and lower limb motor function in patients with stroke by transcranial direct current stimulation. Brain Stimul. 2015;8:561–6.CrossRef
20.
go back to reference Costa-Ribeiro A, et al. Transcranial direct current stimulation associated with gait training in Parkinson’s disease: a pilot randomized clinical trial. Dev Neurorehabil. 2017;20:121–8.CrossRef Costa-Ribeiro A, et al. Transcranial direct current stimulation associated with gait training in Parkinson’s disease: a pilot randomized clinical trial. Dev Neurorehabil. 2017;20:121–8.CrossRef
21.
go back to reference Yotnuengnit P, Bhidayasiri R, Donkhan R, Chaluaysrimuang J, Piravej K. Effects of transcranial direct current stimulation plus physical therapy on gait in patients with Parkinson disease: a randomized controlled trial. Am. J. Phys. Med. Rehabil. 2018;97:7–15.CrossRef Yotnuengnit P, Bhidayasiri R, Donkhan R, Chaluaysrimuang J, Piravej K. Effects of transcranial direct current stimulation plus physical therapy on gait in patients with Parkinson disease: a randomized controlled trial. Am. J. Phys. Med. Rehabil. 2018;97:7–15.CrossRef
22.
go back to reference Lattari E, et al. Can transcranial direct current stimulation improve the resistance strength and decrease the rating perceived scale in recreational weight-training experience? J Strength Cond Res. 2016;30:3381–7.CrossRef Lattari E, et al. Can transcranial direct current stimulation improve the resistance strength and decrease the rating perceived scale in recreational weight-training experience? J Strength Cond Res. 2016;30:3381–7.CrossRef
23.
go back to reference Seo HG, et al. Robotic-assisted gait training combined with transcranial direct current stimulation in chronic stroke patients: a pilot double-blind, randomized controlled trial. Restor Neurol Neurosci. 2017;35:527–36.PubMed Seo HG, et al. Robotic-assisted gait training combined with transcranial direct current stimulation in chronic stroke patients: a pilot double-blind, randomized controlled trial. Restor Neurol Neurosci. 2017;35:527–36.PubMed
24.
go back to reference Geroin C, et al. Combined transcranial direct current stimulation and robot-assisted gait training in patients with chronic stroke: a preliminary comparison. Clin Rehabil. 2011;25:537–48.CrossRef Geroin C, et al. Combined transcranial direct current stimulation and robot-assisted gait training in patients with chronic stroke: a preliminary comparison. Clin Rehabil. 2011;25:537–48.CrossRef
25.
go back to reference Duarte N d AC, Grecco LAC, Galli M, Fregni F, Oliveira CS. Effect of transcranial direct-current stimulation combined with treadmill training on balance and functional performance in children with cerebral palsy: a double-blind randomized controlled trial. PLoS One. 2014;9:e105777.CrossRef Duarte N d AC, Grecco LAC, Galli M, Fregni F, Oliveira CS. Effect of transcranial direct-current stimulation combined with treadmill training on balance and functional performance in children with cerebral palsy: a double-blind randomized controlled trial. PLoS One. 2014;9:e105777.CrossRef
26.
go back to reference Manji A, et al. Effects of transcranial direct current stimulation over the supplementary motor area body weight-supported treadmill gait training in hemiparetic patients after stroke. Neurosci Lett. 2018;662:302–5.CrossRef Manji A, et al. Effects of transcranial direct current stimulation over the supplementary motor area body weight-supported treadmill gait training in hemiparetic patients after stroke. Neurosci Lett. 2018;662:302–5.CrossRef
27.
go back to reference Borgheresi A, et al. Effects of a short physical therapy program combined with transcranial direct current stimulation (tDCS) on freezing of gait in Parkinson’s disease: preliminary data from a randomized, sham-controlled study. Clin Neurophysiol. 2013;124:e200.CrossRef Borgheresi A, et al. Effects of a short physical therapy program combined with transcranial direct current stimulation (tDCS) on freezing of gait in Parkinson’s disease: preliminary data from a randomized, sham-controlled study. Clin Neurophysiol. 2013;124:e200.CrossRef
28.
go back to reference Park SD, Kim JY, Song HS. Effect of application of transcranial direct current stimulation during task-related training on gait ability of patients with stroke. J Phys Ther Sci. 2015;27:623–5.CrossRef Park SD, Kim JY, Song HS. Effect of application of transcranial direct current stimulation during task-related training on gait ability of patients with stroke. J Phys Ther Sci. 2015;27:623–5.CrossRef
29.
go back to reference Wrightson JG, Twomey R, Ross EZ, Smeeton NJ. The effect of transcranial direct current stimulation on task processing and prioritisation during dual-task gait. Exp Brain Res. 2015;233:1575–83.CrossRef Wrightson JG, Twomey R, Ross EZ, Smeeton NJ. The effect of transcranial direct current stimulation on task processing and prioritisation during dual-task gait. Exp Brain Res. 2015;233:1575–83.CrossRef
30.
go back to reference 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;96:801–8.CrossRef 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;96:801–8.CrossRef
31.
go back to reference Collange Grecco LA, et al. Effects of anodal transcranial direct current stimulation combined with virtual reality for improving gait in children with spastic diparetic cerebral palsy: a pilot, randomized, controlled, double-blind, clinical trial. Clin Rehabil. 2015;29:1212–23.CrossRef Collange Grecco LA, et al. Effects of anodal transcranial direct current stimulation combined with virtual reality for improving gait in children with spastic diparetic cerebral palsy: a pilot, randomized, controlled, double-blind, clinical trial. Clin Rehabil. 2015;29:1212–23.CrossRef
32.
go back to reference Swank C, Mehta J, Criminger C. Transcranial direct current stimulation lessens dual task cost in people with Parkinson’s disease. Neurosci Lett. 2016;626:1–5.CrossRef Swank C, Mehta J, Criminger C. Transcranial direct current stimulation lessens dual task cost in people with Parkinson’s disease. Neurosci Lett. 2016;626:1–5.CrossRef
33.
go back to reference Kaski D, Dominguez R, Allum J, Islam A, Bronstein A. Combining physical training with transcranial direct current stimulation to improve gait in Parkinson’s disease: a pilot randomized controlled study. Clin Rehabil. 2014;28:1115–24.CrossRef Kaski D, Dominguez R, Allum J, Islam A, Bronstein A. Combining physical training with transcranial direct current stimulation to improve gait in Parkinson’s disease: a pilot randomized controlled study. Clin Rehabil. 2014;28:1115–24.CrossRef
34.
go back to reference van Asseldonk EHF, Boonstra TA. Transcranial direct current stimulation of the leg motor cortex enhances coordinated motor output during walking with a large inter-individual variability. Brain Stimul. 2016;9:182–90.CrossRef van Asseldonk EHF, Boonstra TA. Transcranial direct current stimulation of the leg motor cortex enhances coordinated motor output during walking with a large inter-individual variability. Brain Stimul. 2016;9:182–90.CrossRef
35.
go back to reference Schabrun SM, Lamont RM, Brauer SG. Transcranial direct current stimulation to enhance dual-task gait training in Parkinson’s disease: a pilot RCT. PLoS One. 2016;11:e0158497.CrossRef Schabrun SM, Lamont RM, Brauer SG. Transcranial direct current stimulation to enhance dual-task gait training in Parkinson’s disease: a pilot RCT. PLoS One. 2016;11:e0158497.CrossRef
36.
go back to reference Grecco LAC, et al. Transcranial direct current stimulation during treadmill training in children with cerebral palsy: a randomized controlled double-blind clinical trial. Res Dev Disabil. 2014;35:2840–8.CrossRef Grecco LAC, et al. Transcranial direct current stimulation during treadmill training in children with cerebral palsy: a randomized controlled double-blind clinical trial. Res Dev Disabil. 2014;35:2840–8.CrossRef
37.
go back to reference Grecco LAC, et al. Transcranial direct current stimulation combined with treadmill gait training in delayed neuro-psychomotor development. J Phys Ther Sci. 2014;26:945–50.CrossRef Grecco LAC, et al. Transcranial direct current stimulation combined with treadmill gait training in delayed neuro-psychomotor development. J Phys Ther Sci. 2014;26:945–50.CrossRef
38.
go back to reference Leon D, et al. tDCS does not enhance the effects of robot-assisted gait training in patients with subacute stroke. Restor Neurol Neurosci. 2017;35:377–84.PubMed Leon D, et al. tDCS does not enhance the effects of robot-assisted gait training in patients with subacute stroke. Restor Neurol Neurosci. 2017;35:377–84.PubMed
39.
go back to reference Grecco LAC, et al. Spared primary motor cortex and the presence of MEP in cerebral palsy dictate the responsiveness to tDCS during gait training. Front Hum Neurosci. 2016;10:361.CrossRef Grecco LAC, et al. Spared primary motor cortex and the presence of MEP in cerebral palsy dictate the responsiveness to tDCS during gait training. Front Hum Neurosci. 2016;10:361.CrossRef
40.
go back to reference Kaski D, Dominguez RO, Allum JH, Bronstein AM. Improving gait and balance in patients with leukoaraiosis using transcranial direct current stimulation and physical training: an exploratory study. Neurorehabil Neural Repair. 2013;27:864–71.CrossRef Kaski D, Dominguez RO, Allum JH, Bronstein AM. Improving gait and balance in patients with leukoaraiosis using transcranial direct current stimulation and physical training: an exploratory study. Neurorehabil Neural Repair. 2013;27:864–71.CrossRef
41.
go back to reference Grecco LAC, et al. Effect of transcranial direct current stimulation combined with gait and mobility training on functionality in children with cerebral palsy: study protocol for a double-blind randomized controlled clinical trial. BMC Pediatr. 2013;13:168.CrossRef Grecco LAC, et al. Effect of transcranial direct current stimulation combined with gait and mobility training on functionality in children with cerebral palsy: study protocol for a double-blind randomized controlled clinical trial. BMC Pediatr. 2013;13:168.CrossRef
42.
go back to reference Danzl MM, Chelette KC, Lee K, Lykins D, Sawaki L. Brain stimulation paired with novel locomotor training with robotic gait orthosis in chronic stroke: a feasibility study. NeuroRehabilitation. 2013;33:67–76.PubMedPubMedCentral Danzl MM, Chelette KC, Lee K, Lykins D, Sawaki L. Brain stimulation paired with novel locomotor training with robotic gait orthosis in chronic stroke: a feasibility study. NeuroRehabilitation. 2013;33:67–76.PubMedPubMedCentral
43.
go back to reference Lattari E, et al. Acute effects of single dose transcranial direct current stimulation on muscle strength: a systematic review and meta-analysis. PLoS One. 2018;13:e0209513.CrossRef Lattari E, et al. Acute effects of single dose transcranial direct current stimulation on muscle strength: a systematic review and meta-analysis. PLoS One. 2018;13:e0209513.CrossRef
44.
go back to reference Vargas VZ, et al. Modulation of isometric quadriceps strength in soccer players with transcranial direct current stimulation: a crossover study. J Strength Cond Res. 2018;32:1336–41.CrossRef Vargas VZ, et al. Modulation of isometric quadriceps strength in soccer players with transcranial direct current stimulation: a crossover study. J Strength Cond Res. 2018;32:1336–41.CrossRef
45.
go back to reference Alam M, Truong DQ, Khadka N, Bikson M. Spatial and polarity precision of concentric high-definition transcranial direct current stimulation (HD-tDCS). Phys Med Biol. 2016;61:4506–21.CrossRef Alam M, Truong DQ, Khadka N, Bikson M. Spatial and polarity precision of concentric high-definition transcranial direct current stimulation (HD-tDCS). Phys Med Biol. 2016;61:4506–21.CrossRef
46.
go back to reference Murray LM, et al. Intensity dependent effects of transcranial direct current stimulation on corticospinal excitability in chronic spinal cord injury. Arch Phys Med Rehabil. 2015;96:S114–21.CrossRef Murray LM, et al. Intensity dependent effects of transcranial direct current stimulation on corticospinal excitability in chronic spinal cord injury. Arch Phys Med Rehabil. 2015;96:S114–21.CrossRef
47.
go back to reference Serrano-Muñoz D, et al. Intensity matters: therapist-dependent dose of spinal transcutaneous electrical nerve stimulation. PLoS One. 2017;12:e0189734.CrossRef Serrano-Muñoz D, et al. Intensity matters: therapist-dependent dose of spinal transcutaneous electrical nerve stimulation. PLoS One. 2017;12:e0189734.CrossRef
48.
go back to reference Antal A, et al. Low intensity transcranial electric stimulation: safety, ethical, legal regulatory and application guidelines. Clin Neurophysiol. 2017;128:1774–809.CrossRef Antal A, et al. Low intensity transcranial electric stimulation: safety, ethical, legal regulatory and application guidelines. Clin Neurophysiol. 2017;128:1774–809.CrossRef
49.
go back to reference Brunoni AR, et al. A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int J Neuropsychopharmacol. 2011;14:1133–45.CrossRef Brunoni AR, et al. A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int J Neuropsychopharmacol. 2011;14:1133–45.CrossRef
Metadata
Title
Combining transcranial direct-current stimulation with gait training in patients with neurological disorders: a systematic review
Authors
Rubén Hernández de Paz
Diego Serrano-Muñoz
Soraya Pérez-Nombela
Elisabeth Bravo-Esteban
Juan Avendaño-Coy
Julio Gómez-Soriano
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2019
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-019-0591-z

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