Effects of Transcranial Direct Current Stimulation Followed by Treadmill Training on Dual-Task Walking and Cortical Activity in Chronic Stroke: A Double-Blinded Randomized Controlled Trial
DOI:
https://doi.org/10.2340/jrm.v55.5258Keywords:
Transcranial Direct Current Stimulation, Treadmill training, Dual task walking, Contralesional cortical activity, Rehabilitation, Chronic strokeAbstract
Objective: To explore the effects of transcranial direct current stimulation followed by treadmill training on dual-task gait performance and contralesional cortical activity in chronic stroke patients.
Methods: Forty-five chronic stroke participants were randomized into 3 groups: a bilateral transcranial direct current stimulation and treadmill training group; a cathodal transcranial direct current stimulation and treadmill training group; and a sham transcranial direct current stimulation and treadmill training group for 50 min per session (20 min transcranial direct current stimulation followed by 30 min treadmill training), 3 sessions per week for 4 weeks. Outcome measures included cognitive dual-task walking, motor dual-task walking, walking performance, contralesional cortical activity, and lower-extremity motor control.
Results: The cathodal transcranial direct current stimulation + treadmill training group showed significantly greater improvements in cognitive dual-task walking speed than the other groups (p cathodal vs sham = 0.006, p cathodal vs bilateral = 0.016). In the cathodal transcranial direct current stimulation + treadmill training group the silent period duration increased significantly more than in the other groups (p < 0.05). Changes in motor evoked potentials in the cathodal transcranial direct current stimulation + treadmill training group were greater than those in the sham transcranial direct current stimulation + treadmill training group (p < 0.05). No significant changes were observed in the bilateral transcranial direct current stimulation + treadmill training group.
Conclusion: Cathodal transcranial direct current stimulation followed by treadmill training is an effective intervention for improving cognitive dual-task walking and modulating contralesional cortical activity in chronic stroke. No beneficial effects were observed after bilateral transcranial direct current stimulation and treadmill training.
LAY ABSTRACT
Dual-task walking is essential for daily functioning, both at home and socially. This study explored the effects of transcranial direct current stimulation followed by treadmill training on dual-task gait performance and contralesional cortical activity in chronic stroke patients. A total of 45 chronic stroke patients were randomized to 1 of 3 groups: a bilateral transcranial direct current stimulation and treadmill training group, a cathodal transcranial direct current stimulation and treadmill training group, or a sham transcranial direct current stimulation and treadmill training group for 50 min per session, 3 sessions per week for 4 weeks. Cognitive dual-task walking, motor dual-task walking, walking performance, contralesional cortical activity, and lower-extremity motor control of the affected side were measured before and after the intervention. The results show that cathodal transcranial direct current stimulation followed by treadmill training is an effective intervention for improving cognitive dual-task walking and modulating contralesional cortical activity
in individuals with chronic stroke.
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References
Balaban B, Tok F. Gait disturbances in patients with stroke. PM R 2014; 6: 635–642. DOI: 10.1016/j.pmrj.2013.12.017. DOI: https://doi.org/10.1016/j.pmrj.2013.12.017
Liu YC, Yang YR, Tsai YA, Wang RY. Cognitive and motor dual task gait training improve dual task gait performance after stroke – a randomized controlled pilot trial. Sci Rep 2017; 7: 4070. DOI: 10.1038/s41598-017-04165-y. DOI: https://doi.org/10.1038/s41598-017-04165-y
Patterson SL, Rodgers MM, Macko RF, Forrester LW. Effect of treadmill exercise training on spatial and temporal gait parameters in subjects with chronic stroke: a preliminary report. J Rehab Res Dev 2008; 45: 221–228. DOI: 10.1682/jrrd.2007.02.0024. DOI: https://doi.org/10.1682/JRRD.2007.02.0024
Meester D, Al-Yahya E, Dennis A, Collett J, Wade DT, Ovington M, et al. A randomized controlled trial of a walking training with simultaneous cognitive demand (dual-task) in chronic stroke. Eur J Neurol 2019; 26: 435–441. DOI: 10.1111/ene.13833. DOI: https://doi.org/10.1111/ene.13833
Parati M, Ambrosini E, DE Maria B, Gallotta M, Dalla Vecchia LA, Ferriero G, et al. The reliability of gait parameters captured via instrumented walkways: a systematic review and meta-analysis. Eur J Phys Rehabil Med 2022; 58: 363–377. DOI: 10.23736/S1973-9087.22.07037-X. DOI: https://doi.org/10.23736/S1973-9087.22.07037-X
Liu YC, Yang YR, Tsai YA, Wang RY, Lu CF. Brain activation and gait alteration during cognitive and motor dual task walking in stroke – a functional near-infrared spectroscopy study. IEEE Trans Neural Syst Rehabil Eng 2018; 26: 2416–2423. DOI: 10.1109/TNSRE.2018.2878045. DOI: https://doi.org/10.1109/TNSRE.2018.2878045
Stagg CJ, Nitsche MA. Physiological basis of transcranial direct current stimulation. Neuroscientist 2011; 17: 37–53. DOI: 10.1177/1073858410386614. DOI: https://doi.org/10.1177/1073858410386614
Kang N, Weingart A, Cauraugh JH. Transcranial direct current stimulation and suppression of contralesional primary motor cortex post-stroke: a systematic review and meta-analysis. Brain Inj 2018; 32: 1063–1070. DOI: 10.1080/02699052.2018.1481526. DOI: https://doi.org/10.1080/02699052.2018.1481526
Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G. Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 2010; 75: 2176–2184. DOI: 10.1212/WNL.0b013e318202013a. DOI: https://doi.org/10.1212/WNL.0b013e318202013a
Zimerman M, Heise KF, Hoppe J, Cohen LG, Gerloff C, Hummel FC. Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand. Stroke 2012; 43: 2185–2191. DOI: 10.1161/STROKEAHA.111.645382. DOI: https://doi.org/10.1161/STROKEAHA.111.645382
Lefebvre S, Laloux P, Peeters A, Desfontaines P, Jamart J, Vandermeeren Y. Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front Hum Neurosci 2013; 6: 343. DOI: 10.3389/fnhum.2012.00343. DOI: https://doi.org/10.3389/fnhum.2012.00343
Sharma R, Aranha VP, Saxena A, Samuel AJ. Effects of dual transcranial direct current stimulation and modified constraint induced movement therapy to improve upper-limb function after stroke: a double-blinded, pilot randomized controlled trial. J Stroke Cerebrovasc Dis 2021; 4: 106227. DOI: 10.1016/j.jstrokecerebrovasdis.2021.106227. DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2021.106227
Wong PL, Yang YR, Tang SC, Huang SF, Wang RY. Comparing different montages of transcranial direct current stimulation on dual-task walking and cortical activity in chronic stroke: double-blinded randomized controlled trial. BMC Neurol 2022; 22: 119. DOI: 10.1186/s12883-022-02644-y. DOI: https://doi.org/10.1186/s12883-022-02644-y
Nitsche MA, Liebetanz D, Lang N, Antal A, Tergau F, Paulus W. Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin Neurophysiol 2003; 114: 2220–2222; author reply 2222-2223. DOI: 10.1016/s1388-2457(03)00235-9. DOI: https://doi.org/10.1016/S1388-2457(03)00235-9
Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc 1982; 14: 377–381. DOI: https://doi.org/10.1249/00005768-198205000-00012
Bilney B, Morris M, Webster K. Concurrent related validity of the GAITRite walkway system for quantification of the spatial and temporal parameters of gait. Gait Posture 2003; 17: 68–74. DOI: 10.1016/s0966-6362(02)00053-x. DOI: https://doi.org/10.1016/S0966-6362(02)00053-X
Cho KH, Lee HJ, Lee WH. Test-retest reliability of the GAITRite walkway system for the spatio-temporal gait parameters while dual-tasking in post-stroke patients. Disabil Rehabil 2015; 37: 512–516. DOI: 10.3109/09638288.2014.932445. DOI: https://doi.org/10.3109/09638288.2014.932445
Plummer P, Eskes G. Measuring treatment effects on dual-task performance: a framework for research and clinical practice. Front Hum Neurosci 2015; 9: 225. DOI: 10.3389/fnhum.2015.00225. DOI: https://doi.org/10.3389/fnhum.2015.00225
Yen CL, Wang RY, Liao KK, Huang CC, Yang YR. Gait training induced change in corticomotor excitability in patients with chronic stroke. Neurorehabil Neural Repair 2008; 22: 22–30. DOI: 10.1177/1545968307301875. DOI: https://doi.org/10.1177/1545968307301875
Murase N, Rothwell JC, Kaji R, Urushihara R, Nakamura K, Murayama N, et al. Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer’s cramp. Brain 2005; 128: 104–115. DOI: 10.1093/brain/awh315. DOI: https://doi.org/10.1093/brain/awh315
Papegaaij S, Taube W, Hogenhout M, Baudry S, Hortobágyi T. Age-related decrease in motor cortical inhibition during standing under different sensory conditions. Front Aging Neurosci 2014; 6: 126. DOI: 10.3389/fnagi.2014.00126. DOI: https://doi.org/10.3389/fnagi.2014.00126
Duncan PW, Propst M, Nelson SG. Reliability of the Fugl-Meyer assessment of sensorimotor recovery following cerebrovascular accident. Phys Ther 1983; 63: 1606–1610. DOI: 10.1093/ptj/63.10.1606. DOI: https://doi.org/10.1093/ptj/63.10.1606
Seo HG, Lee WH, Lee SH, Yi Y, Kim KD, Oh BM. 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: 527–536. DOI: 10.3233/RNN-170745. DOI: https://doi.org/10.3233/RNN-170745
Cohen J. A power primer. Psychol Bull 1992; 112: 155–159. DOI: 10.1037//0033-2909.112.1.155. DOI: https://doi.org/10.1037/0033-2909.112.1.155
McGough JJ, Faraone SV. Estimating the size of treatment effects: moving beyond p values. Psychiatry (Edgmont) 2009; 6: 21–29.
Nair DG, Renga V, Lindenberg R, Zhu L, Schlaug G. Optimizing recovery potential through simultaneous occupational therapy and non-invasive brain-stimulation using tDCS. Restor Neurol Neurosci 2011; 29: 411–420. DOI: 10.3233/RNN-2011-0612. DOI: https://doi.org/10.3233/RNN-2011-0612
Fusco A, Assenza F, Iosa M, Izzo S, Altavilla R, Paolucci S, et al. The ineffective role of cathodal tDCS in enhancing the functional motor outcomes in early phase of stroke rehabilitation: an experimental trial. Biomed Res Int 2014; 2014: 547290. DOI: 10.1155/2014/547290. DOI: https://doi.org/10.1155/2014/547290
Lee SH, Kim WS, Park J, Kim J, Paik NJ. Effects of anodal transcranial direct current stimulation over the contralesional hemisphere on motor recovery in subacute stroke patients with severe upper extremity hemiparesis: study protocol for a randomized controlled trial. Medicine (Baltimore) 2020; 99: e19495. DOI: 10.1097/MD.0000000000019495. DOI: https://doi.org/10.1097/MD.0000000000019495
Dodd KC, Nair VA, Prabhakaran V. Role of the contralesional vs. ipsilesional hemisphere in stroke recovery. Front Hum Neurosci 2017; 21: 469. DOI: 10.3389/fnhum.2017.00469. DOI: https://doi.org/10.3389/fnhum.2017.00469
Collett J, Fleming MK, Meester D, Al-Yahya E, Wade DT, Dennis A, et al. Dual-task walking and automaticity after Stroke: insights from a secondary analysis and imaging sub-study of a randomised controlled trial. Clin Rehabil 2021; 30: 2692155211017360. DOI: 10.1177/02692155211017360. DOI: https://doi.org/10.1177/02692155211017360
Bijleveld-Uitman M, van de Port I, Kwakkel G. Is gait speed or walking distance a better predictor for community walking after stroke? J Rehabil Med 2013; 45: 535–540. DOI: 10.2340/16501977-1147. DOI: https://doi.org/10.2340/16501977-1147
Corp DT, Youssef GJ, Clark RA, Gomes-Osman J, Yücel MA, Oldham SJ, et al. Reduced motor cortex inhibition and a ‘cognitive-first’ prioritisation strategy for older adults during dual-tasking. Exp Gerontol 2018; 113: 95–105. DOI: 10.1016/j.exger.2018.09.018. DOI: https://doi.org/10.1016/j.exger.2018.09.018
Ding Q, Triggs WJ, Kamath SM, Patten C. Short intracortical inhibition during voluntary movement reveals persistent impairment post-stroke. Front Neurol 2019; 9: 1105. DOI: 10.3389/fneur.2018.01105. DOI: https://doi.org/10.3389/fneur.2018.01105
McDonnell MN, Stinear CM. TMS measures of motor cortex function after stroke: a meta-analysis. Brain Stimul 2017; 10: 721–734. DOI: 10.1016/j.brs.2017.03.008. DOI: https://doi.org/10.1016/j.brs.2017.03.008
Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 1999; 517: 591–597. DOI: 10.1111/j.1469-7793.1999.0591t.x. DOI: https://doi.org/10.1111/j.1469-7793.1999.0591t.x
Dimyan MA, Cohen LG. Contribution of transcranial magnetic stimulation to the understanding of functional recovery mechanisms after stroke. Neurorehabil Neural Repair 2010; 24: 125–135. DOI: 10.1177/1545968309345270. DOI: https://doi.org/10.1177/1545968309345270
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: 623–625. DOI: 10.1589/jpts.27.623. DOI: https://doi.org/10.1589/jpts.27.623
Aneksan B, Sawatdipan M, Bovonsunthonchai S, Tretriluxana J, Vachalathiti R, Auvichayapat P, et al. Five-session dual-transcranial direct current stimulation with task-specific training does not improve gait and lower limb performance over training alone in subacute stroke: a pilot randomized controlled trial. Neuromodulation 2022; 25: 558–568. DOI: 10.1111/ner.13526. DOI: https://doi.org/10.1111/ner.13526
Naro A, Billeri L, Manuli A, Balletta T, Cannavò A, Portaro S, et al. Breaking the ice to improve motor outcomes in patients with chronic stroke: a retrospective clinical study on neuromodulation plus robotics. Neurol Sci 2020; 42: 2785–2793. DOI: 10.1007/s10072-020-04875-8. DOI: https://doi.org/10.1007/s10072-020-04875-8
Wang RY, Tseng HY, Liao KK, Wang CJ, Lai KL, Yang YR. rTMS combined with task-oriented training to improve symmetry of interhemispheric corticomotor excitability and gait performance after stroke: a randomized trial. Neurorehabil Neural Repair 2012; 26: 222–230. DOI: 10.1177/1545968311423265. DOI: https://doi.org/10.1177/1545968311423265
Sehle A, Stuerner J, Hassa T, Spiteri S, Schoenfeld MA, Liepert J. Behavioral and neurophysiological effects of an intensified robot-assisted therapy in subacute stroke: a case control study. J Neuroeng Rehabil 2021; 18: 6. DOI: 10.1186/s12984-020-00792-1 DOI: https://doi.org/10.1186/s12984-020-00792-1
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