Skip to main content
Top
Published in: Neurological Sciences 7/2021

01-07-2021 | Stroke | Original Article

Breaking the ice to improve motor outcomes in patients with chronic stroke: a retrospective clinical study on neuromodulation plus robotics

Authors: Antonino Naro, Luana Billeri, Alfredo Manuli, Tina Balletta, Antonino Cannavò, Simona Portaro, Paola Lauria, Fabrizio Ciappina, Rocco Salvatore Calabrò

Published in: Neurological Sciences | Issue 7/2021

Login to get access

Abstract

Background

Stroke is one of the main causes of impairment affecting daily activities and quality of life. There is a growing effort to potentiate the recovery of functional gait and to enable stroke patients to walk independently.

Aim

To estimate the effects of dual-site transcranial direct current stimulation (dstDCS) on gait recovery in chronic stroke patients provided with robot-aided gait training (RAGT).

Methods

Thirty-seven patients were included in this retrospective clinical study. Nine patients were provided with dstDCS during the first 10 min of RAGT by using Lokomat®Pro (on-RAGT), 15 patients immediately after RAGT (post-RAGT), and 13 patients immediately before RAGT (pre-RAGT).

Results

Each group improved over time concerning disability burden and lower limb strength. on-RAGT and post-RAGT experienced better improvement in balance (p < 0.001) and, moderately, gait endurance (p = 0.04) as compared to pre-RAGT. Furthermore, all treatments decreased the facilitation of the unaffected hemisphere (p < 0.001) and the inhibition of the affected hemisphere (p < 0.001). The duration of such aftereffects was found to be greater for post-RAGT.

Discussion and conclusion

This is the first trial with dstDCS coupled with RAGT in chronic stroke patients with gait impairment. When timely coupled with RAGT, dstDCS may be considered an effective tool for the recovery of lower limb function in patients with first unilateral stroke in the chronic phase. Moreover, our data suggest the ductility of dstDCS concerning RAGT timing, thus making this intervention suitable in a neurorehabilitation setting and well adaptable to patients’ needs.
Appendix
Available only for authorised users
Literature
1.
go back to reference Warlow CP, Dennis M S, van Gijn J, Hankey GJ, Sandercock PA, Bamford JM, et al. (2001). Stroke, a practical guide to management. Wiley-Blackwell Warlow CP, Dennis M S, van Gijn J, Hankey GJ, Sandercock PA, Bamford JM, et al. (2001). Stroke, a practical guide to management. Wiley-Blackwell
2.
go back to reference Tedla JS, Dixit S, Gular K, Abohashrh M (2019) Robotic-assisted gait training effect on function and gait speed in subacute and chronic stroke population, a systematic review and meta-analysis of randomized controlled trials. Eur Neurol 81:103–111PubMedCrossRef Tedla JS, Dixit S, Gular K, Abohashrh M (2019) Robotic-assisted gait training effect on function and gait speed in subacute and chronic stroke population, a systematic review and meta-analysis of randomized controlled trials. Eur Neurol 81:103–111PubMedCrossRef
3.
go back to reference Zheng QX, Ge L, Wang CC, Ma QS, Liao YT, Huang PP, Wang GD, Xie QL, Rask M (2019) Robot-assisted therapy for balance function rehabilitation after stroke, a systematic review and meta-analysis. Int J Nurs Stud 95:7–18PubMedCrossRef Zheng QX, Ge L, Wang CC, Ma QS, Liao YT, Huang PP, Wang GD, Xie QL, Rask M (2019) Robot-assisted therapy for balance function rehabilitation after stroke, a systematic review and meta-analysis. Int J Nurs Stud 95:7–18PubMedCrossRef
4.
go back to reference Klamroth-Marganska V (2018) Stroke rehabilitation, therapy robots and assistive devices. Adv Exp Med Biol 1065:579–587PubMedCrossRef Klamroth-Marganska V (2018) Stroke rehabilitation, therapy robots and assistive devices. Adv Exp Med Biol 1065:579–587PubMedCrossRef
5.
go back to reference Bolognini N, Pascual-Leone A, Fregni F (2009) Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil 6:8PubMedPubMedCentralCrossRef Bolognini N, Pascual-Leone A, Fregni F (2009) Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil 6:8PubMedPubMedCentralCrossRef
6.
go back to reference Hummel FC, Cohen LG (2006) Non-invasive brain stimulation, a new strategy to improve neurorehabilitation after stroke? Lancet Neurol 5:708–712PubMedCrossRef Hummel FC, Cohen LG (2006) Non-invasive brain stimulation, a new strategy to improve neurorehabilitation after stroke? Lancet Neurol 5:708–712PubMedCrossRef
7.
go back to reference Mehrholz J, Thomas S, Werner C, Kugler J, Pohl M, Elsner B (2017) Electromechanical-assisted training for walking after stroke. Cochrane Database Syst Rev 5:CD006185PubMed Mehrholz J, Thomas S, Werner C, Kugler J, Pohl M, Elsner B (2017) Electromechanical-assisted training for walking after stroke. Cochrane Database Syst Rev 5:CD006185PubMed
8.
go back to reference Lefaucheur JP, Antal A, Ayache SS, Benninger DH, Brunelin J, Cogiamanian F, Cotelli M, de Ridder D, Ferrucci R, Langguth B, Marangolo P, Mylius V, Nitsche MA, Padberg F, Palm U, Poulet E, Priori A, Rossi S, Schecklmann M, Vanneste S, Ziemann U, Garcia-Larrea L, Paulus W (2017) Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol 128:56–92PubMedCrossRef Lefaucheur JP, Antal A, Ayache SS, Benninger DH, Brunelin J, Cogiamanian F, Cotelli M, de Ridder D, Ferrucci R, Langguth B, Marangolo P, Mylius V, Nitsche MA, Padberg F, Palm U, Poulet E, Priori A, Rossi S, Schecklmann M, Vanneste S, Ziemann U, Garcia-Larrea L, Paulus W (2017) Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol 128:56–92PubMedCrossRef
9.
go back to reference Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 57(10):1899–1901PubMedCrossRef Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 57(10):1899–1901PubMedCrossRef
10.
go back to reference Tazoe T, Endoh T, Kitamura T, Ogata T (2014) Polarity specific effects of transcranial direct current stimulation on interhemispheric inhibition. PLoS One 9:e11424CrossRef Tazoe T, Endoh T, Kitamura T, Ogata T (2014) Polarity specific effects of transcranial direct current stimulation on interhemispheric inhibition. PLoS One 9:e11424CrossRef
11.
go back to reference Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual-Leone A, Fregni F (2006) Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci 249:31–38PubMedCrossRef Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual-Leone A, Fregni F (2006) Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci 249:31–38PubMedCrossRef
12.
go back to reference Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875PubMedCrossRef Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875PubMedCrossRef
13.
go back to reference Cuypers K, Leenus DJF, van den Berg FE, Nitsche MA, Thijs H, Wenderoth N, Meesen RLJ (2013) Is motor learning mediated by tDCS intensity? PLoS One 8:e67344PubMedPubMedCentralCrossRef Cuypers K, Leenus DJF, van den Berg FE, Nitsche MA, Thijs H, Wenderoth N, Meesen RLJ (2013) Is motor learning mediated by tDCS intensity? PLoS One 8:e67344PubMedPubMedCentralCrossRef
14.
go back to reference Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P, Cohen LG, Fregni F, Herrmann CS, Kappenman ES, Knotkova H, Liebetanz D, Miniussi C, Miranda PC, Paulus W, Priori A, Reato D, Stagg C, Wenderoth N, Nitsche MA (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol 127:1031–1048PubMedCrossRef Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P, Cohen LG, Fregni F, Herrmann CS, Kappenman ES, Knotkova H, Liebetanz D, Miniussi C, Miranda PC, Paulus W, Priori A, Reato D, Stagg C, Wenderoth N, Nitsche MA (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol 127:1031–1048PubMedCrossRef
15.
go back to reference Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639PubMedPubMedCentralCrossRef Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639PubMedPubMedCentralCrossRef
16.
go back to reference Kessler SK, Minhas P, Woods AJ, Rosen A, Gorman C, Bikson M (2013) Dosage considerations for transcranial direct current stimulation in children, a computational modeling study. PLoS One 8:e76112PubMedPubMedCentralCrossRef Kessler SK, Minhas P, Woods AJ, Rosen A, Gorman C, Bikson M (2013) Dosage considerations for transcranial direct current stimulation in children, a computational modeling study. PLoS One 8:e76112PubMedPubMedCentralCrossRef
17.
go back to reference Gill J, Shah-Basak PP, Hamilton R (2014) It’s the thought that counts, examining the task-dependent effects of transcranial direct current stimulation on executive function. Brain Stimul 8:253–259PubMedCrossRef Gill J, Shah-Basak PP, Hamilton R (2014) It’s the thought that counts, examining the task-dependent effects of transcranial direct current stimulation on executive function. Brain Stimul 8:253–259PubMedCrossRef
18.
go back to reference Bai X, Guo Z, He L, Ren L, McClure MA, Mu Q (2019) Different therapeutic effects of transcranial direct current stimulation on upper and lower limb recovery of stroke patients with motor dysfunction, a meta-analysis. Neural Plast 2019:1372138PubMedPubMedCentralCrossRef Bai X, Guo Z, He L, Ren L, McClure MA, Mu Q (2019) Different therapeutic effects of transcranial direct current stimulation on upper and lower limb recovery of stroke patients with motor dysfunction, a meta-analysis. Neural Plast 2019:1372138PubMedPubMedCentralCrossRef
19.
go back to reference Gowan S, Hordacre B (2020) Transcranial direct current stimulation to facilitate lower limb recovery following stroke, current evidence and future directions. Brain Sci 10:310PubMedCentralCrossRef Gowan S, Hordacre B (2020) Transcranial direct current stimulation to facilitate lower limb recovery following stroke, current evidence and future directions. Brain Sci 10:310PubMedCentralCrossRef
20.
go back to reference Bornheim S, Thibaut A, Beaudart C, Maquet P, Croisier JL, Kaux JF (2020) Evaluating the effects of tDCS in stroke patients using functional outcomes, a systematic review. Disabil Rehabil:1–11 Bornheim S, Thibaut A, Beaudart C, Maquet P, Croisier JL, Kaux JF (2020) Evaluating the effects of tDCS in stroke patients using functional outcomes, a systematic review. Disabil Rehabil:1–11
21.
go back to reference Kang N, Lee RD, Lee JH, Hwang MH (2020) Functional balance and postural control improvements in patients with stroke after noninvasive brain stimulation, a meta-analysis. Arch Phys Med Rehabil 101:141–153PubMedCrossRef Kang N, Lee RD, Lee JH, Hwang MH (2020) Functional balance and postural control improvements in patients with stroke after noninvasive brain stimulation, a meta-analysis. Arch Phys Med Rehabil 101:141–153PubMedCrossRef
22.
go back to reference Orrù G, Conversano C, Hitchcott PK, Gemignani A (2020) Motor stroke recovery after tDCS, a systematic review. Rev Neurosci 31:201–218PubMedCrossRef Orrù G, Conversano C, Hitchcott PK, Gemignani A (2020) Motor stroke recovery after tDCS, a systematic review. Rev Neurosci 31:201–218PubMedCrossRef
23.
go back to reference Feng W, Kautz SA, Schlaug G, Meinzer C, George MS, Chhatbar PY (2018) Transcranial direct current stimulation for poststroke motor recovery, challenges and opportunities. PM R 10:S157–S164PubMedPubMedCentralCrossRef Feng W, Kautz SA, Schlaug G, Meinzer C, George MS, Chhatbar PY (2018) Transcranial direct current stimulation for poststroke motor recovery, challenges and opportunities. PM R 10:S157–S164PubMedPubMedCentralCrossRef
24.
go back to reference Alsharidah M, Al-Hussain F, Iqbal M, Hamza A, Yoo WK, Bashir S (2018) The effect of transcranial direct current stimulation combined with functional task training on motor recovery in stroke patients. Eur Rev Med Pharmacol Sci 22:7385–7392PubMed Alsharidah M, Al-Hussain F, Iqbal M, Hamza A, Yoo WK, Bashir S (2018) The effect of transcranial direct current stimulation combined with functional task training on motor recovery in stroke patients. Eur Rev Med Pharmacol Sci 22:7385–7392PubMed
25.
go back to reference Danzl MM, Chelette KC, Lee K, Lykins D, Sawaki L (2013) Brain stimulation paired with novel locomotor training with robotic gait orthosis in chronic stroke, a feasibility study. NeuroRehabilitation 33:67–76PubMedPubMedCentralCrossRef Danzl MM, Chelette KC, Lee K, Lykins D, Sawaki L (2013) Brain stimulation paired with novel locomotor training with robotic gait orthosis in chronic stroke, a feasibility study. NeuroRehabilitation 33:67–76PubMedPubMedCentralCrossRef
26.
go back to reference Geroin C, Picelli A, Munari D, Waldner A, Tomelleri C, Smania N (2011) Combined transcranial direct current stimulation and robot-assisted gait training in patients with chronic stroke, a preliminary comparison. Clin Rehabil 25:537–548PubMedCrossRef Geroin C, Picelli A, Munari D, Waldner A, Tomelleri C, Smania N (2011) Combined transcranial direct current stimulation and robot-assisted gait training in patients with chronic stroke, a preliminary comparison. Clin Rehabil 25:537–548PubMedCrossRef
27.
go back to reference Giacobbe V, Krebs HI, Volpe BT, Pascual-Leone A, Rykman A, Zeiai G et al (2013) Transcranial direct current stimulation (tDCS) and robotic practice in chronic stroke, the dimension of timing. NeuroRehabilitation 33(1):49–56PubMedPubMedCentralCrossRef Giacobbe V, Krebs HI, Volpe BT, Pascual-Leone A, Rykman A, Zeiai G et al (2013) Transcranial direct current stimulation (tDCS) and robotic practice in chronic stroke, the dimension of timing. NeuroRehabilitation 33(1):49–56PubMedPubMedCentralCrossRef
28.
go back to reference Jayaram G, Stinear JW (2009) The effects of transcranial stimulation on paretic lower limb motor excitability during walking. J Clin Neurophysiol 26:272–279PubMedCrossRef Jayaram G, Stinear JW (2009) The effects of transcranial stimulation on paretic lower limb motor excitability during walking. J Clin Neurophysiol 26:272–279PubMedCrossRef
29.
go back to reference Leon D, Cortes M, Elder J, Kumru H, Laxe S, Edwards DJ, Tormos JM, Bernabeu M, Pascual-leone A (2017) tDCS does not enhance the effects of robot-assisted gait training in patients with subacute stroke. Restor Neurol Neurosci 35(4):377–384PubMed Leon D, Cortes M, Elder J, Kumru H, Laxe S, Edwards DJ, Tormos JM, Bernabeu M, Pascual-leone A (2017) tDCS does not enhance the effects of robot-assisted gait training in patients with subacute stroke. Restor Neurol Neurosci 35(4):377–384PubMed
30.
go back to reference Seo HG, Lee WH, Lee SH, Yi Y, Kim KD, Oh BM (2017) Robotic-assisted gait training combined with transcranial direct current stimulation in chronic stroke patients, a pilot double-blind, randomized controlled trial. Restor Neurol Neurosci 35(5):527–536PubMed Seo HG, Lee WH, Lee SH, Yi Y, Kim KD, Oh BM (2017) Robotic-assisted gait training combined with transcranial direct current stimulation in chronic stroke patients, a pilot double-blind, randomized controlled trial. Restor Neurol Neurosci 35(5):527–536PubMed
31.
go back to reference Powell ES, Carrico C, Westgate PM, Chelette KC, Nichols L, Reddy L, Salyers E, Ward A, Sawaki L (2016) Time configuration of combined neuromodulation and motor training after stroke, a proof-of-concept study. NeuroRehabilitation 39(3):439–449PubMedCrossRef Powell ES, Carrico C, Westgate PM, Chelette KC, Nichols L, Reddy L, Salyers E, Ward A, Sawaki L (2016) Time configuration of combined neuromodulation and motor training after stroke, a proof-of-concept study. NeuroRehabilitation 39(3):439–449PubMedCrossRef
32.
go back to reference Edwards DJ, Krebs HI, Rykman A, Zipse J, Thickbroom GW, Mastaglia FL, Pascual-Leone A, Volpe BT (2009) Raised corticomotor excitability of M1 forearm area following anodal tDCS is sustained during robotic wrist therapy in chronic stroke. Restor Neurol Neurosci 27:199–207PubMedPubMedCentral Edwards DJ, Krebs HI, Rykman A, Zipse J, Thickbroom GW, Mastaglia FL, Pascual-Leone A, Volpe BT (2009) Raised corticomotor excitability of M1 forearm area following anodal tDCS is sustained during robotic wrist therapy in chronic stroke. Restor Neurol Neurosci 27:199–207PubMedPubMedCentral
33.
go back to reference Lee SY, Cheon HJ, Yoon KJ, Chang WH, Kim YH (2013) Effects of dual transcranial direct current stimulation for aphasia in chronic stroke patients. Ann Rehabil Med 37(5):603–610PubMedPubMedCentralCrossRef Lee SY, Cheon HJ, Yoon KJ, Chang WH, Kim YH (2013) Effects of dual transcranial direct current stimulation for aphasia in chronic stroke patients. Ann Rehabil Med 37(5):603–610PubMedPubMedCentralCrossRef
34.
go back to reference Vines BW, Cerruti C, Schlaug G (2008) Dual-hemisphere tDCS facilitates greater improvements for healthy subjects’ non-dominant hand compared to uni-hemisphere stimulation. BMC Neurosci 9:103PubMedPubMedCentralCrossRef Vines BW, Cerruti C, Schlaug G (2008) Dual-hemisphere tDCS facilitates greater improvements for healthy subjects’ non-dominant hand compared to uni-hemisphere stimulation. BMC Neurosci 9:103PubMedPubMedCentralCrossRef
35.
go back to reference Giglia G, Mattaliano P, Puma A, Rizzo S, Fierro B, Brighina F (2011) Neglect-like effects induced by tDCS modulation of posterior parietal cortices in healthy subjects. Brain Stimul 4:294–299PubMedCrossRef Giglia G, Mattaliano P, Puma A, Rizzo S, Fierro B, Brighina F (2011) Neglect-like effects induced by tDCS modulation of posterior parietal cortices in healthy subjects. Brain Stimul 4:294–299PubMedCrossRef
36.
go back to reference Talimkhani A, Abdollahi I, Mohseni-Bandpei MA, Ehsani F, Khalili S, Jaberzadeh S (2019) Differential effects of unihemispheric concurrent dual-site and conventional tDCS on motor learning, a randomized, sham-controlled study. Basic Clin Neurosci 10(1):59–72PubMedPubMedCentral Talimkhani A, Abdollahi I, Mohseni-Bandpei MA, Ehsani F, Khalili S, Jaberzadeh S (2019) Differential effects of unihemispheric concurrent dual-site and conventional tDCS on motor learning, a randomized, sham-controlled study. Basic Clin Neurosci 10(1):59–72PubMedPubMedCentral
37.
go back to reference Vaseghi B, Zoghi M, Jaberzadeh S (2016) Unihemispheric concurrent dual-site cathodal transcranial direct current stimulation, the effects on corticospinal excitability. Eur J Neurosci 43(9):1161–1172PubMedCrossRef Vaseghi B, Zoghi M, Jaberzadeh S (2016) Unihemispheric concurrent dual-site cathodal transcranial direct current stimulation, the effects on corticospinal excitability. Eur J Neurosci 43(9):1161–1172PubMedCrossRef
38.
go back to reference Vaseghi B, Zoghi M, Jaberzadeh S (2015) The effects of anodal-tDCS on corticospinal excitability enhancement and its after-effects, conventional vs. unihemispheric concurrent dual-site stimulation. Front Hum Neurosci 9:533PubMedPubMedCentralCrossRef Vaseghi B, Zoghi M, Jaberzadeh S (2015) The effects of anodal-tDCS on corticospinal excitability enhancement and its after-effects, conventional vs. unihemispheric concurrent dual-site stimulation. Front Hum Neurosci 9:533PubMedPubMedCentralCrossRef
39.
go back to reference Achacheluee ST, Rahnama L, Karimi N, Abdollahi I, Arslan SA, Jaberzadeh S (2018) The effect of unihemispheric concurrent dual-site transcranial direct current stimulation of primary motor and dorsolateral prefrontal cortices on motor function in patients with sub-acute stroke. Front Hum Neurosci 12:441PubMedPubMedCentralCrossRef Achacheluee ST, Rahnama L, Karimi N, Abdollahi I, Arslan SA, Jaberzadeh S (2018) The effect of unihemispheric concurrent dual-site transcranial direct current stimulation of primary motor and dorsolateral prefrontal cortices on motor function in patients with sub-acute stroke. Front Hum Neurosci 12:441PubMedPubMedCentralCrossRef
40.
go back to reference Sunwoo H, Kim YH, Chang WH, Noh S, Kim EJ, Ko MH (2013) Effects of dual transcranial direct current stimulation on post-stroke unilateral visuospatial neglect. Neurosci Lett 554:94–98PubMedCrossRef Sunwoo H, Kim YH, Chang WH, Noh S, Kim EJ, Ko MH (2013) Effects of dual transcranial direct current stimulation on post-stroke unilateral visuospatial neglect. Neurosci Lett 554:94–98PubMedCrossRef
41.
go back to reference Kwon YH, Jang SH (2012) Onsite-effects of dual-hemisphere versus conventional single-hemisphere transcranial direct current stimulation, a functional MRI study. Neural Regen Res 7:1889–1894PubMedPubMedCentral Kwon YH, Jang SH (2012) Onsite-effects of dual-hemisphere versus conventional single-hemisphere transcranial direct current stimulation, a functional MRI study. Neural Regen Res 7:1889–1894PubMedPubMedCentral
42.
go back to reference Vandermeeren Y, Laloux P, Jamart J, Peeters A, Thonnard JL, Lefebvre S (2012) Dual hemisphere tDCS in chronic stroke patients improves ‘simple’ precision grip and digital dexterity of the paretic hand with a delayed time-course. Cerebrovasc Dis 33:63 Vandermeeren Y, Laloux P, Jamart J, Peeters A, Thonnard JL, Lefebvre S (2012) Dual hemisphere tDCS in chronic stroke patients improves ‘simple’ precision grip and digital dexterity of the paretic hand with a delayed time-course. Cerebrovasc Dis 33:63
43.
go back to reference Lefebvre S, Thonnard JL, Laloux P, Peeters A, Jamart J, Vandermeeren Y (2014) Single session of dual-tDCS transiently improves precision grip and dexterity of the paretic hand after stroke. Neurorehabil Neural Repair 28:100–110PubMedCrossRef Lefebvre S, Thonnard JL, Laloux P, Peeters A, Jamart J, Vandermeeren Y (2014) Single session of dual-tDCS transiently improves precision grip and dexterity of the paretic hand after stroke. Neurorehabil Neural Repair 28:100–110PubMedCrossRef
44.
go back to reference Lefebvre S, Laloux P, Peeters A, Desfontaines P, Jamart J, Vandermeeren Y (2013) Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front Hum Neurosci 6:343PubMedPubMedCentralCrossRef Lefebvre S, Laloux P, Peeters A, Desfontaines P, Jamart J, Vandermeeren Y (2013) Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front Hum Neurosci 6:343PubMedPubMedCentralCrossRef
45.
go back to reference Lefaucheur J-P, Aleman A, Baeken C, Benninger DH, Brunelin J, Di Lazzaro V et al (2020) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS), an update (2014–2018). Clin Neurophysiol 131:474–528PubMedCrossRef Lefaucheur J-P, Aleman A, Baeken C, Benninger DH, Brunelin J, Di Lazzaro V et al (2020) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS), an update (2014–2018). Clin Neurophysiol 131:474–528PubMedCrossRef
46.
go back to reference Polanía R, Nitsche M, Ruff C (2018) Studying and modifying brain function with non-invasive brain stimulation. Nat Neurosci 21:10CrossRef Polanía R, Nitsche M, Ruff C (2018) Studying and modifying brain function with non-invasive brain stimulation. Nat Neurosci 21:10CrossRef
47.
go back to reference Pallmann P, Bedding AW, Choodari-Oskooei B, Dimairo M, Flight L, Hampson LV, Holmes J, Mander AP, Odondi L’, Sydes MR, Villar SS, Wason JMS, Weir CJ, Wheeler GM, Yap C, Jaki T (2018) Adaptive designs in clinical trials, why use them, and how to run and report them. BMC Med 16:29PubMedPubMedCentralCrossRef Pallmann P, Bedding AW, Choodari-Oskooei B, Dimairo M, Flight L, Hampson LV, Holmes J, Mander AP, Odondi L’, Sydes MR, Villar SS, Wason JMS, Weir CJ, Wheeler GM, Yap C, Jaki T (2018) Adaptive designs in clinical trials, why use them, and how to run and report them. BMC Med 16:29PubMedPubMedCentralCrossRef
48.
go back to reference Andrade SM, Ferreira JJA, Rufino TS et al (2017) Effects of different montages of transcranial direct current stimulation on the risk of falls and lower limb function after stroke. Neurol Res 39(12):1037–1043PubMedCrossRef Andrade SM, Ferreira JJA, Rufino TS et al (2017) Effects of different montages of transcranial direct current stimulation on the risk of falls and lower limb function after stroke. Neurol Res 39(12):1037–1043PubMedCrossRef
49.
go back to reference Mahmoudi H, Haghighi AB, Petramfar P, Jahanshahi S, Salehi Z, Fregni F (2011) Transcranial direct current stimulation, electrode montage in stroke. Disabil Rehabil 33(15–16):1383–1388PubMedCrossRef Mahmoudi H, Haghighi AB, Petramfar P, Jahanshahi S, Salehi Z, Fregni F (2011) Transcranial direct current stimulation, electrode montage in stroke. Disabil Rehabil 33(15–16):1383–1388PubMedCrossRef
50.
go back to reference Del Felice A, Daloli V, Masiero S, Manganotti P (2017) Contralesional cathodal versus dual transcranial direct current stimulation for decreasing upper limb spasticity in chronic stroke individuals, a clinical and neurophysiological study. J Stroke Cerebrovasc Dis 26:2693CrossRef Del Felice A, Daloli V, Masiero S, Manganotti P (2017) Contralesional cathodal versus dual transcranial direct current stimulation for decreasing upper limb spasticity in chronic stroke individuals, a clinical and neurophysiological study. J Stroke Cerebrovasc Dis 26:2693CrossRef
51.
go back to reference Saeys WW, Vereeck L, Lafosse C, Truijen S, Wuyts FL, Van De Heyning P (2015) Transcranial direct current stimulation in the recovery of postural control after stroke, a pilot study. Disabil Rehabil 37(20):1857–1863PubMedCrossRef Saeys WW, Vereeck L, Lafosse C, Truijen S, Wuyts FL, Van De Heyning P (2015) Transcranial direct current stimulation in the recovery of postural control after stroke, a pilot study. Disabil Rehabil 37(20):1857–1863PubMedCrossRef
52.
go back to reference Tahtis V, Kaski D, Seemungal BM (2014) The effect of single session bi-cephalic transcranial direct current stimulation on gait performance in sub-acute stroke, a pilot study. Restor Neurol Neurosci 32(4):527–532PubMed Tahtis V, Kaski D, Seemungal BM (2014) The effect of single session bi-cephalic transcranial direct current stimulation on gait performance in sub-acute stroke, a pilot study. Restor Neurol Neurosci 32(4):527–532PubMed
53.
go back to reference Klomjai W, Aneksan B, Pheungphratanatrai A et al (2018) Effect of single-session dual-tDCS before physical therapy on lower-limb performance in sub-acute stroke patients, a randomized sham-controlled crossover study. Ann Phys Rehabil Med 61(5):286–291PubMedCrossRef Klomjai W, Aneksan B, Pheungphratanatrai A et al (2018) Effect of single-session dual-tDCS before physical therapy on lower-limb performance in sub-acute stroke patients, a randomized sham-controlled crossover study. Ann Phys Rehabil Med 61(5):286–291PubMedCrossRef
54.
go back to reference Feng WWW, Bowden MG, Kautz S (2013) Review of transcranial direct current stimulation in poststroke recovery. Top Stroke Rehabil 20(1):68–77PubMedCrossRef Feng WWW, Bowden MG, Kautz S (2013) Review of transcranial direct current stimulation in poststroke recovery. Top Stroke Rehabil 20(1):68–77PubMedCrossRef
55.
go back to reference Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G (2010) Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology. 75:2176–2184PubMedPubMedCentralCrossRef Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G (2010) Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology. 75:2176–2184PubMedPubMedCentralCrossRef
57.
go back to reference Ahmed GM, El Gohary A, Al-Azab IMA, Marzouk S, Mohamed YMY (2017) Effect of transcranial direct current stimulation on gait of stroke patients. JMSCR 5:15466–15472CrossRef Ahmed GM, El Gohary A, Al-Azab IMA, Marzouk S, Mohamed YMY (2017) Effect of transcranial direct current stimulation on gait of stroke patients. JMSCR 5:15466–15472CrossRef
58.
go back to reference Edwards DJ (2009) On the understanding and development of modern physical neurorehabilitation methods, robotics and non-invasive brain stimulation. J Neuroeng Rehabil. 6:3PubMedPubMedCentralCrossRef Edwards DJ (2009) On the understanding and development of modern physical neurorehabilitation methods, robotics and non-invasive brain stimulation. J Neuroeng Rehabil. 6:3PubMedPubMedCentralCrossRef
59.
go back to reference Solomons CD, Shanmugasundaram V (2019) A review of transcranial electrical stimulation methods in stroke rehabilitation. Neurol India 67(2):417–423PubMedCrossRef Solomons CD, Shanmugasundaram V (2019) A review of transcranial electrical stimulation methods in stroke rehabilitation. Neurol India 67(2):417–423PubMedCrossRef
60.
go back to reference Stagg CJ, Antal A, Nitsche MA (2018) Physiology of transcranial direct current stimulation. J ECT 34(3):144–152PubMedCrossRef Stagg CJ, Antal A, Nitsche MA (2018) Physiology of transcranial direct current stimulation. J ECT 34(3):144–152PubMedCrossRef
61.
go back to reference Fricke K, Seeber AA, Thirugnanasambandam N, Paulus W, Nitsche MA, Rothwell JC (2011) Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J Neurophysiol 105:1141–1149PubMedCrossRef Fricke K, Seeber AA, Thirugnanasambandam N, Paulus W, Nitsche MA, Rothwell JC (2011) Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J Neurophysiol 105:1141–1149PubMedCrossRef
62.
go back to reference Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation, evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385PubMedPubMedCentralCrossRef Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation, evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385PubMedPubMedCentralCrossRef
63.
go back to reference Nitsche MA, Roth A, Kuo MF, Fischer AK, Liebetanz D, Lang N, Tergau F, Paulus W (2007) Timingdependent modulation of associative plasticity by general network excitability in the human motor cortex. J Neurosci 27:3807–3812PubMedPubMedCentralCrossRef Nitsche MA, Roth A, Kuo MF, Fischer AK, Liebetanz D, Lang N, Tergau F, Paulus W (2007) Timingdependent modulation of associative plasticity by general network excitability in the human motor cortex. J Neurosci 27:3807–3812PubMedPubMedCentralCrossRef
64.
go back to reference Fusco A, Iosa M, Venturiero V, de Angelis D, Morone G, Maglione L, Bragoni M, Coiro P, Pratesi L, Paolucci S (2014) After vs. priming effects of anodal transcranial direct current stimulation on upper extremity motor recovery in patients with subacute stroke. Restor Neurol Neurosci 32:301–312PubMed Fusco A, Iosa M, Venturiero V, de Angelis D, Morone G, Maglione L, Bragoni M, Coiro P, Pratesi L, Paolucci S (2014) After vs. priming effects of anodal transcranial direct current stimulation on upper extremity motor recovery in patients with subacute stroke. Restor Neurol Neurosci 32:301–312PubMed
65.
go back to reference Bohannon RW (1987) Gait performance of hemiparetic stroke patients, selected variables. Arch Phys Med Rehabil 68:777–781PubMed Bohannon RW (1987) Gait performance of hemiparetic stroke patients, selected variables. Arch Phys Med Rehabil 68:777–781PubMed
66.
go back to reference Duncan PWBM (1987) Therapeutic strategies for rehabilitation of motor deficits. Stroke rehabilitation, the recovery of motor function. Chicago, Year Book Medical Publishers Inc;. p. 161–97 Duncan PWBM (1987) Therapeutic strategies for rehabilitation of motor deficits. Stroke rehabilitation, the recovery of motor function. Chicago, Year Book Medical Publishers Inc;. p. 161–97
67.
go back to reference Geiger M, Supiot A, Zory R, Aegerter P, Pradon D, Roche N (2017) The effect of transcranial direct current stimulation (tDCS) on locomotion and balance in patients with chronic stroke, study protocol for a randomised controlled trial. Trials 18:492PubMedPubMedCentralCrossRef Geiger M, Supiot A, Zory R, Aegerter P, Pradon D, Roche N (2017) The effect of transcranial direct current stimulation (tDCS) on locomotion and balance in patients with chronic stroke, study protocol for a randomised controlled trial. Trials 18:492PubMedPubMedCentralCrossRef
68.
go back to reference Roche N, Lackmy A, Achache V, Bussel B, Katz R (2011) Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects. J Physiol 589:2813–2826PubMedPubMedCentralCrossRef Roche N, Lackmy A, Achache V, Bussel B, Katz R (2011) Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects. J Physiol 589:2813–2826PubMedPubMedCentralCrossRef
69.
go back to reference Roche N, Lackmy A, Achache V, Bussel B, Katz R (2012) Effects of anodal tDCS on lumbar propriospinal system in healthy subjects. Clin Neurophysiol 123:1027–1034PubMedCrossRef Roche N, Lackmy A, Achache V, Bussel B, Katz R (2012) Effects of anodal tDCS on lumbar propriospinal system in healthy subjects. Clin Neurophysiol 123:1027–1034PubMedCrossRef
70.
go back to reference Mellow ML, Goldsworthy MR, Coussens S, Smith AE (2019) Acute aerobic exercise and neuroplasticity of the motor cortex, a systematic review. J Sci Med Sport S1440-2440(19):30799–30796 Mellow ML, Goldsworthy MR, Coussens S, Smith AE (2019) Acute aerobic exercise and neuroplasticity of the motor cortex, a systematic review. J Sci Med Sport S1440-2440(19):30799–30796
71.
go back to reference Bernhardt J, Hayward KS, Dancause N, Lannin NA, Ward NS, Nudo RJ, Farrin A, Churilov L, Boyd LA, Jones TA, Carmichael ST, Corbett D, Cramer SC (2019) A stroke recovery trial development framework, consensus-based core recommendations from the second stroke recovery and rehabilitation roundtable. Neurorehabil NeuralW Repair 33:959–969CrossRef Bernhardt J, Hayward KS, Dancause N, Lannin NA, Ward NS, Nudo RJ, Farrin A, Churilov L, Boyd LA, Jones TA, Carmichael ST, Corbett D, Cramer SC (2019) A stroke recovery trial development framework, consensus-based core recommendations from the second stroke recovery and rehabilitation roundtable. Neurorehabil NeuralW Repair 33:959–969CrossRef
Metadata
Title
Breaking the ice to improve motor outcomes in patients with chronic stroke: a retrospective clinical study on neuromodulation plus robotics
Authors
Antonino Naro
Luana Billeri
Alfredo Manuli
Tina Balletta
Antonino Cannavò
Simona Portaro
Paola Lauria
Fabrizio Ciappina
Rocco Salvatore Calabrò
Publication date
01-07-2021
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 7/2021
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-020-04875-8

Other articles of this Issue 7/2021

Neurological Sciences 7/2021 Go to the issue