Bimanual motor skill learning with robotics in chronic stroke: comparison between minimally impaired and moderately impaired patients, and healthy individuals

Eloïse Gerardin; Damien Bontemps; Nicolas Thomas Babuin; Benoît Herman; Adrien Denis; Benoît Bihin; Maxime Regnier; Maria Leeuwerck; Thierry Deltombe; Audrey Riga; Yves Vandermeeren

doi:10.1186/s12984-022-01009-3

Bimanual motor skill learning with robotics in chronic stroke: comparison between minimally impaired and moderately impaired patients, and healthy individuals

Eloïse Gerardin, Damien Bontemps, Nicolas Thomas Babuin, Benoît Herman, Adrien Denis, Benoît Bihin, Maxime Regnier, Maria Leeuwerck, Thierry Deltombe, Audrey Riga, Yves Vandermeeren

Research output: Contribution to journal › Article › peer-review

Abstract

Background: Most activities of daily life (ADL) require cooperative bimanual movements. A unilateral stroke may severely impair bimanual ADL. How patients with stroke (re)learn to coordinate their upper limbs (ULs) is largely unknown. The objectives are to determine whether patients with chronic supratentorial stroke could achieve bimanual motor skill learning (bim-MSkL) and to compare bim-MSkL between patients and healthy individuals (HIs). Methods: Twenty-four patients and ten HIs trained over 3 consecutive days on an asymmetrical bimanual coordination task (CIRCUIT) implemented as a serious game in the REAplan® robot. With a common cursor controlled by coordinated movements of the ULs through robotic handles, they performed as many laps as possible (speed constraint) on the CIRCUIT while keeping the cursor within the track (accuracy constraint). The primary outcome was a bimanual speed/accuracy trade-off (biSAT), we used a bimanual coordination factor (biCO) and bimanual forces (biFOP) for the secondary outcomes. Several clinical scales were used to evaluate motor and cognitive functions. Results: Overall, the patients showed improvements on biSAT and biCO. Based on biSAT progression, the HI achieved a larger bim-MSkL than the patients with mild to moderate impairment (Fugl-Meyer Assessment Upper Extremity (FMA-UE): 28–55, n = 15) but not significantly different from those with minimal motor impairment (FMA-UE: 66, n = 9). There was a significant positive correlation between biSAT evolution and the FMA-UE and Stroke Impact Scale. Conclusions: Both HI and patients with chronic stroke training on a robotic device achieved bim-MSkL, although the more impaired patients were less efficient. Bim-MSkL with REAplan® may be interesting for neurorehabilitation after stroke. Trial registration: ClinicalTrial.gov identifier: NCT03974750. Registered 05 June 2019. https://clinicaltrials.gov/ct2/show/NCT03974750?cond=NCT03974750&draw=2&rank=1

Original language	English
Article number	28
Journal	Journal of NeuroEngineering and Rehabilitation
Volume	19
Issue number	1
DOIs	https://doi.org/10.1186/s12984-022-01009-3
Publication status	Published - Dec 2022
Externally published	Yes

Funding

The work of YV is supported by the following grants: Fonds de la Recherche Scientifique \u2013 FNRS 1.R.506.16, 1.R.506.18 & 1.R.506.20F, Fonds Sp\u00E9cial de Recherche (FSR) from the UCLouvain, and Fondation Mont-Godinne. The work of AR is supported by grants from the Fondation Mont-Godinne 2015\u20132016, Fonds Sp\u00E9cial de Recherche (FSR) of the UCLouvain 2016\u20132018-2019, and Fondation Roi Baudouin/Fonds Am\u00E9lie 2018\u20132019. The work of EG is supported by a PDR-FNRS grant T.0239.19. We are grateful to the patients with stroke and healthy individuals who participated in the study. We thank the Fondation Baron Albert Fr\u00E8re and the Fondation Louvain, which made it possible to implement and develop the bimanual version of the neurorehabilitation robot REAplan\u00AE (AXINESIS, Wavre, Belgium) in the Stroke Unit of the CHU UCL Namur (site Godinne). We thank Julien Sapin (AXINESIS) for providing help and support with the REAplan\u00AE and Adrien Denis (UCLouvain, Louvain Bionics) for assisting with software development on the CIRCUIT and REACHING serious game and the implementation of these programs in the REAplan\u00AE environment. All procedures performed in this study were approved by the local Ethics Committee of CHU UCL Namur Godinne (approval number of the ethics committee: B039201421432).

Funders	Funder number
Fonds Spéciaux de Recherche
Fondation Roi Baudouin/Fonds
Fondation Baron Albert Frère
Fondation Louvain
Fondation Mont-Godinne
CIRCUIT
Chung Hua University
Fonds De La Recherche Scientifique - FNRS
PDR-FNRS	T.0239.19
CHU UCL	B039201421432
UK Research and Innovation	104544

Keywords

Bimanual
Bimanual coordination
Motor learning
Neurorehabilitation
Robotics
Stroke

Access to Document

10.1186/s12984-022-01009-3

Cite this

Gerardin, E., Bontemps, D., Babuin, N. T., Herman, B., Denis, A., Bihin, B., Regnier, M., Leeuwerck, M., Deltombe, T., Riga, A., & Vandermeeren, Y. (2022). Bimanual motor skill learning with robotics in chronic stroke: comparison between minimally impaired and moderately impaired patients, and healthy individuals. Journal of NeuroEngineering and Rehabilitation, 19(1), Article 28. https://doi.org/10.1186/s12984-022-01009-3

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abstract = "Background: Most activities of daily life (ADL) require cooperative bimanual movements. A unilateral stroke may severely impair bimanual ADL. How patients with stroke (re)learn to coordinate their upper limbs (ULs) is largely unknown. The objectives are to determine whether patients with chronic supratentorial stroke could achieve bimanual motor skill learning (bim-MSkL) and to compare bim-MSkL between patients and healthy individuals (HIs). Methods: Twenty-four patients and ten HIs trained over 3 consecutive days on an asymmetrical bimanual coordination task (CIRCUIT) implemented as a serious game in the REAplan{\textregistered} robot. With a common cursor controlled by coordinated movements of the ULs through robotic handles, they performed as many laps as possible (speed constraint) on the CIRCUIT while keeping the cursor within the track (accuracy constraint). The primary outcome was a bimanual speed/accuracy trade-off (biSAT), we used a bimanual coordination factor (biCO) and bimanual forces (biFOP) for the secondary outcomes. Several clinical scales were used to evaluate motor and cognitive functions. Results: Overall, the patients showed improvements on biSAT and biCO. Based on biSAT progression, the HI achieved a larger bim-MSkL than the patients with mild to moderate impairment (Fugl-Meyer Assessment Upper Extremity (FMA-UE): 28–55, n = 15) but not significantly different from those with minimal motor impairment (FMA-UE: 66, n = 9). There was a significant positive correlation between biSAT evolution and the FMA-UE and Stroke Impact Scale. Conclusions: Both HI and patients with chronic stroke training on a robotic device achieved bim-MSkL, although the more impaired patients were less efficient. Bim-MSkL with REAplan{\textregistered} may be interesting for neurorehabilitation after stroke. Trial registration: ClinicalTrial.gov identifier: NCT03974750. Registered 05 June 2019. https://clinicaltrials.gov/ct2/show/NCT03974750?cond=NCT03974750&draw=2&rank=1",

keywords = "Bimanual, Bimanual coordination, Motor learning, Neurorehabilitation, Robotics, Stroke",

author = "Elo{\"i}se Gerardin and Damien Bontemps and Babuin, {Nicolas Thomas} and Beno{\^i}t Herman and Adrien Denis and Beno{\^i}t Bihin and Maxime Regnier and Maria Leeuwerck and Thierry Deltombe and Audrey Riga and Yves Vandermeeren",

note = "Funding Information: We are grateful to the patients with stroke and healthy individuals who participated in the study. We thank the Fondation Baron Albert Fr{\`e}re and the Fondation Louvain, which made it possible to implement and develop the bimanual version of the neurorehabilitation robot REAplan{\textregistered} (AXINESIS, Wavre, Belgium) in the Stroke Unit of the CHU UCL Namur (site Godinne). We thank Julien Sapin (AXINESIS) for providing help and support with the REAplan{\textregistered} and Adrien Denis (UCLouvain, Louvain Bionics) for assisting with software development on the CIRCUIT and REACHING serious game and the implementation of these programs in the REAplan{\textregistered} environment. All procedures performed in this study were approved by the local Ethics Committee of CHU UCL Namur Godinne (approval number of the ethics committee: B039201421432). Funding Information: The work of YV is supported by the following grants: Fonds de la Recherche Scientifique – FNRS 1.R.506.16, 1.R.506.18 & 1.R.506.20F, Fonds Sp{\'e}cial de Recherche (FSR) from the UCLouvain, and Fondation Mont-Godinne. The work of AR is supported by grants from the Fondation Mont-Godinne 2015–2016, Fonds Sp{\'e}cial de Recherche (FSR) of the UCLouvain 2016–2018-2019, and Fondation Roi Baudouin/Fonds Am{\'e}lie 2018–2019. The work of EG is supported by a PDR-FNRS grant T.0239.19. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s12984-022-01009-3",

language = "English",

volume = "19",

journal = "Journal of NeuroEngineering and Rehabilitation",

issn = "1743-0003",

publisher = "BioMed Central Ltd",

number = "1",

}

Gerardin, E, Bontemps, D, Babuin, NT, Herman, B, Denis, A, Bihin, B , Regnier, M, Leeuwerck, M, Deltombe, T, Riga, A & Vandermeeren, Y 2022, 'Bimanual motor skill learning with robotics in chronic stroke: comparison between minimally impaired and moderately impaired patients, and healthy individuals', Journal of NeuroEngineering and Rehabilitation, vol. 19, no. 1, 28. https://doi.org/10.1186/s12984-022-01009-3

Bimanual motor skill learning with robotics in chronic stroke: comparison between minimally impaired and moderately impaired patients, and healthy individuals. / Gerardin, Eloïse; Bontemps, Damien; Babuin, Nicolas Thomas et al.
In: Journal of NeuroEngineering and Rehabilitation, Vol. 19, No. 1, 28, 12.2022.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Bimanual motor skill learning with robotics in chronic stroke

T2 - comparison between minimally impaired and moderately impaired patients, and healthy individuals

AU - Gerardin, Eloïse

AU - Bontemps, Damien

AU - Babuin, Nicolas Thomas

AU - Herman, Benoît

AU - Denis, Adrien

AU - Bihin, Benoît

AU - Regnier, Maxime

AU - Leeuwerck, Maria

AU - Deltombe, Thierry

AU - Riga, Audrey

AU - Vandermeeren, Yves

N1 - Funding Information: We are grateful to the patients with stroke and healthy individuals who participated in the study. We thank the Fondation Baron Albert Frère and the Fondation Louvain, which made it possible to implement and develop the bimanual version of the neurorehabilitation robot REAplan® (AXINESIS, Wavre, Belgium) in the Stroke Unit of the CHU UCL Namur (site Godinne). We thank Julien Sapin (AXINESIS) for providing help and support with the REAplan® and Adrien Denis (UCLouvain, Louvain Bionics) for assisting with software development on the CIRCUIT and REACHING serious game and the implementation of these programs in the REAplan® environment. All procedures performed in this study were approved by the local Ethics Committee of CHU UCL Namur Godinne (approval number of the ethics committee: B039201421432). Funding Information: The work of YV is supported by the following grants: Fonds de la Recherche Scientifique – FNRS 1.R.506.16, 1.R.506.18 & 1.R.506.20F, Fonds Spécial de Recherche (FSR) from the UCLouvain, and Fondation Mont-Godinne. The work of AR is supported by grants from the Fondation Mont-Godinne 2015–2016, Fonds Spécial de Recherche (FSR) of the UCLouvain 2016–2018-2019, and Fondation Roi Baudouin/Fonds Amélie 2018–2019. The work of EG is supported by a PDR-FNRS grant T.0239.19. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Background: Most activities of daily life (ADL) require cooperative bimanual movements. A unilateral stroke may severely impair bimanual ADL. How patients with stroke (re)learn to coordinate their upper limbs (ULs) is largely unknown. The objectives are to determine whether patients with chronic supratentorial stroke could achieve bimanual motor skill learning (bim-MSkL) and to compare bim-MSkL between patients and healthy individuals (HIs). Methods: Twenty-four patients and ten HIs trained over 3 consecutive days on an asymmetrical bimanual coordination task (CIRCUIT) implemented as a serious game in the REAplan® robot. With a common cursor controlled by coordinated movements of the ULs through robotic handles, they performed as many laps as possible (speed constraint) on the CIRCUIT while keeping the cursor within the track (accuracy constraint). The primary outcome was a bimanual speed/accuracy trade-off (biSAT), we used a bimanual coordination factor (biCO) and bimanual forces (biFOP) for the secondary outcomes. Several clinical scales were used to evaluate motor and cognitive functions. Results: Overall, the patients showed improvements on biSAT and biCO. Based on biSAT progression, the HI achieved a larger bim-MSkL than the patients with mild to moderate impairment (Fugl-Meyer Assessment Upper Extremity (FMA-UE): 28–55, n = 15) but not significantly different from those with minimal motor impairment (FMA-UE: 66, n = 9). There was a significant positive correlation between biSAT evolution and the FMA-UE and Stroke Impact Scale. Conclusions: Both HI and patients with chronic stroke training on a robotic device achieved bim-MSkL, although the more impaired patients were less efficient. Bim-MSkL with REAplan® may be interesting for neurorehabilitation after stroke. Trial registration: ClinicalTrial.gov identifier: NCT03974750. Registered 05 June 2019. https://clinicaltrials.gov/ct2/show/NCT03974750?cond=NCT03974750&draw=2&rank=1

AB - Background: Most activities of daily life (ADL) require cooperative bimanual movements. A unilateral stroke may severely impair bimanual ADL. How patients with stroke (re)learn to coordinate their upper limbs (ULs) is largely unknown. The objectives are to determine whether patients with chronic supratentorial stroke could achieve bimanual motor skill learning (bim-MSkL) and to compare bim-MSkL between patients and healthy individuals (HIs). Methods: Twenty-four patients and ten HIs trained over 3 consecutive days on an asymmetrical bimanual coordination task (CIRCUIT) implemented as a serious game in the REAplan® robot. With a common cursor controlled by coordinated movements of the ULs through robotic handles, they performed as many laps as possible (speed constraint) on the CIRCUIT while keeping the cursor within the track (accuracy constraint). The primary outcome was a bimanual speed/accuracy trade-off (biSAT), we used a bimanual coordination factor (biCO) and bimanual forces (biFOP) for the secondary outcomes. Several clinical scales were used to evaluate motor and cognitive functions. Results: Overall, the patients showed improvements on biSAT and biCO. Based on biSAT progression, the HI achieved a larger bim-MSkL than the patients with mild to moderate impairment (Fugl-Meyer Assessment Upper Extremity (FMA-UE): 28–55, n = 15) but not significantly different from those with minimal motor impairment (FMA-UE: 66, n = 9). There was a significant positive correlation between biSAT evolution and the FMA-UE and Stroke Impact Scale. Conclusions: Both HI and patients with chronic stroke training on a robotic device achieved bim-MSkL, although the more impaired patients were less efficient. Bim-MSkL with REAplan® may be interesting for neurorehabilitation after stroke. Trial registration: ClinicalTrial.gov identifier: NCT03974750. Registered 05 June 2019. https://clinicaltrials.gov/ct2/show/NCT03974750?cond=NCT03974750&draw=2&rank=1

KW - Bimanual

KW - Bimanual coordination

KW - Motor learning

KW - Neurorehabilitation

KW - Robotics

KW - Stroke

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U2 - 10.1186/s12984-022-01009-3

DO - 10.1186/s12984-022-01009-3

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M1 - 28

ER -

Bimanual motor skill learning with robotics in chronic stroke: comparison between minimally impaired and moderately impaired patients, and healthy individuals

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