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Published in: Journal of NeuroEngineering and Rehabilitation 1/2019

Open Access 01-12-2019 | Stroke | Research

Boosting robot-assisted rehabilitation of stroke hemiparesis by individualized selection of upper limb movements – a pilot study

Authors: Orna Rosenthal, Alan M. Wing, Jeremy L. Wyatt, David Punt, Briony Brownless, Chit Ko-Ko, R. Christopher Miall

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

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Abstract

Background

Intensive robot-assisted training of the upper limb after stroke can reduce motor impairment, even at the chronic stage. However, the effectiveness of practice for recovery depends on the selection of the practised movements. We hypothesized that rehabilitation can be optimized by selecting the movements to be practiced based on the trainee’s performance profile.

Methods

We present a novel principle (‘steepest gradients’) for performance-based selection of movements. The principle is based on mapping motor performance across a workspace and then selecting movements located at regions of the steepest transition between better and worse performance.
To assess the benefit of this principle we compared the effect of 15 sessions of robot-assisted reaching training on upper-limb motor impairment, between two groups of people who have moderate-to-severe chronic upper-limb hemiparesis due to stroke. The test group (N = 7) received steepest gradients-based training, iteratively selected according to the steepest gradients principle with weekly remapping, whereas the control group (N = 9) received a standard “centre-out” reaching training. Training intensity was identical.

Results

Both groups showed improvement in Fugl-Meyer upper-extremity scores (the primary outcome measure). Moreover, the test group showed significantly greater improvement (twofold) compared to control. The score remained elevated, on average, for at least 4 weeks although the additional benefit of the steepest-gradients -based training diminished relative to control.

Conclusions

This study provides a proof of concept for the superior benefit of performance-based selection of practiced movements in reducing upper-limb motor impairment due to stroke. This added benefit was most evident in the short term, suggesting that performance-based steepest-gradients training may be effective in increasing the rate of initial phase of practice-based recovery; we discuss how long-term retention may also be improved.

Trial registration

ISRCTN, ISRCTN65226825, registered 12 June 2018 - Retrospectively registered,
Appendix
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Literature
1.
go back to reference Dobkin BH. Impairments, disabilities, and bases for neurological rehabilitation after stroke. J Stroke Cerebrovasc Dis. 1997;6(4):221–6.PubMedCrossRef Dobkin BH. Impairments, disabilities, and bases for neurological rehabilitation after stroke. J Stroke Cerebrovasc Dis. 1997;6(4):221–6.PubMedCrossRef
2.
go back to reference Lai SM, Studenski S, Duncan PW, Perera S. Persisting consequences of stroke measured by the stroke impact scale. Stroke. 2002;33(7):1840–4.PubMedCrossRef Lai SM, Studenski S, Duncan PW, Perera S. Persisting consequences of stroke measured by the stroke impact scale. Stroke. 2002;33(7):1840–4.PubMedCrossRef
3.
go back to reference Lawrence ES, Coshall C, Dundas R, Stewart J, Rudd AG, Howard R, et al. Estimates of the prevalence of acute stroke impairments and disability in a multiethnic population. Stroke. 2001;32(6):1279–84.PubMedCrossRef Lawrence ES, Coshall C, Dundas R, Stewart J, Rudd AG, Howard R, et al. Estimates of the prevalence of acute stroke impairments and disability in a multiethnic population. Stroke. 2001;32(6):1279–84.PubMedCrossRef
4.
go back to reference Van Peppen RP, Kwakkel G, Wood-Dauphinee S, Hendriks HJ, Van der Wees PJ, Dekker J. The impact of physical therapy on functional outcomes after stroke: what's the evidence? Clin Rehabil. 2004;18(8):833–62.PubMedCrossRef Van Peppen RP, Kwakkel G, Wood-Dauphinee S, Hendriks HJ, Van der Wees PJ, Dekker J. The impact of physical therapy on functional outcomes after stroke: what's the evidence? Clin Rehabil. 2004;18(8):833–62.PubMedCrossRef
5.
go back to reference Kwakkel G, Wagenaar RC, Twisk JW, Lankhorst GJ, Koetsier JC. Intensity of leg and arm training after primary middle-cerebral-artery stroke: a randomised trial. Lancet. 1999;354(9174):191–6.PubMedCrossRef Kwakkel G, Wagenaar RC, Twisk JW, Lankhorst GJ, Koetsier JC. Intensity of leg and arm training after primary middle-cerebral-artery stroke: a randomised trial. Lancet. 1999;354(9174):191–6.PubMedCrossRef
6.
go back to reference Langhorne P, Coupar F, Pollock A. Motor recovery after stroke: a systematic review. Lancet Neurol. 2009;8(8):741–54.PubMedCrossRef Langhorne P, Coupar F, Pollock A. Motor recovery after stroke: a systematic review. Lancet Neurol. 2009;8(8):741–54.PubMedCrossRef
7.
go back to reference Lo AC, Guarino PD, Richards LG, Haselkorn JK, Wittenberg GF, Federman DG, et al. Robot-assisted therapy for long-term upper-limb impairment after stroke2010 may 13. p. 1772–83. Lo AC, Guarino PD, Richards LG, Haselkorn JK, Wittenberg GF, Federman DG, et al. Robot-assisted therapy for long-term upper-limb impairment after stroke2010 may 13. p. 1772–83.
8.
go back to reference Hsieh YW, Wu CY, Liao WW, Lin KC, Wu KY, Lee CY. Effects of treatment intensity in upper limb robot-assisted therapy for chronic stroke: a pilot randomized controlled trial. Neurorehabil Neural Repair. 2011;25(6):503–11.PubMedCrossRef Hsieh YW, Wu CY, Liao WW, Lin KC, Wu KY, Lee CY. Effects of treatment intensity in upper limb robot-assisted therapy for chronic stroke: a pilot randomized controlled trial. Neurorehabil Neural Repair. 2011;25(6):503–11.PubMedCrossRef
9.
go back to reference Burgar CG, Lum PS, Scremin AM, Garber SL, Van der Loos HF, Kenney D, et al. Robot-assisted upper-limb therapy in acute rehabilitation setting following stroke: Department of Veterans Affairs multisite clinical trial. J Rehabil Res Dev. 2011;48(4):445–58.PubMedCrossRef Burgar CG, Lum PS, Scremin AM, Garber SL, Van der Loos HF, Kenney D, et al. Robot-assisted upper-limb therapy in acute rehabilitation setting following stroke: Department of Veterans Affairs multisite clinical trial. J Rehabil Res Dev. 2011;48(4):445–58.PubMedCrossRef
10.
go back to reference Kwakkel G, Kollen BJ, Krebs HI. Effects of robot-assisted therapy on upper limb recovery after stroke: a systematic review. Neurorehabil Neural Repair. 2008;22(2):111–21.PubMedCrossRef Kwakkel G, Kollen BJ, Krebs HI. Effects of robot-assisted therapy on upper limb recovery after stroke: a systematic review. Neurorehabil Neural Repair. 2008;22(2):111–21.PubMedCrossRef
11.
go back to reference Prange GB, Jannink MJ, Groothuis-Oudshoorn CG, Hermens HJ, Ijzerman MJ. Systematic review of the effect of robot-aided therapy on recovery of the hemiparetic arm after stroke. J Rehabil Res Dev. 2006;43(2):171–84.PubMedCrossRef Prange GB, Jannink MJ, Groothuis-Oudshoorn CG, Hermens HJ, Ijzerman MJ. Systematic review of the effect of robot-aided therapy on recovery of the hemiparetic arm after stroke. J Rehabil Res Dev. 2006;43(2):171–84.PubMedCrossRef
12.
go back to reference Veerbeek JM, Langbroek-Amersfoort AC, van Wegen EE, Meskers CG, Kwakkel G. Effects of robot-assisted therapy for the upper limb after stroke. Neurorehabil Neural Repair. 2017;31(2):107–21.PubMedCrossRef Veerbeek JM, Langbroek-Amersfoort AC, van Wegen EE, Meskers CG, Kwakkel G. Effects of robot-assisted therapy for the upper limb after stroke. Neurorehabil Neural Repair. 2017;31(2):107–21.PubMedCrossRef
13.
14.
go back to reference Babaiasl M, Mahdioun SH, Jaryani P, Yazdani M. A review of technological and clinical aspects of robot-aided rehabilitation of upper-extremity after stroke. Disabil Rehabil Assist Technol. 2016;11(4):263–80.PubMed Babaiasl M, Mahdioun SH, Jaryani P, Yazdani M. A review of technological and clinical aspects of robot-aided rehabilitation of upper-extremity after stroke. Disabil Rehabil Assist Technol. 2016;11(4):263–80.PubMed
15.
go back to reference Henderson A, Korner-Bitensky N, Levin M. Virtual reality in stroke rehabilitation: a systematic review of its effectiveness for upper limb motor recovery. Top Stroke Rehabil. 2007;14(2):52–61.PubMedCrossRef Henderson A, Korner-Bitensky N, Levin M. Virtual reality in stroke rehabilitation: a systematic review of its effectiveness for upper limb motor recovery. Top Stroke Rehabil. 2007;14(2):52–61.PubMedCrossRef
16.
go back to reference Krebs HI, Palazzolo JJ, Dipietro L, Volpe BT, Hogan N. Rehabilitation robotics: performance-based progressive robot-assisted therapy. Auton Robot. 2003;15(1):7–20.CrossRef Krebs HI, Palazzolo JJ, Dipietro L, Volpe BT, Hogan N. Rehabilitation robotics: performance-based progressive robot-assisted therapy. Auton Robot. 2003;15(1):7–20.CrossRef
17.
go back to reference Grimm F, Naros G, Gharabaghi A. Closed-loop task difficulty adaptation during virtual reality reach-to-grasp training assisted with an exoskeleton for stroke rehabilitation. Front Neurosci. 2016;10:518.PubMedPubMedCentral Grimm F, Naros G, Gharabaghi A. Closed-loop task difficulty adaptation during virtual reality reach-to-grasp training assisted with an exoskeleton for stroke rehabilitation. Front Neurosci. 2016;10:518.PubMedPubMedCentral
18.
go back to reference Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci. 2011;12(12):739–51.PubMedCrossRef Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci. 2011;12(12):739–51.PubMedCrossRef
19.
go back to reference Guadagnoli MA, Lee TD. Challenge point: a framework for conceptualizing the effects of various practice conditions in motor learning. J Mot Behav. 2004;36(2):212–24.PubMedCrossRef Guadagnoli MA, Lee TD. Challenge point: a framework for conceptualizing the effects of various practice conditions in motor learning. J Mot Behav. 2004;36(2):212–24.PubMedCrossRef
20.
go back to reference Woodbury ML, Anderson K, Finetto C, Fortune A, Dellenbach B, Grattan E, et al. Matching task difficulty to patient ability during task practice improves upper extremity motor skill after stroke: A Proof-of-Concept Study. Arch Phys Med Rehab. 2016;97(11):1863–71.CrossRef Woodbury ML, Anderson K, Finetto C, Fortune A, Dellenbach B, Grattan E, et al. Matching task difficulty to patient ability during task practice improves upper extremity motor skill after stroke: A Proof-of-Concept Study. Arch Phys Med Rehab. 2016;97(11):1863–71.CrossRef
21.
go back to reference Wittmann F, Lambercy O, Gonzenbach RR, van Raai MA, Hover R, Held J, et al. Assessment-driven arm therapy at home using an IMU-based virtual reality system. Int C Rehab Robot. 2015:707–12. Wittmann F, Lambercy O, Gonzenbach RR, van Raai MA, Hover R, Held J, et al. Assessment-driven arm therapy at home using an IMU-based virtual reality system. Int C Rehab Robot. 2015:707–12.
22.
go back to reference Rosenthal O, Wing AM, Wyatt JL, Punt D, Miall RC. Mapping upper-limb motor performance after stroke - a novel method with utility for individualized motor training. J Neuroeng Rehabil. 2017;14(1):127.PubMedPubMedCentralCrossRef Rosenthal O, Wing AM, Wyatt JL, Punt D, Miall RC. Mapping upper-limb motor performance after stroke - a novel method with utility for individualized motor training. J Neuroeng Rehabil. 2017;14(1):127.PubMedPubMedCentralCrossRef
23.
go back to reference Ghez C, Scheidt R, Heijink H. Different learned coordinate frames for planning trajectories and final positions in reaching. J Neurophysiol. 2007;98(6):3614–26.PubMedCrossRef Ghez C, Scheidt R, Heijink H. Different learned coordinate frames for planning trajectories and final positions in reaching. J Neurophysiol. 2007;98(6):3614–26.PubMedCrossRef
25.
go back to reference Kettner RE, Schwartz AB, Georgopoulos AP. Primate motor cortex and free arm movements to visual targets in three-dimensional space. III. Positional gradients and population coding of movement direction from various movement origins. J Neurosci. 1988;8(8):2938–47.PubMedCrossRef Kettner RE, Schwartz AB, Georgopoulos AP. Primate motor cortex and free arm movements to visual targets in three-dimensional space. III. Positional gradients and population coding of movement direction from various movement origins. J Neurosci. 1988;8(8):2938–47.PubMedCrossRef
26.
go back to reference Nordin N, Xie SQ, Wunsche B. Assessment of movement quality in robot- assisted upper limb rehabilitation after stroke: a review. J Neuroeng Rehabil. 2014;11:137.PubMedPubMedCentralCrossRef Nordin N, Xie SQ, Wunsche B. Assessment of movement quality in robot- assisted upper limb rehabilitation after stroke: a review. J Neuroeng Rehabil. 2014;11:137.PubMedPubMedCentralCrossRef
27.
go back to reference Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med. 1975;7(1):13–31.PubMed Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med. 1975;7(1):13–31.PubMed
28.
go back to reference Rabadi MH, Galgano M, Lynch D, Akerman M, Lesser M, Volpe BT. A pilot study of activity-based therapy in the arm motor recovery post stroke: a randomized controlled trial. Clin Rehabil. 2008;22(12):1071–82.PubMedCrossRef Rabadi MH, Galgano M, Lynch D, Akerman M, Lesser M, Volpe BT. A pilot study of activity-based therapy in the arm motor recovery post stroke: a randomized controlled trial. Clin Rehabil. 2008;22(12):1071–82.PubMedCrossRef
29.
go back to reference Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206–7.PubMedCrossRef Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206–7.PubMedCrossRef
30.
go back to reference Carr JH, Shepherd RB, Nordholm L, Lynne D. Investigation of a new motor assessment scale for stroke patients. Phys Ther. 1985;65(2):175–80.PubMedCrossRef Carr JH, Shepherd RB, Nordholm L, Lynne D. Investigation of a new motor assessment scale for stroke patients. Phys Ther. 1985;65(2):175–80.PubMedCrossRef
31.
go back to reference Collin C, Wade DT, Davies S, Horne V. The Barthel ADL index: a reliability study. Int Disabil Stud. 1988;10(2):61–3.PubMedCrossRef Collin C, Wade DT, Davies S, Horne V. The Barthel ADL index: a reliability study. Int Disabil Stud. 1988;10(2):61–3.PubMedCrossRef
32.
go back to reference Howard IS, Ingram JN, Wolpert DM. A modular planar robotic manipulandum with end-point torque control. J Neurosci Methods. 2009;181(2):199–211.PubMedCrossRef Howard IS, Ingram JN, Wolpert DM. A modular planar robotic manipulandum with end-point torque control. J Neurosci Methods. 2009;181(2):199–211.PubMedCrossRef
33.
go back to reference Flash T, Hogan N. The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci. 1985;5(7):1688–703.PubMedCrossRef Flash T, Hogan N. The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci. 1985;5(7):1688–703.PubMedCrossRef
35.
go back to reference IBM Corp. IBM SPSS statistics for windows, Version 22.0. Armonk, NY: IBM Corp. ; Released 2013. IBM Corp. IBM SPSS statistics for windows, Version 22.0. Armonk, NY: IBM Corp. ; Released 2013.
36.
go back to reference Kwakkel G, Kollen BJ, van der Grond J, Prevo AJ. Probability of regaining dexterity in the flaccid upper limb: impact of severity of paresis and time since onset in acute stroke. Stroke. 2003;34(9):2181–6.PubMedCrossRef Kwakkel G, Kollen BJ, van der Grond J, Prevo AJ. Probability of regaining dexterity in the flaccid upper limb: impact of severity of paresis and time since onset in acute stroke. Stroke. 2003;34(9):2181–6.PubMedCrossRef
37.
go back to reference Coupar F, Pollock A, Rowe P, Weir C, Langhorne P. Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin Rehabil. 2012;26(4):291–313.PubMedCrossRef Coupar F, Pollock A, Rowe P, Weir C, Langhorne P. Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin Rehabil. 2012;26(4):291–313.PubMedCrossRef
38.
go back to reference Fasoli SE, Krebs HI, Stein J, Frontera WR, Hughes R, Hogan N. Robotic therapy for chronic motor impairments after stroke: follow-up results. Arch Phys Med Rehabil. 2004;85(7):1106–11.PubMedCrossRef Fasoli SE, Krebs HI, Stein J, Frontera WR, Hughes R, Hogan N. Robotic therapy for chronic motor impairments after stroke: follow-up results. Arch Phys Med Rehabil. 2004;85(7):1106–11.PubMedCrossRef
39.
go back to reference Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. P Natl Acad Sci USA. 2009;106(5):1590–5.CrossRef Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. P Natl Acad Sci USA. 2009;106(5):1590–5.CrossRef
40.
go back to reference Sanchez-Kuhn A, Perez-Fernandez C, Canovas R, Flores P, Sanchez-Santed F. Transcranial direct current stimulation as a motor neurorehabilitation tool: an empirical review. Biomed Eng Online. 2017;16(Suppl 1):76.PubMedPubMedCentralCrossRef Sanchez-Kuhn A, Perez-Fernandez C, Canovas R, Flores P, Sanchez-Santed F. Transcranial direct current stimulation as a motor neurorehabilitation tool: an empirical review. Biomed Eng Online. 2017;16(Suppl 1):76.PubMedPubMedCentralCrossRef
41.
go back to reference Leon D, Cortes M, Elder J, Kumru H, Laxe S, Edwards DJ, et al. tDCS does not enhance the effects of robot-assisted gait training in patients with subacute stroke. Restor Neurol Neurosci. 2017;35(4):377–84.PubMed Leon D, Cortes M, Elder J, Kumru H, Laxe S, Edwards DJ, et al. tDCS does not enhance the effects of robot-assisted gait training in patients with subacute stroke. Restor Neurol Neurosci. 2017;35(4):377–84.PubMed
42.
go back to reference Wagner JM, Rhodes JA, Patten C. Reproducibility and minimal detectable change of three-dimensional kinematic analysis of reaching tasks in people with hemiparesis after stroke. Phys Ther. 2008;88(5):652–63.PubMedCrossRef Wagner JM, Rhodes JA, Patten C. Reproducibility and minimal detectable change of three-dimensional kinematic analysis of reaching tasks in people with hemiparesis after stroke. Phys Ther. 2008;88(5):652–63.PubMedCrossRef
43.
go back to reference Park H, Schweighofer N. Nonlinear mixed-effects model reveals a distinction between learning and performance in intensive reach training post-stroke. J Neuroeng Rehabil. 2017;14(1):21.PubMedPubMedCentralCrossRef Park H, Schweighofer N. Nonlinear mixed-effects model reveals a distinction between learning and performance in intensive reach training post-stroke. J Neuroeng Rehabil. 2017;14(1):21.PubMedPubMedCentralCrossRef
44.
go back to reference Klamroth-Marganska V, Blanco J, Campen K, Curt A, Dietz V, Ettlin T, et al. Three-dimensional, task-specific robot therapy of the arm after stroke: a multicentre, parallel-group randomised trial. Lancet Neurol. 2014;13(2):159–66.PubMedCrossRef Klamroth-Marganska V, Blanco J, Campen K, Curt A, Dietz V, Ettlin T, et al. Three-dimensional, task-specific robot therapy of the arm after stroke: a multicentre, parallel-group randomised trial. Lancet Neurol. 2014;13(2):159–66.PubMedCrossRef
Metadata
Title
Boosting robot-assisted rehabilitation of stroke hemiparesis by individualized selection of upper limb movements – a pilot study
Authors
Orna Rosenthal
Alan M. Wing
Jeremy L. Wyatt
David Punt
Briony Brownless
Chit Ko-Ko
R. Christopher Miall
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Stroke
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2019
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-019-0513-0

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