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Original research| Volume 99, ISSUE 8, P1447-1453.e1, August 2018

Virtual Reality Rehabilitation With Functional Electrical Stimulation Improves Upper Extremity Function in Patients With Chronic Stroke: A Pilot Randomized Controlled Study

Published:March 02, 2018DOI:https://doi.org/10.1016/j.apmr.2018.01.030

      Abstract

      Objective

      To compare virtual reality (VR) combined with functional electrical stimulation (FES) with cyclic FES for improving upper extremity function and health-related quality of life in patients with chronic stroke.

      Design

      A pilot, randomized, single-blind, controlled trial.

      Setting

      Stroke rehabilitation inpatient unit.

      Participants

      Participants (N=48) with hemiplegia secondary to a unilateral stroke for >3 months and with a hemiplegic wrist extensor Medical Research Council scale score ranging from 1 to 3.

      Interventions

      FES was applied to the wrist extensors and finger extensors. A VR-based wearable rehabilitation device was used combined with FES and virtual activity–based training for the intervention group. The control group received cyclic FES only. Both groups completed 20 sessions over a 4-week period.

      Main Outcome Measures

      Primary outcome measures were changes in Fugl-Meyer Assessment–Upper Extremity and Wolf Motor Function Test scores. Secondary outcome measures were changes in Box and Block Test, Jebsen-Taylor Hand Function Test, and Stroke Impact Scale scores. Assessments were performed at baseline (t0) and at 2 weeks (t1), 4 weeks (t4), and 8 weeks (t8). Between-group comparisons were evaluated using a repeated-measures analysis of variance.

      Results

      Forty-one participants were included in the analysis. Compared with FES alone, VR-FES produced a substantial increase in Fugl-Meyer Assessment–distal score (P=.011) and marginal improvement in Jebsen-Taylor Hand Function Test–gross score (P=.057). VR-FES produced greater, although nonsignificant, improvements in all other outcome measures, except in the Stroke Impact Scale–activities of daily living/instrumental activities of daily living score.

      Conclusions

      FES with VR-based rehabilitation may be more effective than cyclic FES in improving distal upper extremity gross motor performance poststroke.

      Keywords

      List of abbreviations:

      ADL (activities of daily living), BB (Box and Block Test), FAS (Functional Ability Scale), FES (functional electrical stimulation), FMA (Fugl-Meyer Assessment), JTHFT (Jebsen-Taylor Hand Function Test), MRC (Medical Research Council), SIS (Stroke Impact Scale), VR (virtual reality), WMFT (Wolf Motor Function Test)
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      References

        • Meadmore K.L.
        • Exell T.A.
        • Hallewell E.
        • et al.
        The application of precisely controlled functional electrical stimulation to the shoulder, elbow and wrist for upper limb stroke rehabilitation: a feasibility study.
        J Neuroeng Rehabil. 2014; 11: 105
        • Kimberley T.J.
        • Lewis S.M.
        • Auerbach E.J.
        • Dorsey L.L.
        • Lojovich J.M.
        • Carey J.R.
        Electrical stimulation driving functional improvements and cortical changes in subjects with stroke.
        Exp Brain Res. 2004; 154: 450-460
        • Schuhfried O.
        • Crevenna R.
        • Fialka-Moser V.
        • Paternostro-Sluga T.
        Non-invasive neuromuscular electrical stimulation in patients with central nervous system lesions: an educational review.
        J Rehabil Med. 2012; 44: 99-105
        • Faghri P.D.
        The effects of neuromuscular stimulation-induced muscle contraction versus elevation on hand edema in CVA patients.
        J Hand Ther. 1997; 10: 29-34
        • Francisco G.
        • Chae J.
        • Chawla H.
        • et al.
        Electromyogram-triggered neuromuscular stimulation for improving the arm function of acute stroke survivors: a randomized pilot study.
        Arch Phys Med Rehabil. 1998; 79: 570-575
        • Thrasher T.A.
        • Zivanovic V.
        • McIlroy W.
        • Popovic M.R.
        Rehabilitation of reaching and grasping function in severe hemiplegic patients using functional electrical stimulation therapy.
        Neurorehabil Neural Repair. 2008; 22: 706-714
        • Lin Z.
        • Yan T.
        Long-term effectiveness of neuromuscular electrical stimulation for promoting motor recovery of the upper extremity after stroke.
        J Rehabil Med. 2011; 43: 506-510
        • Popovic M.B.
        • Popovic D.B.
        • Sinkjaer T.
        • Stefanovic A.
        • Schwirtlich L.
        Clinical evaluation of functional electrical therapy in acute hemiplegic subjects.
        J Rehabil Res Dev. 2003; 40: 443-453
        • Popovic D.B.
        • Popovic M.B.
        • Sinkjaer T.
        • Stefanovic A.
        • Schwirtlich L.
        Therapy of paretic arm in hemiplegic subjects augmented with a neural prosthesis: a cross-over study.
        Can J Physiol Pharmacol. 2004; 82: 749-756
        • Chae J.
        • Bethoux F.
        • Bohine T.
        • Dobos L.
        • Davis T.
        • Friedl A.
        Neuromuscular stimulation for upper extremity motor and functional recovery in acute hemiplegia.
        Stroke. 1998; 29: 975-979
        • Pandyan A.D.
        • Granat M.H.
        • Stott D.H.
        Effects of electrical stimulation on flexion contractures in the hemiplegic wrist.
        Clin Rehabil. 1997; 11: 123-130
        • Powell J.
        • Pandyan A.D.
        • Granat M.
        • Cameron M.
        • Stott D.J.
        Electrical stimulation of wrist extensors in poststroke hemiplegia.
        Stroke. 1999; 30: 1384-1389
        • Alon G.
        • Levitt A.F.
        • McCarthy P.A.
        Functional electrical stimulation enhancement of upper extremity functional recovery during stroke rehabilitation: a pilot study.
        Neurorehabil Neural Repair. 2007; 21: 207-215
        • Alon G.
        • Levitt A.F.
        • McCarthy P.A.
        Functional electrical stimulation (FES) may modify the poor prognosis of stroke survivors with severe motor loss of the upper extremity: a preliminary study.
        Am J Phys Med Rehabil. 2008; 87: 627-636
        • Pollock A.
        • Farmer S.E.
        • Brady M.C.
        • et al.
        Interventions for improving upper limb function after stroke.
        Cochrane Database Syst Rev. 2014; : CD010820
        • Vafadar A.K.
        • Cote J.N.
        • Archambault P.S.
        Effectiveness of functional electrical stimulation in improving clinical outcomes in the upper arm following stroke: a systematic review and meta-analysis.
        Biomed Res Int. 2015; 2015: 729768
        • de Kroon J.R.
        • IJzerman M.J.
        Electrical stimulation of the upper extremity in stroke: cyclic versus EMG-triggered stimulation.
        Clin Rehabil. 2008; 22: 690-697
        • Boyaci A.
        • Topuz O.
        • Alkan H.
        • et al.
        Comparison of the effectiveness of active and passive neuromuscular electrical stimulation of hemiplegic upper extremities: a randomized, controlled trial.
        Int J Rehabil Res. 2013; 36: 315-322
        • Wilson R.D.
        • Page S.J.
        • Delahanty M.
        • et al.
        Upper-limb recovery after stroke: a randomized controlled trial comparing EMG-triggered, cyclic, and sensory electrical stimulation.
        Neurorehabil Neural Repair. 2016; 30: 978-987
        • Hong I.K.
        • Choi J.B.
        • Lee J.H.
        Cortical changes after mental imagery training combined with electromyography-triggered electrical stimulation in patients with chronic stroke.
        Stroke. 2012; 43: 2506-2509
        • Holden M.K.
        Virtual environments for motor rehabilitation: review.
        Cyberpsychol Behav. 2005; 8 (discussion 212-9): 187-211
        • Sousa Nanji L.
        • Torres Cardoso A.
        • Costa J.
        • Vaz-Carneiro A.
        [Analysis of the Cochrane Review: interventions for improving upper limb function after stroke. Cochrane Database Syst Rev. 2014,11:CD010820].
        Acta Med Port. 2015; 28 ([Portuguese]): 551-553
        • Shin J.H.
        • Kim M.Y.
        • Lee J.Y.
        • et al.
        Effects of virtual reality-based rehabilitation on distal upper extremity function and health-related quality of life: a single-blinded, randomized controlled trial.
        J Neuroeng Rehabil. 2016; 13: 17
        • Gladstone D.J.
        • Danells C.J.
        • Black S.E.
        The Fugl-Meyer Assessment of motor recovery after stroke: a critical review of its measurement properties.
        Neurorehabil Neural Repair. 2002; 16: 232-240
        • Taub E.
        • Miller N.E.
        • Novack T.A.
        • et al.
        Technique to improve chronic motor deficit after stroke.
        Arch Phys Med Rehabil. 1993; 74: 347-354
        • Wolf S.L.
        • Lecraw D.E.
        • Barton L.A.
        • Jann B.B.
        Forced use of hemiplegic upper extremities to reverse the effect of learned nonuse among chronic stroke and head-injured patients.
        Exp Neurol. 1989; 104: 125-132
        • Kim J.H.
        • Kim I.S.
        • Han T.R.
        New scoring system for Jebsen Hand Function Test.
        J Korean Acad Rehabil Med. 2007; 31: 623-629
        • Carod-Artal F.J.
        • Coral L.F.
        • Trizotto D.S.
        • Moreira C.M.
        The Stroke Impact Scale 3.0: evaluation of acceptability, reliability, and validity of the Brazilian version.
        Stroke. 2008; 39: 2477-2484
        • Kho A.Y.
        • Liu K.P.
        • Chung R.C.
        Meta-analysis on the effect of mental imagery on motor recovery of the hemiplegic upper extremity function.
        Aust Occup Ther J. 2014; 61: 38-48
        • Iso N.
        • Moriuchi T.
        • Sagari A.
        • et al.
        Monitoring local regional hemodynamic signal changes during motor execution and motor imagery using near-infrared spectroscopy.
        Front Physiol. 2016; 6: 416
        • Jeannerod M.
        Neural simulation of action: a unifying mechanism for motor cognition.
        Neuroimage. 2001; 14: S103-S109
        • Kimberley T.J.
        • Khandekar G.
        • Skraba L.L.
        • et al.
        Neural substrates for motor imagery in severe hemiparesis.
        Neurorehabil Neural Repair. 2006; 20: 268-277
        • Rizzolatti G.
        • Fogassi L.
        • Gallese V.
        Neurophysiological mechanisms underlying the understanding and imitation of action.
        Nat Rev Neurosci. 2001; 2: 661-670
        • Franceschini M.
        • Ceravolo M.G.
        • Agosti M.
        • et al.
        Clinical relevance of action observation in upper-limb stroke rehabilitation: a possible role in recovery of functional dexterity. A randomized clinical trial.
        Neurorehabil Neural Repair. 2012; 26: 456-462
        • Ertelt D.
        • Small S.
        • Solodkin A.
        • et al.
        Action observation has a positive impact on rehabilitation of motor deficits after stroke.
        Neuroimage. 2007; 36: T164-T173
        • Stefan K.
        • Cohen L.G.
        • Duque J.
        • et al.
        Formation of a motor memory by action observation.
        J Neurosci. 2005; 25: 9339-9346
        • Celnik P.
        • Webster B.
        • Glasser D.M.
        • Cohen L.G.
        Effects of action observation on physical training after stroke.
        Stroke. 2008; 39: 1814-1820
        • Porro C.A.
        • Francescato M.P.
        • Cettolo V.
        • et al.
        Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study.
        J Neurosci. 1996; 16: 7688-7698
        • Im H.
        • Ku J.
        • Kim H.J.
        • Kang Y.J.
        Virtual reality-guided motor imagery increases corticomotor excitability in healthy volunteers and stroke patients.
        Ann Rehabil Med. 2016; 40: 420-431
        • Jochumsen M.
        • Niazi I.K.
        • Signal N.
        • et al.
        Pairing voluntary movement and muscle-located electrical stimulation increases cortical excitability.
        Front Hum Neurosci. 2016; 10: 482
        • Taylor L.
        • Lewis G.N.
        • Taylor D.
        Short-term effects of electrical stimulation and voluntary activity on corticomotor excitability in healthy individuals and people with stroke.
        J Clin Neurophysiol. 2012; 29: 237-243
        • Khaslavskaia S.
        • Sinkjaer T.
        Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive.
        Exp Brain Res. 2005; 162: 497-502
        • Wolf S.L.
        • Winstein C.J.
        • Miller J.P.
        • et al.
        Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial.
        JAMA. 2006; 296: 2095-2104
        • Lang C.E.
        • Edwards D.F.
        • Birkenmeier R.L.
        • Dromerick A.W.
        Estimating minimal clinically important differences of upper-extremity measures early after stroke.
        Arch Phys Med Rehabil. 2008; 89: 1693-1700
        • Park G.Y.
        • Im S.
        • Lee S.J.
        • Pae C.U.
        The association between post-stroke depression and the activities of daily living/gait balance in patients with first-onset stroke patients.
        Psychiatry Investig. 2016; 13: 659-664
        • Dafer R.M.
        • Rao M.
        • Shareef A.
        • Sharma A.
        Poststroke depression.
        Top Stroke Rehabil. 2008; 15: 13-21