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      BCI-activated electrical stimulation in children with perinatal stroke and hemiparesis: A pilot study

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          Abstract

          Background

          Perinatal stroke (PS) causes most hemiparetic cerebral palsy (CP) and results in lifelong disability. Children with severe hemiparesis have limited rehabilitation options. Brain computer interface- activated functional electrical stimulation (BCI-FES) of target muscles may enhance upper extremity function in hemiparetic adults. We conducted a pilot clinical trial to assess the safety and feasibility of BCI-FES in children with hemiparetic CP.

          Methods

          Thirteen participants (mean age = 12.2 years, 31% female) were recruited from a population-based cohort. Inclusion criteria were: (1) MRI-confirmed PS, (2) disabling hemiparetic CP, (3) age 6–18 years, (4) informed consent/assent. Those with neurological comorbidities or unstable epilepsy were excluded. Participants attended two BCI sessions: training and rehabilitation. They wore an EEG-BCI headset and two forearm extensor stimulation electrodes. Participants’ imagination of wrist extension was classified on EEG, after which muscle stimulation and visual feedback were provided when the correct visualization was detected.

          Results

          No serious adverse events or dropouts occurred. The most common complaints were mild headache, headset discomfort and muscle fatigue. Children ranked the experience as comparable to a long car ride and none reported as unpleasant. Sessions lasted a mean of 87 min with 33 min of stimulation delivered. Mean classification accuracies were ( M = 78.78%, SD = 9.97) for training and ( M = 73.48, SD = 12.41) for rehabilitation. Mean Cohen’s Kappa across rehabilitation trials was M = 0.43, SD = 0.29, range = 0.019–1.00, suggesting BCI competency.

          Conclusion

          Brain computer interface-FES was well -tolerated and feasible in children with hemiparesis. This paves the way for clinical trials to optimize approaches and test efficacy.

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          Most cited references54

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          A systematic review of interventions for children with cerebral palsy: state of the evidence.

          The aim of this study was to describe systematically the best available intervention evidence for children with cerebral palsy (CP). This study was a systematic review of systematic reviews. The following databases were searched: CINAHL, Cochrane Library, DARE, EMBASE, Google Scholar MEDLINE, OTSeeker, PEDro, PsycBITE, PsycINFO, and speechBITE. Two independent reviewers determined whether studies met the inclusion criteria. These were that (1) the study was a systematic review or the next best available; (2) it was a medical/allied health intervention; and (3) that more than 25% of participants were children with CP. Interventions were coded using the Oxford Levels of Evidence; GRADE; Evidence Alert Traffic Light; and the International Classification of Function, Disability and Health. Overall, 166 articles met the inclusion criteria (74% systematic reviews) across 64 discrete interventions seeking 131 outcomes. Of the outcomes assessed, 16% (21 out of 131) were graded 'do it' (green go); 58% (76 out of 131) 'probably do it' (yellow measure); 20% (26 out of 131) 'probably do not do it' (yellow measure); and 6% (8 out of 131) 'do not do it' (red stop). Green interventions included anticonvulsants, bimanual training, botulinum toxin, bisphosphonates, casting, constraint-induced movement therapy, context-focused therapy, diazepam, fitness training, goal-directed training, hip surveillance, home programmes, occupational therapy after botulinum toxin, pressure care, and selective dorsal rhizotomy. Most (70%) evidence for intervention was lower level (yellow) while 6% was ineffective (red). Evidence supports 15 green light interventions. All yellow light interventions should be accompanied by a sensitive outcome measure to monitor progress and red light interventions should be discontinued since alternatives exist. © 2013 Mac Keith Press.
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            Reach and grasp by people with tetraplegia using a neurally controlled robotic arm

            Paralysis following spinal cord injury (SCI), brainstem stroke, amyotrophic lateral sclerosis (ALS) and other disorders can disconnect the brain from the body, eliminating the ability to carry out volitional movements. A neural interface system (NIS) 1–5 could restore mobility and independence for people with paralysis by translating neuronal activity directly into control signals for assistive devices. We have previously shown that people with longstanding tetraplegia can use an NIS to move and click a computer cursor and to control physical devices 6–8 . Able-bodied monkeys have used an NIS to control a robotic arm 9 , but it is unknown whether people with profound upper extremity paralysis or limb loss could use cortical neuronal ensemble signals to direct useful arm actions. Here, we demonstrate the ability of two people with long-standing tetraplegia to use NIS-based control of a robotic arm to perform three-dimensional reach and grasp movements. Participants controlled the arm over a broad space without explicit training, using signals decoded from a small, local population of motor cortex (MI) neurons recorded from a 96-channel microelectrode array. One of the study participants, implanted with the sensor five years earlier, also used a robotic arm to drink coffee from a bottle. While robotic reach and grasp actions were not as fast or accurate as those of an able-bodied person, our results demonstrate the feasibility for people with tetraplegia, years after CNS injury, to recreate useful multidimensional control of complex devices directly from a small sample of neural signals.
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              Canadian stroke best practice recommendations: Stroke rehabilitation practice guidelines, update 2015.

              Stroke rehabilitation is a progressive, dynamic, goal-orientated process aimed at enabling a person with impairment to reach their optimal physical, cognitive, emotional, communicative, social and/or functional activity level. After a stroke, patients often continue to require rehabilitation for persistent deficits related to spasticity, upper and lower extremity dysfunction, shoulder and central pain, mobility/gait, dysphagia, vision, and communication. Each year in Canada 62,000 people experience a stroke. Among stroke survivors, over 6500 individuals access in-patient stroke rehabilitation and stay a median of 30 days (inter-quartile range 19 to 45 days). The 2015 update of the Canadian Stroke Best Practice Recommendations: Stroke Rehabilitation Practice Guidelines is a comprehensive summary of current evidence-based recommendations for all members of multidisciplinary teams working in a range of settings, who provide care to patients following stroke. These recommendations have been developed to address both the organization of stroke rehabilitation within a system of care (i.e., Initial Rehabilitation Assessment; Stroke Rehabilitation Units; Stroke Rehabilitation Teams; Delivery; Outpatient and Community-Based Rehabilitation), and specific interventions and management in stroke recovery and direct clinical care (i.e., Upper Extremity Dysfunction; Lower Extremity Dysfunction; Dysphagia and Malnutrition; Visual-Perceptual Deficits; Central Pain; Communication; Life Roles). In addition, stroke happens at any age, and therefore a new section has been added to the 2015 update to highlight components of stroke rehabilitation for children who have experienced a stroke, either prenatally, as a newborn, or during childhood. All recommendations have been assigned a level of evidence which reflects the strength and quality of current research evidence available to support the recommendation. The updated Rehabilitation Clinical Practice Guidelines feature several additions that reflect new research areas and stronger evidence for already existing recommendations. It is anticipated that these guidelines will provide direction and standardization for patients, families/caregiver(s), and clinicians within Canada and internationally.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                17 March 2023
                2023
                : 17
                : 1006242
                Affiliations
                [1] 1Cumming School of Medicine, University of Calgary , Calgary, AB, Canada
                [2] 2Department of Pediatrics, University of Calgary , Calgary, AB, Canada
                [3] 3Alberta Children’s Hospital Research Institute , Calgary, AB, Canada
                [4] 4Department of Pediatrics, Alberta Children’s Hospital , Calgary, AB, Canada
                [5] 5Department of Clinical Neurosciences, Alberta Children’s Hospital , Calgary, AB, Canada
                Author notes

                Edited by: Fu-Zen Shaw, National Cheng Kung University, Taiwan

                Reviewed by: Mariana P. Branco, University Medical Center Utrecht, Netherlands; Brady A. Riedner, University of Wisconsin-Madison, United States

                *Correspondence: Ephrem Zewdie, Ephrem.Zewdie@ 123456albertahealthservices.ca

                This article was submitted to Brain-Computer Interfaces, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2023.1006242
                10063823
                37007682
                75d2f210-4280-4c7d-81e4-69ec2e124d85
                Copyright © 2023 Jadavji, Kirton, Metzler and Zewdie.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 July 2022
                : 03 March 2023
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 54, Pages: 10, Words: 8025
                Funding
                Funded by: Heart and Stroke Foundation of Canada, doi 10.13039/100004411;
                This study was supported by the Heart and Stroke Foundation Seed Grant under Grant Number (10012689) and the Alberta Children’s Hospital Department of Pediatrics innovation award.
                Categories
                Neuroscience
                Original Research

                Neurosciences
                perinatal stroke,cerebral palsy,electrical stimulation (es),brain computer interface,rehabilitation

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