[ARTICLE] Behavioral Outcomes Following Brain–Computer Interface Intervention for Upper Extremity Rehabilitation in Stroke: A Randomized Controlled Trial – Full Text

Stroke is a leading cause of persistent upper extremity (UE) motor disability in adults. Brain–computer interface (BCI) intervention has demonstrated potential as a motor rehabilitation strategy for stroke survivors. This sub-analysis of ongoing clinical trial (NCT02098265) examines rehabilitative efficacy of this BCI design and seeks to identify stroke participant characteristics associated with behavioral improvement. Stroke participants (n = 21) with UE impairment were assessed using Action Research Arm Test (ARAT) and measures of function. Nine participants completed three assessments during the experimental BCI intervention period and at 1-month follow-up. Twelve other participants first completed three assessments over a parallel time-matched control period and then crossed over into the BCI intervention condition 1-month later. Participants who realized positive change (≥1 point) in total ARAT performance of the stroke affected UE between the first and third assessments of the intervention period were dichotomized as “responders” (<1 = “non-responders”) and similarly analyzed. Of the 14 participants with room for ARAT improvement, 64% (9/14) showed some positive change at completion and approximately 43% (6/14) of the participants had changes of minimal detectable change (MDC = 3 pts) or minimally clinical important difference (MCID = 5.7 points). Participants with room for improvement in the primary outcome measure made significant mean gains in ARATtotalscore at completion (ΔARATtotal = 2, p = 0.028) and 1-month follow-up (ΔARATtotal = 3.4, p= 0.0010), controlling for severity, gender, chronicity, and concordance. Secondary outcome measures, SISmobility, SISadl, SISstrength, and 9HPTaffected, also showed significant improvement over time during intervention. Participants in intervention through follow-up showed a significantly increased improvement rate in SISstrength compared to controls (p = 0.0117), controlling for severity, chronicity, gender, as well as the individual effects of time and intervention type. Participants who best responded to BCI intervention, as evaluated by ARAT score improvement, showed significantly increased outcome values through completion and follow-up for SISmobility (p = 0.0002, p = 0.002) and SISstrength (p = 0.04995, p = 0.0483). These findings may suggest possible secondary outcome measure patterns indicative of increased improvement resulting from this BCI intervention regimen as well as demonstrating primary efficacy of this BCI design for treatment of UE impairment in stroke survivors.

Introduction

Stroke

Each year there are approximately 800,000 new incidences of stroke in the United States (Benjamin et al., 2017), and in 2010 there were an estimated 16.9 million stroke events globally (Mozaffarian et al., 2015). Stroke occurs as a result of a blockage of blood flow in an area of the brain or by rupture of brain vasculature causing death or damage to local and distal brain tissue. In either etiology, survivors may experience some level of upper extremity (UE) physical impairment. Despite recent advances in acute care, an increasing number of stroke survivors face long-term motor deficits (Benjamin et al., 2017). Costs of care for long-term disability resulting from stroke are substantial with the direct medical costs of stroke estimated to $17.9 billion in 2013 (Benjamin et al., 2017). It is crucial that motor therapy for stroke enhances a survivor’s capacity to autonomously participate in activities of daily living (ADLs), thereby decreasing dependency on caregivers as well as the cost and level of care necessary (Dombovy, 2009Stinear, 2016). Efficacious motor therapy should be designed to improve the overall quality of life for the individual survivor based on their goals and needs (Remsik et al., 2016Stinear, 2016).

Need for Treatment

Survivors in the chronic stage of stroke are the most desperate for rehabilitation. Existing pharmacological treatments and behavioral therapy methods primarily serve to treat symptoms associated with stroke (Benjamin et al., 2017) and may not bring about optimal changes in brain function or connectivity (Power et al., 2011Nair et al., 2015). While a growing population of research suggests the greatest potential for recovery in the post-stroke brain occurs within the first months after insult (Stinear and Byblow, 2014), neuroplastic capacity has been demonstrated in both acute and chronic phases (Caria et al., 2011Ang et al., 2015). Spontaneous biological recovery (SBR) (Beebe and Lang, 2009Cramer and Nudo, 2010) in the initial days and weeks following stoke (acute phase) is thought to represent a critical period in the complex progression of motor recovery, which combines neurobiological processes and learning-related elements. After this window of SBR, it is posited a sensitive period of neurorecovery persists, plateauing around 6 months post-stroke (Wolf et al., 20062010Dromerick et al., 2009Cramer and Nudo, 2010). Traditional rehabilitation therapies generally lose efficacy after such time and the course of standard of care treatment options is exhausted leaving chronically impaired persons with few options.

Potential for Treatment

Motor and cognitive recovery after these initial windows may no longer occur in the same spontaneous nature as is observed during SBR. However, innovative therapeutic techniques show some efficacy generating functional motor recovery beyond the traditional rehabilitation windows (Cramer and Nudo, 2010Ang et al., 2015Irimia et al., 2016). Brain–computer interfaces (BCIs), a novel rehabilitation tool, have shown proof of concept for rehabilitating volitional movements in stroke survivors (Muralidharan et al., 2011Song et al., 20142015Young et al., 2014a,b,c,d2015Irimia et al., 2016). In this growing area of research, developing technologies demonstrate promising potential for treating hemiparesis in a clinically viable and efficient manner and they may offer an avenue to increased autonomy for patients reducing their cost and burden of care.

Effectiveness of Current BCI Therapies

There is currently considerable variability in design and efficacy of BCI therapies as well as little consensus with respect to proper arrangement, administration, and dosing (Muralidharan et al., 2011Ang and Guan, 2013Young et al., 2014aAng et al., 2015Irimia et al., 2016Remsik et al., 2016Bundy et al., 2017Dodd et al., 2017). Although acute stroke care has improved morbidity outcomes significantly, current treatments for persistent UE motor impairment resulting from stroke offer only limited restoration of UE motor function the further from stroke a survivor progresses (Wolf et al., 20062010Dromerick et al., 2009Benjamin et al., 2017Stinear et al., 2017). Evidence suggests both acute and chronic stroke patients respond to various neuro-rehabilitative BCI therapy strategies and can achieve clinically significant changes in measures of UE impairment (Young et al., 2014cIrimia et al., 2016Remsik et al., 2016). Furthermore, recent research also suggests that BCI therapy targeted at motor recovery may provide benefits in other brain regions outside of only the motor network (Mohanty et al., 2018).

Overview of This Study

This post hoc analysis of an ongoing clinical trial (NCT02098265) (Song et al., 20142015Young et al., 2014a,b,c,d2015) evaluates the effects of an interventional, non-invasive closed-loop electroencephalography (EEG)-based BCI intervention for the restoration of distal UE motor function in stroke survivors. Participants who showed measurable change in the primary outcome measure were grouped post hoc. This sub-analysis seeks to identify whether there are participant characteristics strongly associated with motor improvement as measured by primary and secondary outcome measures of UE function. These analyses are intended to inform future BCI research approaches and intervention designs as well as suggest and encourage appropriate participant selection.[…]

 

Continue —>  Frontiers | Behavioral Outcomes Following Brain–Computer Interface Intervention for Upper Extremity Rehabilitation in Stroke: A Randomized Controlled Trial | Neuroscience

FIGURE 2. BCI intervention block design: (1) A pre-session open-loop screening task of two attempted and then two imagined grasping tasks (left, right, rest) is used to set control features (BCI classifier) for the forthcoming intervention task (Cursor Task). (2) The closed-loop cursor and target (visual only) intervention condition consists of at least 10 runs of 10 trials of attempted grasping movements for the purpose of guiding a virtual cursor (Ball) either left, or right as cued by the target (Goal) presentation on the horizontal edge of the screen. (3) Following 10 successfully completed runs of the visual only condition, adjuvant stimuli are added to enrich the feedback environment and facilitate volitional movement of the affected extremity (grasping). Subsequent runs are attempted at the preferred pace of the participant, completing as many runs as time allows. (4) With 15 min remaining in the 2-h intervention session, the participant is switched into the post-session open-loop screening task of two imagined and then two attempted grasping tasks (left, right, rest).

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