Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study

Mique Saes; Sarah B. Zandvliet; Aukje S. Andringa; Andreas Daffertshofer; Jos W.R. Twisk; Carel G.M. Meskers; Erwin E.H. van Wegen; Gert Kwakkel

doi:10.1177/1545968320905797

Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study

Mique Saes
, Sarah B. Zandvliet
, Aukje S. Andringa
, Andreas Daffertshofer
, Jos W.R. Twisk
, Carel G.M. Meskers
, Erwin E.H. van Wegen
, Gert Kwakkel^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

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Abstract

Background. The time course of cortical activation and its relation with clinical measures may elucidate mechanisms underlying spontaneous neurobiological recovery after stroke. Objective. We aimed to investigate (1) the time course of cortical activation as revealed by EEG-based spectral characteristics during awake rest and (2) the development of these spectral characteristics in relation to global neurological and upper-limb motor recovery in the first 6 months poststroke. Methods. Resting-state EEG was measured serially in 41 patients after a first-ever ischemic stroke, within 3 and at 5, 12, and 26 weeks poststroke. We computed the brain symmetry index (BSI) and directional BSI (BSIdir) over different frequency bands (1-25 Hz, delta, theta) and delta/alpha ratio (DAR). The National Institutes of Health Stroke Scale (NIHSS) and Fugl-Meyer motor assessment of the upper extremity (FM-UE) were determined as clinical reflections of spontaneous neurobiological recovery. Longitudinal changes in spectral characteristics and within- and between-subject associations with NIHSS and FM-UE were analyzed with linear mixed models. Results. Spectral characteristics showed a gradual normalization over time, within and beyond 12 weeks poststroke. Significant within- and between-subject associations with NIHSS were found for DAR of the affected hemisphere (DAR_AH) and BSIdir_delta. BSIdir_delta also demonstrated significant within- and between-subject associations with FM-UE. Conclusions. Changes in spectral characteristics are not restricted to the time window of recovery of clinical neurological impairments. The present study suggests that decreasing DAR_AH and BSIdir_delta reflect improvement of global neurological impairments, whereas BSIdir_delta was also specifically associated with upper-limb motor recovery early poststroke.

Original language	English
Pages (from-to)	389-402
Number of pages	14
Journal	Neurorehabilitation and Neural Repair
Volume	34
Issue number	5
Early online date	4 Apr 2020
DOIs	https://doi.org/10.1177/1545968320905797
Publication status	Published - May 2020

Funding

In addition to the authors of the present study, the consortium consists of Caroline Winters, Dirk Hoevenaars, Luuk Haring and Elza van Duijnhoven from Amsterdam UMC, location VUmc; Jun Yao and Julius Dewald from Northwestern University, Chicago; and Martijn Vlaar, Teodoro Solis-Escalante, Alfred Schouten, Yuan Yang, Mark van de Ruit, Konstantina Kalogianni, Joost van Kordelaar, Lena Filatova and Frans van der Helm from Delft University of Technology. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was funded by the European Research Council under the European Union?s Seventh Framework Programme (FP/2007?2013 ERC Grant Agreement n. 291339, project ?4DEEG: A New Tool to Investigate the Spatial and Temporal Activity Patterns in the Brain?), as well as by the Dutch Brain Foundation (F2011(1)-25) and the Netherlands Organization of Scientific Research (research programme NeuroCIMT, project number 14905). Sponsors had no other involvement than financial support. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was funded by the European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013 ERC Grant Agreement n. 291339, project “4DEEG: A New Tool to Investigate the Spatial and Temporal Activity Patterns in the Brain”), as well as by the Dutch Brain Foundation (F2011(1)-25) and the Netherlands Organization of Scientific Research (research programme NeuroCIMT, project number 14905). Sponsors had no other involvement than financial support.

Funders	Funder number
Northwestern University
European Commission
European Research Council
Technische Universiteit Delft
Dutch Brain Foundation	F2011(1)-25
Seventh Framework Programme	291339
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	14905

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

biomarker
EEG
longitudinal study
recovery of function
stroke
upper extremity

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Saes, M., Zandvliet, S. B., Andringa, A. S., Daffertshofer, A., Twisk, J. W. R., Meskers, C. G. M., van Wegen, E. E. H., & Kwakkel, G. (2020). Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study. Neurorehabilitation and Neural Repair, 34(5), 389-402. https://doi.org/10.1177/1545968320905797

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title = "Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study",

abstract = "Background. The time course of cortical activation and its relation with clinical measures may elucidate mechanisms underlying spontaneous neurobiological recovery after stroke. Objective. We aimed to investigate (1) the time course of cortical activation as revealed by EEG-based spectral characteristics during awake rest and (2) the development of these spectral characteristics in relation to global neurological and upper-limb motor recovery in the first 6 months poststroke. Methods. Resting-state EEG was measured serially in 41 patients after a first-ever ischemic stroke, within 3 and at 5, 12, and 26 weeks poststroke. We computed the brain symmetry index (BSI) and directional BSI (BSIdir) over different frequency bands (1-25 Hz, delta, theta) and delta/alpha ratio (DAR). The National Institutes of Health Stroke Scale (NIHSS) and Fugl-Meyer motor assessment of the upper extremity (FM-UE) were determined as clinical reflections of spontaneous neurobiological recovery. Longitudinal changes in spectral characteristics and within- and between-subject associations with NIHSS and FM-UE were analyzed with linear mixed models. Results. Spectral characteristics showed a gradual normalization over time, within and beyond 12 weeks poststroke. Significant within- and between-subject associations with NIHSS were found for DAR of the affected hemisphere (DARAH) and BSIdirdelta. BSIdirdelta also demonstrated significant within- and between-subject associations with FM-UE. Conclusions. Changes in spectral characteristics are not restricted to the time window of recovery of clinical neurological impairments. The present study suggests that decreasing DARAH and BSIdirdelta reflect improvement of global neurological impairments, whereas BSIdirdelta was also specifically associated with upper-limb motor recovery early poststroke.",

keywords = "biomarker, EEG, longitudinal study, recovery of function, stroke, upper extremity",

author = "Mique Saes and Zandvliet, \{Sarah B.\} and Andringa, \{Aukje S.\} and Andreas Daffertshofer and Twisk, \{Jos W.R.\} and Meskers, \{Carel G.M.\} and \{van Wegen\}, \{Erwin E.H.\} and Gert Kwakkel",

year = "2020",

month = may,

doi = "10.1177/1545968320905797",

language = "English",

volume = "34",

pages = "389--402",

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Saes, M, Zandvliet, SB, Andringa, AS, Daffertshofer, A, Twisk, JWR, Meskers, CGM, van Wegen, EEH & Kwakkel, G 2020, 'Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study', Neurorehabilitation and Neural Repair, vol. 34, no. 5, pp. 389-402. https://doi.org/10.1177/1545968320905797

TY - JOUR

T1 - Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study

AU - Saes, Mique

AU - Zandvliet, Sarah B.

AU - Andringa, Aukje S.

AU - Daffertshofer, Andreas

AU - Twisk, Jos W.R.

AU - Meskers, Carel G.M.

AU - van Wegen, Erwin E.H.

AU - Kwakkel, Gert

PY - 2020/5

Y1 - 2020/5

N2 - Background. The time course of cortical activation and its relation with clinical measures may elucidate mechanisms underlying spontaneous neurobiological recovery after stroke. Objective. We aimed to investigate (1) the time course of cortical activation as revealed by EEG-based spectral characteristics during awake rest and (2) the development of these spectral characteristics in relation to global neurological and upper-limb motor recovery in the first 6 months poststroke. Methods. Resting-state EEG was measured serially in 41 patients after a first-ever ischemic stroke, within 3 and at 5, 12, and 26 weeks poststroke. We computed the brain symmetry index (BSI) and directional BSI (BSIdir) over different frequency bands (1-25 Hz, delta, theta) and delta/alpha ratio (DAR). The National Institutes of Health Stroke Scale (NIHSS) and Fugl-Meyer motor assessment of the upper extremity (FM-UE) were determined as clinical reflections of spontaneous neurobiological recovery. Longitudinal changes in spectral characteristics and within- and between-subject associations with NIHSS and FM-UE were analyzed with linear mixed models. Results. Spectral characteristics showed a gradual normalization over time, within and beyond 12 weeks poststroke. Significant within- and between-subject associations with NIHSS were found for DAR of the affected hemisphere (DARAH) and BSIdirdelta. BSIdirdelta also demonstrated significant within- and between-subject associations with FM-UE. Conclusions. Changes in spectral characteristics are not restricted to the time window of recovery of clinical neurological impairments. The present study suggests that decreasing DARAH and BSIdirdelta reflect improvement of global neurological impairments, whereas BSIdirdelta was also specifically associated with upper-limb motor recovery early poststroke.

AB - Background. The time course of cortical activation and its relation with clinical measures may elucidate mechanisms underlying spontaneous neurobiological recovery after stroke. Objective. We aimed to investigate (1) the time course of cortical activation as revealed by EEG-based spectral characteristics during awake rest and (2) the development of these spectral characteristics in relation to global neurological and upper-limb motor recovery in the first 6 months poststroke. Methods. Resting-state EEG was measured serially in 41 patients after a first-ever ischemic stroke, within 3 and at 5, 12, and 26 weeks poststroke. We computed the brain symmetry index (BSI) and directional BSI (BSIdir) over different frequency bands (1-25 Hz, delta, theta) and delta/alpha ratio (DAR). The National Institutes of Health Stroke Scale (NIHSS) and Fugl-Meyer motor assessment of the upper extremity (FM-UE) were determined as clinical reflections of spontaneous neurobiological recovery. Longitudinal changes in spectral characteristics and within- and between-subject associations with NIHSS and FM-UE were analyzed with linear mixed models. Results. Spectral characteristics showed a gradual normalization over time, within and beyond 12 weeks poststroke. Significant within- and between-subject associations with NIHSS were found for DAR of the affected hemisphere (DARAH) and BSIdirdelta. BSIdirdelta also demonstrated significant within- and between-subject associations with FM-UE. Conclusions. Changes in spectral characteristics are not restricted to the time window of recovery of clinical neurological impairments. The present study suggests that decreasing DARAH and BSIdirdelta reflect improvement of global neurological impairments, whereas BSIdirdelta was also specifically associated with upper-limb motor recovery early poststroke.

KW - biomarker

KW - EEG

KW - longitudinal study

KW - recovery of function

KW - stroke

KW - upper extremity

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Is Resting-State EEG Longitudinally Associated With Recovery of Clinical Neurological Impairments Early Poststroke? A Prospective Cohort Study

Abstract

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UN SDGs

Keywords

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