Prediction of Behavioral Improvement Through Resting-State Electroencephalography and Clinical Severity in a Randomized Controlled Trial Testing Bumetanide in Autism Spectrum Disorder.

Autism Bumetanide EEG Excitation-inhibition Machine learning RCT Repetitive behavior

Journal

Biological psychiatry. Cognitive neuroscience and neuroimaging
ISSN: 2451-9030
Titre abrégé: Biol Psychiatry Cogn Neurosci Neuroimaging
Pays: United States
ID NLM: 101671285

Informations de publication

Date de publication:
03 2023
Historique:
received: 01 07 2021
revised: 31 07 2021
accepted: 26 08 2021
pubmed: 11 9 2021
medline: 11 3 2023
entrez: 10 9 2021
Statut: ppublish

Résumé

Mechanism-based treatments such as bumetanide are being repurposed for autism spectrum disorder. We recently reported beneficial effects on repetitive behavioral symptoms that might be related to regulating excitation-inhibition (E/I) balance in the brain. Here, we tested the neurophysiological effects of bumetanide and the relationship to clinical outcome variability and investigated the potential for machine learning-based predictions of meaningful clinical improvement. Using modified linear mixed models applied to intention-to-treat population, we analyzed E/I-sensitive electroencephalography (EEG) measures before and after 91 days of treatment in the double-blind, randomized, placebo-controlled Bumetanide in Autism Medication and Biomarker study. Resting-state EEG of 82 subjects out of 92 participants (7-15 years) were available. Alpha frequency band absolute and relative power, central frequency, long-range temporal correlations, and functional E/I ratio treatment effects were related to the Repetitive Behavior Scale-Revised (RBS-R) and the Social Responsiveness Scale 2 as clinical outcomes. We observed superior bumetanide effects on EEG, reflected in increased absolute and relative alpha power and functional E/I ratio and in decreased central frequency. Associations between EEG and clinical outcome change were restricted to subgroups with medium to high RBS-R improvement. Using machine learning, medium and high RBS-R improvement could be predicted by baseline RBS-R score and EEG measures with 80% and 92% accuracy, respectively. Bumetanide exerts neurophysiological effects related to clinical changes in more responsive subsets, in whom prediction of improvement was feasible through EEG and clinical measures.

Sections du résumé

BACKGROUND
Mechanism-based treatments such as bumetanide are being repurposed for autism spectrum disorder. We recently reported beneficial effects on repetitive behavioral symptoms that might be related to regulating excitation-inhibition (E/I) balance in the brain. Here, we tested the neurophysiological effects of bumetanide and the relationship to clinical outcome variability and investigated the potential for machine learning-based predictions of meaningful clinical improvement.
METHODS
Using modified linear mixed models applied to intention-to-treat population, we analyzed E/I-sensitive electroencephalography (EEG) measures before and after 91 days of treatment in the double-blind, randomized, placebo-controlled Bumetanide in Autism Medication and Biomarker study. Resting-state EEG of 82 subjects out of 92 participants (7-15 years) were available. Alpha frequency band absolute and relative power, central frequency, long-range temporal correlations, and functional E/I ratio treatment effects were related to the Repetitive Behavior Scale-Revised (RBS-R) and the Social Responsiveness Scale 2 as clinical outcomes.
RESULTS
We observed superior bumetanide effects on EEG, reflected in increased absolute and relative alpha power and functional E/I ratio and in decreased central frequency. Associations between EEG and clinical outcome change were restricted to subgroups with medium to high RBS-R improvement. Using machine learning, medium and high RBS-R improvement could be predicted by baseline RBS-R score and EEG measures with 80% and 92% accuracy, respectively.
CONCLUSIONS
Bumetanide exerts neurophysiological effects related to clinical changes in more responsive subsets, in whom prediction of improvement was feasible through EEG and clinical measures.

Identifiants

pubmed: 34506972
pii: S2451-9022(21)00251-2
doi: 10.1016/j.bpsc.2021.08.009
pii:
doi:

Substances chimiques

Bumetanide 0Y2S3XUQ5H

Types de publication

Journal Article Randomized Controlled Trial Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

251-261

Informations de copyright

Copyright © 2021 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Erika L Juarez-Martinez (EL)

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Neuroscience, VU University Amsterdam, Amsterdam, The Netherlands; NBT Analytics BV, Amsterdam, The Netherlands; Child and Adolescent Psychiatry and Psychosocial Care, Emma Children's Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.

Jan J Sprengers (JJ)

Department of Psychiatry, UMC Utrecht Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands.

Gianina Cristian (G)

Child and Adolescent Psychiatry and Psychosocial Care, Emma Children's Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands; Department of Health Evidence, Radboud University Medical Center, Nijmegen, The Netherlands; Department of Health Evidence, Radboud University Medical Center, Nijmegen, The Netherlands.

Bob Oranje (B)

Department of Psychiatry, UMC Utrecht Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands.

Dorinde M van Andel (DM)

Department of Psychiatry, UMC Utrecht Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands.

Arthur-Ervin Avramiea (AE)

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Neuroscience, VU University Amsterdam, Amsterdam, The Netherlands.

Sonja Simpraga (S)

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Neuroscience, VU University Amsterdam, Amsterdam, The Netherlands; NBT Analytics BV, Amsterdam, The Netherlands.

Simon J Houtman (SJ)

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Neuroscience, VU University Amsterdam, Amsterdam, The Netherlands.

Richard Hardstone (R)

Neuroscience Institute, New York University School of Medicine, New York, New York.

Cathalijn Gerver (C)

Child and Adolescent Psychiatry and Psychosocial Care, Emma Children's Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands; Department of Psychiatry, UMC Utrecht Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands; N=You Neurodevelopmental Precision Center, Amsterdam Neuroscience, Amsterdam Reproduction and Development, Amsterdam UMC, Amsterdam, The Netherlands.

Gert Jan van der Wilt (G)

Department of Health Evidence, Radboud University Medical Center, Nijmegen, The Netherlands.

Huibert D Mansvelder (HD)

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Neuroscience, VU University Amsterdam, Amsterdam, The Netherlands.

Marinus J C Eijkemans (MJC)

Department of Psychiatry, UMC Utrecht Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands; Department of Biostatistics & Research Support, Julius Center for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht, The Netherlands.

Klaus Linkenkaer-Hansen (K)

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Neuroscience, VU University Amsterdam, Amsterdam, The Netherlands.

Hilgo Bruining (H)

Child and Adolescent Psychiatry and Psychosocial Care, Emma Children's Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands; Department of Psychiatry, UMC Utrecht Brain Center, University Medical Centre Utrecht, Utrecht, The Netherlands; N=You Neurodevelopmental Precision Center, Amsterdam Neuroscience, Amsterdam Reproduction and Development, Amsterdam UMC, Amsterdam, The Netherlands; Levvel, Center for Child and Adolescent Psychiatry, Amsterdam, The Netherlands. Electronic address: h.bruining@amsterdamumc.nl.

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