Motor function and white matter connectivity in children cooled for neonatal encephalopathy

Therapeutic hypothermia reduces the incidence of severe motor disability, such as cerebral palsy, following neonatal hypoxic-ischaemic encephalopathy. However, cooled children without cerebral palsy at school-age demonstrate motor deficits and altered white matter connectivity. In this study, we use...

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Autores principales: Arthur P.C. Spencer, Jonathan C.W. Brooks, Naoki Masuda, Hollie Byrne, Richard Lee-Kelland, Sally Jary, Marianne Thoresen, Marc Goodfellow, Frances M. Cowan, Ela Chakkarapani
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Publicado: Elsevier 2021
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spelling oai:doaj.org-article:f002679766df4fe6850e9aef775487a42021-11-06T04:28:05ZMotor function and white matter connectivity in children cooled for neonatal encephalopathy2213-158210.1016/j.nicl.2021.102872https://doaj.org/article/f002679766df4fe6850e9aef775487a42021-01-01T00:00:00Zhttp://www.sciencedirect.com/science/article/pii/S2213158221003168https://doaj.org/toc/2213-1582Therapeutic hypothermia reduces the incidence of severe motor disability, such as cerebral palsy, following neonatal hypoxic-ischaemic encephalopathy. However, cooled children without cerebral palsy at school-age demonstrate motor deficits and altered white matter connectivity. In this study, we used diffusion-weighted imaging to investigate the relationship between white matter connectivity and motor performance, measured using the Movement Assessment Battery for Children-2, in children aged 6–8 years treated with therapeutic hypothermia for neonatal hypoxic-ischaemic encephalopathy at birth, who did not develop cerebral palsy (cases), and matched typically developing controls. Correlations between total motor scores and diffusion properties in major white matter tracts were assessed in 33 cases and 36 controls. In cases, significant correlations (FDR-corrected P < 0.05) were found in the anterior thalamic radiation bilaterally (left: r = 0.513; right: r = 0.488), the cingulate gyrus part of the left cingulum (r = 0.588), the hippocampal part of the left cingulum (r = 0.541), and the inferior fronto-occipital fasciculus bilaterally (left: r = 0.445; right: r = 0.494). No significant correlations were found in controls. We then constructed structural connectivity networks, for 22 cases and 32 controls, in which nodes represent brain regions and edges were determined by probabilistic tractography and weighted by fractional anisotropy. Analysis of whole-brain network metrics revealed correlations (FDR-corrected P < 0.05), in cases, between total motor scores and average node strength (r = 0.571), local efficiency (r = 0.664), global efficiency (r = 0.677), clustering coefficient (r = 0.608), and characteristic path length (r = -0.652). No significant correlations were found in controls. We then investigated edge-level association with motor function using the network-based statistic. This revealed subnetworks which exhibited group differences in the association between motor outcome and edge weights, for total motor scores (P = 0.0109) as well as for balance (P = 0.0245) and manual dexterity (P = 0.0233) domain scores. All three of these subnetworks comprised numerous frontal lobe regions known to be associated with motor function, including the superior frontal gyrus and middle frontal gyrus. The subnetwork associated with total motor scores was highly left-lateralised. These findings demonstrate an association between impaired motor function and brain organisation in school-age children treated with therapeutic hypothermia for neonatal hypoxic-ischaemic encephalopathy.Arthur P.C. SpencerJonathan C.W. BrooksNaoki MasudaHollie ByrneRichard Lee-KellandSally JaryMarianne ThoresenMarc GoodfellowFrances M. CowanEla ChakkarapaniElsevierarticleTherapeutic hypothermiaNeonatal encephalopathyStructural connectivityBrain networksMotor abilityFractional anisotropyComputer applications to medicine. Medical informaticsR858-859.7Neurology. Diseases of the nervous systemRC346-429ENNeuroImage: Clinical, Vol 32, Iss , Pp 102872- (2021)
institution DOAJ
collection DOAJ
language EN
topic Therapeutic hypothermia
Neonatal encephalopathy
Structural connectivity
Brain networks
Motor ability
Fractional anisotropy
Computer applications to medicine. Medical informatics
R858-859.7
Neurology. Diseases of the nervous system
RC346-429
spellingShingle Therapeutic hypothermia
Neonatal encephalopathy
Structural connectivity
Brain networks
Motor ability
Fractional anisotropy
Computer applications to medicine. Medical informatics
R858-859.7
Neurology. Diseases of the nervous system
RC346-429
Arthur P.C. Spencer
Jonathan C.W. Brooks
Naoki Masuda
Hollie Byrne
Richard Lee-Kelland
Sally Jary
Marianne Thoresen
Marc Goodfellow
Frances M. Cowan
Ela Chakkarapani
Motor function and white matter connectivity in children cooled for neonatal encephalopathy
description Therapeutic hypothermia reduces the incidence of severe motor disability, such as cerebral palsy, following neonatal hypoxic-ischaemic encephalopathy. However, cooled children without cerebral palsy at school-age demonstrate motor deficits and altered white matter connectivity. In this study, we used diffusion-weighted imaging to investigate the relationship between white matter connectivity and motor performance, measured using the Movement Assessment Battery for Children-2, in children aged 6–8 years treated with therapeutic hypothermia for neonatal hypoxic-ischaemic encephalopathy at birth, who did not develop cerebral palsy (cases), and matched typically developing controls. Correlations between total motor scores and diffusion properties in major white matter tracts were assessed in 33 cases and 36 controls. In cases, significant correlations (FDR-corrected P < 0.05) were found in the anterior thalamic radiation bilaterally (left: r = 0.513; right: r = 0.488), the cingulate gyrus part of the left cingulum (r = 0.588), the hippocampal part of the left cingulum (r = 0.541), and the inferior fronto-occipital fasciculus bilaterally (left: r = 0.445; right: r = 0.494). No significant correlations were found in controls. We then constructed structural connectivity networks, for 22 cases and 32 controls, in which nodes represent brain regions and edges were determined by probabilistic tractography and weighted by fractional anisotropy. Analysis of whole-brain network metrics revealed correlations (FDR-corrected P < 0.05), in cases, between total motor scores and average node strength (r = 0.571), local efficiency (r = 0.664), global efficiency (r = 0.677), clustering coefficient (r = 0.608), and characteristic path length (r = -0.652). No significant correlations were found in controls. We then investigated edge-level association with motor function using the network-based statistic. This revealed subnetworks which exhibited group differences in the association between motor outcome and edge weights, for total motor scores (P = 0.0109) as well as for balance (P = 0.0245) and manual dexterity (P = 0.0233) domain scores. All three of these subnetworks comprised numerous frontal lobe regions known to be associated with motor function, including the superior frontal gyrus and middle frontal gyrus. The subnetwork associated with total motor scores was highly left-lateralised. These findings demonstrate an association between impaired motor function and brain organisation in school-age children treated with therapeutic hypothermia for neonatal hypoxic-ischaemic encephalopathy.
format article
author Arthur P.C. Spencer
Jonathan C.W. Brooks
Naoki Masuda
Hollie Byrne
Richard Lee-Kelland
Sally Jary
Marianne Thoresen
Marc Goodfellow
Frances M. Cowan
Ela Chakkarapani
author_facet Arthur P.C. Spencer
Jonathan C.W. Brooks
Naoki Masuda
Hollie Byrne
Richard Lee-Kelland
Sally Jary
Marianne Thoresen
Marc Goodfellow
Frances M. Cowan
Ela Chakkarapani
author_sort Arthur P.C. Spencer
title Motor function and white matter connectivity in children cooled for neonatal encephalopathy
title_short Motor function and white matter connectivity in children cooled for neonatal encephalopathy
title_full Motor function and white matter connectivity in children cooled for neonatal encephalopathy
title_fullStr Motor function and white matter connectivity in children cooled for neonatal encephalopathy
title_full_unstemmed Motor function and white matter connectivity in children cooled for neonatal encephalopathy
title_sort motor function and white matter connectivity in children cooled for neonatal encephalopathy
publisher Elsevier
publishDate 2021
url https://doaj.org/article/f002679766df4fe6850e9aef775487a4
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