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Neonatal brain injury influences structural connectivity and childhood functional outcomes

Neonatal brain injury may impact brain development and lead to lifelong functional impairments. Hypoxic-ischemic encephalopathy (HIE) and congenital heart disease (CHD) are two common causes of neonatal brain injury differing in timing and mechanism. Maturation of whole-brain neural networks can be...

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Autores principales: Ramirez, Alice, Peyvandi, Shabnam, Cox, Stephany, Gano, Dawn, Xu, Duan, Tymofiyeva, Olga, McQuillen, Patrick S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8730412/
https://www.ncbi.nlm.nih.gov/pubmed/34986206
http://dx.doi.org/10.1371/journal.pone.0262310
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author Ramirez, Alice
Peyvandi, Shabnam
Cox, Stephany
Gano, Dawn
Xu, Duan
Tymofiyeva, Olga
McQuillen, Patrick S.
author_facet Ramirez, Alice
Peyvandi, Shabnam
Cox, Stephany
Gano, Dawn
Xu, Duan
Tymofiyeva, Olga
McQuillen, Patrick S.
author_sort Ramirez, Alice
collection PubMed
description Neonatal brain injury may impact brain development and lead to lifelong functional impairments. Hypoxic-ischemic encephalopathy (HIE) and congenital heart disease (CHD) are two common causes of neonatal brain injury differing in timing and mechanism. Maturation of whole-brain neural networks can be quantified during development using diffusion magnetic resonance imaging (dMRI) in combination with graph theory metrics. DMRI of 35 subjects with CHD and 62 subjects with HIE were compared to understand differences in the effects of HIE and CHD on the development of network topological parameters and functional outcomes. CHD newborns had worse 12–18 month language (P<0.01) and 30 month cognitive (P<0.01), language (P = 0.05), motor outcomes (P = 0.01). Global efficiency, a metric of brain integration, was lower in CHD (P = 0.03) than in HIE, but transitivity, modularity and small-worldness were similar. After controlling for clinical factors known to affect neurodevelopmental outcomes, we observed that global efficiency was highly associated with 30 month motor outcomes (P = 0.02) in both groups. To explore neural correlates of adverse language outcomes in CHD, we used hypothesis-based and data-driven approaches to identify pathways with altered structural connectivity. We found that connectivity strength in the superior longitudinal fasciculus (SLF) tract 2 was inversely associated with expressive language. After false discovery rate correction, a whole connectome edge analysis identified 18 pathways that were hypoconnected in the CHD cohort as compared to HIE. In sum, our study shows that neonatal structural connectivity predicts early motor development after HIE or in subjects with CHD, and regional SLF connectivity is associated with language outcomes. Further research is needed to determine if and how brain networks change over time and whether those changes represent recovery or ongoing dysfunction. This knowledge will directly inform strategies to optimize neurologic functional outcomes after neonatal brain injury.
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spelling pubmed-87304122022-01-06 Neonatal brain injury influences structural connectivity and childhood functional outcomes Ramirez, Alice Peyvandi, Shabnam Cox, Stephany Gano, Dawn Xu, Duan Tymofiyeva, Olga McQuillen, Patrick S. PLoS One Research Article Neonatal brain injury may impact brain development and lead to lifelong functional impairments. Hypoxic-ischemic encephalopathy (HIE) and congenital heart disease (CHD) are two common causes of neonatal brain injury differing in timing and mechanism. Maturation of whole-brain neural networks can be quantified during development using diffusion magnetic resonance imaging (dMRI) in combination with graph theory metrics. DMRI of 35 subjects with CHD and 62 subjects with HIE were compared to understand differences in the effects of HIE and CHD on the development of network topological parameters and functional outcomes. CHD newborns had worse 12–18 month language (P<0.01) and 30 month cognitive (P<0.01), language (P = 0.05), motor outcomes (P = 0.01). Global efficiency, a metric of brain integration, was lower in CHD (P = 0.03) than in HIE, but transitivity, modularity and small-worldness were similar. After controlling for clinical factors known to affect neurodevelopmental outcomes, we observed that global efficiency was highly associated with 30 month motor outcomes (P = 0.02) in both groups. To explore neural correlates of adverse language outcomes in CHD, we used hypothesis-based and data-driven approaches to identify pathways with altered structural connectivity. We found that connectivity strength in the superior longitudinal fasciculus (SLF) tract 2 was inversely associated with expressive language. After false discovery rate correction, a whole connectome edge analysis identified 18 pathways that were hypoconnected in the CHD cohort as compared to HIE. In sum, our study shows that neonatal structural connectivity predicts early motor development after HIE or in subjects with CHD, and regional SLF connectivity is associated with language outcomes. Further research is needed to determine if and how brain networks change over time and whether those changes represent recovery or ongoing dysfunction. This knowledge will directly inform strategies to optimize neurologic functional outcomes after neonatal brain injury. Public Library of Science 2022-01-05 /pmc/articles/PMC8730412/ /pubmed/34986206 http://dx.doi.org/10.1371/journal.pone.0262310 Text en © 2022 Ramirez et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ramirez, Alice
Peyvandi, Shabnam
Cox, Stephany
Gano, Dawn
Xu, Duan
Tymofiyeva, Olga
McQuillen, Patrick S.
Neonatal brain injury influences structural connectivity and childhood functional outcomes
title Neonatal brain injury influences structural connectivity and childhood functional outcomes
title_full Neonatal brain injury influences structural connectivity and childhood functional outcomes
title_fullStr Neonatal brain injury influences structural connectivity and childhood functional outcomes
title_full_unstemmed Neonatal brain injury influences structural connectivity and childhood functional outcomes
title_short Neonatal brain injury influences structural connectivity and childhood functional outcomes
title_sort neonatal brain injury influences structural connectivity and childhood functional outcomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8730412/
https://www.ncbi.nlm.nih.gov/pubmed/34986206
http://dx.doi.org/10.1371/journal.pone.0262310
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