Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot

Abstract Background: Cognitive impairment is the most common long‐term complication in children with congenital heart disease (CHD) and is closely related to the brain network. However, little is known about the impact of CHD on brain network organization. This study aims to investigate brain struct...

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Main Authors: Yuting Liu, Liang Hu, Meijiao Zhu, Jingjing Zhong, Mingcui Fu, Mingwen Yang, Shuting Cheng, Ying Wang, Xuming Mo, Ming Yang
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Brain and Behavior
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Online Access:https://doi.org/10.1002/brb3.70153
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author Yuting Liu
Liang Hu
Meijiao Zhu
Jingjing Zhong
Mingcui Fu
Mingwen Yang
Shuting Cheng
Ying Wang
Xuming Mo
Ming Yang
author_facet Yuting Liu
Liang Hu
Meijiao Zhu
Jingjing Zhong
Mingcui Fu
Mingwen Yang
Shuting Cheng
Ying Wang
Xuming Mo
Ming Yang
author_sort Yuting Liu
collection DOAJ
description Abstract Background: Cognitive impairment is the most common long‐term complication in children with congenital heart disease (CHD) and is closely related to the brain network. However, little is known about the impact of CHD on brain network organization. This study aims to investigate brain structural network properties that may underpin cognitive deficits observed in children with Tetralogy of Fallot (TOF). Methods: In this prospective study, 29 preschool‐aged children diagnosed with TOF and 19 without CHD (non‐CHD) were enrolled. Participants underwent diffusion tensor imaging (DTI) scans alongside cognitive assessment using the Chinese version of the Wechsler Preschool and Primary Scale of Intelligence—fourth edition (WPPSI‐IV). We constructed a brain structural network based on DTI and applied graph analysis methodology to investigate alterations in diverse network topological properties in TOF compared with non‐CHD. Additionally, we explored the correlation between brain network topology and cognitive performance in TOF. Results: Although both TOF and non‐CHD exhibited small‐world characteristics in their brain networks, children with TOF significantly demonstrated increased characteristic path length and decreased clustering coefficient, global efficiency, and local efficiency compared with non‐CHD (p < 0.05). Regionally, reduced nodal betweenness and degree were found in the left cingulate gyrus, and nodal efficiency was decreased in the right precentral gyrus and cingulate gyrus, left inferior frontal gyrus (triangular part), and insula (p < 0.05). Furthermore, a positive correlation was identified between local efficiency and cognitive performance (p < 0.05). Conclusion: This study elucidates a disrupted brain structural network characterized by impaired integration and segregation in preschool TOF, correlating with cognitive performance. These findings indicated that the brain structural network may be a promising imaging biomarker and potential target for neurobehavioral interventions aimed at improving brain development and preventing lasting impairments across the lifetime.
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publishDate 2024-11-01
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spelling doaj-art-7d1a9b4a052446498c9ee7f74abcc4a62024-11-28T14:22:33ZengWileyBrain and Behavior2162-32792024-11-011411n/an/a10.1002/brb3.70153Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of FallotYuting Liu0Liang Hu1Meijiao Zhu2Jingjing Zhong3Mingcui Fu4Mingwen Yang5Shuting Cheng6Ying Wang7Xuming Mo8Ming Yang9Department of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Cardiothoracic Surgery Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Cardiothoracic Surgery Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaDepartment of Radiology Children's Hospital of Nanjing Medical University Nanjing Jiangsu Province ChinaAbstract Background: Cognitive impairment is the most common long‐term complication in children with congenital heart disease (CHD) and is closely related to the brain network. However, little is known about the impact of CHD on brain network organization. This study aims to investigate brain structural network properties that may underpin cognitive deficits observed in children with Tetralogy of Fallot (TOF). Methods: In this prospective study, 29 preschool‐aged children diagnosed with TOF and 19 without CHD (non‐CHD) were enrolled. Participants underwent diffusion tensor imaging (DTI) scans alongside cognitive assessment using the Chinese version of the Wechsler Preschool and Primary Scale of Intelligence—fourth edition (WPPSI‐IV). We constructed a brain structural network based on DTI and applied graph analysis methodology to investigate alterations in diverse network topological properties in TOF compared with non‐CHD. Additionally, we explored the correlation between brain network topology and cognitive performance in TOF. Results: Although both TOF and non‐CHD exhibited small‐world characteristics in their brain networks, children with TOF significantly demonstrated increased characteristic path length and decreased clustering coefficient, global efficiency, and local efficiency compared with non‐CHD (p < 0.05). Regionally, reduced nodal betweenness and degree were found in the left cingulate gyrus, and nodal efficiency was decreased in the right precentral gyrus and cingulate gyrus, left inferior frontal gyrus (triangular part), and insula (p < 0.05). Furthermore, a positive correlation was identified between local efficiency and cognitive performance (p < 0.05). Conclusion: This study elucidates a disrupted brain structural network characterized by impaired integration and segregation in preschool TOF, correlating with cognitive performance. These findings indicated that the brain structural network may be a promising imaging biomarker and potential target for neurobehavioral interventions aimed at improving brain development and preventing lasting impairments across the lifetime.https://doi.org/10.1002/brb3.70153brain structural networkcongenital heart diseasecognitive impairmentdiffusion tensor imagingtetralogy of fallot
spellingShingle Yuting Liu
Liang Hu
Meijiao Zhu
Jingjing Zhong
Mingcui Fu
Mingwen Yang
Shuting Cheng
Ying Wang
Xuming Mo
Ming Yang
Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot
Brain and Behavior
brain structural network
congenital heart disease
cognitive impairment
diffusion tensor imaging
tetralogy of fallot
title Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot
title_full Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot
title_fullStr Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot
title_full_unstemmed Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot
title_short Disrupted White Matter Topology Organization in Preschool Children with Tetralogy of Fallot
title_sort disrupted white matter topology organization in preschool children with tetralogy of fallot
topic brain structural network
congenital heart disease
cognitive impairment
diffusion tensor imaging
tetralogy of fallot
url https://doi.org/10.1002/brb3.70153
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