Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline

Purpose: There is a high correlation between white matter hyperintensity (WMH) and cognitive impairment (CI) in elderly people. However, not all WMH will develop into CI, and the potential mechanism of WMH-related CI is still unclear. This study aimed to investigate the topological properties of whi...

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Main Authors: Dan Yang, Lili Huang, Caimei Luo, Mengchun Li, Ruomeng Qin, Junyi Ma, Pengfei Shao, Hengheng Xu, Bing Zhang, Yun Xu, Meijuan Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fneur.2020.00250/full
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author Dan Yang
Dan Yang
Dan Yang
Dan Yang
Lili Huang
Lili Huang
Lili Huang
Lili Huang
Caimei Luo
Caimei Luo
Caimei Luo
Caimei Luo
Mengchun Li
Mengchun Li
Mengchun Li
Mengchun Li
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Junyi Ma
Junyi Ma
Junyi Ma
Junyi Ma
Pengfei Shao
Pengfei Shao
Pengfei Shao
Pengfei Shao
Hengheng Xu
Hengheng Xu
Hengheng Xu
Hengheng Xu
Bing Zhang
Yun Xu
Yun Xu
Yun Xu
Yun Xu
Meijuan Zhang
Meijuan Zhang
Meijuan Zhang
Meijuan Zhang
author_facet Dan Yang
Dan Yang
Dan Yang
Dan Yang
Lili Huang
Lili Huang
Lili Huang
Lili Huang
Caimei Luo
Caimei Luo
Caimei Luo
Caimei Luo
Mengchun Li
Mengchun Li
Mengchun Li
Mengchun Li
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Junyi Ma
Junyi Ma
Junyi Ma
Junyi Ma
Pengfei Shao
Pengfei Shao
Pengfei Shao
Pengfei Shao
Hengheng Xu
Hengheng Xu
Hengheng Xu
Hengheng Xu
Bing Zhang
Yun Xu
Yun Xu
Yun Xu
Yun Xu
Meijuan Zhang
Meijuan Zhang
Meijuan Zhang
Meijuan Zhang
author_sort Dan Yang
collection DOAJ
description Purpose: There is a high correlation between white matter hyperintensity (WMH) and cognitive impairment (CI) in elderly people. However, not all WMH will develop into CI, and the potential mechanism of WMH-related CI is still unclear. This study aimed to investigate the topological properties of white matter structural network in WMH-related CI.Methods: Forty-one WMH subjects with CI (WMH-CI), 42 WMH subjects without CI (WMH-no-CI), and 52 elderly healthy controls (HC) were recruited. Diffusion tensor imaging (DTI) fiber tractography and graph theoretical analysis were applied to construct the structural network. We compared network properties and clinical features among the three groups. Multiple linear regression analysis was performed to investigate the relationships among WMH volumes, impaired network properties, and cognitive functions in the WMH-CI group.Results: Compared with the controls, both WMH groups showed decreased network strength, global efficiency, and increased characteristic path length (Lp) at the level of the whole brain. The WMH-CI group displayed more profound impairments of nodal efficiency and nodal path length (NLp) within multiple regions including precentral, cingulate, and medial temporal gyrus. The disrupted network properties were associated with CI and WMH burdens in the WMH-CI group. Furthermore, a mediation effect of NLp in the left inferior frontal gyrus was observed for the association between periventricular WMH (PWMH) and memory deficit.Conclusions: Brain structural network in WMH-CI is significantly disturbed, and this disturbance is related to the severity of WMH and CI. Increased NLp in the left opercular part of inferior frontal gyrus (IFGoperc.L) was shown to be a mediation framework between PWMH and WMH-related memory, which shed light on investigating the underlying mechanisms of CI caused by WMH.
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spelling doaj.art-9d6b4cf63f434a358f22cccf3a5c27282022-12-22T03:02:13ZengFrontiers Media S.A.Frontiers in Neurology1664-22952020-04-011110.3389/fneur.2020.00250506950Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive DeclineDan Yang0Dan Yang1Dan Yang2Dan Yang3Lili Huang4Lili Huang5Lili Huang6Lili Huang7Caimei Luo8Caimei Luo9Caimei Luo10Caimei Luo11Mengchun Li12Mengchun Li13Mengchun Li14Mengchun Li15Ruomeng Qin16Ruomeng Qin17Ruomeng Qin18Ruomeng Qin19Junyi Ma20Junyi Ma21Junyi Ma22Junyi Ma23Pengfei Shao24Pengfei Shao25Pengfei Shao26Pengfei Shao27Hengheng Xu28Hengheng Xu29Hengheng Xu30Hengheng Xu31Bing Zhang32Yun Xu33Yun Xu34Yun Xu35Yun Xu36Meijuan Zhang37Meijuan Zhang38Meijuan Zhang39Meijuan Zhang40Department of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Radiology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Drum Tower Hospital, Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Key Laboratory for Molecular Medicine, Medical School of Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaPurpose: There is a high correlation between white matter hyperintensity (WMH) and cognitive impairment (CI) in elderly people. However, not all WMH will develop into CI, and the potential mechanism of WMH-related CI is still unclear. This study aimed to investigate the topological properties of white matter structural network in WMH-related CI.Methods: Forty-one WMH subjects with CI (WMH-CI), 42 WMH subjects without CI (WMH-no-CI), and 52 elderly healthy controls (HC) were recruited. Diffusion tensor imaging (DTI) fiber tractography and graph theoretical analysis were applied to construct the structural network. We compared network properties and clinical features among the three groups. Multiple linear regression analysis was performed to investigate the relationships among WMH volumes, impaired network properties, and cognitive functions in the WMH-CI group.Results: Compared with the controls, both WMH groups showed decreased network strength, global efficiency, and increased characteristic path length (Lp) at the level of the whole brain. The WMH-CI group displayed more profound impairments of nodal efficiency and nodal path length (NLp) within multiple regions including precentral, cingulate, and medial temporal gyrus. The disrupted network properties were associated with CI and WMH burdens in the WMH-CI group. Furthermore, a mediation effect of NLp in the left inferior frontal gyrus was observed for the association between periventricular WMH (PWMH) and memory deficit.Conclusions: Brain structural network in WMH-CI is significantly disturbed, and this disturbance is related to the severity of WMH and CI. Increased NLp in the left opercular part of inferior frontal gyrus (IFGoperc.L) was shown to be a mediation framework between PWMH and WMH-related memory, which shed light on investigating the underlying mechanisms of CI caused by WMH.https://www.frontiersin.org/article/10.3389/fneur.2020.00250/fullwhite matter hyperintensitycognitive impairmentwhite matter networkgraph theoretical analysisdiffusion tensor imaging (DTI)
spellingShingle Dan Yang
Dan Yang
Dan Yang
Dan Yang
Lili Huang
Lili Huang
Lili Huang
Lili Huang
Caimei Luo
Caimei Luo
Caimei Luo
Caimei Luo
Mengchun Li
Mengchun Li
Mengchun Li
Mengchun Li
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Junyi Ma
Junyi Ma
Junyi Ma
Junyi Ma
Pengfei Shao
Pengfei Shao
Pengfei Shao
Pengfei Shao
Hengheng Xu
Hengheng Xu
Hengheng Xu
Hengheng Xu
Bing Zhang
Yun Xu
Yun Xu
Yun Xu
Yun Xu
Meijuan Zhang
Meijuan Zhang
Meijuan Zhang
Meijuan Zhang
Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline
Frontiers in Neurology
white matter hyperintensity
cognitive impairment
white matter network
graph theoretical analysis
diffusion tensor imaging (DTI)
title Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline
title_full Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline
title_fullStr Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline
title_full_unstemmed Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline
title_short Impaired Structural Network Properties Caused by White Matter Hyperintensity Related to Cognitive Decline
title_sort impaired structural network properties caused by white matter hyperintensity related to cognitive decline
topic white matter hyperintensity
cognitive impairment
white matter network
graph theoretical analysis
diffusion tensor imaging (DTI)
url https://www.frontiersin.org/article/10.3389/fneur.2020.00250/full
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