Longitudinal changes in rich club organization and cognition in cerebral small vessel disease
Cerebral small vessel disease (SVD) is considered the most important vascular contributor to the development of cognitive impairment and dementia. There is increasing awareness that SVD exerts its clinical effects by disrupting white matter connections, predominantly disrupting connections between r...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2019-01-01
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| Series: | NeuroImage: Clinical |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S221315821930395X |
| _version_ | 1818504214043688960 |
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| author | Esther M.C. van Leijsen Ingeborg W.M. van Uden Mayra I. Bergkamp Helena M. van der Holst David G. Norris Jurgen A.H.R. Claassen Roy P.C. Kessels Frank-Erik de Leeuw Anil M. Tuladhar |
| author_facet | Esther M.C. van Leijsen Ingeborg W.M. van Uden Mayra I. Bergkamp Helena M. van der Holst David G. Norris Jurgen A.H.R. Claassen Roy P.C. Kessels Frank-Erik de Leeuw Anil M. Tuladhar |
| author_sort | Esther M.C. van Leijsen |
| collection | DOAJ |
| description | Cerebral small vessel disease (SVD) is considered the most important vascular contributor to the development of cognitive impairment and dementia. There is increasing awareness that SVD exerts its clinical effects by disrupting white matter connections, predominantly disrupting connections between rich club nodes, a set of highly connected and interconnected regions. Here we examined the progression of disturbances in rich club organization in older adults with SVD and their associations with conventional SVD markers and cognitive decline. We additionally investigated associations of baseline network measures with dementia. In 270 participants of the RUN DMC study, we performed diffusion tensor imaging (DTI) and cognitive assessments longitudinally. Rich club organization was examined in structural networks derived from DTI followed by deterministic tractography. Global efficiency (p<0.05) and strength of rich club connections (p<0.001) declined during follow-up. Decline in strength of peripheral connections was associated with a decline in overall cognition (β=0.164; p<0.01), psychomotor speed (β=0.151; p<0.05) and executive function (β=0.117; p<0.05). Baseline network measures were reduced in participants with dementia, and the association between WMH and dementia was causally mediated by global efficiency (p = =0.037) and peripheral connection strength (p = =0.040). SVD-related disturbances in rich club organization progressed over time, predominantly in participants with severe SVD. In this study, we found no specific role of rich club connectivity disruption in causing cognitive decline or dementia. The effect of WMH on dementia was mediated by global network efficiency and the strength of peripheral connections, suggesting an important role for network disruption in causing cognitive decline and dementia in older adults with SVD. Keywords: Cerebral small vessel disease, Structural neuroimaging, Diffusion tensor imaging, Cognitive decline, Dementia, Rich club organization |
| first_indexed | 2024-12-10T21:34:10Z |
| format | Article |
| id | doaj.art-6b8d21eaeacf46b0b209d39fe9eea9e7 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-10T21:34:10Z |
| publishDate | 2019-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-6b8d21eaeacf46b0b209d39fe9eea9e72022-12-22T01:32:41ZengElsevierNeuroImage: Clinical2213-15822019-01-0124Longitudinal changes in rich club organization and cognition in cerebral small vessel diseaseEsther M.C. van Leijsen0Ingeborg W.M. van Uden1Mayra I. Bergkamp2Helena M. van der Holst3David G. Norris4Jurgen A.H.R. Claassen5Roy P.C. Kessels6Frank-Erik de Leeuw7Anil M. Tuladhar8Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, the NetherlandsDepartment of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, the NetherlandsDepartment of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, the NetherlandsDepartment of Neurology, Jeroen Bosch Ziekenhuis, ’s-Hertogenbosch, the NetherlandsRadboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Nijmegen, the Netherlands; Erwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyDepartment of Geriatric Medicine, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Radboud Alzheimer Centre, Nijmegen, the NetherlandsDepartment of Medical Psychology, Radboud university medical centre, Radboud Alzheimer Centre, Nijmegen, the Netherlands; Radboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognition, Nijmegen, the NetherlandsDepartment of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, the NetherlandsDepartment of Neurology, Donders Institute for Brain, Cognition and Behaviour, Donders Center for Medical Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands; Corresponding author at: Radboudumc, Department of Neurology, PO-box 9101, HP 935, 6500HB Nijmegen, the Netherlands.Cerebral small vessel disease (SVD) is considered the most important vascular contributor to the development of cognitive impairment and dementia. There is increasing awareness that SVD exerts its clinical effects by disrupting white matter connections, predominantly disrupting connections between rich club nodes, a set of highly connected and interconnected regions. Here we examined the progression of disturbances in rich club organization in older adults with SVD and their associations with conventional SVD markers and cognitive decline. We additionally investigated associations of baseline network measures with dementia. In 270 participants of the RUN DMC study, we performed diffusion tensor imaging (DTI) and cognitive assessments longitudinally. Rich club organization was examined in structural networks derived from DTI followed by deterministic tractography. Global efficiency (p<0.05) and strength of rich club connections (p<0.001) declined during follow-up. Decline in strength of peripheral connections was associated with a decline in overall cognition (β=0.164; p<0.01), psychomotor speed (β=0.151; p<0.05) and executive function (β=0.117; p<0.05). Baseline network measures were reduced in participants with dementia, and the association between WMH and dementia was causally mediated by global efficiency (p = =0.037) and peripheral connection strength (p = =0.040). SVD-related disturbances in rich club organization progressed over time, predominantly in participants with severe SVD. In this study, we found no specific role of rich club connectivity disruption in causing cognitive decline or dementia. The effect of WMH on dementia was mediated by global network efficiency and the strength of peripheral connections, suggesting an important role for network disruption in causing cognitive decline and dementia in older adults with SVD. Keywords: Cerebral small vessel disease, Structural neuroimaging, Diffusion tensor imaging, Cognitive decline, Dementia, Rich club organizationhttp://www.sciencedirect.com/science/article/pii/S221315821930395X |
| spellingShingle | Esther M.C. van Leijsen Ingeborg W.M. van Uden Mayra I. Bergkamp Helena M. van der Holst David G. Norris Jurgen A.H.R. Claassen Roy P.C. Kessels Frank-Erik de Leeuw Anil M. Tuladhar Longitudinal changes in rich club organization and cognition in cerebral small vessel disease NeuroImage: Clinical |
| title | Longitudinal changes in rich club organization and cognition in cerebral small vessel disease |
| title_full | Longitudinal changes in rich club organization and cognition in cerebral small vessel disease |
| title_fullStr | Longitudinal changes in rich club organization and cognition in cerebral small vessel disease |
| title_full_unstemmed | Longitudinal changes in rich club organization and cognition in cerebral small vessel disease |
| title_short | Longitudinal changes in rich club organization and cognition in cerebral small vessel disease |
| title_sort | longitudinal changes in rich club organization and cognition in cerebral small vessel disease |
| url | http://www.sciencedirect.com/science/article/pii/S221315821930395X |
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