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Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis

BACKGROUND: Reduced white matter (WM) integrity is a fundamental aspect of pediatric multiple sclerosis (MS), though relations to resting-state functional MRI (fMRI) connectivity remain unknown. The objective of this study was to relate diffusion-tensor imaging (DTI) measures of WM microstructural i...

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Autores principales: Akbar, Nadine, Giorgio, Antonio, Till, Christine, Sled, John G., Doesburg, Sam M., De Stefano, Nicola, Banwell, Brenda
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4701472/
https://www.ncbi.nlm.nih.gov/pubmed/26731278
http://dx.doi.org/10.1371/journal.pone.0145906
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author Akbar, Nadine
Giorgio, Antonio
Till, Christine
Sled, John G.
Doesburg, Sam M.
De Stefano, Nicola
Banwell, Brenda
author_facet Akbar, Nadine
Giorgio, Antonio
Till, Christine
Sled, John G.
Doesburg, Sam M.
De Stefano, Nicola
Banwell, Brenda
author_sort Akbar, Nadine
collection PubMed
description BACKGROUND: Reduced white matter (WM) integrity is a fundamental aspect of pediatric multiple sclerosis (MS), though relations to resting-state functional MRI (fMRI) connectivity remain unknown. The objective of this study was to relate diffusion-tensor imaging (DTI) measures of WM microstructural integrity to resting-state network (RSN) functional connectivity in pediatric-onset MS to test the hypothesis that abnormalities in RSN reflects changes in structural integrity. METHODS: This study enrolled 19 patients with pediatric-onset MS (mean age = 19, range 13–24 years, 14 female, mean disease duration = 65 months, mean age of disease onset = 13 years) and 16 age- and sex-matched healthy controls (HC). All subjects underwent 3.0T anatomical and functional MRI which included DTI and resting-state acquisitions. DTI processing was performed using Tract-Based Spatial Statistics (TBSS). RSNs were identified using Independent Components Analysis, and a dual regression technique was used to detect between-group differences in the functional connectivity of RSNs. Correlations were investigated between DTI measures and RSN connectivity. RESULTS: Lower fractional anisotropy (FA) was observed in the pediatric-onset MS group compared to HC group within the entire WM skeleton, and particularly the corpus callosum, posterior thalamic radiation, corona radiata and sagittal stratum (all p < .01, corrected). Relative to HCs, MS patients showed higher functional connectivity involving the anterior cingulate cortex and right precuneus of the default-mode network, as well as involving the anterior cingulate cortex and left middle frontal gyrus of the frontoparietal network (all p < .005 uncorrected, k≥30 voxels). Higher functional connectivity of the right precuneus within the default-mode network was associated with lower FA of the entire WM skeleton (r = -.525, p = .02), genu of the corpus callosum (r = -.553, p = .014), and left (r = -.467, p = .044) and right (r = -.615, p = .005) sagittal stratum. CONCLUSIONS: Loss of WM microstructural integrity is associated with increased resting-state functional connectivity in pediatric MS, which may reflect a diffuse and potentially compensatory activation early in MS.
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spelling pubmed-47014722016-01-15 Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis Akbar, Nadine Giorgio, Antonio Till, Christine Sled, John G. Doesburg, Sam M. De Stefano, Nicola Banwell, Brenda PLoS One Research Article BACKGROUND: Reduced white matter (WM) integrity is a fundamental aspect of pediatric multiple sclerosis (MS), though relations to resting-state functional MRI (fMRI) connectivity remain unknown. The objective of this study was to relate diffusion-tensor imaging (DTI) measures of WM microstructural integrity to resting-state network (RSN) functional connectivity in pediatric-onset MS to test the hypothesis that abnormalities in RSN reflects changes in structural integrity. METHODS: This study enrolled 19 patients with pediatric-onset MS (mean age = 19, range 13–24 years, 14 female, mean disease duration = 65 months, mean age of disease onset = 13 years) and 16 age- and sex-matched healthy controls (HC). All subjects underwent 3.0T anatomical and functional MRI which included DTI and resting-state acquisitions. DTI processing was performed using Tract-Based Spatial Statistics (TBSS). RSNs were identified using Independent Components Analysis, and a dual regression technique was used to detect between-group differences in the functional connectivity of RSNs. Correlations were investigated between DTI measures and RSN connectivity. RESULTS: Lower fractional anisotropy (FA) was observed in the pediatric-onset MS group compared to HC group within the entire WM skeleton, and particularly the corpus callosum, posterior thalamic radiation, corona radiata and sagittal stratum (all p < .01, corrected). Relative to HCs, MS patients showed higher functional connectivity involving the anterior cingulate cortex and right precuneus of the default-mode network, as well as involving the anterior cingulate cortex and left middle frontal gyrus of the frontoparietal network (all p < .005 uncorrected, k≥30 voxels). Higher functional connectivity of the right precuneus within the default-mode network was associated with lower FA of the entire WM skeleton (r = -.525, p = .02), genu of the corpus callosum (r = -.553, p = .014), and left (r = -.467, p = .044) and right (r = -.615, p = .005) sagittal stratum. CONCLUSIONS: Loss of WM microstructural integrity is associated with increased resting-state functional connectivity in pediatric MS, which may reflect a diffuse and potentially compensatory activation early in MS. Public Library of Science 2016-01-05 /pmc/articles/PMC4701472/ /pubmed/26731278 http://dx.doi.org/10.1371/journal.pone.0145906 Text en © 2016 Akbar et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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
Akbar, Nadine
Giorgio, Antonio
Till, Christine
Sled, John G.
Doesburg, Sam M.
De Stefano, Nicola
Banwell, Brenda
Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis
title Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis
title_full Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis
title_fullStr Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis
title_full_unstemmed Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis
title_short Alterations in Functional and Structural Connectivity in Pediatric-Onset Multiple Sclerosis
title_sort alterations in functional and structural connectivity in pediatric-onset multiple sclerosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4701472/
https://www.ncbi.nlm.nih.gov/pubmed/26731278
http://dx.doi.org/10.1371/journal.pone.0145906
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