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Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis

Recurrent neuroinflammation in relapsing-remitting MS (RRMS) is thought to lead to neurodegeneration, resulting in progressive disability. Repeated magnetic resonance imaging (MRI) of the brain provides non-invasive measures of atrophy over time, a key marker of neurodegeneration. This study investi...

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Autores principales: Meijboom, Rozanna, York, Elizabeth N., Kampaite, Agniete, Harris, Mathew A., White, Nicole, Valdés Hernández, Maria del C., Thrippleton, Michael J., MacDougall, N. J. J., Connick, Peter, Hunt, David P. J., Chandran, Siddharthan, Waldman, Adam D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10381059/
https://www.ncbi.nlm.nih.gov/pubmed/37506096
http://dx.doi.org/10.1371/journal.pone.0288967
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author Meijboom, Rozanna
York, Elizabeth N.
Kampaite, Agniete
Harris, Mathew A.
White, Nicole
Valdés Hernández, Maria del C.
Thrippleton, Michael J.
MacDougall, N. J. J.
Connick, Peter
Hunt, David P. J.
Chandran, Siddharthan
Waldman, Adam D.
author_facet Meijboom, Rozanna
York, Elizabeth N.
Kampaite, Agniete
Harris, Mathew A.
White, Nicole
Valdés Hernández, Maria del C.
Thrippleton, Michael J.
MacDougall, N. J. J.
Connick, Peter
Hunt, David P. J.
Chandran, Siddharthan
Waldman, Adam D.
author_sort Meijboom, Rozanna
collection PubMed
description Recurrent neuroinflammation in relapsing-remitting MS (RRMS) is thought to lead to neurodegeneration, resulting in progressive disability. Repeated magnetic resonance imaging (MRI) of the brain provides non-invasive measures of atrophy over time, a key marker of neurodegeneration. This study investigates regional neurodegeneration of the brain in recently-diagnosed RRMS using volumetry and voxel-based morphometry (VBM). RRMS patients (N = 354) underwent 3T structural MRI <6 months after diagnosis and 1-year follow-up, as part of the Scottish multicentre ‘FutureMS’ study. MRI data were processed using FreeSurfer to derive volumetrics, and FSL for VBM (grey matter (GM) only), to establish regional patterns of change in GM and normal-appearing white matter (NAWM) over time throughout the brain. Volumetric analyses showed a decrease over time (q<0.05) in bilateral cortical GM and NAWM, cerebellar GM, brainstem, amygdala, basal ganglia, hippocampus, accumbens, thalamus and ventral diencephalon. Additionally, NAWM and GM volume decreased respectively in the following cortical regions, frontal: 14 out of 26 regions and 16/26; temporal: 18/18 and 15/18; parietal: 14/14 and 11/14; occipital: 7/8 and 8/8. Left GM and NAWM asymmetry was observed in the frontal lobe. GM VBM analysis showed three major clusters of decrease over time: 1) temporal and subcortical areas, 2) cerebellum, 3) anterior cingulum and supplementary motor cortex; and four smaller clusters within the occipital lobe. Widespread GM and NAWM atrophy was observed in this large recently-diagnosed RRMS cohort, particularly in the brainstem, cerebellar GM, and subcortical and occipital-temporal regions; indicative of neurodegeneration across tissue types, and in accord with limited previous studies in early disease. Volumetric and VBM results emphasise different features of longitudinal lobar and loco-regional change, however identify consistent atrophy patterns across individuals. Atrophy measures targeted to specific brain regions may provide improved markers of neurodegeneration, and potential future imaging stratifiers and endpoints for clinical decision making and therapeutic trials.
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spelling pubmed-103810592023-07-29 Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis Meijboom, Rozanna York, Elizabeth N. Kampaite, Agniete Harris, Mathew A. White, Nicole Valdés Hernández, Maria del C. Thrippleton, Michael J. MacDougall, N. J. J. Connick, Peter Hunt, David P. J. Chandran, Siddharthan Waldman, Adam D. PLoS One Research Article Recurrent neuroinflammation in relapsing-remitting MS (RRMS) is thought to lead to neurodegeneration, resulting in progressive disability. Repeated magnetic resonance imaging (MRI) of the brain provides non-invasive measures of atrophy over time, a key marker of neurodegeneration. This study investigates regional neurodegeneration of the brain in recently-diagnosed RRMS using volumetry and voxel-based morphometry (VBM). RRMS patients (N = 354) underwent 3T structural MRI <6 months after diagnosis and 1-year follow-up, as part of the Scottish multicentre ‘FutureMS’ study. MRI data were processed using FreeSurfer to derive volumetrics, and FSL for VBM (grey matter (GM) only), to establish regional patterns of change in GM and normal-appearing white matter (NAWM) over time throughout the brain. Volumetric analyses showed a decrease over time (q<0.05) in bilateral cortical GM and NAWM, cerebellar GM, brainstem, amygdala, basal ganglia, hippocampus, accumbens, thalamus and ventral diencephalon. Additionally, NAWM and GM volume decreased respectively in the following cortical regions, frontal: 14 out of 26 regions and 16/26; temporal: 18/18 and 15/18; parietal: 14/14 and 11/14; occipital: 7/8 and 8/8. Left GM and NAWM asymmetry was observed in the frontal lobe. GM VBM analysis showed three major clusters of decrease over time: 1) temporal and subcortical areas, 2) cerebellum, 3) anterior cingulum and supplementary motor cortex; and four smaller clusters within the occipital lobe. Widespread GM and NAWM atrophy was observed in this large recently-diagnosed RRMS cohort, particularly in the brainstem, cerebellar GM, and subcortical and occipital-temporal regions; indicative of neurodegeneration across tissue types, and in accord with limited previous studies in early disease. Volumetric and VBM results emphasise different features of longitudinal lobar and loco-regional change, however identify consistent atrophy patterns across individuals. Atrophy measures targeted to specific brain regions may provide improved markers of neurodegeneration, and potential future imaging stratifiers and endpoints for clinical decision making and therapeutic trials. Public Library of Science 2023-07-28 /pmc/articles/PMC10381059/ /pubmed/37506096 http://dx.doi.org/10.1371/journal.pone.0288967 Text en © 2023 Meijboom 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
Meijboom, Rozanna
York, Elizabeth N.
Kampaite, Agniete
Harris, Mathew A.
White, Nicole
Valdés Hernández, Maria del C.
Thrippleton, Michael J.
MacDougall, N. J. J.
Connick, Peter
Hunt, David P. J.
Chandran, Siddharthan
Waldman, Adam D.
Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
title Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
title_full Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
title_fullStr Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
title_full_unstemmed Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
title_short Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
title_sort patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10381059/
https://www.ncbi.nlm.nih.gov/pubmed/37506096
http://dx.doi.org/10.1371/journal.pone.0288967
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