Patterns of brain atrophy in recently-diagnosed relapsing-remitting multiple sclerosis.
Journal
PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081
Informations de publication
Date de publication:
2023
2023
Historique:
received:
07
11
2022
accepted:
07
07
2023
medline:
31
7
2023
pubmed:
28
7
2023
entrez:
28
7
2023
Statut:
epublish
Résumé
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.
Identifiants
pubmed: 37506096
doi: 10.1371/journal.pone.0288967
pii: PONE-D-22-30246
pmc: PMC10381059
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0288967Subventions
Organisme : Chief Scientist Office
ID : SMS_IC010
Pays : United Kingdom
Organisme : Chief Scientist Office
ID : MMPP/01
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 215621/Z/19/Z
Pays : United Kingdom
Organisme : Medical Research Council
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 104916/Z/14/Z
Pays : United Kingdom
Informations de copyright
Copyright: © 2023 Meijboom et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
J Neurol. 2007 Sep;254(9):1212-20
pubmed: 17361339
J Neurol Sci. 2009 Jul 15;282(1-2):47-54
pubmed: 19201003
J Neurol Neurosurg Psychiatry. 2020 May;91(5):493-502
pubmed: 32111638
Cold Spring Harb Perspect Med. 2018 Mar 1;8(3):
pubmed: 29358320
Lancet Neurol. 2019 Mar;18(3):269-285
pubmed: 30679040
Front Neurol. 2020 Jul 15;11:606
pubmed: 32760339
Front Neurol. 2018 Oct 29;9:920
pubmed: 30420834
Neuroimage. 2006 Feb 1;29(3):859-67
pubmed: 16203159
Hum Brain Mapp. 2016 May;37(5):1866-79
pubmed: 26920497
Int J MS Care. 2013 Fall;15(3):146-58
pubmed: 24453777
Neuroimage. 2009 Jan 1;44(1):83-98
pubmed: 18501637
J Neuroimaging. 2018 Jul;28(4):399-405
pubmed: 29749661
Neuroimage. 2000 Jun;11(6 Pt 1):805-21
pubmed: 10860804
Eur J Neurol. 2020 Mar;27(3):454-460
pubmed: 31696586
Brain. 2020 Jul 1;143(7):2089-2105
pubmed: 32572488
Front Neurosci. 2022 Mar 02;16:837452
pubmed: 35310094
J Neurol Sci. 2012 Jan 15;312(1-2):7-12
pubmed: 21920559
Eur J Neurol. 2020 Dec;27(12):2549-2560
pubmed: 32780554
Neurobiol Aging. 2019 Sep;81:30-37
pubmed: 31207467
Neurology. 2011 Mar 29;76(13):1161-7
pubmed: 21444901
J Neurol Sci. 2016 Jul 15;366:229-233
pubmed: 27288812
Neuroimage. 2014 May 15;92:381-97
pubmed: 24530839
Neurotherapeutics. 2020 Jan;17(1):208-217
pubmed: 31452082
J Neurol. 2021 Dec;268(12):4698-4706
pubmed: 33942160
J Neurol Sci. 2018 May 15;388:87-93
pubmed: 29627038
Lancet Neurol. 2018 Feb;17(2):162-173
pubmed: 29275977
Neuroimage. 2012 Jul 16;61(4):1402-18
pubmed: 22430496
J Neurol. 2012 Jan;259(1):139-46
pubmed: 21720932
Brain. 2003 Aug;126(Pt 8):1734-44
pubmed: 12805100
Brain Behav. 2021 Apr;11(4):e02050
pubmed: 33506628
Mult Scler. 2015 Apr;21(4):402-14
pubmed: 25139946
Mult Scler Relat Disord. 2021 Apr;49:102785
pubmed: 33508572
Neurology. 2014 Jul 15;83(3):278-86
pubmed: 24871874
Neuroimage. 2018 Apr 15;170:348-364
pubmed: 28279814
Neurol Sci. 2020 Oct;41(10):2893-2904
pubmed: 32333180
Cerebellum. 2021 Feb;20(1):92-100
pubmed: 32970313
Med Image Anal. 2001 Jun;5(2):143-56
pubmed: 11516708
Arch Clin Neuropsychol. 2021 May 21;36(4):517-526
pubmed: 33067615
Hum Brain Mapp. 2002 Nov;17(3):143-55
pubmed: 12391568
Brain. 2018 Jun 1;141(6):1665-1677
pubmed: 29741648
Hum Brain Mapp. 2020 Mar;41(4):917-927
pubmed: 32026599
J Neurol Neurosurg Psychiatry. 2021 Mar 30;:
pubmed: 33785581
Neuroimage Clin. 2014 Mar 03;6:475-87
pubmed: 25610761
Mult Scler. 2019 Apr;25(4):574-584
pubmed: 29512427
Neuroimage. 2001 Jul;14(1 Pt 1):21-36
pubmed: 11525331
Hum Brain Mapp. 2018 Apr;39(4):1814-1824
pubmed: 29331060
Auto Immun Highlights. 2019 Aug 10;10(1):7
pubmed: 32257063
J Neurol Sci. 2018 May 15;388:175-181
pubmed: 29627017
Wellcome Open Res. 2022 Mar 16;7:94
pubmed: 36865371
J Neurol Sci. 2017 Dec 15;383:221-229
pubmed: 29146095
Prion. 2013 Jan-Feb;7(1):20-7
pubmed: 23093801
Neuroimage. 2006 Jul 1;31(3):968-80
pubmed: 16530430
Nat Rev Neurol. 2020 Mar;16(3):171-182
pubmed: 32094485
Front Neurol. 2020 Jun 30;11:529
pubmed: 32695059
Brain. 2021 Aug 17;144(7):1974-1984
pubmed: 33757115
J Neurol Sci. 2009 Jul 15;282(1-2):106-11
pubmed: 19100997
Brain. 2002 Feb;125(Pt 2):327-37
pubmed: 11844733
Neuroimage. 2004;23 Suppl 1:S208-19
pubmed: 15501092
J Neurol Sci. 2019 Aug 15;403:78-84
pubmed: 31233973
Mult Scler Relat Disord. 2020 Apr;39:101899
pubmed: 31884385
Mult Scler. 2017 Sep;23(10):1358-1366
pubmed: 28273767
Neuroimage. 2002 Oct;17(2):825-41
pubmed: 12377157
Mult Scler. 2020 Mar;26(3):312-321
pubmed: 30741108
Eur J Radiol. 2013 Feb;82(2):e95-9
pubmed: 23079047
Mult Scler. 2003 Feb;9(1):21-7
pubmed: 12617263
Neuroimage Clin. 2021;29:102550
pubmed: 33418173
Mult Scler Relat Disord. 2015 May;4(3):264-72
pubmed: 26008944
Brain Sci. 2020 Oct 30;10(11):
pubmed: 33143012
Front Neurol. 2019 Jan 23;9:1172
pubmed: 30728801
J Neurol Sci. 2009 Jul 15;282(1-2):112-9
pubmed: 19168190
N Engl J Med. 2018 Jan 11;378(2):169-180
pubmed: 29320652
Front Neurol. 2018 Oct 11;9:824
pubmed: 30364223
Hum Brain Mapp. 2017 Nov;38(11):5648-5665
pubmed: 28792103
Brain. 2007 Sep;130(Pt 9):2375-86
pubmed: 17698497
JAMA. 2021 Feb 23;325(8):765-779
pubmed: 33620411
J Neurol Neurosurg Psychiatry. 2001 Jun;70(6):773-80
pubmed: 11385012
Neuroimage Clin. 2018 Apr 24;19:633-639
pubmed: 29984171
Neuroimage Clin. 2017 Nov 05;17:444-451
pubmed: 29159057
J Neurol. 2020 Feb;267(2):395-405
pubmed: 31654116
Neuroimage. 2006 Jul 1;31(3):1116-28
pubmed: 16545965
Mult Scler. 2009 Jul;15(7):811-7
pubmed: 19465449
Front Neurol. 2019 Nov 05;10:1165
pubmed: 31749760
Brain Struct Funct. 2013 Jul;218(4):943-50
pubmed: 22790785
Brain. 2021 Jun 22;144(5):1384-1395
pubmed: 33880511
Neurology. 2013 Jan 8;80(2):210-9
pubmed: 23296131