The clinical and radiological profile of primary lateral sclerosis: a population-based study.


Journal

Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161

Informations de publication

Date de publication:
Nov 2019
Historique:
received: 02 07 2019
accepted: 11 07 2019
revised: 09 07 2019
pubmed: 22 7 2019
medline: 21 3 2020
entrez: 21 7 2019
Statut: ppublish

Résumé

Primary lateral sclerosis is a progressive upper-motor-neuron disorder associated with markedly longer survival than ALS. In contrast to ALS, the genetic susceptibility, histopathological profile and imaging signature of PLS are poorly characterised. Suspected PLS patients often face considerable diagnostic delay and prognostic uncertainty. To characterise the distinguishing clinical, genetic and imaging features of PLS in contrast to ALS and healthy controls. A prospective population-based study was conducted with 49 PLS patients, 100 ALS patients and 100 healthy controls using genetic profiling, standardised clinical assessments and neuroimaging. Whole-brain and region-of-interest analyses were undertaken to evaluate patterns of grey and white matter degeneration. In PLS, disease burden in the motor cortex is more medial than in ALS consistent with its lower limb symptom-predominance. PLS is associated with considerable cerebellar white and grey matter degeneration and the extra-motor profile of PLS includes marked insular, inferior frontal and left pars opercularis pathology. Contrary to ALS, PLS spares the postcentral gyrus. The body and splenium of the corpus callosum are preferentially affected in PLS, in contrast to the genu involvement observed in ALS. Clinical measures show anatomically meaningful correlations with imaging metrics in a somatotopic distribution. PLS patients tested negative for C9orf72 repeat expansions, known ALS and HSP-associated genes. Multiparametric imaging in PLS highlights disease-specific motor and extra-motor involvement distinct from ALS. In a condition where limited post-mortem data are available, imaging offers invaluable pathological insights. Anatomical correlations with clinical metrics confirm the biomarker potential of quantitative neuroimaging in PLS.

Sections du résumé

BACKGROUND BACKGROUND
Primary lateral sclerosis is a progressive upper-motor-neuron disorder associated with markedly longer survival than ALS. In contrast to ALS, the genetic susceptibility, histopathological profile and imaging signature of PLS are poorly characterised. Suspected PLS patients often face considerable diagnostic delay and prognostic uncertainty.
OBJECTIVE OBJECTIVE
To characterise the distinguishing clinical, genetic and imaging features of PLS in contrast to ALS and healthy controls.
METHODS METHODS
A prospective population-based study was conducted with 49 PLS patients, 100 ALS patients and 100 healthy controls using genetic profiling, standardised clinical assessments and neuroimaging. Whole-brain and region-of-interest analyses were undertaken to evaluate patterns of grey and white matter degeneration.
RESULTS RESULTS
In PLS, disease burden in the motor cortex is more medial than in ALS consistent with its lower limb symptom-predominance. PLS is associated with considerable cerebellar white and grey matter degeneration and the extra-motor profile of PLS includes marked insular, inferior frontal and left pars opercularis pathology. Contrary to ALS, PLS spares the postcentral gyrus. The body and splenium of the corpus callosum are preferentially affected in PLS, in contrast to the genu involvement observed in ALS. Clinical measures show anatomically meaningful correlations with imaging metrics in a somatotopic distribution. PLS patients tested negative for C9orf72 repeat expansions, known ALS and HSP-associated genes.
CONCLUSIONS CONCLUSIONS
Multiparametric imaging in PLS highlights disease-specific motor and extra-motor involvement distinct from ALS. In a condition where limited post-mortem data are available, imaging offers invaluable pathological insights. Anatomical correlations with clinical metrics confirm the biomarker potential of quantitative neuroimaging in PLS.

Identifiants

pubmed: 31325016
doi: 10.1007/s00415-019-09473-z
pii: 10.1007/s00415-019-09473-z
doi:

Substances chimiques

C9orf72 Protein 0
C9orf72 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2718-2733

Subventions

Organisme : Iris O'Brien Foundation
ID : 2016
Organisme : Motor Neurone Disease Association
ID : MCLAUGHLIN/OCT15/957-799
Pays : United Kingdom
Organisme : Health Research Board
ID : HRB EIA-2017-019
Pays : Ireland
Organisme : Science Foundation Ireland
ID : 15/SPP/3244
Pays : Ireland
Organisme : Science Foundation Ireland
ID : 17/CDA/4737
Pays : Ireland
Organisme : Andrew Lydon scholarship
ID : 2018
Organisme : Irish Institute of Clinical Neuroscience IICN
ID : 2016
Organisme : Research Motor Neuron
ID : 2017
Organisme : Motor Neurone Disease Association (GB)
ID : 957-799

Commentaires et corrections

Type : CommentIn

Références

Neuropathology. 2012 Aug;32(4):373-84
pubmed: 22098653
J Neurol Neurosurg Psychiatry. 2016 Jan;87(1):12-20
pubmed: 26296871
Neuroimage Clin. 2014 Dec 09;7:288-96
pubmed: 25610792
Amyotroph Lateral Scler Frontotemporal Degener. 2017 Feb;18(1-2):99-106
pubmed: 27894201
Cortex. 2010 Jul-Aug;46(7):831-44
pubmed: 20152963
Amyotroph Lateral Scler Frontotemporal Degener. 2018 Feb;19(1-2):12-20
pubmed: 29034720
Ann Neurol. 2013 Jul;74(1):20-38
pubmed: 23686809
J Neurol Neurosurg Psychiatry. 2015 Oct;86(10):1089-96
pubmed: 25632156
Neurology. 2013 Jul 23;81(4):361-9
pubmed: 23771489
J Neurol Sci. 1999 Oct 31;169(1-2):13-21
pubmed: 10540002
J Neurol. 2013 Nov;260(11):2856-64
pubmed: 23996101
Neuroimage Clin. 2017 Oct 14;17:145-152
pubmed: 29071208
Phys Ther. 1987 Feb;67(2):206-7
pubmed: 3809245
Eur J Hum Genet. 2018 Oct;26(10):1537-1546
pubmed: 29955173
Amyotroph Lateral Scler Frontotemporal Degener. 2013 Mar;14(2):141-5
pubmed: 22957717
Brain. 2011 Sep;134(Pt 9):2642-55
pubmed: 21798965
J Nucl Med. 2016 Aug;57(8):1238-43
pubmed: 26940764
PLoS One. 2013 Dec 05;8(12):e82017
pubmed: 24349172
Amyotroph Lateral Scler Frontotemporal Degener. 2018 Nov;19(7-8):562-569
pubmed: 30299161
Amyotroph Lateral Scler Frontotemporal Degener. 2018 Aug;19(5-6):463-465
pubmed: 29451027
Amyotroph Lateral Scler Other Motor Neuron Disord. 2000 Dec;1(5):293-9
pubmed: 11464847
J Neurol Neurosurg Psychiatry. 2015 Apr;86(4):468-70
pubmed: 25053771
Amyotroph Lateral Scler. 2009 Oct-Dec;10(5-6):339-46
pubmed: 19922121
Nature. 2016 Aug 17;536(7616):285-91
pubmed: 27535533
Neuroimage. 2005 May 15;26(1):132-40
pubmed: 15862213
Neuroimage Clin. 2017 Oct 25;17:347-353
pubmed: 29159046
Amyotroph Lateral Scler Frontotemporal Degener. 2018 Feb;19(1-2):4-6
pubmed: 29092641
Amyotroph Lateral Scler Frontotemporal Degener. 2014 Jun;15(3-4):235-43
pubmed: 24344910
Front Neurol. 2019 Mar 19;10:229
pubmed: 30941088
Amyotroph Lateral Scler Frontotemporal Degener. 2019 May;20(3-4):133-145
pubmed: 30654671
Neuroimage. 2001 Jul;14(1 Pt 1):21-36
pubmed: 11525331
Amyotroph Lateral Scler Frontotemporal Degener. 2017 Nov;18(7-8):534-548
pubmed: 28745069
Lancet Neurol. 2012 Mar;11(3):232-40
pubmed: 22305801
Amyotroph Lateral Scler Frontotemporal Degener. 2019 May;20(3-4):281-284
pubmed: 30663900
Biomark Med. 2012 Jun;6(3):319-37
pubmed: 22731907
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5
pubmed: 10984517
Neurology. 2006 Mar 14;66(5):647-53
pubmed: 16534101
J Magn Reson Imaging. 2004 Jan;19(1):34-9
pubmed: 14696218
Front Neurosci. 2019 Feb 28;13:135
pubmed: 30872992
Neuroimage. 2006 Jul 1;31(3):968-80
pubmed: 16530430
Acta Neuropathol. 2007 Jul;114(1):71-9
pubmed: 17569066
J Neurol Neurosurg Psychiatry. 2013 Jul;84(7):766-73
pubmed: 23085933
Fly (Austin). 2012 Apr-Jun;6(2):80-92
pubmed: 22728672
Hum Genet. 2017 Jun;136(6):665-677
pubmed: 28349240
Nature. 2015 Oct 1;526(7571):68-74
pubmed: 26432245
Hum Brain Mapp. 2010 Nov;31(11):1727-40
pubmed: 20336652
Eur J Neurol. 2016 Aug;23(8):1361-71
pubmed: 27207250
PLoS One. 2016 Dec 1;11(12):e0167331
pubmed: 27907080
AJNR Am J Neuroradiol. 2007 Jan;28(1):87-91
pubmed: 17213431
Neuroimage Clin. 2018 Mar 15;18:762-769
pubmed: 29785360
Am J Hum Genet. 2007 Sep;81(3):559-75
pubmed: 17701901
PLoS One. 2014 Aug 21;9(8):e105753
pubmed: 25144708
Neurol Genet. 2015 Apr 14;1(1):e3
pubmed: 27066542
Brain. 2007 Sep;130(Pt 9):2375-86
pubmed: 17698497
Rev Neurol (Paris). 2015 Jun-Jul;171(6-7):505-30
pubmed: 26008818
J Med Genet. 2013 Nov;50(11):776-83
pubmed: 23881933
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Neuroimage. 2007 Jul 1;36(3):630-44
pubmed: 17481925
Neurology. 2014 Aug 12;83(7):620-7
pubmed: 25008395
JMIR Mhealth Uhealth. 2013 Sep 04;1(2):e18
pubmed: 25098641
Dement Geriatr Cogn Dis Extra. 2013 Aug 16;3(1):233-50
pubmed: 24052798
Hum Brain Mapp. 2014 Apr;35(4):1710-22
pubmed: 23633431
J Clin Neuromuscul Dis. 2005 Sep;7(1):1-9
pubmed: 19078775
BMC Neurol. 2017 Apr 17;17(1):73
pubmed: 28412941
Acta Neuropathol. 2008 Jan;115(1):147-9
pubmed: 18034349
Curr Opin Neurol. 2018 Aug;31(4):431-438
pubmed: 29750730
PLoS Comput Biol. 2013;9(7):e1003153
pubmed: 23874191
Neuroimage Clin. 2014 Feb 27;4:436-43
pubmed: 24624329
Brain. 2001 Oct;124(Pt 10):1989-99
pubmed: 11571217
Neuroimage. 2012 Aug 15;62(2):774-81
pubmed: 22248573
J Neurosci. 2009 Mar 4;29(9):2805-13
pubmed: 19261876
Magn Reson Med. 2006 Feb;55(2):302-8
pubmed: 16408263
Neuroimage. 2002 Nov;17(3):1429-36
pubmed: 12414282

Auteurs

Eoin Finegan (E)

Computational Neuroimaging Group, TBSI, Trinity College Dublin, Dublin, Ireland.

Rangariroyashe H Chipika (RH)

Computational Neuroimaging Group, TBSI, Trinity College Dublin, Dublin, Ireland.

Stacey Li Hi Shing (S)

Computational Neuroimaging Group, TBSI, Trinity College Dublin, Dublin, Ireland.

Mark A Doherty (MA)

Complex Trait Genomics Laboratory, Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.

Jennifer C Hengeveld (JC)

Complex Trait Genomics Laboratory, Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.

Alice Vajda (A)

Complex Trait Genomics Laboratory, Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.

Colette Donaghy (C)

Western Health and Social Care Trust (WHSCT), Northern Ireland, UK.

Russell L McLaughlin (RL)

Complex Trait Genomics Laboratory, Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.

Niall Pender (N)

Computational Neuroimaging Group, TBSI, Trinity College Dublin, Dublin, Ireland.
Department of Psychology, Beaumont Hospital, Dublin, Ireland.

Orla Hardiman (O)

Computational Neuroimaging Group, TBSI, Trinity College Dublin, Dublin, Ireland.

Peter Bede (P)

Computational Neuroimaging Group, TBSI, Trinity College Dublin, Dublin, Ireland. bedep@tcd.ie.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH