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December 14, 2016

Increased total sodium concentration in gray matter better explains cognition than atrophy in MS

Adil Maarouf, MD, Bertrand Audoin, MD, PhD, Fanelly Pariollaud, PhD, Soraya Gherib, MSc, Audrey Rico, MD, PhD, Elisabeth Soulier, Sylviane Confort-Gouny, PhD, Maxime Guye, MD, PhD, Lothar Schad, PhD, Jean Pelletier, MD, PhD, Jean-Philippe Ranjeva, PhD, and Wafaa Zaaraoui, PhDAuthors Info & Affiliations
January 17, 2017 issue
88 (3) 289-295
Letters to the Editor
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Abstract

Objective:

To investigate whether brain total sodium accumulation assessed by 23Na MRI is associated with cognitive deficit in relapsing-remitting multiple sclerosis (RRMS).

Methods:

Eighty-nine participants were enrolled in the study (58 patients with RRMS with a disease duration ≤10 years and 31 matched healthy controls). Patients were classified as cognitively impaired if they failed at least 2 tasks on the Brief Repeatable Battery. MRI was performed at 3T using 23Na MRI to obtain total sodium concentration (TSC) in the different brain compartments (lesions, normal-appearing white matter [NAWM], gray matter [GM]) and 1H- magnetization-prepared rapid gradient echo to assess GM atrophy (GM fraction).

Results:

The mean disease duration was 3.1 years and the median Expanded Disability Status Scale score was 1 (range 0–4.5). Thirty-seven patients were classified as cognitively preserved and 21 as cognitively impaired. TSC was increased in GM and NAWM in cognitively impaired patients compared to cognitively preserved patients and healthy controls. Voxel-wise analysis demonstrated that sodium accumulation was mainly located in the neocortex in cognitively impaired patients. Regression analysis evidenced than the 2 best independent predictors of cognitive impairment were GM TSC and age. Receiver operating characteristic analyses demonstrated that sensitivity and specificity of the GM TSC to classify patients according to their cognitive status were 76% and 71%, respectively.

Conclusions:

This study provides 2 main findings. (1) In RRMS, total sodium accumulation in the GM is better associated with cognitive impairment than GM atrophy; and (2) total sodium accumulation in patients with cognitive impairment is mainly located in the neocortex.

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REFERENCES

1.
Rao SM, Leo GJ, Bernardin L, Unverzagt F. Cognitive dysfunction in multiple sclerosis: I: frequency, patterns, and prediction. Neurology 1991;41:685–691.
PubMed
Google Scholar
2.
Filippi M, Rocca MA. MR imaging of gray matter involvement in multiple sclerosis: implications for understanding disease pathophysiology and monitoring treatment efficacy. AJNR Am J Neuroradiol 2010;31:1171–1177.
PubMed
Google Scholar
3.
Amato MP, Bartolozzi ML, Zipoli V, et al. Neocortical volume decrease in relapsing-remitting MS patients with mild cognitive impairment. Neurology 2004;63:89–93.
PubMed
Google Scholar
4.
Rovaris M, Filippi M, Minicucci L, et al. Cortical/subcortical disease burden and cognitive impairment in patients with multiple sclerosis. AJNR Am J Neuroradiol 2000;21:402–408.
PubMed
Google Scholar
5.
Calabrese M, Agosta F, Rinaldi F, et al. Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch Neurol 2009;66:1144–1150.
PubMed
Google Scholar
6.
Benedict RHB, Bruce JM, Dwyer MG, et al. Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Arch Neurol 2006;63:1301–1306.
PubMed
Google Scholar
7.
Fisniku LK, Chard DT, Jackson JS, et al. Gray matter atrophy is related to long-term disability in multiple sclerosis. Ann Neurol 2008;64:247–254.
PubMed
Google Scholar
8.
Gioia MC, Cerasa A, Liguori M, et al. Impact of individual cognitive profile on visuo-motor reorganization in relapsing–remitting multiple sclerosis. Brain Res 2007;1167:71–79.
PubMed
Google Scholar
9.
Steenwijk MD, Geurts JJ, Daams M, et al. Cortical atrophy patterns in multiple sclerosis are non-random and clinically relevant. Brain 2016;139:115–126.
PubMed
Google Scholar
10.
Waxman SG. Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat Rev Neurosci 2006;7:932–941.
PubMed
Google Scholar
11.
Lassmann H. Axonal and neuronal pathology in multiple sclerosis: what have we learnt from animal models. Exp Neurol 2010;225:2–8.
PubMed
Google Scholar
12.
Mattioli F, Stampatori C, Bellomi F, Capra R. Natalizumab efficacy on cognitive impairment in MS. Neurol Sci 2010;31:321–323.
PubMed
Google Scholar
13.
Inglese M, Madelin G, Oesingmann N, et al. Brain tissue sodium concentration in multiple sclerosis: a sodium imaging study at 3 tesla. Brain 2010;133:847–857.
PubMed
Google Scholar
14.
Zaaraoui W, Konstandin S, Audoin B, et al. Distribution of brain sodium accumulation correlates with disability in multiple sclerosis: a cross-sectional 23Na MR imaging study. Radiology 2012;264:859–867.
PubMed
Google Scholar
15.
Paling D, Solanky BS, Riemer F, et al. Sodium accumulation is associated with disability and a progressive course in multiple sclerosis. Brain 2013;136:2305–2317.
PubMed
Google Scholar
16.
Maarouf A, Audoin B, Konstandin S, et al. Topography of brain sodium accumulation in progressive multiple sclerosis. MAGMA 2014;27:53–62.
PubMed
Google Scholar
17.
Petracca M, Vancea RO, Fleysher L, Jonkman LE, Oesingmann N, Inglese M. Brain intra- and extracellular sodium concentration in multiple sclerosis: a 7 T MRI study. Brain 2016;139:795–806.
PubMed
Google Scholar
18.
Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 2011;69:292–302.
PubMed
Google Scholar
19.
Camp SJ, Stevenson VL, Thompson AJ, et al. A longitudinal study of cognition in primary progressive multiple sclerosis. Brain 2005;128:2891–2898.
PubMed
Google Scholar
20.
Reuter F, Zaaraoui W, Crespy L, et al. Frequency of cognitive impairment dramatically increases during the first 5 years of multiple sclerosis. J Neurol Neurosurg Psychiatry 2011;82:1157–1159.
PubMed
Google Scholar
21.
Nagel AM, Laun FB, Weber MA, Matthies C, Semmler W, Schad LR. Sodium MRI using a density-adapted 3D radial acquisition technique. Magn Reson Med 2009;62:1565–1573.
PubMed
Google Scholar
22.
Wiest-Daesslé N, Prima S, Coupé P, Morrissey SP, Barillot C. Rician noise removal by non-local means filtering for low signal-to-noise ratio MRI: applications to DT-MRI. Med Image Comput Comput Assist Interv 2008;11:171–179.
PubMed
Google Scholar
23.
Ge Y, Grossman RI, Udupa JK, Babb JS, Nyúl LG, Kolson DL. Brain atrophy in relapsing-remitting multiple sclerosis: fractional volumetric analysis of gray matter and white matter. Radiology 2001;220:606–610.
PubMed
Google Scholar
24.
Khaleeli Z, Cercignani M, Audoin B, Ciccarelli O, Miller DH, Thompson AJ. Localized grey matter damage in early primary progressive multiple sclerosis contributes to disability. Neuroimage 2007;37:253–261.
PubMed
Google Scholar
25.
La Corte V, Sperduti M, Malherbe C, et al. Cognitive decline and reorganization of functional connectivity in healthy aging: the pivotal role of the salience network in the prediction of age and cognitive performances. Front Aging Neurosci 2016;8:204.
PubMed
Google Scholar
26.
Nunnari D, De Cola MC, Costa A, Rifici C, Bramanti P, Marino S. Exploring cognitive reserve in multiple sclerosis: new findings from a cross-sectional study. J Clin Exp Neuropsychol 2016;38:1158–1167.
PubMed
Google Scholar
27.
Calabrese M, Magliozzi R, Ciccarelli O, Geurts JJG, Reynolds R, Martin R. Exploring the origins of grey matter damage in multiple sclerosis. Nat Rev Neurosci 2015;16:147–158.
PubMed
Google Scholar
28.
Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 2006;67:960–967.
PubMed
Google Scholar
29.
Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol 2008;7:1139–1151.
PubMed
Google Scholar
30.
Rocca MA, Amato MP, De Stefano N, et al. Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol 2015;14:302–317.
PubMed
Google Scholar
31.
Calabrese M, Rinaldi F, Mattisi I, et al. Widespread cortical thinning characterizes patients with MS with mild cognitive impairment. Neurology 2010;74:321–328.
PubMed
Google Scholar
32.
Rocca MA, Valsasina P, Hulst HE, et al. Functional correlates of cognitive dysfunction in multiple sclerosis: a multicenter fMRI study. Hum Brain Mapp 2014;35:5799–5814.
PubMed
Google Scholar
33.
Madelin G, Lee JS, Regatte RR, Jerschow A, Sodium MRI: methods and applications. Prog Nucl Magn Reson Spectrosc 2014;79:14–47.
PubMed
Google Scholar
34.
Bartha R, Menon RS. Long component time constant of 23Na T*2 relaxation in healthy human brain. Magn Reson Med 2004;52:407–410.
PubMed
Google Scholar
35.
Tsang A, Stobbe RW, Beaulieu C. Triple-quantum-filtered sodium imaging of the human brain at 4.7 T. Magn Reson Med 2012;67:1633–1643.
PubMed
Google Scholar
36.
Weingärtner S, Wetterling F, Konstandin S, Fatar M, Neumaier-Probst E, Schad LR. Scan time reduction in 23Na-magnetic resonance imaging using the chemical shift imaging sequence: evaluation of an iterative reconstruction method. Z Für Med Phys 2015;25:275–286.
PubMed
Google Scholar
37.
Lommen J, Konstandin S, Krämer P, Schad LR. Enhancing the quantification of tissue sodium content by MRI: time-efficient sodium B1 mapping at clinical field strengths. NMR Biomed 2016;29:129–136.
PubMed
Google Scholar
38.
Craner MJ, Damarjian TG, Liu S, et al. Sodium channels contribute to microglia/macrophage activation and function in EAE and MS. Glia 2005;49:220–229.
PubMed
Google Scholar
39.
Black JA, Newcombe J, Waxman SG. Astrocytes within multiple sclerosis lesions upregulate sodium channel Nav1.5. Brain 2010;133:835–846.
PubMed
Google Scholar
40.
Correale J, Farez MF. The role of astrocytes in multiple sclerosis progression. Front Neurol 2015;6:180.
PubMed
Google Scholar

Information & Authors

Information

Published In

Neurology®
Volume 88 • Number 3 • January 17, 2017
Pages: 289-295

Copyright

© 2016 American Academy of Neurology.

Publication History

Received: April 4, 2016
Accepted: October 6, 2016
Published online: December 14, 2016
Published in print: January 17, 2017

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Authors

Affiliations & Disclosures

Adil Maarouf, MD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Travel grant from commercial pharmaceutical companies: Biogen Idec, Novartis, Bayer Schering.
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
ANR-09-MNPS-025-SODIUMS
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
ARSEP Fondation, Association SEP Pays d'Aix
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Bertrand Audoin, MD, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Fanelly Pariollaud, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Soraya Gherib, MSc
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Audrey Rico, MD, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Elisabeth Soulier
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Sylviane Confort-Gouny, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Maxime Guye, MD, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Lothar Schad, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Jean Pelletier, MD, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
(1) BIOGEN IDEC : member of advisory board (2) NOVARTIS : member of advisory board (3) GENZYME : member of advisory board
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
ARSEP: research grants Novartis: research grants
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
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Jean-Philippe Ranjeva, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
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Wafaa Zaaraoui, PhD
From CNRS (A.M., B.A., F.P., S.G., A.R., E.S., S.C.-G., M.G., J.P., J.-P.R., W.Z.), CRMBM UMR 7339, Aix-Marseille Université, Marseille; Service de Neurologie (A.M.), Centre Hospitalier Universitaire de Reims, Université de Reims Champagne Ardennes; Service de Neurologie (A.M., B.A., A.R., J.P.) and CEMEREM (M.G., A.M.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Marseille, France; and Computer Assisted Clinical Medicine (L.S.), Heidelberg University, Mannheim, Germany.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author

Notes

Correspondence to Dr. Maarouf: [email protected]
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Author Contributions

A.M., B.A., A.R., J.P., J.-P.R., W.Z.: study concept and design. A.M., F.P., A.R., E.S., L.S., W.Z.: acquisition and analysis of data. A.M., B.A., S.G., S.C.-G., J.P., J.-P.R., W.Z.: analysis and interpretation of data. A.M., B.A., J.-P.R., W.Z.: study supervision, draft of the manuscript. S.C.G., M.G., L.S., J.P.: critical revision for important intellectual content. M.G., J.P.: administrative, technical, and material support.

Disclosure

A. Maarouf received travel grants from commercial pharmaceutical companies: Biogen Idec, Novartis, Merck Serono, Bayer Schering, MedDay, and Teva santé. B. Audoin received travel grants from commercial pharmaceutical companies: Biogen Idec, Novartis, Merck Serono, Bayer Schering, MedDay, and Teva santé. F. Pariollaud and S. Gherib report no disclosures relevant to the manuscript. A. Rico received travel grants from commercial pharmaceutical companies: Biogen Idec, Novartis, Merck Serono, Bayer Schering, MedDay, and Teva santé. E. Soulier, S. Confort-Gouny, M. Guye, and L. Schad report no disclosures relevant to the manuscript. J. Pelletier received travel grants from commercial pharmaceutical companies: Biogen Idec, Novartis, Merck Serono, Bayer Schering, MedDay, and Teva santé. J.P. received an unconditional grant from Novartis for this study. J.-P. Ranjeva and W. Zaaraoui report no disclosures relevant to the manuscript. Go to Neurology.org for full disclosures.

Study Funding

This study was supported by ARSEP Foundation, Association SEP Pays d'Aix, and Agence Nationale de la Recherche (ANR-09-MNPS-025-SODIUMS for the control group and unconditional grant from Novartis France).

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