Impact of Magnetic Resonance Imaging Markers on the Diagnostic Performance of the International Parkinson and Movement Disorder Society Multiple System Atrophy Criteria.

MRI autopsy‐confirmed brain magnetic resonance imaging multiple system atrophy

Journal

Movement disorders : official journal of the Movement Disorder Society

ISSN: 1531-8257

Titre abrégé: Mov Disord

Pays: United States

ID NLM: 8610688

Informations de publication

Date de publication:
07 Jun 2024

Historique:

revised: 10 05 2024

received: 05 04 2024

accepted: 17 05 2024

medline: 7 6 2024

pubmed: 7 6 2024

entrez: 7 6 2024

Statut: aheadofprint

Résumé

Multiple system atrophy is a neurodegenerative disease with α-synuclein aggregation in glial cytoplasmic inclusions, leading to dysautonomia, parkinsonism, and cerebellar ataxia. The aim of this study was to validate the accuracy of the International Parkinson and Movement Disorder Society Multiple System Atrophy clinical diagnostic criteria, particularly considering the impact of the newly introduced brain magnetic resonance imaging (MRI) markers. Diagnostic accuracy of the clinical diagnostic criteria for multiple system atrophy was estimated retrospectively in autopsy-confirmed patients with multiple system atrophy, Parkinson's disease, progressive supranuclear palsy, and corticobasal degeneration. We identified a total of 240 patients. Sensitivity of the clinically probable criteria was moderate at symptom onset but improved with disease duration (year 1: 9%, year 3: 39%, final ante mortem record: 77%), whereas their specificity remained consistently high (99%-100% throughout). Sensitivity of the clinically established criteria was low during the first 3 years (1%-9%), with mild improvement at the final ante mortem record (22%), whereas specificity remained high (99%-100% throughout). When MRI features were excluded from the clinically established criteria, their sensitivity increased considerably (year 1: 3%, year 3: 22%, final ante mortem record: 48%), and their specificity was not compromised (99%-100% throughout). The International Parkinson and Movement Disorder Society multiple system atrophy diagnostic criteria showed consistently high specificity and low to moderate sensitivity throughout the disease course. The MRI markers for the clinically established criteria reduced their sensitivity without improving specificity. Combining clinically probable and clinically established criteria, but disregarding MRI features, yielded the best sensitivity with excellent specificity and may be most appropriate to select patients for therapeutic trials. © 2024 The Author(s). Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND BACKGROUND

Multiple system atrophy is a neurodegenerative disease with α-synuclein aggregation in glial cytoplasmic inclusions, leading to dysautonomia, parkinsonism, and cerebellar ataxia.

OBJECTIVE OBJECTIVE

The aim of this study was to validate the accuracy of the International Parkinson and Movement Disorder Society Multiple System Atrophy clinical diagnostic criteria, particularly considering the impact of the newly introduced brain magnetic resonance imaging (MRI) markers.

METHODS METHODS

Diagnostic accuracy of the clinical diagnostic criteria for multiple system atrophy was estimated retrospectively in autopsy-confirmed patients with multiple system atrophy, Parkinson's disease, progressive supranuclear palsy, and corticobasal degeneration.

RESULTS RESULTS

We identified a total of 240 patients. Sensitivity of the clinically probable criteria was moderate at symptom onset but improved with disease duration (year 1: 9%, year 3: 39%, final ante mortem record: 77%), whereas their specificity remained consistently high (99%-100% throughout). Sensitivity of the clinically established criteria was low during the first 3 years (1%-9%), with mild improvement at the final ante mortem record (22%), whereas specificity remained high (99%-100% throughout). When MRI features were excluded from the clinically established criteria, their sensitivity increased considerably (year 1: 3%, year 3: 22%, final ante mortem record: 48%), and their specificity was not compromised (99%-100% throughout).

CONCLUSIONS CONCLUSIONS

The International Parkinson and Movement Disorder Society multiple system atrophy diagnostic criteria showed consistently high specificity and low to moderate sensitivity throughout the disease course. The MRI markers for the clinically established criteria reduced their sensitivity without improving specificity. Combining clinically probable and clinically established criteria, but disregarding MRI features, yielded the best sensitivity with excellent specificity and may be most appropriate to select patients for therapeutic trials. © 2024 The Author(s). Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Identifiants

DOI: 10.1002/mds.29879 PMID: 38847384

pubmed: 38847384

doi: 10.1002/mds.29879

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Subventions

Organisme : Deutsche Parkinson Gesellschaft, the Else-Kröner-Fresenius-Stiftung, the CurePSP foundation and the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy within the framework of the Munich Cluster for Systems Neurology

ID : EXC 2145 SyNergy-ID 390857198

Organisme : Frame of E-Rare-3, the ERA-Net for Research on Rare Diseases

ID : ERARE18-124 (MSA-omics)

Informations de copyright

Références

Fanciulli A, Wenning GK. Multiple‐system atrophy. N Engl J Med 2015;372(3):249–263.

Hopfner F, Tietz AK, Ruf VC, et al. Common variants near ZIC1 and ZIC4 in autopsy‐confirmed multiple system atrophy. Mov Disord 2022;37(10):2110–2121.

Wenning GK, Geser F, Krismer F, et al. The natural history of multiple system atrophy: a prospective European cohort study. Lancet Neurol 2013;12(3):264–274.

Klockgether T, Ludtke R, Kramer B, et al. The natural history of degenerative ataxia: a retrospective study in 466 patients. Brain 1998;121(Pt 4):589–600.

Rohrer G, Hoglinger GU, Levin J. Symptomatic therapy of multiple system atrophy. Auton Neurosci 2018;211:26–30.

Levin J, Kurz A, Arzberger T, Giese A, Hoglinger GU. The differential diagnosis and treatment of atypical parkinsonism. Dtsch Arztebl Int 2016;113(5):61–69.

Gilman S, Wenning GK, Low PA, et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 2008;71(9):670–676.

Poewe W, Stankovic I, Halliday G, et al. Multiple system atrophy. Nat Rev Dis Primers 2022;8(1):56.

Stefanova N, Wenning GK. Multiple system atrophy: at the crossroads of cellular, molecular and genetic mechanisms. Nat Rev Neurosci 2023;24(6):334–346.

Huppertz HJ, Moller L, Sudmeyer M, et al. Differentiation of neurodegenerative parkinsonian syndromes by volumetric magnetic resonance imaging analysis and support vector machine classification. Mov Disord 2016;31(10):1506–1517.

Jellinger KA, Lantos PL. Papp‐Lantos inclusions and the pathogenesis of multiple system atrophy: an update. Acta Neuropathol 2010;119(6):657–667.

Wenning GK, Ben‐Shlomo Y, Hughes A, Daniel SE, Lees A, Quinn NP. What clinical features are most useful to distinguish definite multiple system atrophy from Parkinson's disease? J Neurol Neurosurg Psychiatry 2000;68(4):434–440.

Hughes AJ, Daniel SE, Ben‐Shlomo Y, Lees AJ. The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain 2002;125(Pt 4):861–870.

Koga S, Aoki N, Uitti RJ, et al. When DLB, PD, and PSP masquerade as MSA: an autopsy study of 134 patients. Neurology 2015;85(5):404–412.

Wenning GK, Stankovic I, Vignatelli L, et al. The Movement Disorder Society criteria for the diagnosis of multiple system atrophy. Mov Disord 2022;37(6):1131–1148.

Poewe W, Seppi K, Fitzer‐Attas CJ, et al. Efficacy of rasagiline in patients with the parkinsonian variant of multiple system atrophy: a randomised, placebo‐controlled trial. Lancet Neurol 2015;14(2):145–152.

Levin J, Maass S, Schuberth M, et al. Safety and efficacy of epigallocatechin gallate in multiple system atrophy (PROMESA): a randomised, double‐blind, placebo‐controlled trial. Lancet Neurol 2019;18(8):724–735.

Paviour DC, Price SL, Jahanshahi M, Lees AJ, Fox NC. Longitudinal MRI in progressive supranuclear palsy and multiple system atrophy: rates and regions of atrophy. Brain 2006;129(Pt 4):1040–1049.

Burciu RG, Chung JW, Shukla P, et al. Functional MRI of disease progression in Parkinson disease and atypical parkinsonian syndromes. Neurology 2016;87(7):709–717.

Pellecchia MT, Barone P, Vicidomini C, et al. Progression of striatal and extrastriatal degeneration in multiple system atrophy: a longitudinal diffusion‐weighted MR study. Mov Disord 2011;26(7):1303–1309.

Reginold W, Lang AE, Marras C, Heyn C, Alharbi M, Mikulis DJ. Longitudinal quantitative MRI in multiple system atrophy and progressive supranuclear palsy. Parkinsonism Relat Disord 2014;20(2):222–225.

Sekiya H, Koga S, Murakami A, et al. Validation study of the MDS criteria for the diagnosis of multiple system atrophy in the Mayo Clinic Brain Bank. Neurology 2023;101(24):e2460–e2471.

Virameteekul S, Revesz T, Jaunmuktane Z, Warner TT, De Pablo‐Fernandez E. Pathological validation of the MDS criteria for the diagnosis of multiple system atrophy. Mov Disord 2023;38(3):444–452.

Trojanowski JQ, Revesz T. Proposed neuropathological criteria for the post mortem diagnosis of multiple system atrophy. Neuropathol Appl Neurobiol 2007;33(6):615–620.

Dickson DW, Braak H, Duda JE, et al. Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol 2009;8(12):1150–1157.

Dickson DW. Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J Neurol 1999;246(Suppl 2):II6‐15.

Hauw JJ, Daniel SE, Dickson D, et al. Preliminary NINDS neuropathologic criteria for Steele‐Richardson‐Olszewski syndrome (progressive supranuclear palsy). Neurology 1994;44(11):2015–2019.

Kovacs GG. Invited review: neuropathology of tauopathies: principles and practice. Neuropathol Appl Neurobiol 2015;41(1):3–23.

Dickson DW, Bergeron C, Chin SS, et al. Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 2002;61(11):935–946.

Keeney S, Hasson F, McKenna H. Consulting the oracle: ten lessons from using the Delphi technique in nursing research. J Adv Nurs 2006;53(2):205–212.

Eriksen MB, Frandsen TF. The impact of patient, intervention, comparison, outcome (PICO) as a search strategy tool on literature search quality: a systematic review. J Med Libr Assoc 2018;106(4):420–431.

Armstrong MJ, Gronseth GS. Approach to assessing and using clinical practice guidelines. Neurol Clin Pract 2018;8(1):58–61.

Nair R, Aggarwal R, Khanna D. Methods of formal consensus in classification/diagnostic criteria and guideline development. Semin Arthritis Rheum 2011;41(2):95–105.

Massey LA, Micallef C, Paviour DC, et al. Conventional magnetic resonance imaging in confirmed progressive supranuclear palsy and multiple system atrophy. Mov Disord 2012;27(14):1754–1762.

Pellecchia MT, Stankovic I, Fanciulli A, et al. Can autonomic testing and imaging contribute to the early diagnosis of multiple system atrophy? A systematic review and recommendations by the Movement Disorder Society multiple system atrophy study group. Mov Disord Clin Pract 2020;7(7):750–762.