Progressive Spinal Cord Degeneration in Friedreich's Ataxia: Results from ENIGMA-Ataxia.


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:
01 2023
Historique:
revised: 23 08 2022
received: 09 06 2022
accepted: 04 10 2022
pmc-release: 01 01 2024
pubmed: 30 10 2022
medline: 21 1 2023
entrez: 29 10 2022
Statut: ppublish

Résumé

Spinal cord damage is a hallmark of Friedreich's ataxia (FRDA), but its progression and clinical correlates remain unclear. The objective of this study was to perform a characterization of cervical spinal cord structural damage in a large multisite FRDA cohort. We performed a cross-sectional analysis of cervical spinal cord (C1-C4) cross-sectional area (CSA) and eccentricity using magnetic resonance imaging data from eight sites within the ENIGMA-Ataxia initiative, including 256 individuals with FRDA and 223 age- and sex-matched control subjects. Correlations and subgroup analyses within the FRDA cohort were undertaken based on disease duration, ataxia severity, and onset age. Individuals with FRDA, relative to control subjects, had significantly reduced CSA at all examined levels, with large effect sizes (d > 2.1) and significant correlations with disease severity (r < -0.4). Similarly, we found significantly increased eccentricity (d > 1.2), but without significant clinical correlations. Subgroup analyses showed that CSA and eccentricity are abnormal at all disease stages. However, although CSA appears to decrease progressively, eccentricity remains stable over time. Previous research has shown that increased eccentricity reflects dorsal column (DC) damage, while decreased CSA reflects either DC or corticospinal tract (CST) damage, or both. Hence our data support the hypothesis that damage to the DC and damage to CST follow distinct courses in FRDA: developmental abnormalities likely define the DC, while CST alterations may be both developmental and degenerative. These results provide new insights about FRDA pathogenesis and indicate that CSA of the cervical spinal cord should be investigated further as a potential biomarker of disease progression. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND
Spinal cord damage is a hallmark of Friedreich's ataxia (FRDA), but its progression and clinical correlates remain unclear.
OBJECTIVE
The objective of this study was to perform a characterization of cervical spinal cord structural damage in a large multisite FRDA cohort.
METHODS
We performed a cross-sectional analysis of cervical spinal cord (C1-C4) cross-sectional area (CSA) and eccentricity using magnetic resonance imaging data from eight sites within the ENIGMA-Ataxia initiative, including 256 individuals with FRDA and 223 age- and sex-matched control subjects. Correlations and subgroup analyses within the FRDA cohort were undertaken based on disease duration, ataxia severity, and onset age.
RESULTS
Individuals with FRDA, relative to control subjects, had significantly reduced CSA at all examined levels, with large effect sizes (d > 2.1) and significant correlations with disease severity (r < -0.4). Similarly, we found significantly increased eccentricity (d > 1.2), but without significant clinical correlations. Subgroup analyses showed that CSA and eccentricity are abnormal at all disease stages. However, although CSA appears to decrease progressively, eccentricity remains stable over time.
CONCLUSIONS
Previous research has shown that increased eccentricity reflects dorsal column (DC) damage, while decreased CSA reflects either DC or corticospinal tract (CST) damage, or both. Hence our data support the hypothesis that damage to the DC and damage to CST follow distinct courses in FRDA: developmental abnormalities likely define the DC, while CST alterations may be both developmental and degenerative. These results provide new insights about FRDA pathogenesis and indicate that CSA of the cervical spinal cord should be investigated further as a potential biomarker of disease progression. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 36308733
doi: 10.1002/mds.29261
pmc: PMC9852007
mid: NIHMS1841810
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

45-56

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS107513
Pays : United States
Organisme : NIBIB NIH HHS
ID : U54 EB020403
Pays : United States

Informations de copyright

© 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Références

Neurology. 2006 Jun 13;66(11):1717-20
pubmed: 16769946
Hum Gene Ther. 2020 Dec;31(23-24):1226-1236
pubmed: 33238751
J Neuroimaging. 2020 Jan;30(1):110-118
pubmed: 31571307
Mov Disord. 2021 Feb;36(2):283-297
pubmed: 33022077
Commun Biol. 2020 Jul 10;3(1):370
pubmed: 32651439
J Neuropathol Exp Neurol. 2017 Feb 1;76(2):101-108
pubmed: 28082326
Neuroimage. 2018 Jan 15;165:170-179
pubmed: 29061527
Ann Neurol. 2021 Oct;90(4):570-583
pubmed: 34435700
Int J Biomed Imaging. 2014;2014:719520
pubmed: 25132843
Curr Opin Neurol. 2020 Aug;33(4):451-461
pubmed: 32657886
J Neurol Neurosurg Psychiatry. 1994 Aug;57(8):977-9
pubmed: 8057123
J Neurol Neurosurg Psychiatry. 2019 May;90(5):615-617
pubmed: 29945881
Mov Disord. 2009 Sep 15;24(12):1779-84
pubmed: 19562766
Ann Neurol. 2019 Aug;86(2):158-167
pubmed: 31177556
Ann Neurol. 2018 Sep;84(3):401-408
pubmed: 30014526
Mov Disord. 2022 Feb;37(2):354-364
pubmed: 34713932
Eur J Neurol. 2019 Mar;26(3):483-489
pubmed: 30326180
Cerebellum. 2017 Feb;16(1):253-256
pubmed: 26754264
Arch Neurol. 2008 Oct;65(10):1296-303
pubmed: 18852343
Cerebellum. 2013 Feb;12(1):43-7
pubmed: 22562714
J Neuroimaging. 2008 Apr;18(2):168-72
pubmed: 18380696
J Neuropathol Exp Neurol. 2013 Feb;72(2):78-90
pubmed: 23334592
Can J Neurol Sci. 1979 May;6(2):173-6
pubmed: 487306
Lancet Neurol. 2021 May;20(5):362-372
pubmed: 33770527
Science. 1996 Mar 8;271(5254):1423-7
pubmed: 8596916
Arch Neurol. 2005 Dec;62(12):1865-9
pubmed: 16344344
Neurology. 2006 Jun 13;66(11):1711-6
pubmed: 16769945
Brain Commun. 2022 Oct 03;4(5):fcac246
pubmed: 36300142
J Neurol. 2017 Jul;264(7):1526-1528
pubmed: 28620720
Confin Neurol. 1957;17(6):360-71
pubmed: 13511951
Neurol Genet. 2019 Oct 29;5(6):371
pubmed: 32042904
Neurology. 2005 Apr 12;64(7):1261-2
pubmed: 15824358
Neuroimage. 2017 Jan 15;145(Pt A):24-43
pubmed: 27720818
PLoS One. 2015 Feb 06;10(2):e0117666
pubmed: 25658484
Neurobiol Dis. 1997;4(2):103-13
pubmed: 9331900
Neuroimage. 2019 Jan 1;184:901-915
pubmed: 30300751

Auteurs

Thiago J R Rezende (TJR)

Department of Neurology, School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.

Isaac M Adanyeguh (IM)

Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, Minnesota, USA.

Filippo Arrigoni (F)

Neuroimaging Unit, Scientific Institute, IRCCS Eugenio Medea, Bosisio Parini, Italy.

Benjamin Bender (B)

Department of Diagnostic and Interventional Neuroradiology, University Hospital Tübingen, Tübingen, Germany.

Fernando Cendes (F)

Department of Neurology, School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.

Louise A Corben (LA)

Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Clayton, Victoria, Australia.
Bruce Lefroy Centre, Murdoch Children's Research Institute, Parkville, Victoria, Australia.
Department of Paediatrics, University of Melbourne, Parkville, Victoria, Australia.

Andreas Deistung (A)

University Clinic and Outpatient Clinic for Radiology, Department for Radiation Medicine, University Hospital Halle (Saale), Halle (Saale), Germany.
Department of Neurology and Center for Translational and Behavioral Neuroscience (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Essen, Germany.

Martin Delatycki (M)

Bruce Lefroy Centre, Murdoch Children's Research Institute, Parkville, Victoria, Australia.
Department of Paediatrics, University of Melbourne, Parkville, Victoria, Australia.

Imis Dogan (I)

Department of Neurology, RWTH Aachen University, Aachen, Germany.
JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich GmbH, Jülich, Germany.

Gary F Egan (GF)

Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Clayton, Victoria, Australia.
Monash Biomedical Imaging, Monash University, Clayton, Victoria, Australia.

Sophia L Göricke (SL)

Institute of Diagnostic and Interventional Radiology and Neuroradiology, Essen University Hospital, University of Duisburg-Essen, Essen, Germany.

Nellie Georgiou-Karistianis (N)

Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Clayton, Victoria, Australia.

Pierre-Gilles Henry (PG)

Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, Minnesota, USA.

Diane Hutter (D)

Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, Minnesota, USA.

Neda Jahanshad (N)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, California, USA.

James M Joers (JM)

Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, Minnesota, USA.

Christophe Lenglet (C)

Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, Minnesota, USA.

Tobias Lindig (T)

Department of Diagnostic and Interventional Neuroradiology, University Hospital Tübingen, Tübingen, Germany.

Alberto R M Martinez (ARM)

Department of Neurology, School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.

Andrea Martinuzzi (A)

Scientific Institute, IRCCS Eugenio Medea, Conegliano-Pieve di Soligo Research Centre, Conegliano, Italy.

Gabriella Paparella (G)

Scientific Institute, IRCCS Eugenio Medea, Conegliano-Pieve di Soligo Research Centre, Conegliano, Italy.

Denis Peruzzo (D)

Neuroimaging Unit, Scientific Institute, IRCCS Eugenio Medea, Bosisio Parini, Italy.

Kathrin Reetz (K)

Department of Neurology, RWTH Aachen University, Aachen, Germany.
JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich GmbH, Jülich, Germany.

Sandro Romanzetti (S)

Department of Neurology, RWTH Aachen University, Aachen, Germany.
JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich GmbH, Jülich, Germany.

Ludger Schöls (L)

Department of Neurodegenerative Diseases, Center of Neurology and Hertie Institute for Clinical Brain Research, University Tübingen, Tübingen, Germany.
German Center for Neurodegenerative Disease"s (DZNE), Tübingen, Germany.

Jörg B Schulz (JB)

Department of Neurology, RWTH Aachen University, Aachen, Germany.
JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich GmbH, Jülich, Germany.

Matthis Synofzik (M)

Department of Neurodegenerative Diseases, Center of Neurology and Hertie Institute for Clinical Brain Research, University Tübingen, Tübingen, Germany.
German Center for Neurodegenerative Disease"s (DZNE), Tübingen, Germany.

Sophia I Thomopoulos (SI)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, California, USA.

Paul M Thompson (PM)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, California, USA.

Dagmar Timmann (D)

Department of Neurology and Center for Translational and Behavioral Neuroscience (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Essen, Germany.

Ian H Harding (IH)

Monash Biomedical Imaging, Monash University, Clayton, Victoria, Australia.
Department of Neuroscience, Central Clinical School, Monash University, Melbourne, Victoria, Australia.

Marcondes C França (MC)

Department of Neurology, School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), School of Medical Sciences, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.

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