Regional Brain and Spinal Cord Volume Loss in Spinocerebellar Ataxia Type 3.


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:
10 2021
Historique:
revised: 17 03 2021
received: 03 11 2020
accepted: 18 03 2021
pubmed: 6 5 2021
medline: 28 10 2021
entrez: 5 5 2021
Statut: ppublish

Résumé

Given that new therapeutic options for spinocerebellar ataxias are on the horizon, there is a need for markers that reflect disease-related alterations, in particular, in the preataxic stage, in which clinical scales are lacking sensitivity. The objective of this study was to quantify regional brain volumes and upper cervical spinal cord areas in spinocerebellar ataxia type 3 in vivo across the entire time course of the disease. We applied a brain segmentation approach that included a lobular subsegmentation of the cerebellum to magnetic resonance images of 210 ataxic and 48 preataxic spinocerebellar ataxia type 3 mutation carriers and 63 healthy controls. In addition, cervical cord cross-sectional areas were determined at 2 levels. The metrics of cervical spinal cord segments C3 and C2, medulla oblongata, pons, and pallidum, and the cerebellar anterior lobe were reduced in preataxic mutation carriers compared with controls. Those of cervical spinal cord segments C2 and C3, medulla oblongata, pons, midbrain, cerebellar lobules crus II and X, cerebellar white matter, and pallidum were reduced in ataxic compared with nonataxic carriers. Of all metrics studied, pontine volume showed the steepest decline across the disease course. It covaried with ataxia severity, CAG repeat length, and age. The multivariate model derived from this analysis explained 46.33% of the variance of pontine volume. Regional brain and spinal cord tissue loss in spinocerebellar ataxia type 3 starts before ataxia onset. Pontine volume appears to be the most promising imaging biomarker candidate for interventional trials that aim at slowing the progression of spinocerebellar ataxia type 3. © 2021 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND
Given that new therapeutic options for spinocerebellar ataxias are on the horizon, there is a need for markers that reflect disease-related alterations, in particular, in the preataxic stage, in which clinical scales are lacking sensitivity.
OBJECTIVE
The objective of this study was to quantify regional brain volumes and upper cervical spinal cord areas in spinocerebellar ataxia type 3 in vivo across the entire time course of the disease.
METHODS
We applied a brain segmentation approach that included a lobular subsegmentation of the cerebellum to magnetic resonance images of 210 ataxic and 48 preataxic spinocerebellar ataxia type 3 mutation carriers and 63 healthy controls. In addition, cervical cord cross-sectional areas were determined at 2 levels.
RESULTS
The metrics of cervical spinal cord segments C3 and C2, medulla oblongata, pons, and pallidum, and the cerebellar anterior lobe were reduced in preataxic mutation carriers compared with controls. Those of cervical spinal cord segments C2 and C3, medulla oblongata, pons, midbrain, cerebellar lobules crus II and X, cerebellar white matter, and pallidum were reduced in ataxic compared with nonataxic carriers. Of all metrics studied, pontine volume showed the steepest decline across the disease course. It covaried with ataxia severity, CAG repeat length, and age. The multivariate model derived from this analysis explained 46.33% of the variance of pontine volume.
CONCLUSION
Regional brain and spinal cord tissue loss in spinocerebellar ataxia type 3 starts before ataxia onset. Pontine volume appears to be the most promising imaging biomarker candidate for interventional trials that aim at slowing the progression of spinocerebellar ataxia type 3. © 2021 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 33951232
doi: 10.1002/mds.28610
pmc: PMC9521507
mid: NIHMS1837147
doi:

Banques de données

ClinicalTrials.gov
['NCT01470729']

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

2273-2281

Subventions

Organisme : NIBIB NIH HHS
ID : P41 EB027061
Pays : United States
Organisme : NIH HHS
ID : S10 OD017974
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS080816
Pays : United States
Organisme : NINDS NIH HHS
ID : P30 NS076408
Pays : United States
Organisme : Medical Research Council
ID : MR/N028767/1
Pays : United Kingdom

Informations de copyright

© 2021 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Références

Cerebellum. 2015 Apr;14(2):128-32
pubmed: 25370748
Am J Hum Genet. 1995 Jul;57(1):54-61
pubmed: 7611296
Neuroimage. 2010 Jan 1;49(1):158-68
pubmed: 19631275
Lancet Neurol. 2020 Sep;19(9):738-747
pubmed: 32822634
Cerebellum. 2010 Sep;9(3):419-28
pubmed: 20467850
Brain Pathol. 1998 Oct;8(4):669-79
pubmed: 9804376
Neurology. 2008 Sep 23;71(13):982-9
pubmed: 18685131
Hum Brain Mapp. 2015 Mar;36(3):1102-20
pubmed: 25395058
Neuroimage. 2017 Jan 15;145(Pt A):24-43
pubmed: 27720818
Neuroepidemiology. 2014;42(3):174-83
pubmed: 24603320
Ann Neurol. 1996 Apr;39(4):490-9
pubmed: 8619527
Brain. 2013 Mar;136(Pt 3):905-17
pubmed: 23423669
J Med Genet. 2014 Jul;51(7):479-86
pubmed: 24780882
Lancet Neurol. 2015 Nov;14(11):1101-8
pubmed: 26377379
Neuroimage Clin. 2018;20:931-938
pubmed: 30308379
Cereb Cortex. 1999 Oct-Nov;9(7):712-21
pubmed: 10554994
Neurology. 2006 Jun 13;66(11):1717-20
pubmed: 16769946
Mov Disord. 2019 Aug;34(8):1220-1227
pubmed: 31211461
Neuroimage Clin. 2018 Jun 14;19:858-867
pubmed: 29922574
Ann Neurol. 2018 Sep;84(3):401-408
pubmed: 30014526
Acta Neuropathol. 2012 Jul;124(1):1-21
pubmed: 22684686
AJNR Am J Neuroradiol. 2016 Aug;37(8):1405-12
pubmed: 27173364
Mov Disord. 2013 Jul;28(8):1125-32
pubmed: 23553599
Mov Disord. 2020 Sep;35(9):1679-1684
pubmed: 32515873
Ann Clin Transl Neurol. 2018 Jan 07;5(2):128-137
pubmed: 29468174
Neuron. 1997 Aug;19(2):333-44
pubmed: 9292723
Prog Neurobiol. 2013 May;104:38-66
pubmed: 23438480
Adv Exp Med Biol. 2018;1049:233-241
pubmed: 29427106
Brain. 1998 Sep;121 ( Pt 9):1687-93
pubmed: 9762957
Ann Neurol. 2018 Jul;84(1):64-77
pubmed: 29908063
Neuroimage. 2020 Oct 15;220:117062
pubmed: 32592850
Neurosci Lett. 2006 Nov 20;408(3):230-5
pubmed: 17005321
Front Hum Neurosci. 2013 Aug 20;7:462
pubmed: 23970860
Brain Pathol. 2017 May;27(3):345-355
pubmed: 27377427
Neuroimage. 2004 Oct;23(2):724-38
pubmed: 15488422

Auteurs

Jennifer Faber (J)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurology, University Hospital Bonn, Bonn, Germany.

Tamara Schaprian (T)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.

Koyak Berkan (K)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.

Kathrin Reetz (K)

Department of Neurology, RWTH Aachen University, Bonn, Germany.
JARA-Brain Institute Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich, Jülich, Germany.

Marcondes Cavalcante França (MC)

Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), Campinas, Brazil.
Department of Neurology, University of Campinas, Campinas, Brazil.

Thiago Junqueira Ribeiro de Rezende (TJR)

Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), Campinas, Brazil.
Department of Neurology, University of Campinas, Campinas, Brazil.

Jiang Hong (J)

Department of Neurology, Xiangya Hospital, Central South University, Changsha, China.

Weihua Liao (W)

Department of Radiology, Xiangya Hospital, Central South University, Changsha, People's Republic of China.

Bart van de Warrenburg (B)

Department of Neurology, Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands.

Judith van Gaalen (J)

Department of Neurology, Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands.

Alexandra Durr (A)

Sorbonne Université, Paris Brain Institute, AP-HP, INSERM, CNRS, Pitié-Salpêtrière University Hospital, Paris, France.

Fanny Mochel (F)

Sorbonne Université, Paris Brain Institute, AP-HP, INSERM, CNRS, Pitié-Salpêtrière University Hospital, Paris, France.

Paola Giunti (P)

Ataxia Centre, Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, United Kingdom.
National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Foundation Trust, London, United Kingdom.

Hector Garcia-Moreno (H)

Ataxia Centre, Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, United Kingdom.
National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Foundation Trust, London, United Kingdom.

Ludger Schoels (L)

Department of Neurodegenerative Diseases and Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
German Centre for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Holger Hengel (H)

Department of Neurodegenerative Diseases and Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
German Centre for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Matthis Synofzik (M)

Department of Neurodegenerative Diseases and Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
German Centre for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Benjamin Bender (B)

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

Gulin Oz (G)

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

James Joers (J)

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

Jereon J de Vries (JJ)

Department of Neurology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.

Jun-Suk Kang (JS)

Department of Neurology, Goethe University, Frankfurt am Main, Germany.

Dagmar Timmann-Braun (D)

Department of Neurology, Essen University Hospital, Essen, Germany.

Heike Jacobi (H)

Department of Neurology, University Hospital of Heidelberg, Heidelberg, Germany.

Jon Infante (J)

Neurology Service, University Hospital Marques de Valdecilla-IDIVAL, University of Cantabria, Centro de Investigacion Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), Santander, Spain.

Richard Joules (R)

IXICO Plc, London, United Kingdom.

Sandro Romanzetti (S)

JARA-Brain Institute Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich, Jülich, Germany.

Jorn Diedrichsen (J)

Brain Mind Institute, Departmentof Computer Science, Department of Statistics, University of Western Ontario, London, Canada.

Matthias Schmid (M)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.
Institute of Medical Biometry, Informatics and Epidemiology, University Hospital Bonn, Bonn, Germany.

Robin Wolz (R)

IXICO Plc, London, United Kingdom.

Thomas Klockgether (T)

DZNE, German Center for Neurodegenerative Diseases, Bonn, Germany.
Department of Neurology, University Hospital Bonn, Bonn, Germany.

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