Longitudinal motor system changes from acute to chronic spinal cord injury.

MRI acute spinal cord injury iron lesion core neurodegeneration

Journal

European journal of neurology
ISSN: 1468-1331
Titre abrégé: Eur J Neurol
Pays: England
ID NLM: 9506311

Informations de publication

Date de publication:
23 Jan 2024
Historique:
revised: 05 12 2023
received: 06 10 2023
accepted: 19 12 2023
medline: 23 1 2024
pubmed: 23 1 2024
entrez: 23 1 2024
Statut: aheadofprint

Résumé

In acute spinal cord injury (SCI), magnetic resonance imaging (MRI) reveals tissue bridges and neurodegeneration for 2 years. This 5-year study aims to track initial lesion changes, subsequent neurodegeneration, and their impact on recovery. This prospective longitudinal study enrolled acute SCI patients and healthy controls who were assessed clinically-and by MRI-regularly from 3 days postinjury up to 60 months. We employed histologically cross-validated quantitative MRI sequences sensitive to volume, myelin, and iron changes, thereby reflecting indirectly processes of neurodegeneration and neuroinflammation. General linear models tracked lesion and remote changes in volume, myelin- and iron-sensitive magnetic resonance indices over 5 years. Associations between lesion, degeneration, and recovery (using the Spinal Cord Independence Measure [SCIM] questionnaire and the International Standards for Neurological Classification of Spinal Cord Injury total motor score) were assessed. Patients' motor scores improved by an average of 12.86 (95% confidence interval [CI] = 6.70-19.00) points, and SCIM by 26.08 (95% CI = 17.00-35.20) points. Within 3-28 days post-SCI, lesion size decreased by more than two-thirds (3 days: 302.52 ± 185.80 mm Studying acute changes and their impact on longer follow-up provides insights into SCI trajectory, highlighting the importance of acute intervention while indicating the potential to influence outcomes in the later stages.

Sections du résumé

BACKGROUND AND PURPOSE OBJECTIVE
In acute spinal cord injury (SCI), magnetic resonance imaging (MRI) reveals tissue bridges and neurodegeneration for 2 years. This 5-year study aims to track initial lesion changes, subsequent neurodegeneration, and their impact on recovery.
METHODS METHODS
This prospective longitudinal study enrolled acute SCI patients and healthy controls who were assessed clinically-and by MRI-regularly from 3 days postinjury up to 60 months. We employed histologically cross-validated quantitative MRI sequences sensitive to volume, myelin, and iron changes, thereby reflecting indirectly processes of neurodegeneration and neuroinflammation. General linear models tracked lesion and remote changes in volume, myelin- and iron-sensitive magnetic resonance indices over 5 years. Associations between lesion, degeneration, and recovery (using the Spinal Cord Independence Measure [SCIM] questionnaire and the International Standards for Neurological Classification of Spinal Cord Injury total motor score) were assessed.
RESULTS RESULTS
Patients' motor scores improved by an average of 12.86 (95% confidence interval [CI] = 6.70-19.00) points, and SCIM by 26.08 (95% CI = 17.00-35.20) points. Within 3-28 days post-SCI, lesion size decreased by more than two-thirds (3 days: 302.52 ± 185.80 mm
CONCLUSIONS CONCLUSIONS
Studying acute changes and their impact on longer follow-up provides insights into SCI trajectory, highlighting the importance of acute intervention while indicating the potential to influence outcomes in the later stages.

Identifiants

pubmed: 38258488
doi: 10.1111/ene.16196
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e16196

Subventions

Organisme : Wings for Life
ID : WFL-CH-007/14
Organisme : Horizon2020
ID : 681094

Informations de copyright

© 2024 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.

Références

Ahuja CS, Wilson JR, Nori S, et al. Traumatic spinal cord injury. Nat Rev Dis Prim. 2017;3:17018. doi:10.1038/nrdp.2017.18
Freund P, Seif M, Weiskopf N, et al. MRI in traumatic spinal cord injury: from clinical assessment to neuroimaging biomarkers. Lancet Neurol. 2019;18(12):1123-1135. doi:10.1016/S1474-4422(19)30138-3
Ziegler G, Grabher P, Thompson A, et al. Progressive neurodegeneration following spinal cord injury: implications for clinical trials. Neurology. 2018;90(14):e1257-e1266. doi:10.1212/WNL.0000000000005258
Freund P, Papinutto N, Bischof A, et al. Simultaneous assessment of regional distributions of atrophy across the neuraxis in MS patients. NeuroImage Clin. 2022;34(March):102985. doi:10.1016/j.nicl.2022.102985
Weiskopf N, Edwards LJ, Helms G, Mohammadi S, Kirilina E. Quantitative magnetic resonance imaging of brain anatomy and in vivo histology. Nat Rev Phys. 2021;3(8):570-588. doi:10.1038/s42254-021-00326-1
Georgiadis M, Schroeter A, Gao Z, et al. Nanostructure-specific X-ray tomography reveals myelin levels, integrity and axon orientations in mouse and human nervous tissue. Nat Commun. 2021;12(1):2941. doi:10.1038/s41467-021-22719-7
Grabher P, Callaghan MF, Ashburner J, et al. Tracking sensory system atrophy and outcome prediction in spinal cord injury. Ann Neurol. 2015;78(5):751-761. doi:10.1002/ana.24508
Kirshblum SC, Waring W, Biering-Sorensen F, et al. Reference for the 2011 revision of the international standards for neurological classification of spinal cord injury. J Spinal Cord Med. 2011;34(6):547-554. doi:10.1179/107902611X13186000420242
Catz MI, Flavia SA. The Catz-Itzkovich SCIM: a revised version of the Spinal Cord Independence Measure. Disabil Rehabil. 2001;23(6):263-268. doi:10.1080/096382801750110919
Pfyffer D, Huber E, Sutter R, Curt A, Freund P. Tissue bridges predict recovery after traumatic and ischemic thoracic spinal cord injury. Neurology. 2019;93(16):e1550-e1560. doi:10.1212/WNL.0000000000008318
Scivoletto G, Laurenza L, Mammone A, Foti C, Molinari M. Recovery following ischemic myelopathies and traumatic spinal cord lesions. Spinal Cord. 2011;49(8):897-902. doi:10.1038/sc.2011.31
Iseli E, Cavigelli A, Dietz V, Curt A. Prognosis and recovery in ischaemic and traumatic spinal cord injury: clinical and electrophysiological evaluation. J Neurol Neurosurg Psychiatry. 1999;67(5):567-571. doi:10.1136/jnnp.67.5.567
Huber E, Lachappelle P, Sutter R, Curt A, Freund P. Are midsagittal tissue bridges predictive of outcome after cervical spinal cord injury? Ann Neurol. 2017;81(5):740-748. doi:10.1002/ana.24932
O'Dell DR, Weber KA, Berliner JC, et al. Midsagittal tissue bridges are associated with walking ability in incomplete spinal cord injury: a magnetic resonance imaging case series. J Spinal Cord Med. 2020;43(2):268-271. doi:10.1080/10790268.2018.1527079
Berliner JC, O'Dell DR, Albin SR, et al. The influence of conventional T 2 MRI indices in predicting who will walk outside one year after spinal cord injury. J Spinal Cord Med. 2023;46(3):501-507. doi:10.1080/10790268.2021.1907676
Vallotton K, Huber E, Sutter R, Curt A, Hupp M, Freund P. Width and neurophysiologic properties of tissue bridges predict recovery after cervical injury. Neurology. 2019;92(24):e2793-e2802. doi:10.1212/WNL.0000000000007642
Pfyffer D, Vallotton K, Curt A, Freund P. Tissue bridges predict neuropathic pain emergence after spinal cord injury. J Neurol Neurosurg Psychiatry. 2020;91(10):1111-1117. doi:10.1136/jnnp-2020-323150
Pfyffer D, Vallotton K, Curt A, Freund P. Predictive value of midsagittal tissue bridges on functional recovery after spinal cord injury. Neurorehabil Neural Repair. 2021;35(1):33-43. doi:10.1177/1545968320971787
Freund P, Wheeler-Kingshott CA, Nagy Z, et al. Axonal integrity predicts cortical reorganisation following cervical injury. J Neurol Neurosurg Psychiatry. 2012;83(6):629-637. doi:10.1136/jnnp-2011-301875
Seif M, Gandini Wheeler-Kingshott CA, Cohen-Adad J, Flanders AE, Freund P. Guidelines for the conduct of clinical trials in spinal cord injury: neuroimaging biomarkers. Spinal Cord. 2019;57(9):717-728. doi:10.1038/s41393-019-0309-x
Freund P, Friston K, Thompson AJAJ, et al. Embodied neurology: an integrative framework for neurological disorders. Brain. 2016;139(6):1855-1861. doi:10.1093/brain/aww076
Freund P, Weiskopf N, Ashburner J, et al. MRI investigation of the sensorimotor cortex and the corticospinal tract after acute spinal cord injury: a prospective longitudinal study. Lancet Neurol. 2013;12(9):873-881. doi:10.1016/S1474-4422(13)70146-7
Freund P, Weiskopf N, Ward NS, et al. Disability, atrophy and cortical reorganization following spinal cord injury. Brain. 2011;134(6):1610-1622. doi:10.1093/brain/awr093
Weiskopf N, Suckling J, Williams G, et al. Quantitative multi-parameter mapping of R1, PD(*), MT, and R2(*) at 3T: a multi-center validation. Front Neurosci. 2013;7:1-11. doi:10.3389/fnins.2013.00095
Leutritz T, Seif M, Helms G, et al. Multiparameter mapping of relaxation (R1, R2*), proton density and magnetization transfer saturation at 3 T: a multicenter dual-vendor reproducibility and repeatability study. Hum Brain Mapp. 2020;41(15):4232-4247. doi:10.1002/hbm.25122
Seif M, Leutritz T, Schading S, et al. Reliability of multi-parameter mapping (MPM) in the cervical cord: a multi-center multi-vendor quantitative MRI study. Neuroimage. 2022;264(August):119751. doi:10.1016/j.neuroimage.2022.119751
Tabelow K, Balteau E, Ashburner J, et al. hMRI-a toolbox for quantitative MRI in neuroscience and clinical research. Neuroimage. 2019;194:191-210. doi:10.1016/j.neuroimage.2019.01.029
Emmenegger TM, David G, Ashtarayeh M, et al. The influence of radio-frequency transmit field inhomogeneities on the accuracy of G-ratio weighted imaging. Front Neurosci. 2021;15:1-17. doi:10.3389/fnins.2021.674719
Ashburner J. Symmetric diffeomorphic modeling of longitudinal structural MRI. Front Neurosci. 2013;6:197. doi:10.3389/fnins.2012.00197
Ashburner J, Friston KJ. Unified segmentation. Neuroimage. 2005;26(3):839-851. doi:10.1016/j.neuroimage.2005.02.018
Azzarito M, Kyathanahally SP, Balbastre Y, et al. Simultaneous voxel-wise analysis of brain and spinal cord morphometry and microstructure within the SPM framework. Hum Brain Mapp. 2020;42:220-232. doi:10.1002/hbm.25218
Nichols TE. Multiple testing corrections, nonparametric methods, and random field theory. Neuroimage. 2012;62(2):811-815. doi:10.1016/j.neuroimage.2012.04.014
Eickhoff SB, Stephan KE, Mohlberg H, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005;25(4):1325-1335. doi:10.1016/j.neuroimage.2004.12.034
Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage. 2006;33(1):127-138. doi:10.1016/j.neuroimage.2006.05.056
Guillaume B, Hua X, Thompson PM, Waldorp L, Nichols TE, Alzheimer's Disease Neuroimaging Initiative. Fast and accurate modelling of longitudinal and repeated measures neuroimaging data. Neuroimage. 2014;94:287-302. doi:10.1016/j.neuroimage.2014.03.029
Chumbley J, Worsley K, Flandin G, Friston K. Topological FDR for neuroimaging. Neuroimage. 2010;49(4):3057-3064. doi:10.1016/j.neuroimage.2009.10.090
Hellenbrand DJ, Quinn CM, Piper ZJ, Morehouse CN, Fixel JA, Hanna AS. Inflammation after spinal cord injury: a review of the critical timeline of signaling cues and cellular infiltration. J Neuroinflammation. 2021;18(1):284. doi:10.1186/s12974-021-02337-2
Brennan FH, Li Y, Wang C, et al. Microglia coordinate cellular interactions during spinal cord repair in mice. Nat Commun. 2022;13(1):4096. doi:10.1038/s41467-022-31797-0
Buss A, Schwab ME. Sequential loss of myelin proteins during Wallerian degeneration in the rat spinal cord. Glia. 2003;42(4):424-432. doi:10.1002/glia.10220
Sachdeva R, Gao F, Chan CCH, Krassioukov AV. Cognitive function after spinal cord injury: a systematic review. Neurology. 2018;91(13):611-621. doi:10.1212/WNL.0000000000006244
Maas AIR, Menon DK, Adelson PD, et al. Traumatic brain injury: integrated approaches to improve prevention, clinical care, and research. Lancet Neurol. 2017;16(12):987-1048. doi:10.1016/S1474-4422(17)30371-X
Rink S, Pavlov S, Wöhler A, et al. Numbers of axons in spared neural tissue bridges but not their widths or areas correlate with functional recovery in spinal cord-injured rats. J Neuropathol Exp Neurol. 2020;79(11):1203-1217. doi:10.1093/jnen/nlaa050
Zrzavy T, Schwaiger C, Wimmer I, et al. Acute and non-resolving inflammation associate with oxidative injury after human spinal cord injury. Brain. 2021;144(1):144-161. doi:10.1093/brain/awaa360
David G, Pfyffer D, Vallotton K, et al. Longitudinal changes of spinal cord grey and white matter following spinal cord injury. J Neurol Neurosurg Psychiatry. 2021;92(11):1222-1230. doi:10.1136/jnnp-2021-326337
Pfyffer D, Huber E, Sutter R, et al. Are midsagittal tissue bridges predictive of outcome after cervical spinal cord injury? Ann Neurol. 2020;81(5):33-43. doi:10.1136/jnnp-2020-323150
Scivoletto G, Torre M, Mammone A, et al. Acute traumatic and ischemic spinal cord injuries have a comparable course of recovery. Neurorehabil Neural Repair. 2020;34(8):723-732. doi:10.1177/1545968320939569

Auteurs

Tim M Emmenegger (TM)

Spinal Cord Injury Centre, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.

Dario Pfyffer (D)

Spinal Cord Injury Centre, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.
Systems Neuroscience and Pain Lab, Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Palo Alto, California, USA.

Armin Curt (A)

Spinal Cord Injury Centre, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.

Simon Schading-Sassenhausen (S)

Spinal Cord Injury Centre, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.

Markus Hupp (M)

Spinal Cord Injury Centre, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.

John Ashburner (J)

Wellcome Trust Centre for Neuroimaging, Queen Square Institute of Neurology, University College London, London, UK.

Karl Friston (K)

Wellcome Trust Centre for Neuroimaging, Queen Square Institute of Neurology, University College London, London, UK.

Nikolaus Weiskopf (N)

Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
Felix Bloch Institute for Solid State Physics, Faculty of Physics and Earth Sciences, Leipzig University, Leipzig, Germany.

Alan Thompson (A)

Queen Square Multiple Sclerosis Centre, Institute of Neurology, University College London, London, UK.

Patrick Freund (P)

Spinal Cord Injury Centre, Balgrist University Hospital, University of Zurich, Zurich, Switzerland.
Wellcome Trust Centre for Neuroimaging, Queen Square Institute of Neurology, University College London, London, UK.
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.

Classifications MeSH