Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy

IntroductionDegenerative cervical myelopathy (DCM) is the most common cause of non-traumatic incomplete spinal cord injury, but its pathophysiology is poorly understood. As spinal cord compression observed in standard MRI often fails to explain a patient's status, new diagnostic techniques to a...

Full description

Bibliographic Details
Main Authors: Nikolai Pfender, Jan Rosner, Carl M. Zipser, Susanne Friedl, Martin Schubert, Reto Sutter, Markus Klarhoefer, José M. Spirig, Michael Betz, Patrick Freund, Mazda Farshad, Armin Curt, Markus Hupp
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2023.1217526/full
_version_ 1797632976816701440
author Nikolai Pfender
Nikolai Pfender
Jan Rosner
Jan Rosner
Carl M. Zipser
Carl M. Zipser
Susanne Friedl
Susanne Friedl
Martin Schubert
Martin Schubert
Reto Sutter
Markus Klarhoefer
José M. Spirig
Michael Betz
Patrick Freund
Mazda Farshad
Armin Curt
Armin Curt
Markus Hupp
author_facet Nikolai Pfender
Nikolai Pfender
Jan Rosner
Jan Rosner
Carl M. Zipser
Carl M. Zipser
Susanne Friedl
Susanne Friedl
Martin Schubert
Martin Schubert
Reto Sutter
Markus Klarhoefer
José M. Spirig
Michael Betz
Patrick Freund
Mazda Farshad
Armin Curt
Armin Curt
Markus Hupp
author_sort Nikolai Pfender
collection DOAJ
description IntroductionDegenerative cervical myelopathy (DCM) is the most common cause of non-traumatic incomplete spinal cord injury, but its pathophysiology is poorly understood. As spinal cord compression observed in standard MRI often fails to explain a patient's status, new diagnostic techniques to assess DCM are one of the research priorities. Minor cardiac-related cranio-caudal oscillations of the cervical spinal cord are observed by phase-contrast MRI (PC-MRI) in healthy controls (HCs), while they become pathologically increased in patients suffering from degenerative cervical myelopathy. Whether transversal oscillations (i.e., anterior–posterior and right–left) also change in DCM patients is not known.MethodsWe assessed spinal cord motion simultaneously in all three spatial directions (i.e., cranio-caudal, anterior–posterior, and right–left) using sagittal PC-MRI and compared physiological oscillations in 18 HCs to pathological changes in 72 DCM patients with spinal canal stenosis. The parameter of interest was the amplitude of the velocity signal (i.e., maximum positive to maximum negative peak) during the cardiac cycle.ResultsMost patients suffered from mild DCM (mJOA score 16 (14–18) points), and the majority (68.1%) presented with multisegmental stenosis. The spinal canal was considerably constricted in DCM patients in all segments compared to HCs. Under physiological conditions in HCs, the cervical spinal cord oscillates in the cranio-caudal and anterior–posterior directions, while right–left motion was marginal [e.g., segment C5 amplitudes: cranio-caudal: 0.40 (0.27–0.48) cm/s; anterior–posterior: 0.18 (0.16–0.29) cm/s; right–left: 0.10 (0.08–0.13) cm/s]. Compared to HCs, DCM patients presented with considerably increased cranio-caudal oscillations due to the cardinal pathophysiologic change in non-stenotic [e.g., segment C5 amplitudes: 0.79 (0.49–1.32) cm/s] and stenotic segments [.g., segment C5 amplitudes: 0.99 (0.69–1.42) cm/s]). In contrast, right–left [e.g., segment C5 amplitudes: non-stenotic segment: 0.20 (0.13–0.32) cm/s; stenotic segment: 0.11 (0.09–0.18) cm/s] and anterior–posterior oscillations [e.g., segment C5 amplitudes: non-stenotic segment: 0.26 (0.15–0.45) cm/s; stenotic segment: 0.11 (0.09–0.18) cm/s] remained on low magnitudes comparable to HCs.ConclusionIncreased cranio-caudal oscillations of the cervical cord are the cardinal pathophysiologic change and can be quantified using PC-MRI in DCM patients. This study addresses spinal cord oscillations as a relevant biomarker reflecting dynamic mechanical cord stress in DCM patients, potentially contributing to a loss of function.
first_indexed 2024-03-11T11:44:21Z
format Article
id doaj.art-28355401b8eb42a290bd8a212a5606be
institution Directory Open Access Journal
issn 1664-2295
language English
last_indexed 2024-03-11T11:44:21Z
publishDate 2023-11-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neurology
spelling doaj.art-28355401b8eb42a290bd8a212a5606be2023-11-09T15:10:56ZengFrontiers Media S.A.Frontiers in Neurology1664-22952023-11-011410.3389/fneur.2023.12175261217526Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathyNikolai Pfender0Nikolai Pfender1Jan Rosner2Jan Rosner3Carl M. Zipser4Carl M. Zipser5Susanne Friedl6Susanne Friedl7Martin Schubert8Martin Schubert9Reto Sutter10Markus Klarhoefer11José M. Spirig12Michael Betz13Patrick Freund14Mazda Farshad15Armin Curt16Armin Curt17Markus Hupp18Spinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandDepartment of Neurology, University Hospital Bern, Inselspital, Bern, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandRadiology, Balgrist University Hospital, Zurich, SwitzerlandSiemens Healthineers AG, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandUniversity Spine Center Zurich, Balgrist University Hospital, Zurich, SwitzerlandSpinal Cord Injury Center, Balgrist University Hospital, Zurich, SwitzerlandIntroductionDegenerative cervical myelopathy (DCM) is the most common cause of non-traumatic incomplete spinal cord injury, but its pathophysiology is poorly understood. As spinal cord compression observed in standard MRI often fails to explain a patient's status, new diagnostic techniques to assess DCM are one of the research priorities. Minor cardiac-related cranio-caudal oscillations of the cervical spinal cord are observed by phase-contrast MRI (PC-MRI) in healthy controls (HCs), while they become pathologically increased in patients suffering from degenerative cervical myelopathy. Whether transversal oscillations (i.e., anterior–posterior and right–left) also change in DCM patients is not known.MethodsWe assessed spinal cord motion simultaneously in all three spatial directions (i.e., cranio-caudal, anterior–posterior, and right–left) using sagittal PC-MRI and compared physiological oscillations in 18 HCs to pathological changes in 72 DCM patients with spinal canal stenosis. The parameter of interest was the amplitude of the velocity signal (i.e., maximum positive to maximum negative peak) during the cardiac cycle.ResultsMost patients suffered from mild DCM (mJOA score 16 (14–18) points), and the majority (68.1%) presented with multisegmental stenosis. The spinal canal was considerably constricted in DCM patients in all segments compared to HCs. Under physiological conditions in HCs, the cervical spinal cord oscillates in the cranio-caudal and anterior–posterior directions, while right–left motion was marginal [e.g., segment C5 amplitudes: cranio-caudal: 0.40 (0.27–0.48) cm/s; anterior–posterior: 0.18 (0.16–0.29) cm/s; right–left: 0.10 (0.08–0.13) cm/s]. Compared to HCs, DCM patients presented with considerably increased cranio-caudal oscillations due to the cardinal pathophysiologic change in non-stenotic [e.g., segment C5 amplitudes: 0.79 (0.49–1.32) cm/s] and stenotic segments [.g., segment C5 amplitudes: 0.99 (0.69–1.42) cm/s]). In contrast, right–left [e.g., segment C5 amplitudes: non-stenotic segment: 0.20 (0.13–0.32) cm/s; stenotic segment: 0.11 (0.09–0.18) cm/s] and anterior–posterior oscillations [e.g., segment C5 amplitudes: non-stenotic segment: 0.26 (0.15–0.45) cm/s; stenotic segment: 0.11 (0.09–0.18) cm/s] remained on low magnitudes comparable to HCs.ConclusionIncreased cranio-caudal oscillations of the cervical cord are the cardinal pathophysiologic change and can be quantified using PC-MRI in DCM patients. This study addresses spinal cord oscillations as a relevant biomarker reflecting dynamic mechanical cord stress in DCM patients, potentially contributing to a loss of function.https://www.frontiersin.org/articles/10.3389/fneur.2023.1217526/fullspinal cord motionspinal cord oscillationsspinal stenosisdegenerative cervical myelopathyphase contrast MRI
spellingShingle Nikolai Pfender
Nikolai Pfender
Jan Rosner
Jan Rosner
Carl M. Zipser
Carl M. Zipser
Susanne Friedl
Susanne Friedl
Martin Schubert
Martin Schubert
Reto Sutter
Markus Klarhoefer
José M. Spirig
Michael Betz
Patrick Freund
Mazda Farshad
Armin Curt
Armin Curt
Markus Hupp
Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
Frontiers in Neurology
spinal cord motion
spinal cord oscillations
spinal stenosis
degenerative cervical myelopathy
phase contrast MRI
title Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
title_full Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
title_fullStr Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
title_full_unstemmed Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
title_short Increased cranio-caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
title_sort increased cranio caudal spinal cord oscillations are the cardinal pathophysiological change in degenerative cervical myelopathy
topic spinal cord motion
spinal cord oscillations
spinal stenosis
degenerative cervical myelopathy
phase contrast MRI
url https://www.frontiersin.org/articles/10.3389/fneur.2023.1217526/full
work_keys_str_mv AT nikolaipfender increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT nikolaipfender increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT janrosner increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT janrosner increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT carlmzipser increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT carlmzipser increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT susannefriedl increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT susannefriedl increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT martinschubert increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT martinschubert increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT retosutter increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT markusklarhoefer increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT josemspirig increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT michaelbetz increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT patrickfreund increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT mazdafarshad increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT armincurt increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT armincurt increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy
AT markushupp increasedcraniocaudalspinalcordoscillationsarethecardinalpathophysiologicalchangeindegenerativecervicalmyelopathy