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

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

doi:10.3389/fneur.2023.1217526

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

Front Neurol. 2023 Nov 8:14:1217526. doi: 10.3389/fneur.2023.1217526. eCollection 2023.

Authors

Nikolai Pfender^{1

2}, Jan Rosner^{1

3}, Carl M Zipser^{1

2}, Susanne Friedl^{1

2}, Martin Schubert^{1

2}, Reto Sutter⁴, Markus Klarhoefer⁵, José M Spirig², Michael Betz², Patrick Freund¹, Mazda Farshad², Armin Curt^{1

2}, Markus Hupp¹

Affiliations

¹ Spinal Cord Injury Center, Balgrist University Hospital, Zurich, Switzerland.
² University Spine Center Zurich, Balgrist University Hospital, Zurich, Switzerland.
³ Department of Neurology, University Hospital Bern, Inselspital, Bern, Switzerland.
⁴ Radiology, Balgrist University Hospital, Zurich, Switzerland.
⁵ Siemens Healthineers AG, Zurich, Switzerland.

Abstract

Introduction: Degenerative 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.

Methods: We 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.

Results: Most 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.

Conclusion: Increased 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.

Keywords: degenerative cervical myelopathy; phase contrast MRI; spinal cord motion; spinal cord oscillations; spinal stenosis.

Grants and funding

This study (i.e., cost for MRI examinations) was supported by Balgrist Stiftung, Zurich, Switzerland. PF was funded by the Swiss National Science Foundation Eccellenza Professorial Fellowship grant (PCEFP3_181362/1). JR was supported by the postdoctoral fellowship grant from the International Foundation for Research in Paraplegia. The funding sources had no involvement in the study design, data collection, analysis and interpretation, report writing, or decision to submit the article for publication.