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Research ArticleSpine Imaging and Spine Image-Guided Interventions
Open Access

The Restless Spinal Cord in Degenerative Cervical Myelopathy

M. Hupp, N. Pfender, K. Vallotton, J. Rosner, S. Friedl, C.M. Zipser, R. Sutter, M. Klarhöfer, J.M. Spirig, M. Betz, M. Schubert, P. Freund, M. Farshad and A. Curt
American Journal of Neuroradiology March 2021, 42 (3) 597-609; DOI: https://doi.org/10.3174/ajnr.A6958
M. Hupp
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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  • ORCID record for M. Hupp
N. Pfender
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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K. Vallotton
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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J. Rosner
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
dDepartment of Neurology (J.R.), University Hospital Bern, Inselspital, University of Bern, Bern, Switzerland
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S. Friedl
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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C.M. Zipser
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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R. Sutter
bDepartment of Radiology (R.S.)
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M. Klarhöfer
eSiemens Healthcare AG (M.K.), Zurich, Switzerland
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J.M. Spirig
cUniversity Spine Center Zurich (J.M.S., M.B., M.F., A.C.), Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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M. Betz
cUniversity Spine Center Zurich (J.M.S., M.B., M.F., A.C.), Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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M. Schubert
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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P. Freund
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
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M. Farshad
cUniversity Spine Center Zurich (J.M.S., M.B., M.F., A.C.), Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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A. Curt
aFrom the Spinal Cord Injury Center (M.H., N.P., K.V., J.R., S.F., C.M.Z., M.S., P.F., A.C.)
cUniversity Spine Center Zurich (J.M.S., M.B., M.F., A.C.), Balgrist University Hospital, University of Zurich, Zurich, Switzerland
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  • FIG 1.
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    FIG 1.

    CSF space in controls and patients The CSF cross-sectional area (CSA) was smaller in patients with segments classified as stenotic (dark gray plots) compared with segments classified as nonstenotic (light gray plots). At C7 in 32 patients, the CSA was available, but no segment was classified as stenotic. The asterisk indicates P < .001.

  • FIG 2.
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    FIG 2.

    Spinal cord motion pattern in healthy controls and patients (stenotic segments). Spinal cord velocity values are displayed within 20 time points during the cardiac cycle in healthy controls (left column) and stenotic segments in patients (monosegmental and multisegmental stenoses, right column). Velocity values are pooled per cervical segment. Single measures are displayed in light gray; the black line represents the group mean.

  • FIG 3.
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    FIG 3.

    Displacement values in controls and patients. Displacement values (entire cardiac cycle) are increased manifold in patients (monosegmental and multisegmental stenoses) in segments classified as stenotic (dark gray plots) and nonstenotic (light gray plots) compared with controls (white plots). In groups with only 1 measurement, no analysis was possible. Double asterisks indicate P < .001; asterisk, P = .015.

  • FIG 4.
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    FIG 4.

    Timing of the positive motion peaks in controls and patients. The positive motion peak was delayed in patients (monosegmental and multisegmental stenoses) in segments classified as stenotic (dark gray plots) at C3, C4, C5, and C6 and in segments classified as nonstenotic (light gray plots) at C4 compared with controls (white plots). In groups with only 1 measurement, no analysis was possible. Double asterisks indicate P < .01; asterisk, P ≤ .021.

  • FIG 5.
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    FIG 5.

    Spinal cord motion at C2 regarding the distance to the next stenosis and the number of stenotic segments. In patients (monosegmental and multisegmental stenoses), displacement (entire cardiac cycle) differs with the distance to the next stenosis (A) and the number of stenotic segments (B).

  • FIG 6.
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    FIG 6.

    Comparison of physiologic and pathologic spinal cord motion. At C5 in a nonstenotic segment in a healthy control (A, axial T2-weighted), only moderate velocities can be observed in phase-contrast imaging with light gray shading of the cord (B, axial PCMR, red dotted circle). In contrast, in a patient’s stenotic segment (C, axial T2-weighted), extensively increased spinal cord motion velocity can be identified by black shading of the spinal cord (D; axial PCMR; red dotted circle). While the phase-contrast images (B, healthy control; D, patient) show the maximum caudal velocity, the velocity graphs (E, healthy control; F, patient) display the velocity at 20 time points during 1 cardiac cycle. While in physiologic conditions, only a moderate biphasic oscillation in the second half of the cardiac cycle (E, time points 11–20) and no motion during the first half (E, time points 1–10) can be observed; in cervical stenosis, the spinal cord shows an extensively increased oscillation in the second half (F, time points 11–20; red arrows) and ongoing upward motion in the first half (F, time points 1–10; red dotted arrow).

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    Table 1:

    Number of stenotic segments and number of sufficient phase-contrast measurements in patients

    SegmentNo. Sufficient Measurements
    No. Stenotic SegmentsMonosegmental Stenosis, Stenotic SegmentMultisegmental Stenosis, Stenotic SegmentMonosegmental Stenosis, Nonstenotic SegmentMultisegmental Stenosis, Nonstenotic Segment
    C21011834
    C32211401
    C42341443
    C541101942
    C6220541
    C710101
    Total11015543042
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    Table 2:

    Basic demographics of the control and patient group

    Controls (n = 18)Patients (n = 55)P
    Sex (male)9 (50%)37 (67.3%).368
    Age (yr)62.2 [SD, 6.5]56.2 [SD, 12.0].024
    Body size (m)1.70 [SD, 0.06]1.70 [SD, 0.08].947
    Body weight (kg)67.2 [SD, 12.3]77.9 [SD, 13.6].007
    Monosegmental stenosis19 (34.5%)
    Multisegmental stenosis36 (65.5%)
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American Journal of Neuroradiology: 42 (3)
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M. Hupp, N. Pfender, K. Vallotton, J. Rosner, S. Friedl, C.M. Zipser, R. Sutter, M. Klarhöfer, J.M. Spirig, M. Betz, M. Schubert, P. Freund, M. Farshad, A. Curt
The Restless Spinal Cord in Degenerative Cervical Myelopathy
American Journal of Neuroradiology Mar 2021, 42 (3) 597-609; DOI: 10.3174/ajnr.A6958

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The Restless Spinal Cord in Degenerative Cervical Myelopathy
M. Hupp, N. Pfender, K. Vallotton, J. Rosner, S. Friedl, C.M. Zipser, R. Sutter, M. Klarhöfer, J.M. Spirig, M. Betz, M. Schubert, P. Freund, M. Farshad, A. Curt
American Journal of Neuroradiology Mar 2021, 42 (3) 597-609; DOI: 10.3174/ajnr.A6958
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