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Research ArticleSpine Imaging and Spine Image-Guided Interventions
Open Access

Clinically Feasible Microstructural MRI to Quantify Cervical Spinal Cord Tissue Injury Using DTI, MT, and T2*-Weighted Imaging: Assessment of Normative Data and Reliability

A.R. Martin, B. De Leener, J. Cohen-Adad, D.W. Cadotte, S. Kalsi-Ryan, S.F. Lange, L. Tetreault, A. Nouri, A. Crawley, D.J. Mikulis, H. Ginsberg and M.G. Fehlings
American Journal of Neuroradiology June 2017, 38 (6) 1257-1265; DOI: https://doi.org/10.3174/ajnr.A5163
A.R. Martin
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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B. De Leener
cPolytechnique Montreal (B.D.L., J.C.-A.), Montréal, Quebec, Canada
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J. Cohen-Adad
cPolytechnique Montreal (B.D.L., J.C.-A.), Montréal, Quebec, Canada
dFunctional Neuroimaging Unit (J.C.-A.), Centre de recherche de l'Institut universitaire de gériatrie de Montréal, Université de Montréal, Montréal, Quebec, Canada
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D.W. Cadotte
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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S. Kalsi-Ryan
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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S.F. Lange
eUniversity of Groningen (S.F.L.), Groningen, the Netherlands.
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L. Tetreault
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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A. Nouri
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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A. Crawley
bDepartment of Medical Imaging (A.C., D.J.M.), University of Toronto and the University Health Network, Toronto Western Hospital, Toronto, Ontario, Canada
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D.J. Mikulis
bDepartment of Medical Imaging (A.C., D.J.M.), University of Toronto and the University Health Network, Toronto Western Hospital, Toronto, Ontario, Canada
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H. Ginsberg
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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M.G. Fehlings
aFrom the Division of Neurosurgery, Department of Surgery (A.R.M., D.W.C., S.K.-R., L.T., A.N., H.G., M.G.F.)
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    Fig 1.

    Representative images showing FA maps (A), MTR maps (B), and T2*WI (C) with probabilistic maps of the lateral corticospinal tracts (blue) and dorsal columns (red-yellow) overlaid (D–F) following registration to the SCT atlas.

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    Fig 2.

    Normative data in the rostral cervical cord for FA, MTR, and T2*WI WM/GM ratios. Metrics are extracted from SC, WM, GM, and key WM tracts averaged over rostral sections (C1–C3). Values are displayed as mean ± intersubject SD (error bars). The asterisk denotes P < .05 with paired t tests between WM and GM and ANOVA among WM tracts. L indicates left; R, right; FC, fasciculus cuneatus; FG, fasciculus gracilis; SL, spinal lemniscus; LCST, lateral corticospinal tract.

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    Fig 3.

    Variations by rostrocaudal level. MR imaging metrics displayed for each vertebral and intervertebral level from C1 to C7. FA, MTR, and T2*WI WM/GM ratios are extracted from WM. ANOVA shows significant differences by level for all metrics. Monotonic variations are present for CSA, FA, and MTR.

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    Fig 4.

    Test-retest coefficients of variation of FA, MTR, and T2*WI WM/GM extracted from SC, WM, GM, and key WM tracts in rostral sections (C1–C3) are displayed. T2*WI WM/GM ratio shows better reliability than FA and MTR. Metrics derived from the SC and WM show TRCOV < 3%, while GM and key WM tracts show TRCOV < 5% except for FA of the spinal lemniscus. FC indicates fasciculus cuneatus; FG, fasciculus gracilis; SL, spinal lemniscus; LCST, lateral corticospinal tract; R, right; L, left.

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    Table 1:

    Acquisition protocola

    Imaging TypePulse Sequence; OrientationTechnical DetailsAcquisition TimeMetric
    T2WI3D FIESTA-C; sagittalTR/TE = 5.4/2.6 s, FOV = 200 × 200 mm2, matrix = 256 × 256, resolution = 0.8 × 0.8 × 0.8 mm3, NEX = 2, flip angle = 35°6 min 56 sCSA
    DTISpin-echo ssEPI with OVS; axialTR/TE = 4050/91.2 ms, FOV = 80 × 80 mm2, matrix = 64 × 64, resolution = 1.25 × 1.25 × 5 mm3, 25 directions (b=800 s/mm2), 5 b=0 s/mm2 images, AP saturation bands, phase encoding = AP, 2nd-order shimming3 × 2 min 6 s, 1 min 30 s for shimmingFA
    MT2D SPGR with/without prepulse; axialTR/TE = 32/5.9 ms, FOV = 190 × 190 mm2, matrix = 192 × 192, resolution = 1 × 1 × 5 mm3, NEX = 3, flip angle = 6°, flow compensation, phase encoding = AP, prepulse: Gaussian, duration = 9984 μs, offset = 1200 Hz3 min 45 s each, with and without prepulseMTR
    T2*WI2D MERGE; axialTR/TE = 650/5, 10, 15 ms, FOV = 200 × 200 mm2, matrix = 320 × 320, resolution = 0.6 × 0.6 × 4 mm3, NEX = 1, flip angle = 20°, BW = 62 kHz per line3 min 33 sWM/GM ratio
    • Note:—AP indicates anteroposterior; BW, bandwidth; FIESTA-C, FIESTA-cycled phases; MERGE, multiecho recombined gradient echo; OVS, outer volume suppression; SPGR, echo-spoiled gradient echo; ssEPI, single-shot echo-planar imaging.

    • ↵a Technical specifications of our multiparametric cervical SC MRI protocol, with an acquisition time of 25 minutes (30–35 minutes, including positioning, section prescription, shimming, and prescans).

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    Table 2:

    Subject characteristicsa

    CharacteristicHealthy Subjects (n = 40)Subjects with DCM (n = 18)
    Age (yr)47.1 ± 15.3 (range, 19–79)56.4 ± 11.0 (range, 36–76)
    Sex21 men, 19 women11 men, 7 women
    Height (cm)171.4 ± 8.6172.8 ± 8.9
    Weight (kg)74.6 ± 11.579.0 ± 15.1
    Cervical cord length (cm)10.6 ± 1.011.1 ± 0.9
    • ↵a Demographics and characteristics of 40 healthy subjects and 18 with DCM are shown. Data (other than sex) are reported as mean ± SD.

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    Table 3:

    Univariate relationships of MRI metrics with healthy subject characteristicsa

    MetricAgeSex (M vs F)HeightWeightCervical Cord Length
    CSA (mm2)r = −0.25 (P = .12)80.0 ± 11.2 vs 73.5 ± 8.5 (P = .03b)r = 0.31 (P = .06c)r = 0.34 (P = .03b)r = 0.51 (P < .001b)
    FAr = −0.43 (P = .009b)0.658 ± 0.037 vs 0.663 ± 0.034 (P = .75)r = −0.02 (P = .89)r = −0.26 (P = .12)r = 0.11 (P = .53)
    MTRr = −0.25 (P = .11)48.8 ± 2.5 vs 51.4 ± 2.7 (P = .006b)r = −0.41 (P = .008b)r = −0.40 (P = .01)r = −0.18 (P = .26)
    T2*WI WM/GMr = 0.31 (P = .06)0.863 ± 0.034 vs 0.858 ± 0.031 (P = .64)r = −0.12 (P = .48)r = 0.31 (P = .06c)r = −0.09 (P = .55)
    • ↵a Values for sex are reported as mean ± SD, and other values are Pearson correlation coefficient. FA, MTR, and T2*WI WM/GM ratios are extracted from WM, while CSA of the spinal cord is measured, averaged across C1–C7.

    • ↵b Significance (P < .05).

    • ↵c Trends (P < .10).

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    Table 4:

    Test-retest reliability across rostrocaudal levelsa

    LevelMetricHealthyDCMP ValuePooled
    Rostral (C1–C3)FA2.5 ± 2.0%2.8 ± 1.8%.712.6 ± 1.9%
    MTR2.7 ± 1.9%1.3 ± 0.5%.172.4 ± 1.9%
    T2*WI WM/GM0.9 ± 0.6%1.0 ± 0.7%.770.9 ± 0.7%b
    Midcervical (C4–C5) or MCLFA3.0 ± 2.2%5.0 ± 5.7%.213.6 ± 3.6%
    MTR3.2 ± 3.0%6.1 ± 0.9%.08c3.7 ± 3.2%
    T2*WI WM/GM1.4 ± 1.1%3.5 ± 2.2%.112.9 ± 2.2%
    Caudal (C6–C7)FA2.2 ± 1.6%4.6 ± 4.7%.07c3.2 ± 3.5%
    MTR4.4 ± 3.8%3.1 ± 3.9%.564.2 ± 3.7%
    T2*WI WM/GM3.4 ± 3.0%2.2 ± 2.1%.372.6 ± 2.4%
    • ↵a TRCOV ± SD is displayed for healthy subjects and those with DCM at rostral (C1–C3), midcervical (C4–5), or maximally compressed levels in subjects with DCM, and caudal (C6–C7) levels. Sample size was 26 subjects (17 healthy, 9 with DCM) for DTI, 17 subjects (13 healthy, 4 with DCM) for MT, and 16 subjects (5 healthy, 11 with DCM) for T2*WI.

    • ↵b Significant differences (P < .05) between pooled TRCOV of metrics at each level.

    • ↵c Trends (P < .10) in reliability between healthy subjects and those with DCM for each level/metric, and pooled reliability was calculated if no significant differences were found.

    • View popup
    Table 5:

    DTI with and without cardiac triggeringa

    MeasureLevelNo TriggeringTriggeringP Value
    FARostral0.651 ± 0.0540.664 ± 0.064.41
    Mid/MCL0.514 ± 0.0680.558 ± 0.081.06b
    Caudal0.534 ± 0.0570.562 ± 0.044.07b
    TRCOVRostral2.6 ± 1.9%1.5 ± 1.2%.11
    Mid/MCL3.6 ± 3.6%2.2 ± 2.3%.27
    Caudal3.2 ± 3.5%2.4 ± 2.3%.52
    • ↵a Paired t tests were used to compare FA values extracted from WM at rostral (C1–C3), midcervical (C4–5, healthy subjects), or MCL (subjects with DCM), and caudal (C6–C7) levels between no triggering vs triggering in 10 subjects (4 healthy, 6 with DCM). Welch t tests were used to compare test-retest coefficient of variation between no triggering (n = 26) and triggering (n = 10).

    • ↵b Trends (P < .10).

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A.R. Martin, B. De Leener, J. Cohen-Adad, D.W. Cadotte, S. Kalsi-Ryan, S.F. Lange, L. Tetreault, A. Nouri, A. Crawley, D.J. Mikulis, H. Ginsberg, M.G. Fehlings
Clinically Feasible Microstructural MRI to Quantify Cervical Spinal Cord Tissue Injury Using DTI, MT, and T2*-Weighted Imaging: Assessment of Normative Data and Reliability
American Journal of Neuroradiology Jun 2017, 38 (6) 1257-1265; DOI: 10.3174/ajnr.A5163

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Clinically Feasible Microstructural MRI to Quantify Cervical Spinal Cord Tissue Injury Using DTI, MT, and T2*-Weighted Imaging: Assessment of Normative Data and Reliability
A.R. Martin, B. De Leener, J. Cohen-Adad, D.W. Cadotte, S. Kalsi-Ryan, S.F. Lange, L. Tetreault, A. Nouri, A. Crawley, D.J. Mikulis, H. Ginsberg, M.G. Fehlings
American Journal of Neuroradiology Jun 2017, 38 (6) 1257-1265; DOI: 10.3174/ajnr.A5163
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