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Research ArticleSpine Imaging and Spine Image-Guided Interventions
Open Access

Sensitivity of the Inhomogeneous Magnetization Transfer Imaging Technique to Spinal Cord Damage in Multiple Sclerosis

H. Rasoanandrianina, S. Demortière, A. Trabelsi, J.P. Ranjeva, O. Girard, G. Duhamel, M. Guye, J. Pelletier, B. Audoin and V. Callot
American Journal of Neuroradiology May 2020, 41 (5) 929-937; DOI: https://doi.org/10.3174/ajnr.A6554
H. Rasoanandrianina
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
cLaboratoire de Biomécanique Appliquée, Institut Français des Sciences et Technologies des Transports, de l’Aménagement et des Reseaux, Aix-Marseille Université; iLab-Spine International Associated Laboratory (H.R., J.P.R., V.C.), Marseille-Montreal, France-Canada
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S. Demortière
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
dDepartment of Neurology (S.D., J.P., B.A.), Centre Hospitalier Universitaire Timone, Assistance Publique-Hopitaux de Marseille, Marseille, France.
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A. Trabelsi
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
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J.P. Ranjeva
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
cLaboratoire de Biomécanique Appliquée, Institut Français des Sciences et Technologies des Transports, de l’Aménagement et des Reseaux, Aix-Marseille Université; iLab-Spine International Associated Laboratory (H.R., J.P.R., V.C.), Marseille-Montreal, France-Canada
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O. Girard
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
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G. Duhamel
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
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M. Guye
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
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J. Pelletier
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
dDepartment of Neurology (S.D., J.P., B.A.), Centre Hospitalier Universitaire Timone, Assistance Publique-Hopitaux de Marseille, Marseille, France.
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B. Audoin
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
dDepartment of Neurology (S.D., J.P., B.A.), Centre Hospitalier Universitaire Timone, Assistance Publique-Hopitaux de Marseille, Marseille, France.
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V. Callot
aFrom the Center for Magnetic Resonance in Biology and Medicine (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France
bCentre d’Exploration Métabolique par Résonance Magnétique (H.R., S.D., A.T., J.P.R., O.G., G.D., M.G., J.P., B.A., V.C.), Assistance Publique-Hopitaux de Marseille, Hôpital Universitaire Timone, Marseille, France
cLaboratoire de Biomécanique Appliquée, Institut Français des Sciences et Technologies des Transports, de l’Aménagement et des Reseaux, Aix-Marseille Université; iLab-Spine International Associated Laboratory (H.R., J.P.R., V.C.), Marseille-Montreal, France-Canada
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Abstract

BACKGROUND AND PURPOSE: The inhomogeneous magnetization transfer technique has demonstrated high specificity for myelin, and has shown sensitivity to multiple sclerosis-related impairment in brain tissue. Our aim was to investigate its sensitivity to spinal cord impairment in MS relative to more established MR imaging techniques (volumetry, magnetization transfer, DTI).

MATERIALS AND METHODS: Anatomic images covering the cervical spinal cord from the C1 to C6 levels and DTI, magnetization transfer/inhomogeneous magnetization transfer images at the C2/C5 levels were acquired in 19 patients with MS and 19 paired healthy controls. Anatomic images were segmented in spinal cord GM and WM, both manually and using the AMU40 atlases. MS lesions were manually delineated. MR metrics were analyzed within normal-appearing and lesion regions in anterolateral and posterolateral WM and compared using Wilcoxon rank tests and z scores. Correlations between MR metrics and clinical scores in patients with MS were evaluated using the Spearman rank correlation.

RESULTS: AMU40-based C1-to-C6 GM/WM automatic segmentations in patients with MS were evaluated relative to manual delineation. Mean Dice coefficients were 0.75/0.89, respectively. All MR metrics (WM/GM cross-sectional areas, normal-appearing and lesion diffusivities, and magnetization transfer/inhomogeneous magnetization transfer ratios) were observed altered in patients compared with controls (P < .05). Additionally, the absolute inhomogeneous magnetization transfer ratio z scores were significantly higher than those of the other MR metrics (P < .0001), suggesting a higher inhomogeneous magnetization transfer sensitivity toward spinal cord impairment in MS. Significant correlations with the Expanded Disability Status Scale (ρ = –0.73/P = .02, ρ = –0.81/P = .004) and the total Medical Research Council scale (ρ = 0.80/P = .009, ρ = –0.74/P = .02) were observed for inhomogeneous magnetization transfer and magnetization transfer ratio z scores, respectively, in normal-appearing WM regions, while weaker and nonsignificant correlations were obtained for DTI metrics.

CONCLUSIONS: With inhomogeneous magnetization transfer being highly sensitive to spinal cord damage in MS compared with conventional magnetization transfer and DTI, it could generate great clinical interest for longitudinal follow-up and potential remyelinating clinical trials. In line with other advanced myelin techniques with which it could be compared, it opens perspectives for multicentric investigations.

ABBREVIATIONS:

AMU
Aix-Marseille University
CSA
cross-sectional areas
EDSS
Expanded Disability Status Scale
FA
fractional anisotropy
HC
healthy controls
ihMT
inhomogeneous magnetization transfer
ihMTR
inhomogeneous magnetization transfer ratio
λ//
axial diffusivity
λ⊥
radial diffusivity
MRC
Medical Research Council
MT
magnetization transfer
MTR
magnetization transfer ratio
NA
normal-appearing
SC
spinal cord
TWT
Timed 25-Foot Walk Test
SCT
Spinal Cord Toolbox
  • © 2020 by American Journal of Neuroradiology

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H. Rasoanandrianina, S. Demortière, A. Trabelsi, J.P. Ranjeva, O. Girard, G. Duhamel, M. Guye, J. Pelletier, B. Audoin, V. Callot
Sensitivity of the Inhomogeneous Magnetization Transfer Imaging Technique to Spinal Cord Damage in Multiple Sclerosis
American Journal of Neuroradiology May 2020, 41 (5) 929-937; DOI: 10.3174/ajnr.A6554

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Sensitivity of the Inhomogeneous Magnetization Transfer Imaging Technique to Spinal Cord Damage in Multiple Sclerosis
H. Rasoanandrianina, S. Demortière, A. Trabelsi, J.P. Ranjeva, O. Girard, G. Duhamel, M. Guye, J. Pelletier, B. Audoin, V. Callot
American Journal of Neuroradiology May 2020, 41 (5) 929-937; DOI: 10.3174/ajnr.A6554
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