Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression

Jan Valošek; René Labounek; Tomáš Horák; Magda Horáková; Petr Bednařík; Miloš Keřkovský; Jan Kočica; Tomáš Rohan; Christophe Lenglet; Julien Cohen-Adad; Petr Hluštík; Eva Vlčková; Zdeněk Kadaňka; Josef Bednařík; Alena Svatkova

doi:10.1111/ene.15027

Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression

Jan Valošek, René Labounek, Tomáš Horák, Magda Horáková, Petr Bednařík, Miloš Keřkovský, Jan Kočica, Tomáš Rohan, Christophe Lenglet, Julien Cohen-Adad, Petr Hluštík, Eva Vlčková, Zdeněk Kadaňka, Josef Bednařík, Alena Svatkova

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

Background and purpose: Non-myelopathic degenerative cervical spinal cord compression (NMDC) frequently occurs throughout aging and may progress to potentially irreversible degenerative cervical myelopathy (DCM). Whereas standard clinical magnetic resonance imaging (MRI) and electrophysiological measures assess compression severity and neurological dysfunction, respectively, underlying microstructural deficits still have to be established in NMDC and DCM patients. The study aims to establish tract-specific diffusion MRI markers of electrophysiological deficits to predict the progression of asymptomatic NMDC to symptomatic DCM. Methods: High-resolution 3 T diffusion MRI was acquired for 103 NMDC and 21 DCM patients compared to 60 healthy controls to reveal diffusion alterations and relationships between tract-specific diffusion metrics and corresponding electrophysiological measures and compression severity. Relationship between the degree of DCM disability, assessed by the modified Japanese Orthopaedic Association scale, and tract-specific microstructural changes in DCM patients was also explored. Results: The study identified diffusion-derived abnormalities in the gray matter, dorsal and lateral tracts congruent with trans-synaptic degeneration and demyelination in chronic degenerative spinal cord compression with more profound alterations in DCM than NMDC. Diffusion metrics were affected in the C3-6 area as well as above the compression level at C3 with more profound rostral deficits in DCM than NMDC. Alterations in lateral motor and dorsal sensory tracts correlated with motor and sensory evoked potentials, respectively, whereas electromyography outcomes corresponded with gray matter microstructure. DCM disability corresponded with microstructure alteration in lateral columns. Conclusions: Outcomes imply the necessity of high-resolution tract-specific diffusion MRI for monitoring degenerative spinal pathology in longitudinal studies.

Original language	English (US)
Pages (from-to)	3784-3797
Number of pages	14
Journal	European Journal of Neurology
Volume	28
Issue number	11
Early online date	Jul 21 2021
DOIs	https://doi.org/10.1111/ene.15027
State	Published - Nov 2021

Bibliographical note

Funding Information:
The core facility Multimodal and Functional Imaging Laboratory, Masaryk University, CEITEC, supported by the MEYS CR (LM2018129 Czech‐BioImaging) is acknowledged. This research is funded by the Czech Health Research Council grants NV18‐04‐00159 and by the Ministry of Health of the Czech Republic project for conceptual development in research organizations, ref. 65269705 (University Hospital, Brno, Czech Republic). JV has received “Aktion Österreich‐Tschechien, AÖCZ‐Semesterstipendien” scholarship MPC‐2020‐00013 from Austrian Agency for International Cooperation in Education and Research (OeAD‐GmbH), Mobility Programmes, Bilateral and Multilateral Cooperation (MPC) financed by Federal Ministry of Education, Science and Research (BMBWF) of Austria. AS has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska‐Curie grant agreement no. 794986. PB was partially supported by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (grant no. 27238) and by the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska‐Curie grant agreement no. 846793. CL is partly supported by NIH grants P41 EB027061 and P30 NS076408. Computational resources were supplied by the project “e‐Infrastruktura CZ” (e‐INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. JCA is funded by the Canada Research Chair in Quantitative Magnetic Resonance Imaging (950‐230815), the Canadian Institute of Health Research (CIHR FDN‐143263), the Canada Foundation for Innovation (32454, 34824), the Fonds de Recherche du Québec—Santé (28826), the Natural Sciences and Engineering Research Council of Canada (RGPIN‐2019‐07244), the Canada First Research Excellence Fund (IVADO and TransMedTech), the Courtois NeuroMod project and the Quebec BioImaging Network (5886, 35450).

Funding Information:
The core facility Multimodal and Functional Imaging Laboratory, Masaryk University, CEITEC, supported by the MEYS CR (LM2018129 Czech-BioImaging) is acknowledged. This research is funded by the Czech Health Research Council grants NV18-04-00159 and by the Ministry of Health of the Czech Republic project for conceptual development in research organizations, ref. 65269705 (University Hospital, Brno, Czech Republic). JV has received ?Aktion ?sterreich-Tschechien, A?CZ-Semesterstipendien? scholarship MPC-2020-00013 from Austrian Agency for International Cooperation in Education and Research (OeAD-GmbH), Mobility Programmes, Bilateral and Multilateral Cooperation (MPC) financed by Federal Ministry of Education, Science and Research (BMBWF) of Austria. AS has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement no. 794986. PB was partially supported by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (grant no. 27238) and by the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement no. 846793. CL is partly supported by NIH grants P41 EB027061 and P30 NS076408. Computational resources were supplied by the project ?e-Infrastruktura CZ? (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. JCA is funded by the Canada Research Chair in Quantitative Magnetic Resonance Imaging (950-230815), the Canadian Institute of Health Research (CIHR FDN-143263), the Canada Foundation for Innovation (32454, 34824), the Fonds de Recherche du Qu?bec?Sant? (28826), the Natural Sciences and Engineering Research Council of Canada (RGPIN-2019-07244), the Canada First Research Excellence Fund (IVADO and TransMedTech), the Courtois NeuroMod project and the Quebec BioImaging Network (5886, 35450). The authors would like to thank to Pavel Hok for help with data processing, Petr Kudli?ka and Veronika F?b?kov? for MRI data acquisition and Dagmar Kratochv?lov? for subject recruitment.

Publisher Copyright:
© 2021 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.

Keywords

diffusion magnetic resonance imaging
diffusion tensor imaging
spinal cord compression

Center for Magnetic Resonance Research (CMRR) tags

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ANDI
P41

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

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10.1111/ene.15027License: CC BY-NC

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Valošek, J., Labounek, R., Horák, T., Horáková, M., Bednařík, P., Keřkovský, M., Kočica, J., Rohan, T., Lenglet, C., Cohen-Adad, J., Hluštík, P., Vlčková, E., Kadaňka, Z., Bednařík, J., & Svatkova, A. (2021). Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression. European Journal of Neurology, 28(11), 3784-3797. https://doi.org/10.1111/ene.15027

Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression. / Valošek, Jan; Labounek, René; Horák, Tomáš et al.
In: European Journal of Neurology, Vol. 28, No. 11, 11.2021, p. 3784-3797.

Research output: Contribution to journal › Article › peer-review

Valošek, J, Labounek, R, Horák, T, Horáková, M, Bednařík, P, Keřkovský, M, Kočica, J, Rohan, T, Lenglet, C, Cohen-Adad, J, Hluštík, P, Vlčková, E, Kadaňka, Z, Bednařík, J & Svatkova, A 2021, 'Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression', European Journal of Neurology, vol. 28, no. 11, pp. 3784-3797. https://doi.org/10.1111/ene.15027

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title = "Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression",

abstract = "Background and purpose: Non-myelopathic degenerative cervical spinal cord compression (NMDC) frequently occurs throughout aging and may progress to potentially irreversible degenerative cervical myelopathy (DCM). Whereas standard clinical magnetic resonance imaging (MRI) and electrophysiological measures assess compression severity and neurological dysfunction, respectively, underlying microstructural deficits still have to be established in NMDC and DCM patients. The study aims to establish tract-specific diffusion MRI markers of electrophysiological deficits to predict the progression of asymptomatic NMDC to symptomatic DCM. Methods: High-resolution 3 T diffusion MRI was acquired for 103 NMDC and 21 DCM patients compared to 60 healthy controls to reveal diffusion alterations and relationships between tract-specific diffusion metrics and corresponding electrophysiological measures and compression severity. Relationship between the degree of DCM disability, assessed by the modified Japanese Orthopaedic Association scale, and tract-specific microstructural changes in DCM patients was also explored. Results: The study identified diffusion-derived abnormalities in the gray matter, dorsal and lateral tracts congruent with trans-synaptic degeneration and demyelination in chronic degenerative spinal cord compression with more profound alterations in DCM than NMDC. Diffusion metrics were affected in the C3-6 area as well as above the compression level at C3 with more profound rostral deficits in DCM than NMDC. Alterations in lateral motor and dorsal sensory tracts correlated with motor and sensory evoked potentials, respectively, whereas electromyography outcomes corresponded with gray matter microstructure. DCM disability corresponded with microstructure alteration in lateral columns. Conclusions: Outcomes imply the necessity of high-resolution tract-specific diffusion MRI for monitoring degenerative spinal pathology in longitudinal studies.",

keywords = "diffusion magnetic resonance imaging, diffusion tensor imaging, spinal cord compression",

author = "Jan Valo{\v s}ek and Ren{\'e} Labounek and Tom{\'a}{\v s} Hor{\'a}k and Magda Hor{\'a}kov{\'a} and Petr Bedna{\v r}{\'i}k and Milo{\v s} Ke{\v r}kovsk{\'y} and Jan Ko{\v c}ica and Tom{\'a}{\v s} Rohan and Christophe Lenglet and Julien Cohen-Adad and Petr Hlu{\v s}t{\'i}k and Eva Vl{\v c}kov{\'a} and Zden{\v e}k Kada{\v n}ka and Josef Bedna{\v r}{\'i}k and Alena Svatkova",

note = "Funding Information: The core facility Multimodal and Functional Imaging Laboratory, Masaryk University, CEITEC, supported by the MEYS CR (LM2018129 Czech‐BioImaging) is acknowledged. This research is funded by the Czech Health Research Council grants NV18‐04‐00159 and by the Ministry of Health of the Czech Republic project for conceptual development in research organizations, ref. 65269705 (University Hospital, Brno, Czech Republic). JV has received “Aktion {\"O}sterreich‐Tschechien, A{\"O}CZ‐Semesterstipendien” scholarship MPC‐2020‐00013 from Austrian Agency for International Cooperation in Education and Research (OeAD‐GmbH), Mobility Programmes, Bilateral and Multilateral Cooperation (MPC) financed by Federal Ministry of Education, Science and Research (BMBWF) of Austria. AS has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska‐Curie grant agreement no. 794986. PB was partially supported by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (grant no. 27238) and by the European Union's Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska‐Curie grant agreement no. 846793. CL is partly supported by NIH grants P41 EB027061 and P30 NS076408. Computational resources were supplied by the project “e‐Infrastruktura CZ” (e‐INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. JCA is funded by the Canada Research Chair in Quantitative Magnetic Resonance Imaging (950‐230815), the Canadian Institute of Health Research (CIHR FDN‐143263), the Canada Foundation for Innovation (32454, 34824), the Fonds de Recherche du Qu{\'e}bec—Sant{\'e} (28826), the Natural Sciences and Engineering Research Council of Canada (RGPIN‐2019‐07244), the Canada First Research Excellence Fund (IVADO and TransMedTech), the Courtois NeuroMod project and the Quebec BioImaging Network (5886, 35450). Funding Information: The core facility Multimodal and Functional Imaging Laboratory, Masaryk University, CEITEC, supported by the MEYS CR (LM2018129 Czech-BioImaging) is acknowledged. This research is funded by the Czech Health Research Council grants NV18-04-00159 and by the Ministry of Health of the Czech Republic project for conceptual development in research organizations, ref. 65269705 (University Hospital, Brno, Czech Republic). JV has received ?Aktion ?sterreich-Tschechien, A?CZ-Semesterstipendien? scholarship MPC-2020-00013 from Austrian Agency for International Cooperation in Education and Research (OeAD-GmbH), Mobility Programmes, Bilateral and Multilateral Cooperation (MPC) financed by Federal Ministry of Education, Science and Research (BMBWF) of Austria. AS has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement no. 794986. PB was partially supported by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (grant no. 27238) and by the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement no. 846793. CL is partly supported by NIH grants P41 EB027061 and P30 NS076408. Computational resources were supplied by the project ?e-Infrastruktura CZ? (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. JCA is funded by the Canada Research Chair in Quantitative Magnetic Resonance Imaging (950-230815), the Canadian Institute of Health Research (CIHR FDN-143263), the Canada Foundation for Innovation (32454, 34824), the Fonds de Recherche du Qu?bec?Sant? (28826), the Natural Sciences and Engineering Research Council of Canada (RGPIN-2019-07244), the Canada First Research Excellence Fund (IVADO and TransMedTech), the Courtois NeuroMod project and the Quebec BioImaging Network (5886, 35450). The authors would like to thank to Pavel Hok for help with data processing, Petr Kudli?ka and Veronika F?b?kov? for MRI data acquisition and Dagmar Kratochv?lov? for subject recruitment. Publisher Copyright: {\textcopyright} 2021 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.",

year = "2021",

month = nov,

doi = "10.1111/ene.15027",

language = "English (US)",

volume = "28",

pages = "3784--3797",

journal = "European Journal of Neurology",

issn = "1351-5101",

publisher = "Wiley-Blackwell",

number = "11",

}

TY - JOUR

T1 - Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression

AU - Valošek, Jan

AU - Labounek, René

AU - Horák, Tomáš

AU - Horáková, Magda

AU - Bednařík, Petr

AU - Keřkovský, Miloš

AU - Kočica, Jan

AU - Rohan, Tomáš

AU - Lenglet, Christophe

AU - Cohen-Adad, Julien

AU - Hluštík, Petr

AU - Vlčková, Eva

AU - Kadaňka, Zdeněk

AU - Bednařík, Josef

AU - Svatkova, Alena

N1 - Funding Information: The core facility Multimodal and Functional Imaging Laboratory, Masaryk University, CEITEC, supported by the MEYS CR (LM2018129 Czech‐BioImaging) is acknowledged. This research is funded by the Czech Health Research Council grants NV18‐04‐00159 and by the Ministry of Health of the Czech Republic project for conceptual development in research organizations, ref. 65269705 (University Hospital, Brno, Czech Republic). JV has received “Aktion Österreich‐Tschechien, AÖCZ‐Semesterstipendien” scholarship MPC‐2020‐00013 from Austrian Agency for International Cooperation in Education and Research (OeAD‐GmbH), Mobility Programmes, Bilateral and Multilateral Cooperation (MPC) financed by Federal Ministry of Education, Science and Research (BMBWF) of Austria. AS has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska‐Curie grant agreement no. 794986. PB was partially supported by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (grant no. 27238) and by the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska‐Curie grant agreement no. 846793. CL is partly supported by NIH grants P41 EB027061 and P30 NS076408. Computational resources were supplied by the project “e‐Infrastruktura CZ” (e‐INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. JCA is funded by the Canada Research Chair in Quantitative Magnetic Resonance Imaging (950‐230815), the Canadian Institute of Health Research (CIHR FDN‐143263), the Canada Foundation for Innovation (32454, 34824), the Fonds de Recherche du Québec—Santé (28826), the Natural Sciences and Engineering Research Council of Canada (RGPIN‐2019‐07244), the Canada First Research Excellence Fund (IVADO and TransMedTech), the Courtois NeuroMod project and the Quebec BioImaging Network (5886, 35450). Funding Information: The core facility Multimodal and Functional Imaging Laboratory, Masaryk University, CEITEC, supported by the MEYS CR (LM2018129 Czech-BioImaging) is acknowledged. This research is funded by the Czech Health Research Council grants NV18-04-00159 and by the Ministry of Health of the Czech Republic project for conceptual development in research organizations, ref. 65269705 (University Hospital, Brno, Czech Republic). JV has received ?Aktion ?sterreich-Tschechien, A?CZ-Semesterstipendien? scholarship MPC-2020-00013 from Austrian Agency for International Cooperation in Education and Research (OeAD-GmbH), Mobility Programmes, Bilateral and Multilateral Cooperation (MPC) financed by Federal Ministry of Education, Science and Research (BMBWF) of Austria. AS has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement no. 794986. PB was partially supported by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (grant no. 27238) and by the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement no. 846793. CL is partly supported by NIH grants P41 EB027061 and P30 NS076408. Computational resources were supplied by the project ?e-Infrastruktura CZ? (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. JCA is funded by the Canada Research Chair in Quantitative Magnetic Resonance Imaging (950-230815), the Canadian Institute of Health Research (CIHR FDN-143263), the Canada Foundation for Innovation (32454, 34824), the Fonds de Recherche du Qu?bec?Sant? (28826), the Natural Sciences and Engineering Research Council of Canada (RGPIN-2019-07244), the Canada First Research Excellence Fund (IVADO and TransMedTech), the Courtois NeuroMod project and the Quebec BioImaging Network (5886, 35450). The authors would like to thank to Pavel Hok for help with data processing, Petr Kudli?ka and Veronika F?b?kov? for MRI data acquisition and Dagmar Kratochv?lov? for subject recruitment. Publisher Copyright: © 2021 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.

PY - 2021/11

Y1 - 2021/11

N2 - Background and purpose: Non-myelopathic degenerative cervical spinal cord compression (NMDC) frequently occurs throughout aging and may progress to potentially irreversible degenerative cervical myelopathy (DCM). Whereas standard clinical magnetic resonance imaging (MRI) and electrophysiological measures assess compression severity and neurological dysfunction, respectively, underlying microstructural deficits still have to be established in NMDC and DCM patients. The study aims to establish tract-specific diffusion MRI markers of electrophysiological deficits to predict the progression of asymptomatic NMDC to symptomatic DCM. Methods: High-resolution 3 T diffusion MRI was acquired for 103 NMDC and 21 DCM patients compared to 60 healthy controls to reveal diffusion alterations and relationships between tract-specific diffusion metrics and corresponding electrophysiological measures and compression severity. Relationship between the degree of DCM disability, assessed by the modified Japanese Orthopaedic Association scale, and tract-specific microstructural changes in DCM patients was also explored. Results: The study identified diffusion-derived abnormalities in the gray matter, dorsal and lateral tracts congruent with trans-synaptic degeneration and demyelination in chronic degenerative spinal cord compression with more profound alterations in DCM than NMDC. Diffusion metrics were affected in the C3-6 area as well as above the compression level at C3 with more profound rostral deficits in DCM than NMDC. Alterations in lateral motor and dorsal sensory tracts correlated with motor and sensory evoked potentials, respectively, whereas electromyography outcomes corresponded with gray matter microstructure. DCM disability corresponded with microstructure alteration in lateral columns. Conclusions: Outcomes imply the necessity of high-resolution tract-specific diffusion MRI for monitoring degenerative spinal pathology in longitudinal studies.

AB - Background and purpose: Non-myelopathic degenerative cervical spinal cord compression (NMDC) frequently occurs throughout aging and may progress to potentially irreversible degenerative cervical myelopathy (DCM). Whereas standard clinical magnetic resonance imaging (MRI) and electrophysiological measures assess compression severity and neurological dysfunction, respectively, underlying microstructural deficits still have to be established in NMDC and DCM patients. The study aims to establish tract-specific diffusion MRI markers of electrophysiological deficits to predict the progression of asymptomatic NMDC to symptomatic DCM. Methods: High-resolution 3 T diffusion MRI was acquired for 103 NMDC and 21 DCM patients compared to 60 healthy controls to reveal diffusion alterations and relationships between tract-specific diffusion metrics and corresponding electrophysiological measures and compression severity. Relationship between the degree of DCM disability, assessed by the modified Japanese Orthopaedic Association scale, and tract-specific microstructural changes in DCM patients was also explored. Results: The study identified diffusion-derived abnormalities in the gray matter, dorsal and lateral tracts congruent with trans-synaptic degeneration and demyelination in chronic degenerative spinal cord compression with more profound alterations in DCM than NMDC. Diffusion metrics were affected in the C3-6 area as well as above the compression level at C3 with more profound rostral deficits in DCM than NMDC. Alterations in lateral motor and dorsal sensory tracts correlated with motor and sensory evoked potentials, respectively, whereas electromyography outcomes corresponded with gray matter microstructure. DCM disability corresponded with microstructure alteration in lateral columns. Conclusions: Outcomes imply the necessity of high-resolution tract-specific diffusion MRI for monitoring degenerative spinal pathology in longitudinal studies.

KW - diffusion magnetic resonance imaging

KW - diffusion tensor imaging

KW - spinal cord compression

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JF - European Journal of Neurology

IS - 11

ER -

Diffusion magnetic resonance imaging reveals tract-specific microstructural correlates of electrophysiological impairments in non-myelopathic and myelopathic spinal cord compression

Abstract

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