The spinal and cerebral profile of adult spinal-muscular atrophy: A multimodal imaging study

Giorgia Querin; Mohamed Mounir El Mendili; Timothée Lenglet; Anthony Behin; Tanya Stojkovic; François Salachas; David Devos; Nadine Le Forestier; Maria del Mar Amador; Rabab Debs; Lucette Lacomblez; Vincent Meninger; Gaëlle Bruneteau; Julien Cohen-Adad; Stéphane Lehéricy; Pascal Laforêt; Sophie Blancho; Habib Benali; Martin Catala; Menghan Li; Véronique Marchand-Pauvert; Jean Yves Hogrel; Peter Bede; Pierre François Pradat

doi:10.1016/j.nicl.2018.101618

The spinal and cerebral profile of adult spinal-muscular atrophy: A multimodal imaging study

Giorgia Querin
, Mohamed Mounir El Mendili
, Timothée Lenglet
, Anthony Behin
, Tanya Stojkovic
, François Salachas
, David Devos
, Nadine Le Forestier
, Maria del Mar Amador
, Rabab Debs
, Lucette Lacomblez
, Vincent Meninger
, Gaëlle Bruneteau
, Julien Cohen-Adad
, Stéphane Lehéricy
, Pascal Laforêt
, Sophie Blancho
, Habib Benali
, Martin Catala
, Menghan Li

Véronique Marchand-Pauvert, Jean Yves Hogrel, Peter Bede, Pierre François Pradat

School of Biomedical Sciences

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

74 Citations (Scopus)

49 Downloads (Pure)

Abstract

Spinal muscular atrophy (SMA) type III and IV are autosomal recessive, slowly progressive lower motor neuron syndromes. Nevertheless, wider cerebral involvement has been consistently reported in mouse models. The objective of this study is the characterisation of spinal and cerebral pathology in adult forms of SMA using multimodal quantitative imaging. Methods: Twenty-five type III and IV adult SMA patients and 25 age-matched healthy controls were enrolled in a spinal cord and brain imaging study. Structural measures of grey and white matter involvement and diffusion parameters of white matter integrity were evaluated at each cervical spinal level. Whole-brain and region-of-interest analyses were also conducted in the brain to explore cortical thickness, grey matter density and tract-based white matter alterations. Results: In the spinal cord, considerable grey matter atrophy was detected between C2-C6 vertebral levels. In the brain, increased grey matter density was detected in motor and extra-motor regions of SMA patients. No white matter pathology was identified neither at brain and spinal level. Conclusions: Adult forms of SMA are associated with selective grey matter degeneration in the spinal cord with preserved white matter integrity. The observed increased grey matter density in the motor cortex may represent adaptive reorganisation.

Original language	English
Article number	101618
Pages (from-to)	1-9
Number of pages	9
Journal	NeuroImage: Clinical
Volume	21
Early online date	28 Nov 2018
DOIs	https://doi.org/10.1016/j.nicl.2018.101618
Publication status	Published (in print/issue) - 28 Feb 2019

Funding

This study was supported by the Association Française contre les Myopathies (AFM) and the Institut pour la Recherche sur la Moelle épinière et l'Encéphale (IRME). The research leading to these results has also received funding from the program “ Investissements d'avenir ” ANR-10-IAIHU-06. This study was sponsored by Association Française contre les Myopathies (AFM) and the Institut pour la Recherche sur la Moelle épinière et l'Encéphale (IRME). The research leading to these results has also received funding from the program “ Investissements d'avenir ” ANR-10-IAIHU-06. Dr. Giorgia Querin, Dr. Mohamed-Mounir El Mendili, Dr. Timothée Lenglet, Dr. Anthony Behin, Dr. Tanya Stojkovic, Dr. François Salachas, Dr. Nadine Le Forestier, Dr. Maria del Mar Amador, Dr. Rabab Debs, Dr. Lucette Lacomblez, Prof. Vincent Meninger, Dr. Gaelle Brunetau, De Julien Cohen-Adad, Prof. Pascal Laforêt and Prof. Stéphane Lehéricy, Sophie Blancho, Dr. Habib Benali, Dr. Martin Catala, Prof. Véronique Marchand-Pauvert, Dr. Jean-Yves Hogrel and Prof. Pierre-François Pradat report no disclosures. Prof. Peter Bede is supported by the Health Research Board (HRB – Ireland; HRB EIA-2017-019), the Irish Institute of Clinical Neuroscience IICN − Novartis Ireland Research Grant, and the Iris O'Brien Foundation Ireland. We gratefully acknowledge the kindness and generosity of our patients for participating in this study, their caregivers and our control participants. We thank Eric Bardinet for his contribution to data acquisition and Dr. Henrik Lundell for his computational assistance to quantify spinal cord dimensions. We thank Gwenn Olivier for her technical assistance in the functional evaluation. This study was supported by the Association Française contre les Myopathies (AFM) and the Institut pour la Recherche sur la Moelle épinière et l'Encéphale (IRME). The research leading to these results has also received funding from the program “ Investissements d'avenir ” ANR-10-IAIHU-06. Peter Bede is supported by the Health Research Board (HRB – Ireland; HRB EIA-2017-019), the Irish Institute of Clinical Neuroscience IICN − Novartis Ireland Research Grant, and the Iris O'Brien Foundation Ireland.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

Grey matter and white matter degeneration
Multimodal MRI
SMA
Spinal cord MRI
Spinal muscular atrophy

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10.1016/j.nicl.2018.101618

1-s2.0-S2213158218303668-mainFinal published version, 2.2 MBLicence: CC BY-NC-ND

Cite this

Querin, G., El Mendili, M. M., Lenglet, T., Behin, A., Stojkovic, T., Salachas, F., Devos, D., Le Forestier, N., del Mar Amador, M., Debs, R., Lacomblez, L., Meninger, V., Bruneteau, G., Cohen-Adad, J., Lehéricy, S., Laforêt, P., Blancho, S., Benali, H., Catala, M., ... Pradat, P. F. (2019). The spinal and cerebral profile of adult spinal-muscular atrophy: A multimodal imaging study. NeuroImage: Clinical, 21, 1-9. Article 101618. https://doi.org/10.1016/j.nicl.2018.101618

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title = "The spinal and cerebral profile of adult spinal-muscular atrophy: A multimodal imaging study",

abstract = "Spinal muscular atrophy (SMA) type III and IV are autosomal recessive, slowly progressive lower motor neuron syndromes. Nevertheless, wider cerebral involvement has been consistently reported in mouse models. The objective of this study is the characterisation of spinal and cerebral pathology in adult forms of SMA using multimodal quantitative imaging. Methods: Twenty-five type III and IV adult SMA patients and 25 age-matched healthy controls were enrolled in a spinal cord and brain imaging study. Structural measures of grey and white matter involvement and diffusion parameters of white matter integrity were evaluated at each cervical spinal level. Whole-brain and region-of-interest analyses were also conducted in the brain to explore cortical thickness, grey matter density and tract-based white matter alterations. Results: In the spinal cord, considerable grey matter atrophy was detected between C2-C6 vertebral levels. In the brain, increased grey matter density was detected in motor and extra-motor regions of SMA patients. No white matter pathology was identified neither at brain and spinal level. Conclusions: Adult forms of SMA are associated with selective grey matter degeneration in the spinal cord with preserved white matter integrity. The observed increased grey matter density in the motor cortex may represent adaptive reorganisation.",

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author = "Giorgia Querin and \{El Mendili\}, \{Mohamed Mounir\} and Timoth{\'e}e Lenglet and Anthony Behin and Tanya Stojkovic and Fran{\c c}ois Salachas and David Devos and \{Le Forestier\}, Nadine and \{del Mar Amador\}, Maria and Rabab Debs and Lucette Lacomblez and Vincent Meninger and Ga{\"e}lle Bruneteau and Julien Cohen-Adad and St{\'e}phane Leh{\'e}ricy and Pascal Lafor{\^e}t and Sophie Blancho and Habib Benali and Martin Catala and Menghan Li and V{\'e}ronique Marchand-Pauvert and Hogrel, \{Jean Yves\} and Peter Bede and Pradat, \{Pierre Fran{\c c}ois\}",

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Querin, G, El Mendili, MM, Lenglet, T, Behin, A, Stojkovic, T, Salachas, F, Devos, D, Le Forestier, N, del Mar Amador, M, Debs, R, Lacomblez, L, Meninger, V, Bruneteau, G, Cohen-Adad, J, Lehéricy, S, Laforêt, P, Blancho, S, Benali, H, Catala, M, Li, M, Marchand-Pauvert, V, Hogrel, JY, Bede, P & Pradat, PF 2019, 'The spinal and cerebral profile of adult spinal-muscular atrophy: A multimodal imaging study', NeuroImage: Clinical, vol. 21, 101618, pp. 1-9. https://doi.org/10.1016/j.nicl.2018.101618

TY - JOUR

T1 - The spinal and cerebral profile of adult spinal-muscular atrophy

T2 - A multimodal imaging study

AU - Querin, Giorgia

AU - El Mendili, Mohamed Mounir

AU - Lenglet, Timothée

AU - Behin, Anthony

AU - Stojkovic, Tanya

AU - Salachas, François

AU - Devos, David

AU - Le Forestier, Nadine

AU - del Mar Amador, Maria

AU - Debs, Rabab

AU - Lacomblez, Lucette

AU - Meninger, Vincent

AU - Bruneteau, Gaëlle

AU - Cohen-Adad, Julien

AU - Lehéricy, Stéphane

AU - Laforêt, Pascal

AU - Blancho, Sophie

AU - Benali, Habib

AU - Catala, Martin

AU - Li, Menghan

AU - Marchand-Pauvert, Véronique

AU - Hogrel, Jean Yves

AU - Bede, Peter

AU - Pradat, Pierre François

PY - 2019/2/28

Y1 - 2019/2/28

N2 - Spinal muscular atrophy (SMA) type III and IV are autosomal recessive, slowly progressive lower motor neuron syndromes. Nevertheless, wider cerebral involvement has been consistently reported in mouse models. The objective of this study is the characterisation of spinal and cerebral pathology in adult forms of SMA using multimodal quantitative imaging. Methods: Twenty-five type III and IV adult SMA patients and 25 age-matched healthy controls were enrolled in a spinal cord and brain imaging study. Structural measures of grey and white matter involvement and diffusion parameters of white matter integrity were evaluated at each cervical spinal level. Whole-brain and region-of-interest analyses were also conducted in the brain to explore cortical thickness, grey matter density and tract-based white matter alterations. Results: In the spinal cord, considerable grey matter atrophy was detected between C2-C6 vertebral levels. In the brain, increased grey matter density was detected in motor and extra-motor regions of SMA patients. No white matter pathology was identified neither at brain and spinal level. Conclusions: Adult forms of SMA are associated with selective grey matter degeneration in the spinal cord with preserved white matter integrity. The observed increased grey matter density in the motor cortex may represent adaptive reorganisation.

AB - Spinal muscular atrophy (SMA) type III and IV are autosomal recessive, slowly progressive lower motor neuron syndromes. Nevertheless, wider cerebral involvement has been consistently reported in mouse models. The objective of this study is the characterisation of spinal and cerebral pathology in adult forms of SMA using multimodal quantitative imaging. Methods: Twenty-five type III and IV adult SMA patients and 25 age-matched healthy controls were enrolled in a spinal cord and brain imaging study. Structural measures of grey and white matter involvement and diffusion parameters of white matter integrity were evaluated at each cervical spinal level. Whole-brain and region-of-interest analyses were also conducted in the brain to explore cortical thickness, grey matter density and tract-based white matter alterations. Results: In the spinal cord, considerable grey matter atrophy was detected between C2-C6 vertebral levels. In the brain, increased grey matter density was detected in motor and extra-motor regions of SMA patients. No white matter pathology was identified neither at brain and spinal level. Conclusions: Adult forms of SMA are associated with selective grey matter degeneration in the spinal cord with preserved white matter integrity. The observed increased grey matter density in the motor cortex may represent adaptive reorganisation.

KW - Grey matter and white matter degeneration

KW - Multimodal MRI

KW - SMA

KW - Spinal cord MRI

KW - Spinal muscular atrophy

UR - https://www.scopus.com/pages/publications/85057774911

U2 - 10.1016/j.nicl.2018.101618

DO - 10.1016/j.nicl.2018.101618

M3 - Article

C2 - 30522974

AN - SCOPUS:85057774911

SN - 2213-1582

VL - 21

SP - 1

EP - 9

JO - NeuroImage: Clinical

JF - NeuroImage: Clinical

M1 - 101618

ER -

The spinal and cerebral profile of adult spinal-muscular atrophy: A multimodal imaging study

Abstract

Funding

UN SDGs

Keywords

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