Metabolic voxel-based analysis of the complete human brain using fast 3D-MRSI: Proof of concept in multiple sclerosis

Maxime Donadieu, Yann Le Fur, Angèle Lecocq, Andrew A Maudsley, Soraya Gherib, Elisabeth Soulier, Sylviane Confort-Gouny, Fanelly Pariollaud, Marie Pierre Ranjeva, Jean Pelletier, Maxime Guye, Wafaa Zaaraoui, Bertrand Audoin, Jean Philippe Ranjeva

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Purpose: To detect local metabolic abnormalities over the complete human brain in multiple sclerosis (MS) patients, we used optimized fast volumic echo planar spectroscopic imaging (3D-EPSI). Materials and Methods: Weighted mean combination of two 3D-EPSI covering the whole brain acquired at 3T in AC-PC and AC-PC+15° axial planes was performed to obtain high-quality metabolite maps for five metabolites: N-acetyl aspartate (NAA), glutamate+glutamine (Glx), choline (Cho), myo-inositol (m-Ins), and creatine+phosphocreatine (tCr). After spatial normalization, maps from 19 patients suffering from relapsing-remitting MS were compared to 19 matched controls using statistical mapping analyses to determine the topography of metabolic abnormalities. Probabilistic white matter (WM) T2 lesion maps and gray matter (GM) atrophy maps were also generated. Results: Two-group analysis of variance (ANOVA) (SPM8, P < 0.005, false discovery rate [FDR]-corrected P < 0.05 at the cluster level with age and sex as confounding covariates) comparing patients and controls matched for age and sex showed clusters of abnormal metabolite levels with 1) decreased NAA (around –15%) and Glx (around 20%) predominantly in GM within prefrontal cortices, motor cortices, bilateral thalami, and mesial temporal cortices in line with neuronal/neuro-astrocytic dysfunction; 2) increased m-Ins (around + 20%) inside WM T2 lesions and in the normal-appearing WM of temporal-occipital lobes, suggesting glial activation. Conclusion: We demonstrate the ability to noninvasively map over the complete brain—from vertex to cerebellum—with a validated sequence, the metabolic abnormalities associated with MS, for characterizing the topography of pathological processes affecting widespread areas of WM and GM and its functional impact. J. Magn. Reson. Imaging 2016;44:411–419.

Original languageEnglish (US)
Pages (from-to)411-419
Number of pages9
JournalJournal of Magnetic Resonance Imaging
Volume44
Issue number2
DOIs
StatePublished - Aug 1 2016

Fingerprint

Multiple Sclerosis
Brain
Inositol
Temporal Lobe
Echo-Planar Imaging
Relapsing-Remitting Multiple Sclerosis
Occipital Lobe
Phosphocreatine
Creatine
Motor Cortex
Pathologic Processes
Choline
Prefrontal Cortex
Glutamine
Thalamus
Neuroglia
Atrophy
Glutamic Acid
Analysis of Variance
White Matter

Keywords

  • inflammation
  • multiple sclerosis
  • neurodegeneration
  • proton magnetic resonance spectroscopic imaging
  • statistical mapping analysis
  • whole brain

ASJC Scopus subject areas

  • Radiology Nuclear Medicine and imaging

Cite this

Metabolic voxel-based analysis of the complete human brain using fast 3D-MRSI : Proof of concept in multiple sclerosis. / Donadieu, Maxime; Le Fur, Yann; Lecocq, Angèle; Maudsley, Andrew A; Gherib, Soraya; Soulier, Elisabeth; Confort-Gouny, Sylviane; Pariollaud, Fanelly; Ranjeva, Marie Pierre; Pelletier, Jean; Guye, Maxime; Zaaraoui, Wafaa; Audoin, Bertrand; Ranjeva, Jean Philippe.

In: Journal of Magnetic Resonance Imaging, Vol. 44, No. 2, 01.08.2016, p. 411-419.

Research output: Contribution to journalArticle

Donadieu, M, Le Fur, Y, Lecocq, A, Maudsley, AA, Gherib, S, Soulier, E, Confort-Gouny, S, Pariollaud, F, Ranjeva, MP, Pelletier, J, Guye, M, Zaaraoui, W, Audoin, B & Ranjeva, JP 2016, 'Metabolic voxel-based analysis of the complete human brain using fast 3D-MRSI: Proof of concept in multiple sclerosis', Journal of Magnetic Resonance Imaging, vol. 44, no. 2, pp. 411-419. https://doi.org/10.1002/jmri.25139
Donadieu, Maxime ; Le Fur, Yann ; Lecocq, Angèle ; Maudsley, Andrew A ; Gherib, Soraya ; Soulier, Elisabeth ; Confort-Gouny, Sylviane ; Pariollaud, Fanelly ; Ranjeva, Marie Pierre ; Pelletier, Jean ; Guye, Maxime ; Zaaraoui, Wafaa ; Audoin, Bertrand ; Ranjeva, Jean Philippe. / Metabolic voxel-based analysis of the complete human brain using fast 3D-MRSI : Proof of concept in multiple sclerosis. In: Journal of Magnetic Resonance Imaging. 2016 ; Vol. 44, No. 2. pp. 411-419.
@article{ce896857c11e4548a361b13cb4b6af4b,
title = "Metabolic voxel-based analysis of the complete human brain using fast 3D-MRSI: Proof of concept in multiple sclerosis",
abstract = "Purpose: To detect local metabolic abnormalities over the complete human brain in multiple sclerosis (MS) patients, we used optimized fast volumic echo planar spectroscopic imaging (3D-EPSI). Materials and Methods: Weighted mean combination of two 3D-EPSI covering the whole brain acquired at 3T in AC-PC and AC-PC+15° axial planes was performed to obtain high-quality metabolite maps for five metabolites: N-acetyl aspartate (NAA), glutamate+glutamine (Glx), choline (Cho), myo-inositol (m-Ins), and creatine+phosphocreatine (tCr). After spatial normalization, maps from 19 patients suffering from relapsing-remitting MS were compared to 19 matched controls using statistical mapping analyses to determine the topography of metabolic abnormalities. Probabilistic white matter (WM) T2 lesion maps and gray matter (GM) atrophy maps were also generated. Results: Two-group analysis of variance (ANOVA) (SPM8, P < 0.005, false discovery rate [FDR]-corrected P < 0.05 at the cluster level with age and sex as confounding covariates) comparing patients and controls matched for age and sex showed clusters of abnormal metabolite levels with 1) decreased NAA (around –15{\%}) and Glx (around 20{\%}) predominantly in GM within prefrontal cortices, motor cortices, bilateral thalami, and mesial temporal cortices in line with neuronal/neuro-astrocytic dysfunction; 2) increased m-Ins (around + 20{\%}) inside WM T2 lesions and in the normal-appearing WM of temporal-occipital lobes, suggesting glial activation. Conclusion: We demonstrate the ability to noninvasively map over the complete brain—from vertex to cerebellum—with a validated sequence, the metabolic abnormalities associated with MS, for characterizing the topography of pathological processes affecting widespread areas of WM and GM and its functional impact. J. Magn. Reson. Imaging 2016;44:411–419.",
keywords = "inflammation, multiple sclerosis, neurodegeneration, proton magnetic resonance spectroscopic imaging, statistical mapping analysis, whole brain",
author = "Maxime Donadieu and {Le Fur}, Yann and Ang{\`e}le Lecocq and Maudsley, {Andrew A} and Soraya Gherib and Elisabeth Soulier and Sylviane Confort-Gouny and Fanelly Pariollaud and Ranjeva, {Marie Pierre} and Jean Pelletier and Maxime Guye and Wafaa Zaaraoui and Bertrand Audoin and Ranjeva, {Jean Philippe}",
year = "2016",
month = "8",
day = "1",
doi = "10.1002/jmri.25139",
language = "English (US)",
volume = "44",
pages = "411--419",
journal = "Journal of Magnetic Resonance Imaging",
issn = "1053-1807",
publisher = "John Wiley and Sons Inc.",
number = "2",

}

TY - JOUR

T1 - Metabolic voxel-based analysis of the complete human brain using fast 3D-MRSI

T2 - Proof of concept in multiple sclerosis

AU - Donadieu, Maxime

AU - Le Fur, Yann

AU - Lecocq, Angèle

AU - Maudsley, Andrew A

AU - Gherib, Soraya

AU - Soulier, Elisabeth

AU - Confort-Gouny, Sylviane

AU - Pariollaud, Fanelly

AU - Ranjeva, Marie Pierre

AU - Pelletier, Jean

AU - Guye, Maxime

AU - Zaaraoui, Wafaa

AU - Audoin, Bertrand

AU - Ranjeva, Jean Philippe

PY - 2016/8/1

Y1 - 2016/8/1

N2 - Purpose: To detect local metabolic abnormalities over the complete human brain in multiple sclerosis (MS) patients, we used optimized fast volumic echo planar spectroscopic imaging (3D-EPSI). Materials and Methods: Weighted mean combination of two 3D-EPSI covering the whole brain acquired at 3T in AC-PC and AC-PC+15° axial planes was performed to obtain high-quality metabolite maps for five metabolites: N-acetyl aspartate (NAA), glutamate+glutamine (Glx), choline (Cho), myo-inositol (m-Ins), and creatine+phosphocreatine (tCr). After spatial normalization, maps from 19 patients suffering from relapsing-remitting MS were compared to 19 matched controls using statistical mapping analyses to determine the topography of metabolic abnormalities. Probabilistic white matter (WM) T2 lesion maps and gray matter (GM) atrophy maps were also generated. Results: Two-group analysis of variance (ANOVA) (SPM8, P < 0.005, false discovery rate [FDR]-corrected P < 0.05 at the cluster level with age and sex as confounding covariates) comparing patients and controls matched for age and sex showed clusters of abnormal metabolite levels with 1) decreased NAA (around –15%) and Glx (around 20%) predominantly in GM within prefrontal cortices, motor cortices, bilateral thalami, and mesial temporal cortices in line with neuronal/neuro-astrocytic dysfunction; 2) increased m-Ins (around + 20%) inside WM T2 lesions and in the normal-appearing WM of temporal-occipital lobes, suggesting glial activation. Conclusion: We demonstrate the ability to noninvasively map over the complete brain—from vertex to cerebellum—with a validated sequence, the metabolic abnormalities associated with MS, for characterizing the topography of pathological processes affecting widespread areas of WM and GM and its functional impact. J. Magn. Reson. Imaging 2016;44:411–419.

AB - Purpose: To detect local metabolic abnormalities over the complete human brain in multiple sclerosis (MS) patients, we used optimized fast volumic echo planar spectroscopic imaging (3D-EPSI). Materials and Methods: Weighted mean combination of two 3D-EPSI covering the whole brain acquired at 3T in AC-PC and AC-PC+15° axial planes was performed to obtain high-quality metabolite maps for five metabolites: N-acetyl aspartate (NAA), glutamate+glutamine (Glx), choline (Cho), myo-inositol (m-Ins), and creatine+phosphocreatine (tCr). After spatial normalization, maps from 19 patients suffering from relapsing-remitting MS were compared to 19 matched controls using statistical mapping analyses to determine the topography of metabolic abnormalities. Probabilistic white matter (WM) T2 lesion maps and gray matter (GM) atrophy maps were also generated. Results: Two-group analysis of variance (ANOVA) (SPM8, P < 0.005, false discovery rate [FDR]-corrected P < 0.05 at the cluster level with age and sex as confounding covariates) comparing patients and controls matched for age and sex showed clusters of abnormal metabolite levels with 1) decreased NAA (around –15%) and Glx (around 20%) predominantly in GM within prefrontal cortices, motor cortices, bilateral thalami, and mesial temporal cortices in line with neuronal/neuro-astrocytic dysfunction; 2) increased m-Ins (around + 20%) inside WM T2 lesions and in the normal-appearing WM of temporal-occipital lobes, suggesting glial activation. Conclusion: We demonstrate the ability to noninvasively map over the complete brain—from vertex to cerebellum—with a validated sequence, the metabolic abnormalities associated with MS, for characterizing the topography of pathological processes affecting widespread areas of WM and GM and its functional impact. J. Magn. Reson. Imaging 2016;44:411–419.

KW - inflammation

KW - multiple sclerosis

KW - neurodegeneration

KW - proton magnetic resonance spectroscopic imaging

KW - statistical mapping analysis

KW - whole brain

UR - http://www.scopus.com/inward/record.url?scp=84990222674&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84990222674&partnerID=8YFLogxK

U2 - 10.1002/jmri.25139

DO - 10.1002/jmri.25139

M3 - Article

C2 - 26756662

AN - SCOPUS:84990222674

VL - 44

SP - 411

EP - 419

JO - Journal of Magnetic Resonance Imaging

JF - Journal of Magnetic Resonance Imaging

SN - 1053-1807

IS - 2

ER -