Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions

In light of technical advancements supporting exploration of MR signals other than 1H, sodium (23Na) has received attention as a marker of ionic homeostasis and cell viability. Here, we evaluate for the first time the possibility that 23Na-MRI is sensitive to pathological processes occurring in huma...

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Main Authors: Ben Ridley, Angela Marchi, Jonathan Wirsich, Elisabeth Soulier, Sylviane Confort-Gouny, Lothar Schad, Fabrice Bartolomei, Jean-Philippe Ranjeva, Maxime Guye, Wafaa Zaaraoui
Format: Article
Language:English
Published: Elsevier 2017-08-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811917304809
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author Ben Ridley
Angela Marchi
Jonathan Wirsich
Elisabeth Soulier
Sylviane Confort-Gouny
Lothar Schad
Fabrice Bartolomei
Jean-Philippe Ranjeva
Maxime Guye
Wafaa Zaaraoui
author_facet Ben Ridley
Angela Marchi
Jonathan Wirsich
Elisabeth Soulier
Sylviane Confort-Gouny
Lothar Schad
Fabrice Bartolomei
Jean-Philippe Ranjeva
Maxime Guye
Wafaa Zaaraoui
author_sort Ben Ridley
collection DOAJ
description In light of technical advancements supporting exploration of MR signals other than 1H, sodium (23Na) has received attention as a marker of ionic homeostasis and cell viability. Here, we evaluate for the first time the possibility that 23Na-MRI is sensitive to pathological processes occurring in human epilepsy. A normative sample of 27 controls was used to normalize regions of interest (ROIs) from 1424 unique brain locales on quantitative 23Na-MRI and high-resolution 1H-MPRAGE images. ROIs were based on intracerebral electrodes in ten patients undergoing epileptic network mapping. The stereo-EEG gold standard was used to define regions as belonging to primarily epileptogenic, secondarily irritative and to non-involved regions. Estimates of total sodium concentration (TSC) on 23Na-MRI and cerebrospinal fluid (CSF) on 1H imaging were extracted for each patient ROI, and normalized against the same region in controls. ROIs with disproportionate CSF contributions (ZCSF≥1.96) were excluded. TSC levels were found to be elevated in patients relative to controls except in one patient, who suffered non-convulsive seizures during the scan, in whom we found reduced TSC levels. In the remaining patients, an ANOVA (F1100= 12.37, p<0.0001) revealed a highly significant effect of clinically-defined zones (F1100= 11.13, p<0.0001), with higher normalized TSC in the epileptogenic zone relative to both secondarily irritative (F1100= 11, p=0.0009) and non-involved regions (F1100= 17.8, p<0.0001). We provide the first non-invasive, in vivo evidence of a chronic TSC elevation alongside ZCSF levels within the normative range, associated with the epileptogenic region even during the interictal period in human epilepsy, and the possibility of reduced TSC levels due to seizure. In line with modified homeostatic mechanisms in epilepsy – including altered mechanisms underlying ionic gating, clearance and exchange – we provide the first indication of 23Na-MRI as an assay of altered sodium concentrations occurring in epilepsy associated with the organization of clinically relevant divisions of pathological cortex.
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spelling doaj.art-01995569fb2c46fdaafff3d92f35013f2022-12-22T00:57:35ZengElsevierNeuroImage1095-95722017-08-01157173183Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regionsBen Ridley0Angela Marchi1Jonathan Wirsich2Elisabeth Soulier3Sylviane Confort-Gouny4Lothar Schad5Fabrice Bartolomei6Jean-Philippe Ranjeva7Maxime Guye8Wafaa Zaaraoui9Aix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, FranceAPHM, Hôpital de la Timone, Clinical Neurophysiology and Epileptology Department, Marseille, France; Aix Marseille Univ, Inserm, INS, Institut de Neurosciences des Systèmes, Marseille, FranceAix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, France; Aix Marseille Univ, Inserm, INS, Institut de Neurosciences des Systèmes, Marseille, FranceAix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, FranceAix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, FranceComputer Assisted Clinical Medicine, Heidelberg University, Mannheim, GermanyAix Marseille Univ, Inserm, INS, Institut de Neurosciences des Systèmes, Marseille, France; APHM, Hôpitaux de la Timone, Service de Neurophysiologie Clinique, Marseille, FranceAix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, FranceAix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, France; Correspondnce to: CRMBM UMR CNRS 7339, Aix-Marseille Université, 27 Bd Jean Moulin, 13005 Marseille, France.Aix-Marseille Univ, CNRS, CRMBM UMR 7339, Marseille, France; APHM, Hôpital de la Timone, Pôle d′Imagerie Médicale, CEMEREM, Marseille, FranceIn light of technical advancements supporting exploration of MR signals other than 1H, sodium (23Na) has received attention as a marker of ionic homeostasis and cell viability. Here, we evaluate for the first time the possibility that 23Na-MRI is sensitive to pathological processes occurring in human epilepsy. A normative sample of 27 controls was used to normalize regions of interest (ROIs) from 1424 unique brain locales on quantitative 23Na-MRI and high-resolution 1H-MPRAGE images. ROIs were based on intracerebral electrodes in ten patients undergoing epileptic network mapping. The stereo-EEG gold standard was used to define regions as belonging to primarily epileptogenic, secondarily irritative and to non-involved regions. Estimates of total sodium concentration (TSC) on 23Na-MRI and cerebrospinal fluid (CSF) on 1H imaging were extracted for each patient ROI, and normalized against the same region in controls. ROIs with disproportionate CSF contributions (ZCSF≥1.96) were excluded. TSC levels were found to be elevated in patients relative to controls except in one patient, who suffered non-convulsive seizures during the scan, in whom we found reduced TSC levels. In the remaining patients, an ANOVA (F1100= 12.37, p<0.0001) revealed a highly significant effect of clinically-defined zones (F1100= 11.13, p<0.0001), with higher normalized TSC in the epileptogenic zone relative to both secondarily irritative (F1100= 11, p=0.0009) and non-involved regions (F1100= 17.8, p<0.0001). We provide the first non-invasive, in vivo evidence of a chronic TSC elevation alongside ZCSF levels within the normative range, associated with the epileptogenic region even during the interictal period in human epilepsy, and the possibility of reduced TSC levels due to seizure. In line with modified homeostatic mechanisms in epilepsy – including altered mechanisms underlying ionic gating, clearance and exchange – we provide the first indication of 23Na-MRI as an assay of altered sodium concentrations occurring in epilepsy associated with the organization of clinically relevant divisions of pathological cortex.http://www.sciencedirect.com/science/article/pii/S1053811917304809Sodium MRIEpilepsyIntracranial EEGCortical localisationEpilepsy surgeryIonic imaging
spellingShingle Ben Ridley
Angela Marchi
Jonathan Wirsich
Elisabeth Soulier
Sylviane Confort-Gouny
Lothar Schad
Fabrice Bartolomei
Jean-Philippe Ranjeva
Maxime Guye
Wafaa Zaaraoui
Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions
NeuroImage
Sodium MRI
Epilepsy
Intracranial EEG
Cortical localisation
Epilepsy surgery
Ionic imaging
title Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions
title_full Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions
title_fullStr Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions
title_full_unstemmed Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions
title_short Brain sodium MRI in human epilepsy: Disturbances of ionic homeostasis reflect the organization of pathological regions
title_sort brain sodium mri in human epilepsy disturbances of ionic homeostasis reflect the organization of pathological regions
topic Sodium MRI
Epilepsy
Intracranial EEG
Cortical localisation
Epilepsy surgery
Ionic imaging
url http://www.sciencedirect.com/science/article/pii/S1053811917304809
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