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Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging

Periodic discharges are a rare peculiar electroencephalogram pattern, occasionally associated with motor or other clinical manifestations, usually observed in critically ill patients. Their underlying pathophysiology remains poorly understood. Epileptic spasms in clusters and periodic discharges wit...

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Autores principales: Eisermann, Monika, Fillon, Ludovic, Saitovitch, Ana, Boisgontier, Jennifer, Vinçon-Leite, Alice, Dangouloff-Ros, Volodia, Blauwblomme, Thomas, Bourgeois, Marie, Dangles, Marie-Thérèse, Coste-Zeitoun, Delphine, Vignolo-Diard, Patricia, Aubart, Mélodie, Kossorotoff, Manoelle, Hully, Marie, Losito, Emma, Chemaly, Nicole, Zilbovicius, Monica, Desguerre, Isabelle, Nabbout, Rima, Boddaert, Nathalie, Kaminska, Anna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9598541/
https://www.ncbi.nlm.nih.gov/pubmed/36324869
http://dx.doi.org/10.1093/braincomms/fcac250
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author Eisermann, Monika
Fillon, Ludovic
Saitovitch, Ana
Boisgontier, Jennifer
Vinçon-Leite, Alice
Dangouloff-Ros, Volodia
Blauwblomme, Thomas
Bourgeois, Marie
Dangles, Marie-Thérèse
Coste-Zeitoun, Delphine
Vignolo-Diard, Patricia
Aubart, Mélodie
Kossorotoff, Manoelle
Hully, Marie
Losito, Emma
Chemaly, Nicole
Zilbovicius, Monica
Desguerre, Isabelle
Nabbout, Rima
Boddaert, Nathalie
Kaminska, Anna
author_facet Eisermann, Monika
Fillon, Ludovic
Saitovitch, Ana
Boisgontier, Jennifer
Vinçon-Leite, Alice
Dangouloff-Ros, Volodia
Blauwblomme, Thomas
Bourgeois, Marie
Dangles, Marie-Thérèse
Coste-Zeitoun, Delphine
Vignolo-Diard, Patricia
Aubart, Mélodie
Kossorotoff, Manoelle
Hully, Marie
Losito, Emma
Chemaly, Nicole
Zilbovicius, Monica
Desguerre, Isabelle
Nabbout, Rima
Boddaert, Nathalie
Kaminska, Anna
author_sort Eisermann, Monika
collection PubMed
description Periodic discharges are a rare peculiar electroencephalogram pattern, occasionally associated with motor or other clinical manifestations, usually observed in critically ill patients. Their underlying pathophysiology remains poorly understood. Epileptic spasms in clusters and periodic discharges with motor manifestations share similar electroencephalogram pattern and some aetiologies of unfavourable prognosis such as subacute sclerosing panencephalitis or herpes encephalitis. Arterial spin labelling magnetic resonance imaging identifies localizing ictal and inter-ictal changes in neurovascular coupling, therefore assumed able to reveal concerned cerebral structures. Here, we retrospectively analysed ictal and inter-ictal arterial spin labelling magnetic resonance imaging in patients aged 6 months to 15 years (median 3 years 4 months) with periodic discharges including epileptic spasms, and compared these findings with those of patients with drug-resistant focal epilepsy who never presented periodic discharges nor epileptic spasms as well as to those of age-matched healthy controls. Ictal electroencephalogram was recorded either simultaneously with arterial spin labelling magnetic resonance imaging or during the close time lapse of patients’ periodic discharges, whereas inter-ictal examinations were performed during the patients’ active epilepsy but without seizures during the arterial spin labelling magnetic resonance imaging. Ictal arterial spin labelling magnetic resonance imaging was acquired in five patients with periodic discharges [subacute sclerosing panencephalitis (1), stroke-like events (3), West syndrome with cortical malformation (1), two of them also had inter-ictal arterial spin labelling magnetic resonance imaging]. Inter-ictal group included patients with drug-resistant epileptic spasms of various aetiologies (14) and structural drug-resistant focal epilepsy (8). Cortex, striatum and thalamus were segmented and divided in six functional subregions: prefrontal, motor (rostral, caudal), parietal, occipital and temporal. Rest cerebral blood flow values, absolute and relative to whole brain, were compared with those of age-matched controls for each subregion. Main findings were diffuse striatal as well as cortical motor cerebral blood flow increase during ictal examinations in generalized periodic discharges with motor manifestations (subacute sclerosing panencephalitis) and focal cerebral blood flow increase in corresponding cortical-striatal-thalamic subdivisions in lateralized periodic discharges with or without motor manifestations (stroke-like events and asymmetrical epileptic spasms) with straight topographical correlation with the electroencephalogram focus. For inter-ictal examinations, patients with epileptic spasms disclosed cerebral blood flow changes in corresponding cortical-striatal-thalamic subdivisions (absolute-cerebral blood flow decrease and relative-cerebral blood flow increase), more frequently when compared with the group of drug-resistant focal epilepsies, and not related to Vigabatrin treatment. Our results suggest that corresponding cortical-striatal-thalamic circuits are involved in periodic discharges with and without motor manifestations, including epileptic spasms, opening new insights in their pathophysiology and new therapeutical perspectives. Based on these findings, we propose a model for the generation of periodic discharges and of epileptic spasms combining existing pathophysiological models of cortical-striatal-thalamic network dynamics.
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spelling pubmed-95985412022-11-01 Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging Eisermann, Monika Fillon, Ludovic Saitovitch, Ana Boisgontier, Jennifer Vinçon-Leite, Alice Dangouloff-Ros, Volodia Blauwblomme, Thomas Bourgeois, Marie Dangles, Marie-Thérèse Coste-Zeitoun, Delphine Vignolo-Diard, Patricia Aubart, Mélodie Kossorotoff, Manoelle Hully, Marie Losito, Emma Chemaly, Nicole Zilbovicius, Monica Desguerre, Isabelle Nabbout, Rima Boddaert, Nathalie Kaminska, Anna Brain Commun Original Article Periodic discharges are a rare peculiar electroencephalogram pattern, occasionally associated with motor or other clinical manifestations, usually observed in critically ill patients. Their underlying pathophysiology remains poorly understood. Epileptic spasms in clusters and periodic discharges with motor manifestations share similar electroencephalogram pattern and some aetiologies of unfavourable prognosis such as subacute sclerosing panencephalitis or herpes encephalitis. Arterial spin labelling magnetic resonance imaging identifies localizing ictal and inter-ictal changes in neurovascular coupling, therefore assumed able to reveal concerned cerebral structures. Here, we retrospectively analysed ictal and inter-ictal arterial spin labelling magnetic resonance imaging in patients aged 6 months to 15 years (median 3 years 4 months) with periodic discharges including epileptic spasms, and compared these findings with those of patients with drug-resistant focal epilepsy who never presented periodic discharges nor epileptic spasms as well as to those of age-matched healthy controls. Ictal electroencephalogram was recorded either simultaneously with arterial spin labelling magnetic resonance imaging or during the close time lapse of patients’ periodic discharges, whereas inter-ictal examinations were performed during the patients’ active epilepsy but without seizures during the arterial spin labelling magnetic resonance imaging. Ictal arterial spin labelling magnetic resonance imaging was acquired in five patients with periodic discharges [subacute sclerosing panencephalitis (1), stroke-like events (3), West syndrome with cortical malformation (1), two of them also had inter-ictal arterial spin labelling magnetic resonance imaging]. Inter-ictal group included patients with drug-resistant epileptic spasms of various aetiologies (14) and structural drug-resistant focal epilepsy (8). Cortex, striatum and thalamus were segmented and divided in six functional subregions: prefrontal, motor (rostral, caudal), parietal, occipital and temporal. Rest cerebral blood flow values, absolute and relative to whole brain, were compared with those of age-matched controls for each subregion. Main findings were diffuse striatal as well as cortical motor cerebral blood flow increase during ictal examinations in generalized periodic discharges with motor manifestations (subacute sclerosing panencephalitis) and focal cerebral blood flow increase in corresponding cortical-striatal-thalamic subdivisions in lateralized periodic discharges with or without motor manifestations (stroke-like events and asymmetrical epileptic spasms) with straight topographical correlation with the electroencephalogram focus. For inter-ictal examinations, patients with epileptic spasms disclosed cerebral blood flow changes in corresponding cortical-striatal-thalamic subdivisions (absolute-cerebral blood flow decrease and relative-cerebral blood flow increase), more frequently when compared with the group of drug-resistant focal epilepsies, and not related to Vigabatrin treatment. Our results suggest that corresponding cortical-striatal-thalamic circuits are involved in periodic discharges with and without motor manifestations, including epileptic spasms, opening new insights in their pathophysiology and new therapeutical perspectives. Based on these findings, we propose a model for the generation of periodic discharges and of epileptic spasms combining existing pathophysiological models of cortical-striatal-thalamic network dynamics. Oxford University Press 2022-10-06 /pmc/articles/PMC9598541/ /pubmed/36324869 http://dx.doi.org/10.1093/braincomms/fcac250 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Eisermann, Monika
Fillon, Ludovic
Saitovitch, Ana
Boisgontier, Jennifer
Vinçon-Leite, Alice
Dangouloff-Ros, Volodia
Blauwblomme, Thomas
Bourgeois, Marie
Dangles, Marie-Thérèse
Coste-Zeitoun, Delphine
Vignolo-Diard, Patricia
Aubart, Mélodie
Kossorotoff, Manoelle
Hully, Marie
Losito, Emma
Chemaly, Nicole
Zilbovicius, Monica
Desguerre, Isabelle
Nabbout, Rima
Boddaert, Nathalie
Kaminska, Anna
Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging
title Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging
title_full Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging
title_fullStr Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging
title_full_unstemmed Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging
title_short Periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on Arterial Spin Labeling Magnetic Resonance Imaging
title_sort periodic electroencephalographic discharges and epileptic spasms involve cortico-striatal-thalamic loops on arterial spin labeling magnetic resonance imaging
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9598541/
https://www.ncbi.nlm.nih.gov/pubmed/36324869
http://dx.doi.org/10.1093/braincomms/fcac250
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