Spatial patterns of gray and white matter compromise relate to age of seizure onset in temporal lobe epilepsy

Alice Ballerini; Donatello Arienzo; Alena Stasenko; Adam Schadler; Anna Elisabetta Vaudano; Stefano Meletti; Erik Kaestner; Carrie R. McDonald

NeuroImage: Clinical (Jan 2023)

Spatial patterns of gray and white matter compromise relate to age of seizure onset in temporal lobe epilepsy

Alice Ballerini,
Donatello Arienzo,
Alena Stasenko,
Adam Schadler,
Anna Elisabetta Vaudano,
Stefano Meletti,
Erik Kaestner,
Carrie R. McDonald

Affiliations

Alice Ballerini: Department of Biomedical, Metabolic and Neural Science, University of Modena and Reggio Emilia, Modena, Italy; Department of Psychiatry, University of California, San Diego, USA
Donatello Arienzo: Department of Psychiatry, University of California, San Diego, USA; Center for Multimodal Imaging and Genetics, University of California, San Diego, USA
Alena Stasenko: Department of Psychiatry, University of California, San Diego, USA; Center for Multimodal Imaging and Genetics, University of California, San Diego, USA
Adam Schadler: Department of Psychiatry, University of California, San Diego, USA; Center for Multimodal Imaging and Genetics, University of California, San Diego, USA
Anna Elisabetta Vaudano: Department of Biomedical, Metabolic and Neural Science, University of Modena and Reggio Emilia, Modena, Italy; Neurology Unit, OCB Hospital, AOU Modena, Italy
Stefano Meletti: Department of Biomedical, Metabolic and Neural Science, University of Modena and Reggio Emilia, Modena, Italy; Neurology Unit, OCB Hospital, AOU Modena, Italy
Erik Kaestner: Department of Psychiatry, University of California, San Diego, USA; Center for Multimodal Imaging and Genetics, University of California, San Diego, USA
Carrie R. McDonald: Department of Psychiatry, University of California, San Diego, USA; Center for Multimodal Imaging and Genetics, University of California, San Diego, USA; Department of Radiation Medicine & Applied Sciences, University of California, San Diego, USA; Corresponding author at: UC San Diego Altman Clinical and Translational Research Institute, 9452 Medical Ctr Dr, La Jolla 92037, CA, USA.

Journal volume & issue: Vol. 39
p. 103473

Abstract

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Objective: Temporal Lobe Epilepsy (TLE) is frequently a neurodevelopmental disorder, involving subcortical volume loss, cortical atrophy, and white matter (WM) disruption. However, few studies have addressed how these pathological changes in TLE relate to one another. In this study, we investigate spatial patterns of gray and white matter degeneration in TLE and evaluate the hypothesis that the relationship among these patterns varies as a function of the age at which seizures begin. Methods: Eighty-two patients with TLE and 59 healthy controls were enrolled. T1-weighted images were used to obtain hippocampal volumes and cortical thickness estimates. Diffusion-weighted imaging was used to obtain fractional anisotropy (FA) and mean diffusivity (MD) of the superficial WM (SWM) and deep WM tracts. Analysis of covariance was used to examine patterns of WM and gray matter alterations in TLE relative to controls, controlling for age and sex. Sliding window correlations were then performed to examine the relationships between SWM degeneration, cortical thinning, and hippocampal atrophy across ages of seizure onset. Results: Cortical thinning in TLE followed a widespread, bilateral pattern that was pronounced in posterior centroparietal regions, whereas SWM and deep WM loss occurred mostly in ipsilateral, temporolimbic regions compared to controls. Window correlations revealed a relationship between hippocampal volume loss and whole brain SWM disruption in patients who developed epilepsy during childhood. On the other hand, in patients with adult-onset TLE, co-occurring cortical and SWM alterations were observed in the medial temporal lobe ipsilateral to the seizure focus. Significance: Our results suggest that although cortical, hippocampal and WM alterations appear spatially discordant at the group level, the relationship among these features depends on the age at which seizures begin. Whereas neurodevelopmental aspects of TLE may result in co-occurring WM and hippocampal degeneration near the epileptogenic zone, the onset of seizures in adulthood may set off a cascade of SWM microstructural loss and cortical atrophy of a neurodegenerative nature.

Published in NeuroImage: Clinical

ISSN: 2213-1582 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General): Computer applications to medicine. Medical informatics; Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry: Neurology. Diseases of the nervous system
Website: http://www.journals.elsevier.com/neuroimage-clinical/

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