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Regional variation in brain tissue texture in patients with tonic-clonic seizures

Patients with epilepsy, who later succumb to sudden unexpected death, show altered brain tissue volumes in selected regions. It is unclear whether the alterations in brain tissue volume represent changes in neurons or glial properties, since volumetric procedures have limited sensitivity to assess t...

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Autores principales: Ogren, Jennifer A., Allen, Luke A., Roy, Bhaswati, Diehl, Beate, Stern, John M., Eliashiv, Dawn S., Lhatoo, Samden D., Harper, Ronald M., Kumar, Rajesh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499268/
https://www.ncbi.nlm.nih.gov/pubmed/36137154
http://dx.doi.org/10.1371/journal.pone.0274514
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author Ogren, Jennifer A.
Allen, Luke A.
Roy, Bhaswati
Diehl, Beate
Stern, John M.
Eliashiv, Dawn S.
Lhatoo, Samden D.
Harper, Ronald M.
Kumar, Rajesh
author_facet Ogren, Jennifer A.
Allen, Luke A.
Roy, Bhaswati
Diehl, Beate
Stern, John M.
Eliashiv, Dawn S.
Lhatoo, Samden D.
Harper, Ronald M.
Kumar, Rajesh
author_sort Ogren, Jennifer A.
collection PubMed
description Patients with epilepsy, who later succumb to sudden unexpected death, show altered brain tissue volumes in selected regions. It is unclear whether the alterations in brain tissue volume represent changes in neurons or glial properties, since volumetric procedures have limited sensitivity to assess the source of volume changes (e.g., neuronal loss or glial cell swelling). We assessed a measure, entropy, which can determine tissue homogeneity by evaluating tissue randomness, and thus, shows tissue integrity; the measure is easily calculated from T1-weighted images. T1-weighted images were collected with a 3.0-Tesla MRI from 53 patients with tonic-clonic (TC) seizures and 53 healthy controls; images were bias-corrected, entropy maps calculated, normalized to a common space, smoothed, and compared between groups (TC patients and controls using ANCOVA; covariates, age and sex; SPM12, family-wise error correction for multiple comparisons, p<0.01). Decreased entropy, indicative of increased tissue homogeneity, appeared in major autonomic (ventromedial prefrontal cortex, hippocampus, dorsal and ventral medulla, deep cerebellar nuclei), motor (sensory and motor cortex), or both motor and autonomic regulatory sites (basal-ganglia, ventral-basal cerebellum), and external surfaces of the pons. The anterior and posterior thalamus and midbrain also showed entropy declines. Only a few isolated regions showed increased entropy. Among the spared autonomic regions was the anterior cingulate and anterior insula; the posterior insula and cingulate were, however, affected. The entropy alterations overlapped areas of tissue changes found earlier with volumetric measures, but were more extensive, and indicate widespread injury to tissue within critical autonomic and breathing regulatory areas, as well as prominent damage to more-rostral sites that exert influences on both breathing and cardiovascular regulation. The entropy measures provide easily-collected supplementary information using only T1-weighted images, showing aspects of tissue integrity other than volume change that are important for assessing function.
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spelling pubmed-94992682022-09-23 Regional variation in brain tissue texture in patients with tonic-clonic seizures Ogren, Jennifer A. Allen, Luke A. Roy, Bhaswati Diehl, Beate Stern, John M. Eliashiv, Dawn S. Lhatoo, Samden D. Harper, Ronald M. Kumar, Rajesh PLoS One Research Article Patients with epilepsy, who later succumb to sudden unexpected death, show altered brain tissue volumes in selected regions. It is unclear whether the alterations in brain tissue volume represent changes in neurons or glial properties, since volumetric procedures have limited sensitivity to assess the source of volume changes (e.g., neuronal loss or glial cell swelling). We assessed a measure, entropy, which can determine tissue homogeneity by evaluating tissue randomness, and thus, shows tissue integrity; the measure is easily calculated from T1-weighted images. T1-weighted images were collected with a 3.0-Tesla MRI from 53 patients with tonic-clonic (TC) seizures and 53 healthy controls; images were bias-corrected, entropy maps calculated, normalized to a common space, smoothed, and compared between groups (TC patients and controls using ANCOVA; covariates, age and sex; SPM12, family-wise error correction for multiple comparisons, p<0.01). Decreased entropy, indicative of increased tissue homogeneity, appeared in major autonomic (ventromedial prefrontal cortex, hippocampus, dorsal and ventral medulla, deep cerebellar nuclei), motor (sensory and motor cortex), or both motor and autonomic regulatory sites (basal-ganglia, ventral-basal cerebellum), and external surfaces of the pons. The anterior and posterior thalamus and midbrain also showed entropy declines. Only a few isolated regions showed increased entropy. Among the spared autonomic regions was the anterior cingulate and anterior insula; the posterior insula and cingulate were, however, affected. The entropy alterations overlapped areas of tissue changes found earlier with volumetric measures, but were more extensive, and indicate widespread injury to tissue within critical autonomic and breathing regulatory areas, as well as prominent damage to more-rostral sites that exert influences on both breathing and cardiovascular regulation. The entropy measures provide easily-collected supplementary information using only T1-weighted images, showing aspects of tissue integrity other than volume change that are important for assessing function. Public Library of Science 2022-09-22 /pmc/articles/PMC9499268/ /pubmed/36137154 http://dx.doi.org/10.1371/journal.pone.0274514 Text en © 2022 Ogren et al 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 use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ogren, Jennifer A.
Allen, Luke A.
Roy, Bhaswati
Diehl, Beate
Stern, John M.
Eliashiv, Dawn S.
Lhatoo, Samden D.
Harper, Ronald M.
Kumar, Rajesh
Regional variation in brain tissue texture in patients with tonic-clonic seizures
title Regional variation in brain tissue texture in patients with tonic-clonic seizures
title_full Regional variation in brain tissue texture in patients with tonic-clonic seizures
title_fullStr Regional variation in brain tissue texture in patients with tonic-clonic seizures
title_full_unstemmed Regional variation in brain tissue texture in patients with tonic-clonic seizures
title_short Regional variation in brain tissue texture in patients with tonic-clonic seizures
title_sort regional variation in brain tissue texture in patients with tonic-clonic seizures
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499268/
https://www.ncbi.nlm.nih.gov/pubmed/36137154
http://dx.doi.org/10.1371/journal.pone.0274514
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