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Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis

Hippocampal sclerosis (HS) is a common cause of pharmacoresistant focal epilepsy. Here, we (1) performed a histological approach to the anterior temporal pole of patients with HS to evaluate cortical and white matter (WM) cell populations, alteration of myelin integrity and markers of neuronal activ...

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Autores principales: Zaidan, Bruna Cunha, Cardoso, Ingrid Carolina da Silva, de Campos, Brunno Machado, da Silva, Luciana Ramalho Pimentel, Coelho, Vanessa C. Mendes, Silveira, Kairo Alexandre Alves, Amorim, Bárbara Juarez, Alvim, Marina Koutsodontis Machado, Tedeschi, Helder, Yasuda, Clarissa Lin, Ghizoni, Enrico, Cendes, Fernando, Rogerio, Fabio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8739995/
https://www.ncbi.nlm.nih.gov/pubmed/35002940
http://dx.doi.org/10.3389/fneur.2021.801195
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author Zaidan, Bruna Cunha
Cardoso, Ingrid Carolina da Silva
de Campos, Brunno Machado
da Silva, Luciana Ramalho Pimentel
Coelho, Vanessa C. Mendes
Silveira, Kairo Alexandre Alves
Amorim, Bárbara Juarez
Alvim, Marina Koutsodontis Machado
Tedeschi, Helder
Yasuda, Clarissa Lin
Ghizoni, Enrico
Cendes, Fernando
Rogerio, Fabio
author_facet Zaidan, Bruna Cunha
Cardoso, Ingrid Carolina da Silva
de Campos, Brunno Machado
da Silva, Luciana Ramalho Pimentel
Coelho, Vanessa C. Mendes
Silveira, Kairo Alexandre Alves
Amorim, Bárbara Juarez
Alvim, Marina Koutsodontis Machado
Tedeschi, Helder
Yasuda, Clarissa Lin
Ghizoni, Enrico
Cendes, Fernando
Rogerio, Fabio
author_sort Zaidan, Bruna Cunha
collection PubMed
description Hippocampal sclerosis (HS) is a common cause of pharmacoresistant focal epilepsy. Here, we (1) performed a histological approach to the anterior temporal pole of patients with HS to evaluate cortical and white matter (WM) cell populations, alteration of myelin integrity and markers of neuronal activity, and (2) correlated microscopic data with magnetic resonance imaging (MRI) findings. Our aim was to contribute with the understanding of neuroimaging and pathophysiological mechanisms of temporal lobe epilepsy (TLE) associated with HS. We examined MRIs and surgical specimens from the anterior temporal pole from TLE-HS patients (n = 9) and compared them with 10 autopsy controls. MRIs from healthy volunteers (n = 13) were used as neuroimaging controls. Histological techniques were performed to assess oligodendrocytes, heterotopic neurons, cellular proliferative index, and myeloarchitecture integrity of the WM, as well as markers of acute (c-fos) and chronic (ΔFosB) activities of neocortical neurons. Microscopic data were compared with neuroimaging findings, including T2-weighted/FLAIR MRI temporopolar blurring and values of fractional anisotropy (FA) from diffusion-weighed imaging (DWI). We found a significant increase in WM oligodendrocyte number, both in hematoxylin and eosin, and in Olig2-stained sections. The frequencies of oligodendrocytes in perivascular spaces and around heterotopic neurons were significantly higher in patients with TLE–HS compared with controls. The percentage of 2',3'-cyclic-nucleotide 3'-phosphodiesterase (CNPase; a marker of myeloarchitecture integrity) immunopositive area in the WM was significantly higher in TLE-HS, as well as the numbers of c-fos- and ΔFosB-immunostained neocortical neurons. Additionally, we demonstrated a decrease in axonal bundle integrity on neuroimaging, with a significant reduction in the FA in the anterior temporal pole. No differences were detected between individuals with and without temporopolar blurring on visual MRI analysis, considering the number of oligodendroglial cells and percentage of WM CNPase-positive areas. Also, there was no relationship between T2 relaxometry and oligodendrocyte count. In conclusion, our histopathological data support the following: (1) the hypothesis that repetitive neocortical neuronal activity could induce changes in the WM cellular constitution and myelin remodeling in the anterior temporal pole from patients with TLE-HS, (2) that oligodendroglial hyperplasia is not related to temporal blurring or T2 signal intensity on MRI, and (3) that reduced FA is a marker of increase in Olig2-immunopositive cells in superficial temporopolar WM from patients with TLE-HS.
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spelling pubmed-87399952022-01-08 Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis Zaidan, Bruna Cunha Cardoso, Ingrid Carolina da Silva de Campos, Brunno Machado da Silva, Luciana Ramalho Pimentel Coelho, Vanessa C. Mendes Silveira, Kairo Alexandre Alves Amorim, Bárbara Juarez Alvim, Marina Koutsodontis Machado Tedeschi, Helder Yasuda, Clarissa Lin Ghizoni, Enrico Cendes, Fernando Rogerio, Fabio Front Neurol Neurology Hippocampal sclerosis (HS) is a common cause of pharmacoresistant focal epilepsy. Here, we (1) performed a histological approach to the anterior temporal pole of patients with HS to evaluate cortical and white matter (WM) cell populations, alteration of myelin integrity and markers of neuronal activity, and (2) correlated microscopic data with magnetic resonance imaging (MRI) findings. Our aim was to contribute with the understanding of neuroimaging and pathophysiological mechanisms of temporal lobe epilepsy (TLE) associated with HS. We examined MRIs and surgical specimens from the anterior temporal pole from TLE-HS patients (n = 9) and compared them with 10 autopsy controls. MRIs from healthy volunteers (n = 13) were used as neuroimaging controls. Histological techniques were performed to assess oligodendrocytes, heterotopic neurons, cellular proliferative index, and myeloarchitecture integrity of the WM, as well as markers of acute (c-fos) and chronic (ΔFosB) activities of neocortical neurons. Microscopic data were compared with neuroimaging findings, including T2-weighted/FLAIR MRI temporopolar blurring and values of fractional anisotropy (FA) from diffusion-weighed imaging (DWI). We found a significant increase in WM oligodendrocyte number, both in hematoxylin and eosin, and in Olig2-stained sections. The frequencies of oligodendrocytes in perivascular spaces and around heterotopic neurons were significantly higher in patients with TLE–HS compared with controls. The percentage of 2',3'-cyclic-nucleotide 3'-phosphodiesterase (CNPase; a marker of myeloarchitecture integrity) immunopositive area in the WM was significantly higher in TLE-HS, as well as the numbers of c-fos- and ΔFosB-immunostained neocortical neurons. Additionally, we demonstrated a decrease in axonal bundle integrity on neuroimaging, with a significant reduction in the FA in the anterior temporal pole. No differences were detected between individuals with and without temporopolar blurring on visual MRI analysis, considering the number of oligodendroglial cells and percentage of WM CNPase-positive areas. Also, there was no relationship between T2 relaxometry and oligodendrocyte count. In conclusion, our histopathological data support the following: (1) the hypothesis that repetitive neocortical neuronal activity could induce changes in the WM cellular constitution and myelin remodeling in the anterior temporal pole from patients with TLE-HS, (2) that oligodendroglial hyperplasia is not related to temporal blurring or T2 signal intensity on MRI, and (3) that reduced FA is a marker of increase in Olig2-immunopositive cells in superficial temporopolar WM from patients with TLE-HS. Frontiers Media S.A. 2021-12-24 /pmc/articles/PMC8739995/ /pubmed/35002940 http://dx.doi.org/10.3389/fneur.2021.801195 Text en Copyright © 2021 Zaidan, Cardoso, Campos, Silva, Coelho, Silveira, Amorim, Alvim, Tedeschi, Yasuda, Ghizoni, Cendes and Rogerio. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Zaidan, Bruna Cunha
Cardoso, Ingrid Carolina da Silva
de Campos, Brunno Machado
da Silva, Luciana Ramalho Pimentel
Coelho, Vanessa C. Mendes
Silveira, Kairo Alexandre Alves
Amorim, Bárbara Juarez
Alvim, Marina Koutsodontis Machado
Tedeschi, Helder
Yasuda, Clarissa Lin
Ghizoni, Enrico
Cendes, Fernando
Rogerio, Fabio
Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis
title Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis
title_full Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis
title_fullStr Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis
title_full_unstemmed Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis
title_short Histopathological Correlations of Qualitative and Quantitative Temporopolar MRI Analyses in Patients With Hippocampal Sclerosis
title_sort histopathological correlations of qualitative and quantitative temporopolar mri analyses in patients with hippocampal sclerosis
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8739995/
https://www.ncbi.nlm.nih.gov/pubmed/35002940
http://dx.doi.org/10.3389/fneur.2021.801195
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