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Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy

PURPOSE: This study aimed to use graph theoretical analysis of anatomical covariance derived from structural MRI to reveal how the gray matter connectivity pattern is altered after corpus callosotomy (CC). MATERIALS AND METHODS: We recruited 21 patients with epilepsy who had undergone CC. Enrollment...

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Autores principales: Ueda, Riyo, Matsuda, Hiroshi, Sato, Noriko, Iwasaki, Masaki, Sone, Daichi, Takeshita, Eri, Shimizu-Motohashi, Yuko, Ishiyama, Akihiko, Saito, Takashi, Komaki, Hirofumi, Nakagawa, Eiji, Sugai, Kenji, Sasaki, Masayuki, Kaga, Yoshimi, Takeichi, Hiroshige, Inagaki, Masumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894802/
https://www.ncbi.nlm.nih.gov/pubmed/31805047
http://dx.doi.org/10.1371/journal.pone.0222876
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author Ueda, Riyo
Matsuda, Hiroshi
Sato, Noriko
Iwasaki, Masaki
Sone, Daichi
Takeshita, Eri
Shimizu-Motohashi, Yuko
Ishiyama, Akihiko
Saito, Takashi
Komaki, Hirofumi
Nakagawa, Eiji
Sugai, Kenji
Sasaki, Masayuki
Kaga, Yoshimi
Takeichi, Hiroshige
Inagaki, Masumi
author_facet Ueda, Riyo
Matsuda, Hiroshi
Sato, Noriko
Iwasaki, Masaki
Sone, Daichi
Takeshita, Eri
Shimizu-Motohashi, Yuko
Ishiyama, Akihiko
Saito, Takashi
Komaki, Hirofumi
Nakagawa, Eiji
Sugai, Kenji
Sasaki, Masayuki
Kaga, Yoshimi
Takeichi, Hiroshige
Inagaki, Masumi
author_sort Ueda, Riyo
collection PubMed
description PURPOSE: This study aimed to use graph theoretical analysis of anatomical covariance derived from structural MRI to reveal how the gray matter connectivity pattern is altered after corpus callosotomy (CC). MATERIALS AND METHODS: We recruited 21 patients with epilepsy who had undergone CC. Enrollment criteria were applied: (1) no lesion identified on brain MRI; (2) no history of other brain surgery; and (3) age not younger than 3 years and not older than 18 years at preoperative MRI evaluation. The most common epilepsy syndrome was Lennox-Gastaut syndrome (11 patients). For voxel-based morphometry, the normalized gray matter images of pre-CC and post-CC patients were analyzed with SPM12 (voxel-level threshold of p<0.05 [familywise error-corrected]). Secondly, the images of both groups were subjected to graph theoretical analysis using the Graph Analysis Toolbox with SPM8. Each group was also compared with 32 age- and sex-matched control patients without brain diseases. RESULTS: Comparisons between the pre- and post-CC groups revealed a significant reduction in seizure frequency with no change in mean intelligence quotient/developmental quotient levels. There was no relationship among the three groups in global network metrics or in targeted attack. A regional comparison of betweenness centrality revealed decreased connectivity to and from the right middle cingulate gyri and medial side of the right superior frontal gyrus and a partial shift in the distribution of betweenness centrality hubs to the normal location. Significantly lower resilience to random failure was found after versus before CC and versus controls (p = 0.0450 and p = 0.0200, respectively). CONCLUSION: Graph theoretical analysis of anatomical covariance derived from structural imaging revealed two neural network effects of resection associated with seizure reduction: the reappearance of a structural network comparable to that in healthy children and reduced connectivity along the median line, including the middle cingulate gyrus.
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spelling pubmed-68948022019-12-14 Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy Ueda, Riyo Matsuda, Hiroshi Sato, Noriko Iwasaki, Masaki Sone, Daichi Takeshita, Eri Shimizu-Motohashi, Yuko Ishiyama, Akihiko Saito, Takashi Komaki, Hirofumi Nakagawa, Eiji Sugai, Kenji Sasaki, Masayuki Kaga, Yoshimi Takeichi, Hiroshige Inagaki, Masumi PLoS One Research Article PURPOSE: This study aimed to use graph theoretical analysis of anatomical covariance derived from structural MRI to reveal how the gray matter connectivity pattern is altered after corpus callosotomy (CC). MATERIALS AND METHODS: We recruited 21 patients with epilepsy who had undergone CC. Enrollment criteria were applied: (1) no lesion identified on brain MRI; (2) no history of other brain surgery; and (3) age not younger than 3 years and not older than 18 years at preoperative MRI evaluation. The most common epilepsy syndrome was Lennox-Gastaut syndrome (11 patients). For voxel-based morphometry, the normalized gray matter images of pre-CC and post-CC patients were analyzed with SPM12 (voxel-level threshold of p<0.05 [familywise error-corrected]). Secondly, the images of both groups were subjected to graph theoretical analysis using the Graph Analysis Toolbox with SPM8. Each group was also compared with 32 age- and sex-matched control patients without brain diseases. RESULTS: Comparisons between the pre- and post-CC groups revealed a significant reduction in seizure frequency with no change in mean intelligence quotient/developmental quotient levels. There was no relationship among the three groups in global network metrics or in targeted attack. A regional comparison of betweenness centrality revealed decreased connectivity to and from the right middle cingulate gyri and medial side of the right superior frontal gyrus and a partial shift in the distribution of betweenness centrality hubs to the normal location. Significantly lower resilience to random failure was found after versus before CC and versus controls (p = 0.0450 and p = 0.0200, respectively). CONCLUSION: Graph theoretical analysis of anatomical covariance derived from structural imaging revealed two neural network effects of resection associated with seizure reduction: the reappearance of a structural network comparable to that in healthy children and reduced connectivity along the median line, including the middle cingulate gyrus. Public Library of Science 2019-12-05 /pmc/articles/PMC6894802/ /pubmed/31805047 http://dx.doi.org/10.1371/journal.pone.0222876 Text en © 2019 Ueda et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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
Ueda, Riyo
Matsuda, Hiroshi
Sato, Noriko
Iwasaki, Masaki
Sone, Daichi
Takeshita, Eri
Shimizu-Motohashi, Yuko
Ishiyama, Akihiko
Saito, Takashi
Komaki, Hirofumi
Nakagawa, Eiji
Sugai, Kenji
Sasaki, Masayuki
Kaga, Yoshimi
Takeichi, Hiroshige
Inagaki, Masumi
Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
title Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
title_full Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
title_fullStr Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
title_full_unstemmed Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
title_short Alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
title_sort alteration of the anatomical covariance network after corpus callosotomy in pediatric intractable epilepsy
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894802/
https://www.ncbi.nlm.nih.gov/pubmed/31805047
http://dx.doi.org/10.1371/journal.pone.0222876
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