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Functional brain connectivity in young adults with post-stroke epilepsy

Approximately 1 in 10 young stroke patients (18–50 years) will develop post-stroke epilepsy, which is associated with cognitive impairment. While previous studies have shown altered brain connectivity in patients with epilepsy, little is however known about the changes in functional brain connectivi...

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Autores principales: Boot, Esther M, Omes, Quinty P M, Maaijwee, Noortje, Schaapsmeerders, Pauline, Arntz, Renate M, Rutten-Jacobs, Loes C A, Kessels, Roy P C, de Leeuw, Frank-Erik, Tuladhar, Anil M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10639092/
https://www.ncbi.nlm.nih.gov/pubmed/37953839
http://dx.doi.org/10.1093/braincomms/fcad277
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author Boot, Esther M
Omes, Quinty P M
Maaijwee, Noortje
Schaapsmeerders, Pauline
Arntz, Renate M
Rutten-Jacobs, Loes C A
Kessels, Roy P C
de Leeuw, Frank-Erik
Tuladhar, Anil M
author_facet Boot, Esther M
Omes, Quinty P M
Maaijwee, Noortje
Schaapsmeerders, Pauline
Arntz, Renate M
Rutten-Jacobs, Loes C A
Kessels, Roy P C
de Leeuw, Frank-Erik
Tuladhar, Anil M
author_sort Boot, Esther M
collection PubMed
description Approximately 1 in 10 young stroke patients (18–50 years) will develop post-stroke epilepsy, which is associated with cognitive impairment. While previous studies have shown altered brain connectivity in patients with epilepsy, little is however known about the changes in functional brain connectivity in young stroke patients with post-stroke epilepsy and their relationship with cognitive impairment. Therefore, we aimed to investigate whether young ischaemic stroke patients have altered functional networks and whether this alteration is related to cognitive impairment. We included 164 participants with a first-ever cerebral infarction at young age (18–50 years), along with 77 age- and sex-matched controls, from the Follow-Up of Transient Ischemic Attack and Stroke patients and Unelucidated Risk Factor Evaluation study. All participants underwent neuropsychological testing and resting-state functional MRI to generate functional connectivity networks. At follow-up (10.5 years after the index event), 23 participants developed post-stroke epilepsy. Graph theoretical analysis revealed functional network reorganization in participants with post-stroke epilepsy, in whom a weaker (i.e. network strength), less-integrated (i.e. global efficiency) and less-segregated (i.e. clustering coefficient and local efficiency) functional network was observed compared with the participants without post-stroke epilepsy group and the controls (P < 0.05). Regional analysis showed a trend towards decreased clustering coefficient, local efficiency and nodal efficiency in contralesional brain regions, including the caudal anterior cingulate cortex, posterior cingulate cortex, precuneus, superior frontal gyrus and insula in participants with post-stroke epilepsy compared with those without post-stroke epilepsy. Furthermore, participants with post-stroke epilepsy more often had impairment in the processing speed domain than the group without post-stroke epilepsy, in whom the network properties of the precuneus were positively associated with processing speed performance. Our findings suggest that post-stroke epilepsy is associated with functional reorganization of the brain network after stroke that is characterized by a weaker, less-integrated and less-segregated brain network in young ischaemic stroke patients compared with patients without post-stroke epilepsy. The contralesional brain regions, which are mostly considered as hub regions, might be particularly involved in the altered functional network and may contribute to cognitive impairment in post-stroke epilepsy patients. Overall, our findings provide additional evidence for a potential role of disrupted functional network as underlying pathophysiological mechanism for cognitive impairment in patients with post-stroke epilepsy.
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spelling pubmed-106390922023-11-11 Functional brain connectivity in young adults with post-stroke epilepsy Boot, Esther M Omes, Quinty P M Maaijwee, Noortje Schaapsmeerders, Pauline Arntz, Renate M Rutten-Jacobs, Loes C A Kessels, Roy P C de Leeuw, Frank-Erik Tuladhar, Anil M Brain Commun Original Article Approximately 1 in 10 young stroke patients (18–50 years) will develop post-stroke epilepsy, which is associated with cognitive impairment. While previous studies have shown altered brain connectivity in patients with epilepsy, little is however known about the changes in functional brain connectivity in young stroke patients with post-stroke epilepsy and their relationship with cognitive impairment. Therefore, we aimed to investigate whether young ischaemic stroke patients have altered functional networks and whether this alteration is related to cognitive impairment. We included 164 participants with a first-ever cerebral infarction at young age (18–50 years), along with 77 age- and sex-matched controls, from the Follow-Up of Transient Ischemic Attack and Stroke patients and Unelucidated Risk Factor Evaluation study. All participants underwent neuropsychological testing and resting-state functional MRI to generate functional connectivity networks. At follow-up (10.5 years after the index event), 23 participants developed post-stroke epilepsy. Graph theoretical analysis revealed functional network reorganization in participants with post-stroke epilepsy, in whom a weaker (i.e. network strength), less-integrated (i.e. global efficiency) and less-segregated (i.e. clustering coefficient and local efficiency) functional network was observed compared with the participants without post-stroke epilepsy group and the controls (P < 0.05). Regional analysis showed a trend towards decreased clustering coefficient, local efficiency and nodal efficiency in contralesional brain regions, including the caudal anterior cingulate cortex, posterior cingulate cortex, precuneus, superior frontal gyrus and insula in participants with post-stroke epilepsy compared with those without post-stroke epilepsy. Furthermore, participants with post-stroke epilepsy more often had impairment in the processing speed domain than the group without post-stroke epilepsy, in whom the network properties of the precuneus were positively associated with processing speed performance. Our findings suggest that post-stroke epilepsy is associated with functional reorganization of the brain network after stroke that is characterized by a weaker, less-integrated and less-segregated brain network in young ischaemic stroke patients compared with patients without post-stroke epilepsy. The contralesional brain regions, which are mostly considered as hub regions, might be particularly involved in the altered functional network and may contribute to cognitive impairment in post-stroke epilepsy patients. Overall, our findings provide additional evidence for a potential role of disrupted functional network as underlying pathophysiological mechanism for cognitive impairment in patients with post-stroke epilepsy. Oxford University Press 2023-10-18 /pmc/articles/PMC10639092/ /pubmed/37953839 http://dx.doi.org/10.1093/braincomms/fcad277 Text en © The Author(s) 2023. 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
Boot, Esther M
Omes, Quinty P M
Maaijwee, Noortje
Schaapsmeerders, Pauline
Arntz, Renate M
Rutten-Jacobs, Loes C A
Kessels, Roy P C
de Leeuw, Frank-Erik
Tuladhar, Anil M
Functional brain connectivity in young adults with post-stroke epilepsy
title Functional brain connectivity in young adults with post-stroke epilepsy
title_full Functional brain connectivity in young adults with post-stroke epilepsy
title_fullStr Functional brain connectivity in young adults with post-stroke epilepsy
title_full_unstemmed Functional brain connectivity in young adults with post-stroke epilepsy
title_short Functional brain connectivity in young adults with post-stroke epilepsy
title_sort functional brain connectivity in young adults with post-stroke epilepsy
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10639092/
https://www.ncbi.nlm.nih.gov/pubmed/37953839
http://dx.doi.org/10.1093/braincomms/fcad277
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