Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition
Objective Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magneti...
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Veröffentlicht in: | Epilepsia (Copenhagen) 2019-09, Vol.60 (9), p.1838-1848 |
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creator | Garcia‐Ramos, Camille Dabbs, Kevin Lin, Jack J. Jones, Jana E. Stafstrom, Carl E. Hsu, David A. Meyerand, Mary Elizabeth Prabhakaran, Vivek Hermann, Bruce P. |
description | Objective
Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magnetic resonance anomalies. Network science, including graph theory (GT) analyses, facilitates understanding of brain covariance patterns, potentially informing in important ways how this common self‐limiting epilepsy syndrome may impact normal patterns of brain and cognitive development.
Methods
GT analyses examined the developmental covariance among cortical and subcortical regions in children with new/recent onset BECTS (n = 19) and typically developing healthy controls (n = 22) who underwent high‐resolution MRI and cognitive assessment at baseline and 2 years later. Global (transitivity, global efficiency, and modularity index [Q]) and regional measures (local efficiency and hubs) were investigated to characterize network development in each group. Associations between baseline‐based GT measures and cognition at both time points addressed the implications of GT analyses for cognition and prospective cognitive development. Furthermore, an individual contribution measure was investigated, reflecting how important for cognition it is for BECTS to resemble the correlation matrices of controls.
Results
Groups exhibited similar Q and overall network configuration, with BECTS presenting significantly higher transitivity and both global and local efficiency. Furthermore, both groups presented a similar number of hubs, with BECTS showing a higher number in temporal lobe regions compared to controls. The investigated measures were negatively associated with 2‐year cognitive outcomes in BECTS.
Significance
Children with BECTS present a higher‐than‐normal global developmental configuration compared to controls, along with divergence from normality in terms of regional configuration. Baseline GT measures demonstrate potential as a cognitive biomarker to predict cognitive outcome in BECTS 2 years after diagnosis. Similarities and differences in developmental network configurations and their implications for cognition and behavior across common epilepsy syndromes are of theoretical interest and clinical relevance. |
doi_str_mv | 10.1111/epi.16290 |
format | Article |
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Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magnetic resonance anomalies. Network science, including graph theory (GT) analyses, facilitates understanding of brain covariance patterns, potentially informing in important ways how this common self‐limiting epilepsy syndrome may impact normal patterns of brain and cognitive development.
Methods
GT analyses examined the developmental covariance among cortical and subcortical regions in children with new/recent onset BECTS (n = 19) and typically developing healthy controls (n = 22) who underwent high‐resolution MRI and cognitive assessment at baseline and 2 years later. Global (transitivity, global efficiency, and modularity index [Q]) and regional measures (local efficiency and hubs) were investigated to characterize network development in each group. Associations between baseline‐based GT measures and cognition at both time points addressed the implications of GT analyses for cognition and prospective cognitive development. Furthermore, an individual contribution measure was investigated, reflecting how important for cognition it is for BECTS to resemble the correlation matrices of controls.
Results
Groups exhibited similar Q and overall network configuration, with BECTS presenting significantly higher transitivity and both global and local efficiency. Furthermore, both groups presented a similar number of hubs, with BECTS showing a higher number in temporal lobe regions compared to controls. The investigated measures were negatively associated with 2‐year cognitive outcomes in BECTS.
Significance
Children with BECTS present a higher‐than‐normal global developmental configuration compared to controls, along with divergence from normality in terms of regional configuration. Baseline GT measures demonstrate potential as a cognitive biomarker to predict cognitive outcome in BECTS 2 years after diagnosis. Similarities and differences in developmental network configurations and their implications for cognition and behavior across common epilepsy syndromes are of theoretical interest and clinical relevance.</description><identifier>ISSN: 0013-9580</identifier><identifier>EISSN: 1528-1167</identifier><identifier>DOI: 10.1111/epi.16290</identifier><identifier>PMID: 31347155</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Adolescent ; Algorithms ; Benign ; benign epilepsy with centrotemporal spikes ; Brain - diagnostic imaging ; brain volume development ; Child ; Children ; cognition ; Cognition & reasoning ; Cognition - physiology ; Cognitive ability ; Cognitive development ; Cortex ; Efficiency ; Epilepsy ; Epilepsy, Rolandic - diagnostic imaging ; Epilepsy, Rolandic - psychology ; Female ; graph theory ; Humans ; Localization ; Magnetic Resonance Imaging ; Male ; Nerve Net - diagnostic imaging ; Neuroimaging ; Neuropsychological Tests ; NMR ; Nuclear magnetic resonance ; Rolandic epilepsy ; Temporal lobe</subject><ispartof>Epilepsia (Copenhagen), 2019-09, Vol.60 (9), p.1838-1848</ispartof><rights>Wiley Periodicals, Inc. © 2019 International League Against Epilepsy</rights><rights>Wiley Periodicals, Inc. © 2019 International League Against Epilepsy.</rights><rights>Copyright © 2019 International League Against Epilepsy</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3880-8997f1bd1afd940001063780e32eb77883490165adb3420cb70964020b3075d83</citedby><cites>FETCH-LOGICAL-c3880-8997f1bd1afd940001063780e32eb77883490165adb3420cb70964020b3075d83</cites><orcidid>0000-0003-4365-9895</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fepi.16290$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fepi.16290$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31347155$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Garcia‐Ramos, Camille</creatorcontrib><creatorcontrib>Dabbs, Kevin</creatorcontrib><creatorcontrib>Lin, Jack J.</creatorcontrib><creatorcontrib>Jones, Jana E.</creatorcontrib><creatorcontrib>Stafstrom, Carl E.</creatorcontrib><creatorcontrib>Hsu, David A.</creatorcontrib><creatorcontrib>Meyerand, Mary Elizabeth</creatorcontrib><creatorcontrib>Prabhakaran, Vivek</creatorcontrib><creatorcontrib>Hermann, Bruce P.</creatorcontrib><title>Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition</title><title>Epilepsia (Copenhagen)</title><addtitle>Epilepsia</addtitle><description>Objective
Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magnetic resonance anomalies. Network science, including graph theory (GT) analyses, facilitates understanding of brain covariance patterns, potentially informing in important ways how this common self‐limiting epilepsy syndrome may impact normal patterns of brain and cognitive development.
Methods
GT analyses examined the developmental covariance among cortical and subcortical regions in children with new/recent onset BECTS (n = 19) and typically developing healthy controls (n = 22) who underwent high‐resolution MRI and cognitive assessment at baseline and 2 years later. Global (transitivity, global efficiency, and modularity index [Q]) and regional measures (local efficiency and hubs) were investigated to characterize network development in each group. Associations between baseline‐based GT measures and cognition at both time points addressed the implications of GT analyses for cognition and prospective cognitive development. Furthermore, an individual contribution measure was investigated, reflecting how important for cognition it is for BECTS to resemble the correlation matrices of controls.
Results
Groups exhibited similar Q and overall network configuration, with BECTS presenting significantly higher transitivity and both global and local efficiency. Furthermore, both groups presented a similar number of hubs, with BECTS showing a higher number in temporal lobe regions compared to controls. The investigated measures were negatively associated with 2‐year cognitive outcomes in BECTS.
Significance
Children with BECTS present a higher‐than‐normal global developmental configuration compared to controls, along with divergence from normality in terms of regional configuration. Baseline GT measures demonstrate potential as a cognitive biomarker to predict cognitive outcome in BECTS 2 years after diagnosis. Similarities and differences in developmental network configurations and their implications for cognition and behavior across common epilepsy syndromes are of theoretical interest and clinical relevance.</description><subject>Adolescent</subject><subject>Algorithms</subject><subject>Benign</subject><subject>benign epilepsy with centrotemporal spikes</subject><subject>Brain - diagnostic imaging</subject><subject>brain volume development</subject><subject>Child</subject><subject>Children</subject><subject>cognition</subject><subject>Cognition & reasoning</subject><subject>Cognition - physiology</subject><subject>Cognitive ability</subject><subject>Cognitive development</subject><subject>Cortex</subject><subject>Efficiency</subject><subject>Epilepsy</subject><subject>Epilepsy, Rolandic - diagnostic imaging</subject><subject>Epilepsy, Rolandic - psychology</subject><subject>Female</subject><subject>graph theory</subject><subject>Humans</subject><subject>Localization</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Nerve Net - diagnostic imaging</subject><subject>Neuroimaging</subject><subject>Neuropsychological Tests</subject><subject>NMR</subject><subject>Nuclear magnetic resonance</subject><subject>Rolandic epilepsy</subject><subject>Temporal lobe</subject><issn>0013-9580</issn><issn>1528-1167</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc1u1TAQhS0EoreFBS-ALLFpF2nHcfyTJaoKVKqABawjJ5m0bpPY2E6v8g48NL6ksEDCi7Fm9OnYcw4hbxics3wu0NtzJssanpEdE6UuGJPqOdkBMF7UQsMROY7xHgCUVPwlOeKMV4oJsSM_P2Pau_BAzWzGNdpI3UB9cNFjl-wj0jYYO9MeH3F0fsI50dyubkl3dG9zaXG2tzPNXxjRx3UbdpkLLuHkXTAjjd4-YMxP9NSmSAOOJlk3xzvraXK0c7ezPQxekReDGSO-frpPyPcPV98uPxU3Xz5eX76_KTquNRS6rtXA2p6Zoa-rvBUDyZUG5CW2SmnNqxqYFKZveVVC1yqoZQUltByU6DU_Iaebbl70x4IxNZONHY6jmdEtsSlLKVQlha4y-u4f9N4tIXt1oLRQdS0BMnW2UV12LgYcGh_sZMLaMGgOETXZn-Z3RJl9-6S4tBP2f8k_mWTgYgP22dL1_0rN1dfrTfIXqcGcLQ</recordid><startdate>201909</startdate><enddate>201909</enddate><creator>Garcia‐Ramos, Camille</creator><creator>Dabbs, Kevin</creator><creator>Lin, Jack J.</creator><creator>Jones, Jana E.</creator><creator>Stafstrom, Carl E.</creator><creator>Hsu, David A.</creator><creator>Meyerand, Mary Elizabeth</creator><creator>Prabhakaran, Vivek</creator><creator>Hermann, Bruce P.</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-4365-9895</orcidid></search><sort><creationdate>201909</creationdate><title>Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition</title><author>Garcia‐Ramos, Camille ; Dabbs, Kevin ; Lin, Jack J. ; Jones, Jana E. ; Stafstrom, Carl E. ; Hsu, David A. ; Meyerand, Mary Elizabeth ; Prabhakaran, Vivek ; Hermann, Bruce P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3880-8997f1bd1afd940001063780e32eb77883490165adb3420cb70964020b3075d83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adolescent</topic><topic>Algorithms</topic><topic>Benign</topic><topic>benign epilepsy with centrotemporal spikes</topic><topic>Brain - diagnostic imaging</topic><topic>brain volume development</topic><topic>Child</topic><topic>Children</topic><topic>cognition</topic><topic>Cognition & reasoning</topic><topic>Cognition - physiology</topic><topic>Cognitive ability</topic><topic>Cognitive development</topic><topic>Cortex</topic><topic>Efficiency</topic><topic>Epilepsy</topic><topic>Epilepsy, Rolandic - diagnostic imaging</topic><topic>Epilepsy, Rolandic - psychology</topic><topic>Female</topic><topic>graph theory</topic><topic>Humans</topic><topic>Localization</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Nerve Net - diagnostic imaging</topic><topic>Neuroimaging</topic><topic>Neuropsychological Tests</topic><topic>NMR</topic><topic>Nuclear magnetic resonance</topic><topic>Rolandic epilepsy</topic><topic>Temporal lobe</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Garcia‐Ramos, Camille</creatorcontrib><creatorcontrib>Dabbs, Kevin</creatorcontrib><creatorcontrib>Lin, Jack J.</creatorcontrib><creatorcontrib>Jones, Jana E.</creatorcontrib><creatorcontrib>Stafstrom, Carl E.</creatorcontrib><creatorcontrib>Hsu, David A.</creatorcontrib><creatorcontrib>Meyerand, Mary Elizabeth</creatorcontrib><creatorcontrib>Prabhakaran, Vivek</creatorcontrib><creatorcontrib>Hermann, Bruce P.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Epilepsia (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Garcia‐Ramos, Camille</au><au>Dabbs, Kevin</au><au>Lin, Jack J.</au><au>Jones, Jana E.</au><au>Stafstrom, Carl E.</au><au>Hsu, David A.</au><au>Meyerand, Mary Elizabeth</au><au>Prabhakaran, Vivek</au><au>Hermann, Bruce P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition</atitle><jtitle>Epilepsia (Copenhagen)</jtitle><addtitle>Epilepsia</addtitle><date>2019-09</date><risdate>2019</risdate><volume>60</volume><issue>9</issue><spage>1838</spage><epage>1848</epage><pages>1838-1848</pages><issn>0013-9580</issn><eissn>1528-1167</eissn><abstract>Objective
Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magnetic resonance anomalies. Network science, including graph theory (GT) analyses, facilitates understanding of brain covariance patterns, potentially informing in important ways how this common self‐limiting epilepsy syndrome may impact normal patterns of brain and cognitive development.
Methods
GT analyses examined the developmental covariance among cortical and subcortical regions in children with new/recent onset BECTS (n = 19) and typically developing healthy controls (n = 22) who underwent high‐resolution MRI and cognitive assessment at baseline and 2 years later. Global (transitivity, global efficiency, and modularity index [Q]) and regional measures (local efficiency and hubs) were investigated to characterize network development in each group. Associations between baseline‐based GT measures and cognition at both time points addressed the implications of GT analyses for cognition and prospective cognitive development. Furthermore, an individual contribution measure was investigated, reflecting how important for cognition it is for BECTS to resemble the correlation matrices of controls.
Results
Groups exhibited similar Q and overall network configuration, with BECTS presenting significantly higher transitivity and both global and local efficiency. Furthermore, both groups presented a similar number of hubs, with BECTS showing a higher number in temporal lobe regions compared to controls. The investigated measures were negatively associated with 2‐year cognitive outcomes in BECTS.
Significance
Children with BECTS present a higher‐than‐normal global developmental configuration compared to controls, along with divergence from normality in terms of regional configuration. Baseline GT measures demonstrate potential as a cognitive biomarker to predict cognitive outcome in BECTS 2 years after diagnosis. Similarities and differences in developmental network configurations and their implications for cognition and behavior across common epilepsy syndromes are of theoretical interest and clinical relevance.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>31347155</pmid><doi>10.1111/epi.16290</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-4365-9895</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adolescent Algorithms Benign benign epilepsy with centrotemporal spikes Brain - diagnostic imaging brain volume development Child Children cognition Cognition & reasoning Cognition - physiology Cognitive ability Cognitive development Cortex Efficiency Epilepsy Epilepsy, Rolandic - diagnostic imaging Epilepsy, Rolandic - psychology Female graph theory Humans Localization Magnetic Resonance Imaging Male Nerve Net - diagnostic imaging Neuroimaging Neuropsychological Tests NMR Nuclear magnetic resonance Rolandic epilepsy Temporal lobe |
title | Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition |
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