Noninvasive Mapping of Ripple Onset Predicts Outcome in Epilepsy Surgery
Objective Intracranial electroencephalographic (icEEG) studies show that interictal ripples propagate across the brain of children with medically refractory epilepsy (MRE), and the onset of this propagation (ripple onset zone [ROZ]) estimates the epileptogenic zone. It is still unknown whether we ca...
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| Veröffentlicht in: | Annals of neurology 2021-05, Vol.89 (5), p.911-925 |
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| container_title | Annals of neurology |
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| creator | Tamilia, Eleonora Matarrese, Margherita A. G. Ntolkeras, Georgios Grant, P. Ellen Madsen, Joseph R. Stufflebeam, Steve M. Pearl, Phillip L. Papadelis, Christos |
| description | Objective
Intracranial electroencephalographic (icEEG) studies show that interictal ripples propagate across the brain of children with medically refractory epilepsy (MRE), and the onset of this propagation (ripple onset zone [ROZ]) estimates the epileptogenic zone. It is still unknown whether we can map this propagation noninvasively. The goal of this study is to map ripples (ripple zone [RZ]) and their propagation onset (ROZ) using high‐density EEG (HD‐EEG) and magnetoencephalography (MEG), and to estimate their prognostic value in pediatric epilepsy surgery.
Methods
We retrospectively analyzed simultaneous HD‐EEG and MEG data from 28 children with MRE who underwent icEEG and epilepsy surgery. Using electric and magnetic source imaging, we estimated virtual sensors (VSs) at brain locations that matched the icEEG implantation. We detected ripples on VSs, defined the virtual RZ and virtual ROZ, and estimated their distance from icEEG. We assessed the predictive value of resecting virtual RZ and virtual ROZ for postsurgical outcome. Interictal spike localization on HD‐EEG and MEG was also performed and compared with ripples.
Results
We mapped ripple propagation in all patients with HD‐EEG and in 27 (96%) patients with MEG. The distance from icEEG did not differ between HD‐EEG and MEG when mapping the RZ (26–27mm, p = 0.6) or ROZ (22–24mm, p = 0.4). Resecting the virtual ROZ, but not virtual RZ or the sources of spikes, was associated with good outcome for HD‐EEG (p = 0.016) and MEG (p = 0.047).
Interpretation
HD‐EEG and MEG can map interictal ripples and their propagation onset (virtual ROZ). Noninvasively mapping the ripple onset may augment epilepsy surgery planning and improve surgical outcome of children with MRE. ANN NEUROL 2021;89:911–925 |
| doi_str_mv | 10.1002/ana.26066 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8229023</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2501255082</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4436-477cb67c28632bbcc8f265e531adb79b850370aff9af0349fba5c034908e0e653</originalsourceid><addsrcrecordid>eNp1kV1rFDEUhoModlu98A9IwBt7Me1JMslkboSlVCvUrvhxHTLZM2vKbDImMyv7703dWlTwKgfy8PCe8xLygsEZA-DnNtgzrkCpR2TBpGCV5nX7mCxAqLqSTNRH5DjnWwBoFYOn5EiIhoFq1IJc3cTgw85mv0P6wY6jDxsae_rJj-OAdBUyTvRjwrV3U6areXJxi9QHejn6Ace8p5_ntMG0f0ae9HbI-Pz-PSFf315-ubiqrlfv3l8srytX10JVddO4TjWOayV41zmne64kltB23TVtpyWIBmzft7YHUbd9Z6W7G0AjoJLihLw5eMe52-LaYZiSHcyY_NamvYnWm79_gv9mNnFnNOctcFEEr-8FKX6fMU9m67PDYbAB45wNl8C4lKB5QV_9g97GOYWyXqFYOaIWtS7U6YFyKeacsH8Iw8Dc9WNKP-ZXP4V9-Wf6B_J3IQU4PwA_ynn3_zeZ5c3yoPwJKheZgw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2513378348</pqid></control><display><type>article</type><title>Noninvasive Mapping of Ripple Onset Predicts Outcome in Epilepsy Surgery</title><source>Access via Wiley Online Library</source><creator>Tamilia, Eleonora ; Matarrese, Margherita A. G. ; Ntolkeras, Georgios ; Grant, P. Ellen ; Madsen, Joseph R. ; Stufflebeam, Steve M. ; Pearl, Phillip L. ; Papadelis, Christos</creator><creatorcontrib>Tamilia, Eleonora ; Matarrese, Margherita A. G. ; Ntolkeras, Georgios ; Grant, P. Ellen ; Madsen, Joseph R. ; Stufflebeam, Steve M. ; Pearl, Phillip L. ; Papadelis, Christos</creatorcontrib><description>Objective
Intracranial electroencephalographic (icEEG) studies show that interictal ripples propagate across the brain of children with medically refractory epilepsy (MRE), and the onset of this propagation (ripple onset zone [ROZ]) estimates the epileptogenic zone. It is still unknown whether we can map this propagation noninvasively. The goal of this study is to map ripples (ripple zone [RZ]) and their propagation onset (ROZ) using high‐density EEG (HD‐EEG) and magnetoencephalography (MEG), and to estimate their prognostic value in pediatric epilepsy surgery.
Methods
We retrospectively analyzed simultaneous HD‐EEG and MEG data from 28 children with MRE who underwent icEEG and epilepsy surgery. Using electric and magnetic source imaging, we estimated virtual sensors (VSs) at brain locations that matched the icEEG implantation. We detected ripples on VSs, defined the virtual RZ and virtual ROZ, and estimated their distance from icEEG. We assessed the predictive value of resecting virtual RZ and virtual ROZ for postsurgical outcome. Interictal spike localization on HD‐EEG and MEG was also performed and compared with ripples.
Results
We mapped ripple propagation in all patients with HD‐EEG and in 27 (96%) patients with MEG. The distance from icEEG did not differ between HD‐EEG and MEG when mapping the RZ (26–27mm, p = 0.6) or ROZ (22–24mm, p = 0.4). Resecting the virtual ROZ, but not virtual RZ or the sources of spikes, was associated with good outcome for HD‐EEG (p = 0.016) and MEG (p = 0.047).
Interpretation
HD‐EEG and MEG can map interictal ripples and their propagation onset (virtual ROZ). Noninvasively mapping the ripple onset may augment epilepsy surgery planning and improve surgical outcome of children with MRE. ANN NEUROL 2021;89:911–925</description><identifier>ISSN: 0364-5134</identifier><identifier>EISSN: 1531-8249</identifier><identifier>DOI: 10.1002/ana.26066</identifier><identifier>PMID: 33710676</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Brain ; Children ; EEG ; Electroencephalography ; Epilepsy ; Localization ; Magnetoencephalography ; Mapping ; Neuroimaging ; Patients ; Propagation ; Ripples ; Spikes ; Surgery ; Virtual sensors</subject><ispartof>Annals of neurology, 2021-05, Vol.89 (5), p.911-925</ispartof><rights>2021 The Authors. published by Wiley Periodicals LLC on behalf of American Neurological Association.</rights><rights>2021 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.</rights><rights>2021. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4436-477cb67c28632bbcc8f265e531adb79b850370aff9af0349fba5c034908e0e653</citedby><cites>FETCH-LOGICAL-c4436-477cb67c28632bbcc8f265e531adb79b850370aff9af0349fba5c034908e0e653</cites><orcidid>0000-0002-1235-3052 ; 0000-0001-6125-9217 ; 0000-0001-9833-9886 ; 0000-0002-2281-035X ; 0000-0002-6373-1068</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fana.26066$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fana.26066$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33710676$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tamilia, Eleonora</creatorcontrib><creatorcontrib>Matarrese, Margherita A. G.</creatorcontrib><creatorcontrib>Ntolkeras, Georgios</creatorcontrib><creatorcontrib>Grant, P. Ellen</creatorcontrib><creatorcontrib>Madsen, Joseph R.</creatorcontrib><creatorcontrib>Stufflebeam, Steve M.</creatorcontrib><creatorcontrib>Pearl, Phillip L.</creatorcontrib><creatorcontrib>Papadelis, Christos</creatorcontrib><title>Noninvasive Mapping of Ripple Onset Predicts Outcome in Epilepsy Surgery</title><title>Annals of neurology</title><addtitle>Ann Neurol</addtitle><description>Objective
Intracranial electroencephalographic (icEEG) studies show that interictal ripples propagate across the brain of children with medically refractory epilepsy (MRE), and the onset of this propagation (ripple onset zone [ROZ]) estimates the epileptogenic zone. It is still unknown whether we can map this propagation noninvasively. The goal of this study is to map ripples (ripple zone [RZ]) and their propagation onset (ROZ) using high‐density EEG (HD‐EEG) and magnetoencephalography (MEG), and to estimate their prognostic value in pediatric epilepsy surgery.
Methods
We retrospectively analyzed simultaneous HD‐EEG and MEG data from 28 children with MRE who underwent icEEG and epilepsy surgery. Using electric and magnetic source imaging, we estimated virtual sensors (VSs) at brain locations that matched the icEEG implantation. We detected ripples on VSs, defined the virtual RZ and virtual ROZ, and estimated their distance from icEEG. We assessed the predictive value of resecting virtual RZ and virtual ROZ for postsurgical outcome. Interictal spike localization on HD‐EEG and MEG was also performed and compared with ripples.
Results
We mapped ripple propagation in all patients with HD‐EEG and in 27 (96%) patients with MEG. The distance from icEEG did not differ between HD‐EEG and MEG when mapping the RZ (26–27mm, p = 0.6) or ROZ (22–24mm, p = 0.4). Resecting the virtual ROZ, but not virtual RZ or the sources of spikes, was associated with good outcome for HD‐EEG (p = 0.016) and MEG (p = 0.047).
Interpretation
HD‐EEG and MEG can map interictal ripples and their propagation onset (virtual ROZ). Noninvasively mapping the ripple onset may augment epilepsy surgery planning and improve surgical outcome of children with MRE. ANN NEUROL 2021;89:911–925</description><subject>Brain</subject><subject>Children</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>Epilepsy</subject><subject>Localization</subject><subject>Magnetoencephalography</subject><subject>Mapping</subject><subject>Neuroimaging</subject><subject>Patients</subject><subject>Propagation</subject><subject>Ripples</subject><subject>Spikes</subject><subject>Surgery</subject><subject>Virtual sensors</subject><issn>0364-5134</issn><issn>1531-8249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><recordid>eNp1kV1rFDEUhoModlu98A9IwBt7Me1JMslkboSlVCvUrvhxHTLZM2vKbDImMyv7703dWlTwKgfy8PCe8xLygsEZA-DnNtgzrkCpR2TBpGCV5nX7mCxAqLqSTNRH5DjnWwBoFYOn5EiIhoFq1IJc3cTgw85mv0P6wY6jDxsae_rJj-OAdBUyTvRjwrV3U6areXJxi9QHejn6Ace8p5_ntMG0f0ae9HbI-Pz-PSFf315-ubiqrlfv3l8srytX10JVddO4TjWOayV41zmne64kltB23TVtpyWIBmzft7YHUbd9Z6W7G0AjoJLihLw5eMe52-LaYZiSHcyY_NamvYnWm79_gv9mNnFnNOctcFEEr-8FKX6fMU9m67PDYbAB45wNl8C4lKB5QV_9g97GOYWyXqFYOaIWtS7U6YFyKeacsH8Iw8Dc9WNKP-ZXP4V9-Wf6B_J3IQU4PwA_ynn3_zeZ5c3yoPwJKheZgw</recordid><startdate>202105</startdate><enddate>202105</enddate><creator>Tamilia, Eleonora</creator><creator>Matarrese, Margherita A. G.</creator><creator>Ntolkeras, Georgios</creator><creator>Grant, P. Ellen</creator><creator>Madsen, Joseph R.</creator><creator>Stufflebeam, Steve M.</creator><creator>Pearl, Phillip L.</creator><creator>Papadelis, Christos</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7U7</scope><scope>C1K</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1235-3052</orcidid><orcidid>https://orcid.org/0000-0001-6125-9217</orcidid><orcidid>https://orcid.org/0000-0001-9833-9886</orcidid><orcidid>https://orcid.org/0000-0002-2281-035X</orcidid><orcidid>https://orcid.org/0000-0002-6373-1068</orcidid></search><sort><creationdate>202105</creationdate><title>Noninvasive Mapping of Ripple Onset Predicts Outcome in Epilepsy Surgery</title><author>Tamilia, Eleonora ; Matarrese, Margherita A. G. ; Ntolkeras, Georgios ; Grant, P. Ellen ; Madsen, Joseph R. ; Stufflebeam, Steve M. ; Pearl, Phillip L. ; Papadelis, Christos</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4436-477cb67c28632bbcc8f265e531adb79b850370aff9af0349fba5c034908e0e653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Brain</topic><topic>Children</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>Epilepsy</topic><topic>Localization</topic><topic>Magnetoencephalography</topic><topic>Mapping</topic><topic>Neuroimaging</topic><topic>Patients</topic><topic>Propagation</topic><topic>Ripples</topic><topic>Spikes</topic><topic>Surgery</topic><topic>Virtual sensors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tamilia, Eleonora</creatorcontrib><creatorcontrib>Matarrese, Margherita A. G.</creatorcontrib><creatorcontrib>Ntolkeras, Georgios</creatorcontrib><creatorcontrib>Grant, P. Ellen</creatorcontrib><creatorcontrib>Madsen, Joseph R.</creatorcontrib><creatorcontrib>Stufflebeam, Steve M.</creatorcontrib><creatorcontrib>Pearl, Phillip L.</creatorcontrib><creatorcontrib>Papadelis, Christos</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Annals of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tamilia, Eleonora</au><au>Matarrese, Margherita A. G.</au><au>Ntolkeras, Georgios</au><au>Grant, P. Ellen</au><au>Madsen, Joseph R.</au><au>Stufflebeam, Steve M.</au><au>Pearl, Phillip L.</au><au>Papadelis, Christos</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Noninvasive Mapping of Ripple Onset Predicts Outcome in Epilepsy Surgery</atitle><jtitle>Annals of neurology</jtitle><addtitle>Ann Neurol</addtitle><date>2021-05</date><risdate>2021</risdate><volume>89</volume><issue>5</issue><spage>911</spage><epage>925</epage><pages>911-925</pages><issn>0364-5134</issn><eissn>1531-8249</eissn><abstract>Objective
Intracranial electroencephalographic (icEEG) studies show that interictal ripples propagate across the brain of children with medically refractory epilepsy (MRE), and the onset of this propagation (ripple onset zone [ROZ]) estimates the epileptogenic zone. It is still unknown whether we can map this propagation noninvasively. The goal of this study is to map ripples (ripple zone [RZ]) and their propagation onset (ROZ) using high‐density EEG (HD‐EEG) and magnetoencephalography (MEG), and to estimate their prognostic value in pediatric epilepsy surgery.
Methods
We retrospectively analyzed simultaneous HD‐EEG and MEG data from 28 children with MRE who underwent icEEG and epilepsy surgery. Using electric and magnetic source imaging, we estimated virtual sensors (VSs) at brain locations that matched the icEEG implantation. We detected ripples on VSs, defined the virtual RZ and virtual ROZ, and estimated their distance from icEEG. We assessed the predictive value of resecting virtual RZ and virtual ROZ for postsurgical outcome. Interictal spike localization on HD‐EEG and MEG was also performed and compared with ripples.
Results
We mapped ripple propagation in all patients with HD‐EEG and in 27 (96%) patients with MEG. The distance from icEEG did not differ between HD‐EEG and MEG when mapping the RZ (26–27mm, p = 0.6) or ROZ (22–24mm, p = 0.4). Resecting the virtual ROZ, but not virtual RZ or the sources of spikes, was associated with good outcome for HD‐EEG (p = 0.016) and MEG (p = 0.047).
Interpretation
HD‐EEG and MEG can map interictal ripples and their propagation onset (virtual ROZ). Noninvasively mapping the ripple onset may augment epilepsy surgery planning and improve surgical outcome of children with MRE. ANN NEUROL 2021;89:911–925</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>33710676</pmid><doi>10.1002/ana.26066</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-1235-3052</orcidid><orcidid>https://orcid.org/0000-0001-6125-9217</orcidid><orcidid>https://orcid.org/0000-0001-9833-9886</orcidid><orcidid>https://orcid.org/0000-0002-2281-035X</orcidid><orcidid>https://orcid.org/0000-0002-6373-1068</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Access via Wiley Online Library |
| subjects | Brain Children EEG Electroencephalography Epilepsy Localization Magnetoencephalography Mapping Neuroimaging Patients Propagation Ripples Spikes Surgery Virtual sensors |
| title | Noninvasive Mapping of Ripple Onset Predicts Outcome in Epilepsy Surgery |
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