Oscillatory brain activity associates with neuroligin-3 expression and predicts progression free survival in patients with diffuse glioma
Introduction Diffuse gliomas have local and global effects on neurophysiological brain functioning, which are often seen as ‘passive’ consequences of the tumor. However, seminal preclinical work has shown a prominent role for neuronal activity in glioma growth: mediated by neuroligin-3 (NLGN3), incr...
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| Veröffentlicht in: | Journal of neuro-oncology 2018-11, Vol.140 (2), p.403-412 |
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| creator | Derks, Jolanda Wesseling, Pieter Carbo, Ellen W. S. Hillebrand, Arjan van Dellen, Edwin de Witt Hamer, Philip C. Klein, Martin Schenk, Geert J. Geurts, Jeroen J. G. Reijneveld, Jaap C. Douw, Linda |
| description | Introduction
Diffuse gliomas have local and global effects on neurophysiological brain functioning, which are often seen as ‘passive’ consequences of the tumor. However, seminal preclinical work has shown a prominent role for neuronal activity in glioma growth: mediated by neuroligin-3 (NLGN3), increased neuronal activity causes faster glioma growth. It is unclear whether the same holds true in patients. Here, we investigate whether lower levels of oscillatory brain activity relate to lower NLGN3 expression and predict longer progression free survival (PFS) in diffuse glioma patients.
Methods
Twenty-four newly diagnosed patients with diffuse glioma underwent magnetoencephalography and subsequent tumor resection. Oscillatory brain activity was approximated by calculating broadband power (0.5–48 Hz) of the magnetoencephalography. NLGN3 expression in glioma tissue was semi-quantitatively assessed by immunohistochemistry. Peritumor and global oscillatory brain activity was then compared between different levels of NLGN3 expression with Kruskal–Wallis tests. Cox proportional hazards analyses were performed to estimate the predictive value of oscillatory brain activity for PFS.
Results
Patients with low expression of NLGN3 had lower levels of global oscillatory brain activity than patients with higher NLGN3 expression (P |
| doi_str_mv | 10.1007/s11060-018-2967-5 |
| format | Article |
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Diffuse gliomas have local and global effects on neurophysiological brain functioning, which are often seen as ‘passive’ consequences of the tumor. However, seminal preclinical work has shown a prominent role for neuronal activity in glioma growth: mediated by neuroligin-3 (NLGN3), increased neuronal activity causes faster glioma growth. It is unclear whether the same holds true in patients. Here, we investigate whether lower levels of oscillatory brain activity relate to lower NLGN3 expression and predict longer progression free survival (PFS) in diffuse glioma patients.
Methods
Twenty-four newly diagnosed patients with diffuse glioma underwent magnetoencephalography and subsequent tumor resection. Oscillatory brain activity was approximated by calculating broadband power (0.5–48 Hz) of the magnetoencephalography. NLGN3 expression in glioma tissue was semi-quantitatively assessed by immunohistochemistry. Peritumor and global oscillatory brain activity was then compared between different levels of NLGN3 expression with Kruskal–Wallis tests. Cox proportional hazards analyses were performed to estimate the predictive value of oscillatory brain activity for PFS.
Results
Patients with low expression of NLGN3 had lower levels of global oscillatory brain activity than patients with higher NLGN3 expression (P < 0.001). Moreover, lower peritumor (hazard ratio 2.17, P = 0.008) and global oscillatory brain activity (hazard ratio 2.10, P = 0.008) predicted longer PFS.
Conclusions
Lower levels of peritumor and global oscillatory brain activity are related to lower NLGN3 expression and longer PFS, corroborating preclinical research. This study highlights the important interplay between macroscopically measured brain activity and glioma progression, and may lead to new therapeutic interventions in diffuse glioma patients.</description><identifier>ISSN: 0167-594X</identifier><identifier>EISSN: 1573-7373</identifier><identifier>DOI: 10.1007/s11060-018-2967-5</identifier><identifier>PMID: 30094719</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Adolescent ; Adult ; Biomarkers, Tumor - metabolism ; Brain - pathology ; Brain - physiopathology ; Brain Neoplasms - diagnosis ; Brain Neoplasms - pathology ; Brain Neoplasms - physiopathology ; Brain tumors ; Brain Waves - physiology ; Cell Adhesion Molecules, Neuronal - metabolism ; Clinical Study ; Cohort Studies ; Disease Progression ; Dreams ; Female ; Gene Expression Regulation, Neoplastic ; Glioma ; Glioma - diagnosis ; Glioma - pathology ; Glioma - physiopathology ; Humans ; Immunohistochemistry ; Magnetoencephalography ; Male ; Medicine ; Medicine & Public Health ; Membrane Proteins - metabolism ; Middle Aged ; Nerve Tissue Proteins - metabolism ; Neurology ; Oncology ; Prognosis ; Progression-Free Survival ; Therapeutic applications</subject><ispartof>Journal of neuro-oncology, 2018-11, Vol.140 (2), p.403-412</ispartof><rights>The Author(s) 2018</rights><rights>Journal of Neuro-Oncology is a copyright of Springer, (2018). All Rights Reserved. © 2018. This work is published under http://creativecommons.org/licenses/by/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-c470t-7559746c9db00b8681bff7873f64aa86269f0b951f630fdf8e9dc38598bc066a3</citedby><cites>FETCH-LOGICAL-c470t-7559746c9db00b8681bff7873f64aa86269f0b951f630fdf8e9dc38598bc066a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s11060-018-2967-5$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s11060-018-2967-5$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,315,781,785,886,27929,27930,41493,42562,51324</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30094719$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Derks, Jolanda</creatorcontrib><creatorcontrib>Wesseling, Pieter</creatorcontrib><creatorcontrib>Carbo, Ellen W. S.</creatorcontrib><creatorcontrib>Hillebrand, Arjan</creatorcontrib><creatorcontrib>van Dellen, Edwin</creatorcontrib><creatorcontrib>de Witt Hamer, Philip C.</creatorcontrib><creatorcontrib>Klein, Martin</creatorcontrib><creatorcontrib>Schenk, Geert J.</creatorcontrib><creatorcontrib>Geurts, Jeroen J. G.</creatorcontrib><creatorcontrib>Reijneveld, Jaap C.</creatorcontrib><creatorcontrib>Douw, Linda</creatorcontrib><title>Oscillatory brain activity associates with neuroligin-3 expression and predicts progression free survival in patients with diffuse glioma</title><title>Journal of neuro-oncology</title><addtitle>J Neurooncol</addtitle><addtitle>J Neurooncol</addtitle><description>Introduction
Diffuse gliomas have local and global effects on neurophysiological brain functioning, which are often seen as ‘passive’ consequences of the tumor. However, seminal preclinical work has shown a prominent role for neuronal activity in glioma growth: mediated by neuroligin-3 (NLGN3), increased neuronal activity causes faster glioma growth. It is unclear whether the same holds true in patients. Here, we investigate whether lower levels of oscillatory brain activity relate to lower NLGN3 expression and predict longer progression free survival (PFS) in diffuse glioma patients.
Methods
Twenty-four newly diagnosed patients with diffuse glioma underwent magnetoencephalography and subsequent tumor resection. Oscillatory brain activity was approximated by calculating broadband power (0.5–48 Hz) of the magnetoencephalography. NLGN3 expression in glioma tissue was semi-quantitatively assessed by immunohistochemistry. Peritumor and global oscillatory brain activity was then compared between different levels of NLGN3 expression with Kruskal–Wallis tests. Cox proportional hazards analyses were performed to estimate the predictive value of oscillatory brain activity for PFS.
Results
Patients with low expression of NLGN3 had lower levels of global oscillatory brain activity than patients with higher NLGN3 expression (P < 0.001). Moreover, lower peritumor (hazard ratio 2.17, P = 0.008) and global oscillatory brain activity (hazard ratio 2.10, P = 0.008) predicted longer PFS.
Conclusions
Lower levels of peritumor and global oscillatory brain activity are related to lower NLGN3 expression and longer PFS, corroborating preclinical research. This study highlights the important interplay between macroscopically measured brain activity and glioma progression, and may lead to new therapeutic interventions in diffuse glioma patients.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Biomarkers, Tumor - metabolism</subject><subject>Brain - pathology</subject><subject>Brain - physiopathology</subject><subject>Brain Neoplasms - diagnosis</subject><subject>Brain Neoplasms - pathology</subject><subject>Brain Neoplasms - physiopathology</subject><subject>Brain tumors</subject><subject>Brain Waves - physiology</subject><subject>Cell Adhesion Molecules, Neuronal - metabolism</subject><subject>Clinical Study</subject><subject>Cohort Studies</subject><subject>Disease Progression</subject><subject>Dreams</subject><subject>Female</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Glioma</subject><subject>Glioma - diagnosis</subject><subject>Glioma - pathology</subject><subject>Glioma - physiopathology</subject><subject>Humans</subject><subject>Immunohistochemistry</subject><subject>Magnetoencephalography</subject><subject>Male</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Membrane Proteins - metabolism</subject><subject>Middle Aged</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Neurology</subject><subject>Oncology</subject><subject>Prognosis</subject><subject>Progression-Free Survival</subject><subject>Therapeutic applications</subject><issn>0167-594X</issn><issn>1573-7373</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNp1kcuKFDEUhoMoTjv6AG4k4MZN6UmlKpeNIIM3GJiNgruQSiU9GaorbU6qx34E39o03TNewFUu_3f-nJOfkOcMXjMA-QYZAwENMNW0Wsimf0BWrJe8kVzyh2QF7HCpu29n5AniDQB0krPH5IwD6E4yvSI_r9DFabIl5T0dso0zta7EXSx7ahGTi7Z4pLexXNPZLzlNcR3nhlP_Y5s9Yky1YB5pPYzRFaybtL4TQvae4pJ3cWcnWq23tkQ_l5PfGENY0NP1FNPGPiWPgp3QPzut5-Trh_dfLj41l1cfP1-8u2xcJ6E0su-17ITT4wAwKKHYEIJUkgfRWatEK3SAQfcsCA5hDMrr0XHVazU4EMLyc_L26Ltdho0fXe0n28lsc9zYvDfJRvO3Msdrs047I9quk7KrBq9OBjl9XzwWs4nofP3E2acFTQtK9ppLBRV9-Q96k5Y81_EOlAAueqkqxY6Uywkx-3DfDANzCNocgzY1aHMI2vS15sWfU9xX3CVbgfYIYJXmtc-_n_6_6y8pbLfT</recordid><startdate>20181101</startdate><enddate>20181101</enddate><creator>Derks, Jolanda</creator><creator>Wesseling, Pieter</creator><creator>Carbo, Ellen W. S.</creator><creator>Hillebrand, Arjan</creator><creator>van Dellen, Edwin</creator><creator>de Witt Hamer, Philip C.</creator><creator>Klein, Martin</creator><creator>Schenk, Geert J.</creator><creator>Geurts, Jeroen J. G.</creator><creator>Reijneveld, Jaap C.</creator><creator>Douw, Linda</creator><general>Springer US</general><general>Springer Nature B.V</general><scope>C6C</scope><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>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20181101</creationdate><title>Oscillatory brain activity associates with neuroligin-3 expression and predicts progression free survival in patients with diffuse glioma</title><author>Derks, Jolanda ; Wesseling, Pieter ; Carbo, Ellen W. S. ; Hillebrand, Arjan ; van Dellen, Edwin ; de Witt Hamer, Philip C. ; Klein, Martin ; Schenk, Geert J. ; Geurts, Jeroen J. G. ; Reijneveld, Jaap C. ; Douw, Linda</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-7559746c9db00b8681bff7873f64aa86269f0b951f630fdf8e9dc38598bc066a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Biomarkers, Tumor - metabolism</topic><topic>Brain - pathology</topic><topic>Brain - physiopathology</topic><topic>Brain Neoplasms - diagnosis</topic><topic>Brain Neoplasms - pathology</topic><topic>Brain Neoplasms - physiopathology</topic><topic>Brain tumors</topic><topic>Brain Waves - physiology</topic><topic>Cell Adhesion Molecules, Neuronal - metabolism</topic><topic>Clinical Study</topic><topic>Cohort Studies</topic><topic>Disease Progression</topic><topic>Dreams</topic><topic>Female</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>Glioma</topic><topic>Glioma - diagnosis</topic><topic>Glioma - pathology</topic><topic>Glioma - physiopathology</topic><topic>Humans</topic><topic>Immunohistochemistry</topic><topic>Magnetoencephalography</topic><topic>Male</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Membrane Proteins - metabolism</topic><topic>Middle Aged</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neurology</topic><topic>Oncology</topic><topic>Prognosis</topic><topic>Progression-Free Survival</topic><topic>Therapeutic applications</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Derks, Jolanda</creatorcontrib><creatorcontrib>Wesseling, Pieter</creatorcontrib><creatorcontrib>Carbo, Ellen W. 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G.</creatorcontrib><creatorcontrib>Reijneveld, Jaap C.</creatorcontrib><creatorcontrib>Douw, Linda</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neuro-oncology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Derks, Jolanda</au><au>Wesseling, Pieter</au><au>Carbo, Ellen W. S.</au><au>Hillebrand, Arjan</au><au>van Dellen, Edwin</au><au>de Witt Hamer, Philip C.</au><au>Klein, Martin</au><au>Schenk, Geert J.</au><au>Geurts, Jeroen J. G.</au><au>Reijneveld, Jaap C.</au><au>Douw, Linda</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oscillatory brain activity associates with neuroligin-3 expression and predicts progression free survival in patients with diffuse glioma</atitle><jtitle>Journal of neuro-oncology</jtitle><stitle>J Neurooncol</stitle><addtitle>J Neurooncol</addtitle><date>2018-11-01</date><risdate>2018</risdate><volume>140</volume><issue>2</issue><spage>403</spage><epage>412</epage><pages>403-412</pages><issn>0167-594X</issn><eissn>1573-7373</eissn><abstract>Introduction
Diffuse gliomas have local and global effects on neurophysiological brain functioning, which are often seen as ‘passive’ consequences of the tumor. However, seminal preclinical work has shown a prominent role for neuronal activity in glioma growth: mediated by neuroligin-3 (NLGN3), increased neuronal activity causes faster glioma growth. It is unclear whether the same holds true in patients. Here, we investigate whether lower levels of oscillatory brain activity relate to lower NLGN3 expression and predict longer progression free survival (PFS) in diffuse glioma patients.
Methods
Twenty-four newly diagnosed patients with diffuse glioma underwent magnetoencephalography and subsequent tumor resection. Oscillatory brain activity was approximated by calculating broadband power (0.5–48 Hz) of the magnetoencephalography. NLGN3 expression in glioma tissue was semi-quantitatively assessed by immunohistochemistry. Peritumor and global oscillatory brain activity was then compared between different levels of NLGN3 expression with Kruskal–Wallis tests. Cox proportional hazards analyses were performed to estimate the predictive value of oscillatory brain activity for PFS.
Results
Patients with low expression of NLGN3 had lower levels of global oscillatory brain activity than patients with higher NLGN3 expression (P < 0.001). Moreover, lower peritumor (hazard ratio 2.17, P = 0.008) and global oscillatory brain activity (hazard ratio 2.10, P = 0.008) predicted longer PFS.
Conclusions
Lower levels of peritumor and global oscillatory brain activity are related to lower NLGN3 expression and longer PFS, corroborating preclinical research. This study highlights the important interplay between macroscopically measured brain activity and glioma progression, and may lead to new therapeutic interventions in diffuse glioma patients.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>30094719</pmid><doi>10.1007/s11060-018-2967-5</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adolescent Adult Biomarkers, Tumor - metabolism Brain - pathology Brain - physiopathology Brain Neoplasms - diagnosis Brain Neoplasms - pathology Brain Neoplasms - physiopathology Brain tumors Brain Waves - physiology Cell Adhesion Molecules, Neuronal - metabolism Clinical Study Cohort Studies Disease Progression Dreams Female Gene Expression Regulation, Neoplastic Glioma Glioma - diagnosis Glioma - pathology Glioma - physiopathology Humans Immunohistochemistry Magnetoencephalography Male Medicine Medicine & Public Health Membrane Proteins - metabolism Middle Aged Nerve Tissue Proteins - metabolism Neurology Oncology Prognosis Progression-Free Survival Therapeutic applications |
| title | Oscillatory brain activity associates with neuroligin-3 expression and predicts progression free survival in patients with diffuse glioma |
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