Utility of texture analysis for objective quantitative ex vivo assessment of meningioma consistency: method proposal and validation
Background Tumor consistency is considered to be a critical factor for the surgical removal of meningiomas and its preoperative assessment is intensively studied. A significant drawback in the research of predictive methods is the lack of a clear shared definition of tumor consistency, with most aut...
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| Veröffentlicht in: | Acta neurochirurgica 2023-12, Vol.165 (12), p.4203-4211 |
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| creator | Černý, Martin Lesáková, Veronika Soukup, Jiří Sedlák, Vojtěch Šíma, Luděk May, Michaela Netuka, David Štěpánek, František Beneš, Vladimír |
| description | Background
Tumor consistency is considered to be a critical factor for the surgical removal of meningiomas and its preoperative assessment is intensively studied. A significant drawback in the research of predictive methods is the lack of a clear shared definition of tumor consistency, with most authors resorting to subjective binary classification labeling the samples as “soft” and “hard.” This classification is highly observer-dependent and its discrete nature fails to capture the fine nuances in tumor consistency. To compensate for these shortcomings, we examined the utility of texture analysis to provide an objective observer-independent continuous measure of meningioma consistency.
Methods
A total of 169 texturometric measurements were conducted using the Brookfield CT3 Texture Analyzer on meningioma samples from five patients immediately after the removal and on the first, second, and seventh postoperative day. The relationship between measured stiffness and time from sample extraction, subjectively assessed consistency grade and histopathological features (amount of collagen and reticulin fibers, presence of psammoma bodies, predominant microscopic morphology) was analyzed.
Results
The stiffness measurements exhibited significantly lower variance within a sample than among samples (
p
= 0.0225) and significant increase with a higher objectively assessed consistency grade (
p
= 0.0161,
p
= 0.0055). A significant negative correlation was found between the measured stiffness and the time from sample extraction (
p
|
| doi_str_mv | 10.1007/s00701-023-05867-1 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2897489078</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2897489078</sourcerecordid><originalsourceid>FETCH-LOGICAL-c326t-1d7c96f73304c80a520fd6f543732bb525de08640e2d56d17d8c1f63e77ca43e3</originalsourceid><addsrcrecordid>eNp9kT1vHCEQhlGUKHac_AEXEVKaNJsMH7vsurMs50OylCauEQezNqddOAN7uqvzx4N9jh2lSDPDwDPvAC8hpww-MQD1OdcArAEuGmj7TjXsBTmGQfKmBnj51_qIvMl5DcC4kuI1ORI9SCmUPCa_rouffNnTONKCu7IkpCaYaZ99pmNMNK7WaIvfIr1bTCi-mIcCd3Trt5GanDHnGUO5V6jZhxsfZ0NtDFWiYLD7s7pfbqOjmxQ3MZupTnB0aybvqlgMb8mr0UwZ3z3mE3L95fLnxbfm6sfX7xfnV40VvCsNc8oO3aiEAGl7MC2H0XVjWx8i-GrV8tYh9J0E5K7tHFOut2zsBCpljRQoTsjHg269x92CuejZZ4vTZALGJWveD0r2A6i-oh_-QddxSfVfKjWAbJlSAirFD5RNMeeEo94kP5u01wz0vUX6YJGuFukHizSrTe8fpZfVjO6p5Y8nFRAHINejcIPpefZ_ZH8D8OSecQ</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2904517730</pqid></control><display><type>article</type><title>Utility of texture analysis for objective quantitative ex vivo assessment of meningioma consistency: method proposal and validation</title><source>MEDLINE</source><source>SpringerLink Journals - AutoHoldings</source><creator>Černý, Martin ; Lesáková, Veronika ; Soukup, Jiří ; Sedlák, Vojtěch ; Šíma, Luděk ; May, Michaela ; Netuka, David ; Štěpánek, František ; Beneš, Vladimír</creator><creatorcontrib>Černý, Martin ; Lesáková, Veronika ; Soukup, Jiří ; Sedlák, Vojtěch ; Šíma, Luděk ; May, Michaela ; Netuka, David ; Štěpánek, František ; Beneš, Vladimír</creatorcontrib><description>Background
Tumor consistency is considered to be a critical factor for the surgical removal of meningiomas and its preoperative assessment is intensively studied. A significant drawback in the research of predictive methods is the lack of a clear shared definition of tumor consistency, with most authors resorting to subjective binary classification labeling the samples as “soft” and “hard.” This classification is highly observer-dependent and its discrete nature fails to capture the fine nuances in tumor consistency. To compensate for these shortcomings, we examined the utility of texture analysis to provide an objective observer-independent continuous measure of meningioma consistency.
Methods
A total of 169 texturometric measurements were conducted using the Brookfield CT3 Texture Analyzer on meningioma samples from five patients immediately after the removal and on the first, second, and seventh postoperative day. The relationship between measured stiffness and time from sample extraction, subjectively assessed consistency grade and histopathological features (amount of collagen and reticulin fibers, presence of psammoma bodies, predominant microscopic morphology) was analyzed.
Results
The stiffness measurements exhibited significantly lower variance within a sample than among samples (
p
= 0.0225) and significant increase with a higher objectively assessed consistency grade (
p
= 0.0161,
p
= 0.0055). A significant negative correlation was found between the measured stiffness and the time from sample extraction (
p
< 0.01). A significant monotonic relationship was revealed between stiffness values and amount of collagen I and reticulin fibers; there were no statistically significant differences between histological phenotypes in regard to presence of psammoma bodies and predominant microscopic morphology.
Conclusions
We conclude that the values yielded by texture analysis are highly representative of an intrinsic consistency-related quality of the sample despite the influence of intra-sample heterogeneity and that our proposed method can be used to conduct quantitative studies on the role of meningioma consistency.</description><identifier>ISSN: 0942-0940</identifier><identifier>ISSN: 0001-6268</identifier><identifier>EISSN: 0942-0940</identifier><identifier>DOI: 10.1007/s00701-023-05867-1</identifier><identifier>PMID: 38044374</identifier><language>eng</language><publisher>Vienna: Springer Vienna</publisher><subject>Brain cancer ; Classification ; Collagen ; Collagen (type I) ; Fibers ; Humans ; Interventional Radiology ; Magnetic Resonance Imaging - methods ; Medicine ; Medicine & Public Health ; Meningeal Neoplasms - pathology ; Meningeal Neoplasms - surgery ; Meningioma ; Meningioma - diagnostic imaging ; Meningioma - pathology ; Meningioma - surgery ; Minimally Invasive Surgery ; Morphology ; Neurology ; Neuroradiology ; Neurosurgery ; Original Article ; Phenotypes ; Reticulin ; Statistical analysis ; Surgical Orthopedics ; Tumor – Meningioma ; Tumors</subject><ispartof>Acta neurochirurgica, 2023-12, Vol.165 (12), p.4203-4211</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c326t-1d7c96f73304c80a520fd6f543732bb525de08640e2d56d17d8c1f63e77ca43e3</cites><orcidid>0000-0002-8601-0554</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00701-023-05867-1$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00701-023-05867-1$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27903,27904,41467,42536,51297</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38044374$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Černý, Martin</creatorcontrib><creatorcontrib>Lesáková, Veronika</creatorcontrib><creatorcontrib>Soukup, Jiří</creatorcontrib><creatorcontrib>Sedlák, Vojtěch</creatorcontrib><creatorcontrib>Šíma, Luděk</creatorcontrib><creatorcontrib>May, Michaela</creatorcontrib><creatorcontrib>Netuka, David</creatorcontrib><creatorcontrib>Štěpánek, František</creatorcontrib><creatorcontrib>Beneš, Vladimír</creatorcontrib><title>Utility of texture analysis for objective quantitative ex vivo assessment of meningioma consistency: method proposal and validation</title><title>Acta neurochirurgica</title><addtitle>Acta Neurochir</addtitle><addtitle>Acta Neurochir (Wien)</addtitle><description>Background
Tumor consistency is considered to be a critical factor for the surgical removal of meningiomas and its preoperative assessment is intensively studied. A significant drawback in the research of predictive methods is the lack of a clear shared definition of tumor consistency, with most authors resorting to subjective binary classification labeling the samples as “soft” and “hard.” This classification is highly observer-dependent and its discrete nature fails to capture the fine nuances in tumor consistency. To compensate for these shortcomings, we examined the utility of texture analysis to provide an objective observer-independent continuous measure of meningioma consistency.
Methods
A total of 169 texturometric measurements were conducted using the Brookfield CT3 Texture Analyzer on meningioma samples from five patients immediately after the removal and on the first, second, and seventh postoperative day. The relationship between measured stiffness and time from sample extraction, subjectively assessed consistency grade and histopathological features (amount of collagen and reticulin fibers, presence of psammoma bodies, predominant microscopic morphology) was analyzed.
Results
The stiffness measurements exhibited significantly lower variance within a sample than among samples (
p
= 0.0225) and significant increase with a higher objectively assessed consistency grade (
p
= 0.0161,
p
= 0.0055). A significant negative correlation was found between the measured stiffness and the time from sample extraction (
p
< 0.01). A significant monotonic relationship was revealed between stiffness values and amount of collagen I and reticulin fibers; there were no statistically significant differences between histological phenotypes in regard to presence of psammoma bodies and predominant microscopic morphology.
Conclusions
We conclude that the values yielded by texture analysis are highly representative of an intrinsic consistency-related quality of the sample despite the influence of intra-sample heterogeneity and that our proposed method can be used to conduct quantitative studies on the role of meningioma consistency.</description><subject>Brain cancer</subject><subject>Classification</subject><subject>Collagen</subject><subject>Collagen (type I)</subject><subject>Fibers</subject><subject>Humans</subject><subject>Interventional Radiology</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Meningeal Neoplasms - pathology</subject><subject>Meningeal Neoplasms - surgery</subject><subject>Meningioma</subject><subject>Meningioma - diagnostic imaging</subject><subject>Meningioma - pathology</subject><subject>Meningioma - surgery</subject><subject>Minimally Invasive Surgery</subject><subject>Morphology</subject><subject>Neurology</subject><subject>Neuroradiology</subject><subject>Neurosurgery</subject><subject>Original Article</subject><subject>Phenotypes</subject><subject>Reticulin</subject><subject>Statistical analysis</subject><subject>Surgical Orthopedics</subject><subject>Tumor – Meningioma</subject><subject>Tumors</subject><issn>0942-0940</issn><issn>0001-6268</issn><issn>0942-0940</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kT1vHCEQhlGUKHac_AEXEVKaNJsMH7vsurMs50OylCauEQezNqddOAN7uqvzx4N9jh2lSDPDwDPvAC8hpww-MQD1OdcArAEuGmj7TjXsBTmGQfKmBnj51_qIvMl5DcC4kuI1ORI9SCmUPCa_rouffNnTONKCu7IkpCaYaZ99pmNMNK7WaIvfIr1bTCi-mIcCd3Trt5GanDHnGUO5V6jZhxsfZ0NtDFWiYLD7s7pfbqOjmxQ3MZupTnB0aybvqlgMb8mr0UwZ3z3mE3L95fLnxbfm6sfX7xfnV40VvCsNc8oO3aiEAGl7MC2H0XVjWx8i-GrV8tYh9J0E5K7tHFOut2zsBCpljRQoTsjHg269x92CuejZZ4vTZALGJWveD0r2A6i-oh_-QddxSfVfKjWAbJlSAirFD5RNMeeEo94kP5u01wz0vUX6YJGuFukHizSrTe8fpZfVjO6p5Y8nFRAHINejcIPpefZ_ZH8D8OSecQ</recordid><startdate>20231201</startdate><enddate>20231201</enddate><creator>Černý, Martin</creator><creator>Lesáková, Veronika</creator><creator>Soukup, Jiří</creator><creator>Sedlák, Vojtěch</creator><creator>Šíma, Luděk</creator><creator>May, Michaela</creator><creator>Netuka, David</creator><creator>Štěpánek, František</creator><creator>Beneš, Vladimír</creator><general>Springer Vienna</general><general>Springer Nature B.V</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>3V.</scope><scope>7TK</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</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>H94</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-8601-0554</orcidid></search><sort><creationdate>20231201</creationdate><title>Utility of texture analysis for objective quantitative ex vivo assessment of meningioma consistency: method proposal and validation</title><author>Černý, Martin ; Lesáková, Veronika ; Soukup, Jiří ; Sedlák, Vojtěch ; Šíma, Luděk ; May, Michaela ; Netuka, David ; Štěpánek, František ; Beneš, Vladimír</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c326t-1d7c96f73304c80a520fd6f543732bb525de08640e2d56d17d8c1f63e77ca43e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Brain cancer</topic><topic>Classification</topic><topic>Collagen</topic><topic>Collagen (type I)</topic><topic>Fibers</topic><topic>Humans</topic><topic>Interventional Radiology</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Meningeal Neoplasms - pathology</topic><topic>Meningeal Neoplasms - surgery</topic><topic>Meningioma</topic><topic>Meningioma - diagnostic imaging</topic><topic>Meningioma - pathology</topic><topic>Meningioma - surgery</topic><topic>Minimally Invasive Surgery</topic><topic>Morphology</topic><topic>Neurology</topic><topic>Neuroradiology</topic><topic>Neurosurgery</topic><topic>Original Article</topic><topic>Phenotypes</topic><topic>Reticulin</topic><topic>Statistical analysis</topic><topic>Surgical Orthopedics</topic><topic>Tumor – Meningioma</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Černý, Martin</creatorcontrib><creatorcontrib>Lesáková, Veronika</creatorcontrib><creatorcontrib>Soukup, Jiří</creatorcontrib><creatorcontrib>Sedlák, Vojtěch</creatorcontrib><creatorcontrib>Šíma, Luděk</creatorcontrib><creatorcontrib>May, Michaela</creatorcontrib><creatorcontrib>Netuka, David</creatorcontrib><creatorcontrib>Štěpánek, František</creatorcontrib><creatorcontrib>Beneš, Vladimír</creatorcontrib><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>Virology and AIDS 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>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>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</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><jtitle>Acta neurochirurgica</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Černý, Martin</au><au>Lesáková, Veronika</au><au>Soukup, Jiří</au><au>Sedlák, Vojtěch</au><au>Šíma, Luděk</au><au>May, Michaela</au><au>Netuka, David</au><au>Štěpánek, František</au><au>Beneš, Vladimír</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Utility of texture analysis for objective quantitative ex vivo assessment of meningioma consistency: method proposal and validation</atitle><jtitle>Acta neurochirurgica</jtitle><stitle>Acta Neurochir</stitle><addtitle>Acta Neurochir (Wien)</addtitle><date>2023-12-01</date><risdate>2023</risdate><volume>165</volume><issue>12</issue><spage>4203</spage><epage>4211</epage><pages>4203-4211</pages><issn>0942-0940</issn><issn>0001-6268</issn><eissn>0942-0940</eissn><abstract>Background
Tumor consistency is considered to be a critical factor for the surgical removal of meningiomas and its preoperative assessment is intensively studied. A significant drawback in the research of predictive methods is the lack of a clear shared definition of tumor consistency, with most authors resorting to subjective binary classification labeling the samples as “soft” and “hard.” This classification is highly observer-dependent and its discrete nature fails to capture the fine nuances in tumor consistency. To compensate for these shortcomings, we examined the utility of texture analysis to provide an objective observer-independent continuous measure of meningioma consistency.
Methods
A total of 169 texturometric measurements were conducted using the Brookfield CT3 Texture Analyzer on meningioma samples from five patients immediately after the removal and on the first, second, and seventh postoperative day. The relationship between measured stiffness and time from sample extraction, subjectively assessed consistency grade and histopathological features (amount of collagen and reticulin fibers, presence of psammoma bodies, predominant microscopic morphology) was analyzed.
Results
The stiffness measurements exhibited significantly lower variance within a sample than among samples (
p
= 0.0225) and significant increase with a higher objectively assessed consistency grade (
p
= 0.0161,
p
= 0.0055). A significant negative correlation was found between the measured stiffness and the time from sample extraction (
p
< 0.01). A significant monotonic relationship was revealed between stiffness values and amount of collagen I and reticulin fibers; there were no statistically significant differences between histological phenotypes in regard to presence of psammoma bodies and predominant microscopic morphology.
Conclusions
We conclude that the values yielded by texture analysis are highly representative of an intrinsic consistency-related quality of the sample despite the influence of intra-sample heterogeneity and that our proposed method can be used to conduct quantitative studies on the role of meningioma consistency.</abstract><cop>Vienna</cop><pub>Springer Vienna</pub><pmid>38044374</pmid><doi>10.1007/s00701-023-05867-1</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-8601-0554</orcidid></addata></record> |
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| subjects | Brain cancer Classification Collagen Collagen (type I) Fibers Humans Interventional Radiology Magnetic Resonance Imaging - methods Medicine Medicine & Public Health Meningeal Neoplasms - pathology Meningeal Neoplasms - surgery Meningioma Meningioma - diagnostic imaging Meningioma - pathology Meningioma - surgery Minimally Invasive Surgery Morphology Neurology Neuroradiology Neurosurgery Original Article Phenotypes Reticulin Statistical analysis Surgical Orthopedics Tumor – Meningioma Tumors |
| title | Utility of texture analysis for objective quantitative ex vivo assessment of meningioma consistency: method proposal and validation |
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