Olivia Kertels, Claire Delbridge, Felix Sahm, Felix Ehret, Güliz Acker, David Capper, Jan C Peeken, Christian Diehl, Michael Griessmair, Marie-Christin Metz, Chiara Negwer, Sandro M Krieg, Julia Onken, Igor Yakushev, Peter Vajkoczy, Bernhard Meyer, Daniel Zips, Stephanie E Combs, Claus Zimmer, David Kaul, Denise Bernhardt, Benedikt Wiestler
{"title":"脑膜瘤生物学成像:机器学习预测世卫组织 2/3 级脑膜瘤的综合风险评分。","authors":"Olivia Kertels, Claire Delbridge, Felix Sahm, Felix Ehret, Güliz Acker, David Capper, Jan C Peeken, Christian Diehl, Michael Griessmair, Marie-Christin Metz, Chiara Negwer, Sandro M Krieg, Julia Onken, Igor Yakushev, Peter Vajkoczy, Bernhard Meyer, Daniel Zips, Stephanie E Combs, Claus Zimmer, David Kaul, Denise Bernhardt, Benedikt Wiestler","doi":"10.1093/noajnl/vdae080","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Meningiomas are the most common primary brain tumors. While most are benign (WHO grade 1) and have a favorable prognosis, up to one-fourth are classified as higher-grade, falling into WHO grade 2 or 3 categories. Recently, an integrated risk score (IRS) pertaining to tumor biology was developed and its prognostic relevance was validated in a large, multicenter study. We hypothesized imaging data to be reflective of the IRS. Thus, we assessed the potential of a machine learning classifier for its noninvasive prediction using preoperative magnetic resonance imaging (MRI).</p><p><strong>Methods: </strong>In total, 160 WHO grade 2 and 3 meningioma patients from 2 university centers were included in this study. All patients underwent surgery with histopathological workup including methylation analysis. Preoperative MRI scans were automatically segmented, and radiomic parameters were extracted. Using a random forest classifier, 3 machine learning classifiers (1 multiclass classifier for IRS and 2 binary classifiers for low-risk and high-risk prediction, respectively) were developed in a training set (120 patients) and independently tested in a hold-out test set (40 patients).</p><p><strong>Results: </strong>Multiclass IRS classification had a test set area under the curve (AUC) of 0.7, mostly driven by the difficulties in clearly separating medium-risk from high-risk patients. Consequently, a classifier predicting low-risk IRS versus medium-/high-risk showed a very high test accuracy of 90% (AUC 0.88). In particular, \"sphericity\" was associated with low-risk IRS classification.</p><p><strong>Conclusion: </strong>The IRS, in particular molecular low-risk, can be predicted from imaging data with high accuracy, making this important prognostic classification accessible by imaging.</p>","PeriodicalId":94157,"journal":{"name":"Neuro-oncology advances","volume":null,"pages":null},"PeriodicalIF":3.7000,"publicationDate":"2024-05-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11217900/pdf/","citationCount":"0","resultStr":"{\"title\":\"Imaging meningioma biology: Machine learning predicts integrated risk score in WHO grade 2/3 meningioma.\",\"authors\":\"Olivia Kertels, Claire Delbridge, Felix Sahm, Felix Ehret, Güliz Acker, David Capper, Jan C Peeken, Christian Diehl, Michael Griessmair, Marie-Christin Metz, Chiara Negwer, Sandro M Krieg, Julia Onken, Igor Yakushev, Peter Vajkoczy, Bernhard Meyer, Daniel Zips, Stephanie E Combs, Claus Zimmer, David Kaul, Denise Bernhardt, Benedikt Wiestler\",\"doi\":\"10.1093/noajnl/vdae080\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>Meningiomas are the most common primary brain tumors. While most are benign (WHO grade 1) and have a favorable prognosis, up to one-fourth are classified as higher-grade, falling into WHO grade 2 or 3 categories. Recently, an integrated risk score (IRS) pertaining to tumor biology was developed and its prognostic relevance was validated in a large, multicenter study. We hypothesized imaging data to be reflective of the IRS. Thus, we assessed the potential of a machine learning classifier for its noninvasive prediction using preoperative magnetic resonance imaging (MRI).</p><p><strong>Methods: </strong>In total, 160 WHO grade 2 and 3 meningioma patients from 2 university centers were included in this study. All patients underwent surgery with histopathological workup including methylation analysis. Preoperative MRI scans were automatically segmented, and radiomic parameters were extracted. Using a random forest classifier, 3 machine learning classifiers (1 multiclass classifier for IRS and 2 binary classifiers for low-risk and high-risk prediction, respectively) were developed in a training set (120 patients) and independently tested in a hold-out test set (40 patients).</p><p><strong>Results: </strong>Multiclass IRS classification had a test set area under the curve (AUC) of 0.7, mostly driven by the difficulties in clearly separating medium-risk from high-risk patients. Consequently, a classifier predicting low-risk IRS versus medium-/high-risk showed a very high test accuracy of 90% (AUC 0.88). In particular, \\\"sphericity\\\" was associated with low-risk IRS classification.</p><p><strong>Conclusion: </strong>The IRS, in particular molecular low-risk, can be predicted from imaging data with high accuracy, making this important prognostic classification accessible by imaging.</p>\",\"PeriodicalId\":94157,\"journal\":{\"name\":\"Neuro-oncology advances\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2024-05-30\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11217900/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Neuro-oncology advances\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1093/noajnl/vdae080\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/1/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"CLINICAL NEUROLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuro-oncology advances","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/noajnl/vdae080","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
Imaging meningioma biology: Machine learning predicts integrated risk score in WHO grade 2/3 meningioma.
Background: Meningiomas are the most common primary brain tumors. While most are benign (WHO grade 1) and have a favorable prognosis, up to one-fourth are classified as higher-grade, falling into WHO grade 2 or 3 categories. Recently, an integrated risk score (IRS) pertaining to tumor biology was developed and its prognostic relevance was validated in a large, multicenter study. We hypothesized imaging data to be reflective of the IRS. Thus, we assessed the potential of a machine learning classifier for its noninvasive prediction using preoperative magnetic resonance imaging (MRI).
Methods: In total, 160 WHO grade 2 and 3 meningioma patients from 2 university centers were included in this study. All patients underwent surgery with histopathological workup including methylation analysis. Preoperative MRI scans were automatically segmented, and radiomic parameters were extracted. Using a random forest classifier, 3 machine learning classifiers (1 multiclass classifier for IRS and 2 binary classifiers for low-risk and high-risk prediction, respectively) were developed in a training set (120 patients) and independently tested in a hold-out test set (40 patients).
Results: Multiclass IRS classification had a test set area under the curve (AUC) of 0.7, mostly driven by the difficulties in clearly separating medium-risk from high-risk patients. Consequently, a classifier predicting low-risk IRS versus medium-/high-risk showed a very high test accuracy of 90% (AUC 0.88). In particular, "sphericity" was associated with low-risk IRS classification.
Conclusion: The IRS, in particular molecular low-risk, can be predicted from imaging data with high accuracy, making this important prognostic classification accessible by imaging.