Imaging meningioma biology: Machine Learning predicts integrated risk score in WHO grade 2/3 meningioma (2024)

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,

Olivia Kertels, MD

Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar

, Technical University of Munich, Munich,

Germany

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,

Claire Delbridge, MD

Department of Neuropathology, School of Medicine, Institute of Pathology

, Technical University of Munich, Munich,

Germany

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,

Felix Sahm, MD

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg

, 69120 Heidelberg, Germany; Clinical Cooperation Unit Neuropathology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), 69120 Heidelberg,

Germany

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Felix Ehret, MD

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Radiation Oncology

, 13353, Berlin,

Germany

German Cancer Consortium (DKTK), Partner Site Berlin, German Cancer Research Center (DKFZ)

, Heidelberg,

Germany

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Güliz Acker, MD

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Radiation Oncology

, 13353, Berlin,

Germany

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David Capper, MD

German Cancer Consortium (DKTK), Partner Site Berlin, German Cancer Research Center (DKFZ)

, Heidelberg,

Germany

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin

, Department of Neuropathology, 10117, Berlin,

Germany

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Jan C Peeken, MD

Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München

, Institut für Innovative Radiotherapy (iRT),

Germany

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Christian Diehl, MD

Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München

, Institut für Innovative Radiotherapy (iRT),

Germany

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Michael Griessmair, MD

Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar

, Technical University of Munich, Munich,

Germany

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Marie-Christin Metz, MD

Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar

, Technical University of Munich, Munich,

Germany

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Chiara Negwer, MD

Department of Neurosurgery, Technical University of Munich, Germany

, School of Medicine, Klinikum rechts der Isar, Ismaninger Strasse 22, Munich 81675,

Germany

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Sandro M Krieg, MD

Department of Neurosurgery, University Hospital Heidelberg, Im Neuenheimer Feld 400

, 69120, Heidelberg,

Germany

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Julia Onken, MD

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin

, Department of Neurosurgery, 10117 Berlin,

Germany

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Igor Yakushev, MD

Department of Nuclear Medicine, Klinikum Rechts der Isar, TU Munich

, 81675 München,

Germany

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Peter Vajkoczy, MD

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin

, Department of Neurosurgery, 10117 Berlin,

Germany

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Bernhard Meyer, MD

Department of Neurosurgery, Technical University of Munich, Germany

, School of Medicine, Klinikum rechts der Isar, Ismaninger Strasse 22, Munich 81675,

Germany

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Daniel Zips, MD

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Radiation Oncology

, 13353, Berlin,

Germany

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Stephanie E Combs, MD

Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München

, Institut für Innovative Radiotherapy (iRT),

Germany

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Claus Zimmer, MD

Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar

, Technical University of Munich, Munich,

Germany

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David Kaul, MD

Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Radiation Oncology

, 13353, Berlin,

Germany

HMU Health and Medical University, Potsdam, Olympischer Weg 1

, 14471 Potsdam,

Germany

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Denise Bernhardt, MD

Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München

, Institut für Innovative Radiotherapy (iRT),

Germany

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Benedikt Wiestler, MD

Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar

, Technical University of Munich, Munich,

Germany

TranslaTUM, Center for Translational Cancer Research, Technical University of Munich

, Ismaninger Str. 22, Munich, 81675,

Germany

Corresponding author: Benedikt Wiestler, Department of Diagnostic and Interventional Neuroradiology, Klinikum rechts der Isar, Technical University of Munich, Ismaningerstr. 22, 81675 Munich, Germany, Email: b.wiestler@tum.de

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OK and CD contributed equally as first authors

DK, DB and BW contributed equally as senior authors

Author Notes

Neuro-Oncology Advances, vdae080, https://doi.org/10.1093/noajnl/vdae080

Published:

30 May 2024

Article history

Received:

11 January 2024

Published:

30 May 2024

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    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, Imaging meningioma biology: Machine Learning predicts integrated risk score in WHO grade 2/3 meningioma, Neuro-Oncology Advances, 2024;, vdae080, https://doi.org/10.1093/noajnl/vdae080

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Abstract

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, multi-center study. We hypothesized imaging data to be reflective of the IRS. Thus, we assessed the potential of a machine learning classifier for its non-invasive prediction using preoperative magnetic resonance imaging (MRI).

Methods

In total, 160 WHO grade 2 and 3 meningioma patients from two university centers were included in this study. All patients underwent surgery with histopathological work-up including methylation analysis. Preoperative MRI scans were automatically segmented, and radiomics parameters were extracted. Using a random forest classifier, three machine learning classifiers (one multi-class classifier for IRS and two 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

Multi-class IRS classification had a test set 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 vs. 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.

meningioma, neuro-oncology, radiomics, integrated risk score

Imaging meningioma biology: Machine Learning predicts integrated risk score in WHO grade 2/3 meningioma (7) Accepted manuscripts

Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout.

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Author notes

OK and CD contributed equally as first authors

DK, DB and BW contributed equally as senior authors

© The Author(s) 2024. Published by Oxford University Press, the Society for Neuro-Oncology and the European Association of Neuro-Oncology.

This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.

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