Skip to main content
Top
Published in:

13-02-2024 | Meningioma

MRI- and DWI-Based Radiomics Features for Preoperatively Predicting Meningioma Sinus Invasion

Authors: Yuan Gui, Fen Chen, Jialiang Ren, Limei Wang, Kuntao Chen, Jing Zhang

Published in: Journal of Imaging Informatics in Medicine | Issue 3/2024

Login to get access

Abstract

The aim of this study was to use multimodal imaging (contrast-enhanced T1-weighted (T1C), T2-weighted (T2), and diffusion-weighted imaging (DWI)) to develop a radiomics model for preoperatively predicting venous sinus invasion in meningiomas. This prediction would assist in selecting the appropriate surgical approach and forecasting the prognosis of meningiomas. A retrospective analysis was conducted on 331 participants who had been pathologically diagnosed with meningiomas. For each participant, 3948 radiomics features were acquired from the T1C, T2, and DWI images. Minimum redundancy maximum correlation, rank sum test, and multi-factor recursive elimination were used to extract the most significant features of different models. Then, multivariate logistic regression was used to build classification models to predict meningioma venous sinus invasion. The diagnostic capabilities were assessed using receiver operating characteristic (ROC) analysis. In addition, a nomogram was constructed by incorporating clinical and radiological characteristics and a radiomics signature. To assess the clinical usefulness of the nomogram, a decision curve analysis (DCA) was performed. Tumor shape, boundary, and enhancement features were independent predictors of meningioma venous sinus invasion (p = 0.013, p = 0.013, p = 0.005, respectively). Eleven (T2:1, T1C:4, DWI:6) of the 3948 radiomics features were screened for strong association with meningioma sinus invasion. The areas under the ROC curves for the training and external test sets were 0.946 and 0.874, respectively. The clinicoradiomic model showed excellent predictive performance for invasive meningioma, which may help to guide surgical approaches and predict prognosis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ostrom QT, Price M, Neff C, et al. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2015-2019. Neuro Oncol. 2022; 24(Suppl 5):v1-v95.PubMedPubMedCentralCrossRef Ostrom QT, Price M, Neff C, et al. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2015-2019. Neuro Oncol. 2022; 24(Suppl 5):v1-v95.PubMedPubMedCentralCrossRef
2.
go back to reference Rogers L, Barani L, Chamberlain M, et al. Meningiomas: knowledge base, treatment outcomes, and uncertainties. A RANO review. J Neurosurg. 2015;122(1):4-23.PubMedCrossRef Rogers L, Barani L, Chamberlain M, et al. Meningiomas: knowledge base, treatment outcomes, and uncertainties. A RANO review. J Neurosurg. 2015;122(1):4-23.PubMedCrossRef
3.
go back to reference Ong T, Bharatha A, Alsufayan R, et al. MRI predictors for brain invasion in meningiomas. Neuroradiol J. 2021;34(1):3-7.PubMedCrossRef Ong T, Bharatha A, Alsufayan R, et al. MRI predictors for brain invasion in meningiomas. Neuroradiol J. 2021;34(1):3-7.PubMedCrossRef
4.
go back to reference Wang XC, Wu RF, Zhang P, et al. Superior Sagittal Sinus Obstruction by Giant Meningiomas: Is Total Removal Feasible? World Neurosurg. 2016;94:111-119.PubMedCrossRef Wang XC, Wu RF, Zhang P, et al. Superior Sagittal Sinus Obstruction by Giant Meningiomas: Is Total Removal Feasible? World Neurosurg. 2016;94:111-119.PubMedCrossRef
5.
go back to reference Yin TK, Gu JJ, Huang YX, et al. Assessment and Treatment of Peritumoral Cortical Veins in Parasagittal Meningiomas with Application of 3-Dimensional Imaging Fusion Model. World Neurosurg. 2017;104:220-228.PubMedCrossRef Yin TK, Gu JJ, Huang YX, et al. Assessment and Treatment of Peritumoral Cortical Veins in Parasagittal Meningiomas with Application of 3-Dimensional Imaging Fusion Model. World Neurosurg. 2017;104:220-228.PubMedCrossRef
6.
go back to reference Han MS, Kim YJ, Moon KS, et al. Lessons from surgical outcome for intracranial meningioma involving major venous sinus. Medicine (Baltimore). 2016;95(35):e4705.PubMedPubMedCentralCrossRef Han MS, Kim YJ, Moon KS, et al. Lessons from surgical outcome for intracranial meningioma involving major venous sinus. Medicine (Baltimore). 2016;95(35):e4705.PubMedPubMedCentralCrossRef
7.
go back to reference Raza SM, Gallia GL, Brem H, et al. Perioperative and long-term outcomes from the management of parasagittal meningiomas invading the superior sagittal sinus. Neurosurgery. 2010;67(4):885-893.PubMedCrossRef Raza SM, Gallia GL, Brem H, et al. Perioperative and long-term outcomes from the management of parasagittal meningiomas invading the superior sagittal sinus. Neurosurgery. 2010;67(4):885-893.PubMedCrossRef
8.
go back to reference Tomasello F, Conti A, Cardali S, et al. Venous preservation-guided resection: a changing paradigm in parasagittal meningioma surgery. J Neurosurg. 2013;119(1):74-81.PubMedCrossRef Tomasello F, Conti A, Cardali S, et al. Venous preservation-guided resection: a changing paradigm in parasagittal meningioma surgery. J Neurosurg. 2013;119(1):74-81.PubMedCrossRef
9.
go back to reference Mathiesen T, Segerlind JP, Kihlstrom L, et al. Meningiomas engaging major venous sinuses. World Neurosurg. 2014;81(1):116-124.PubMedCrossRef Mathiesen T, Segerlind JP, Kihlstrom L, et al. Meningiomas engaging major venous sinuses. World Neurosurg. 2014;81(1):116-124.PubMedCrossRef
10.
go back to reference Ricci A, Vitantonio HD, Paulis DD, et al. Parasagittal meningiomas: Our surgical experience and the reconstruction technique of the superior sagittal sinus. Surg Neurol Int. 2017;8:1.PubMedPubMedCentralCrossRef Ricci A, Vitantonio HD, Paulis DD, et al. Parasagittal meningiomas: Our surgical experience and the reconstruction technique of the superior sagittal sinus. Surg Neurol Int. 2017;8:1.PubMedPubMedCentralCrossRef
11.
go back to reference Zeeshan Q, Patel A, Cheng CY, et al. Resection of Meningiomas Involving Major Dural Venous Sinuses: Classification, Technique, and Long-Term Results. World Neurosurg. 2019;125:e521-e536.PubMedCrossRef Zeeshan Q, Patel A, Cheng CY, et al. Resection of Meningiomas Involving Major Dural Venous Sinuses: Classification, Technique, and Long-Term Results. World Neurosurg. 2019;125:e521-e536.PubMedCrossRef
12.
go back to reference Goldbrunner R, Minniti G, Preusser M, et al. EANO guidelines for the diagnosis and treatment of meningiomas. Lancet Oncol. 2016;17(9):e383-e391.PubMedCrossRef Goldbrunner R, Minniti G, Preusser M, et al. EANO guidelines for the diagnosis and treatment of meningiomas. Lancet Oncol. 2016;17(9):e383-e391.PubMedCrossRef
13.
go back to reference Wang DD, Lu YP, Yin B, et al. 3D Fast Spin-Echo T1 Black-Blood Imaging for the Preoperative Detection of Venous Sinus Invasion by Meningioma : Comparison with Contrast-Enhanced MRV. Clin Neuroradiol. 2019;29(1):65-73.PubMedCrossRef Wang DD, Lu YP, Yin B, et al. 3D Fast Spin-Echo T1 Black-Blood Imaging for the Preoperative Detection of Venous Sinus Invasion by Meningioma : Comparison with Contrast-Enhanced MRV. Clin Neuroradiol. 2019;29(1):65-73.PubMedCrossRef
14.
go back to reference Lee JM, Jung S, Moon KS, et al. Preoperative evaluation of venous systems with 3-dimensional contrast-enhanced magnetic resonance venography in brain tumors: comparison with time-of-flight magnetic resonance venography and digital subtraction angiography. Surg Neurol. 2005; 64(2):128-133.PubMedCrossRef Lee JM, Jung S, Moon KS, et al. Preoperative evaluation of venous systems with 3-dimensional contrast-enhanced magnetic resonance venography in brain tumors: comparison with time-of-flight magnetic resonance venography and digital subtraction angiography. Surg Neurol. 2005; 64(2):128-133.PubMedCrossRef
15.
go back to reference Wetzel SG, Kirsch E, Stock KW, et al. Cerebral veins: comparative study of CT venography with intraarterial digital subtraction angiography. AJNR Am J Neuroradiol. 1999;20(2):249-255.PubMedPubMedCentral Wetzel SG, Kirsch E, Stock KW, et al. Cerebral veins: comparative study of CT venography with intraarterial digital subtraction angiography. AJNR Am J Neuroradiol. 1999;20(2):249-255.PubMedPubMedCentral
18.
go back to reference Park HJ, Lee SS, Park B, et al. Radiomics Analysis of Gadoxetic Acid-enhanced MRI for Staging Liver Fibrosis. Radiology. 2019;290(2):380-387.PubMedCrossRef Park HJ, Lee SS, Park B, et al. Radiomics Analysis of Gadoxetic Acid-enhanced MRI for Staging Liver Fibrosis. Radiology. 2019;290(2):380-387.PubMedCrossRef
20.
go back to reference Huang YQ, Liang CH, He L, et al. Development and Validation of a Radiomics Nomogram for Preoperative Prediction of Lymph Node Metastasis in Colorectal Cancer. J Clin Oncol. 2016; 34(18):2157-2164.PubMedCrossRef Huang YQ, Liang CH, He L, et al. Development and Validation of a Radiomics Nomogram for Preoperative Prediction of Lymph Node Metastasis in Colorectal Cancer. J Clin Oncol. 2016; 34(18):2157-2164.PubMedCrossRef
21.
22.
go back to reference Zhang J, Yao K, Liu PP, et al. A radiomics model for preoperative prediction of brain invasion in meningioma non-invasively based on MRI. A multicentre study. EBioMedicine. 2020; 58:102933.PubMedCrossRef Zhang J, Yao K, Liu PP, et al. A radiomics model for preoperative prediction of brain invasion in meningioma non-invasively based on MRI. A multicentre study. EBioMedicine. 2020; 58:102933.PubMedCrossRef
23.
go back to reference Zhang J, Sun JQ, Han T, et al. Radiomic features of magnetic resonance images as novel preoperative predictive factors of bone invasion in meningiomas. Eur J Radiol. 2020; 132:109287.PubMedCrossRef Zhang J, Sun JQ, Han T, et al. Radiomic features of magnetic resonance images as novel preoperative predictive factors of bone invasion in meningiomas. Eur J Radiol. 2020; 132:109287.PubMedCrossRef
24.
go back to reference Jiang L, Miao ZF, Chen HY, et al. Radiomics Analysis of Diffusion-Weighted Imaging and Long-Term Unfavorable Outcomes Risk for Acute Stroke. Stroke. 2023;54(2):488-498.PubMedCrossRef Jiang L, Miao ZF, Chen HY, et al. Radiomics Analysis of Diffusion-Weighted Imaging and Long-Term Unfavorable Outcomes Risk for Acute Stroke. Stroke. 2023;54(2):488-498.PubMedCrossRef
25.
go back to reference Hectors SJ, Lewis S, Besa C, et al. MRI radiomics features predict immuno-oncological characteristics of hepatocellular carcinoma. Eur Radiol. 2020;30(7):3759-3769.PubMedPubMedCentralCrossRef Hectors SJ, Lewis S, Besa C, et al. MRI radiomics features predict immuno-oncological characteristics of hepatocellular carcinoma. Eur Radiol. 2020;30(7):3759-3769.PubMedPubMedCentralCrossRef
26.
go back to reference Lin MY, Lin N, Yu SH, et al. Automated Prediction of Early Recurrence in Advanced Sinonasal Squamous Cell Carcinoma With Deep Learning and Multi-parametric MRI-based Radiomics Nomogram. Acad Radiol. 2023;30(10):2201-2211.PubMedCrossRef Lin MY, Lin N, Yu SH, et al. Automated Prediction of Early Recurrence in Advanced Sinonasal Squamous Cell Carcinoma With Deep Learning and Multi-parametric MRI-based Radiomics Nomogram. Acad Radiol. 2023;30(10):2201-2211.PubMedCrossRef
27.
go back to reference Maiuri F, Donzelli R, Pagano S, et al. The Management of the Venous Sinuses During Surgery for Posterior Fossa Meningiomas. World Neurosurg. 2019;125:357-363.PubMedCrossRef Maiuri F, Donzelli R, Pagano S, et al. The Management of the Venous Sinuses During Surgery for Posterior Fossa Meningiomas. World Neurosurg. 2019;125:357-363.PubMedCrossRef
28.
go back to reference van Griethuysen JJM, Fedorov A, Parmar C, et al. Computational Radiomics System to Decode the Radiographic Phenotype. Cancer Res. 2017;77(21):e104-e107.PubMedPubMedCentralCrossRef van Griethuysen JJM, Fedorov A, Parmar C, et al. Computational Radiomics System to Decode the Radiographic Phenotype. Cancer Res. 2017;77(21):e104-e107.PubMedPubMedCentralCrossRef
29.
go back to reference Zwanenburg A, Vallieres M, Abdalah MA, et al. The Image Biomarker Standardization Initiative: Standardized Quantitative Radiomics for High-Throughput Image-based Phenotyping. Radiology. 2020;295(2):328-338.PubMedCrossRef Zwanenburg A, Vallieres M, Abdalah MA, et al. The Image Biomarker Standardization Initiative: Standardized Quantitative Radiomics for High-Throughput Image-based Phenotyping. Radiology. 2020;295(2):328-338.PubMedCrossRef
30.
go back to reference Calster BV, Wynants L, Verbeek JFM, et al. Reporting and Interpreting Decision Curve Analysis: A Guide for Investigators. Eur Urol. 2018;74(6):796-804.PubMedPubMedCentralCrossRef Calster BV, Wynants L, Verbeek JFM, et al. Reporting and Interpreting Decision Curve Analysis: A Guide for Investigators. Eur Urol. 2018;74(6):796-804.PubMedPubMedCentralCrossRef
31.
go back to reference Solheim O, Torsteinsen M, Johannesen TB, et al. Effects of cerebral magnetic resonance imaging in outpatients on observed incidence of intracranial tumors and patient survival: a national observational study. J Neurosurg. 2014;120(4):827-832.PubMedCrossRef Solheim O, Torsteinsen M, Johannesen TB, et al. Effects of cerebral magnetic resonance imaging in outpatients on observed incidence of intracranial tumors and patient survival: a national observational study. J Neurosurg. 2014;120(4):827-832.PubMedCrossRef
34.
35.
go back to reference Sapkota MR, Yang ZH, Zhu D, et al. Evaluation of Epidemiologic Factors, Radiographic Features, and Pathologic Findings for Predicting Peritumoral Brain Edema in Meningiomas. J Magn Reson Imaging. 2020;52(1):174-182.PubMedCrossRef Sapkota MR, Yang ZH, Zhu D, et al. Evaluation of Epidemiologic Factors, Radiographic Features, and Pathologic Findings for Predicting Peritumoral Brain Edema in Meningiomas. J Magn Reson Imaging. 2020;52(1):174-182.PubMedCrossRef
36.
go back to reference Jiang YM, Yuan QY, Lv WB, et al. Radiomic signature of (18)F fluorodeoxyglucose PET/CT for prediction of gastric cancer survival and chemotherapeutic benefits. Theranostics. 2018;8(21):5915-5928.PubMedPubMedCentralCrossRef Jiang YM, Yuan QY, Lv WB, et al. Radiomic signature of (18)F fluorodeoxyglucose PET/CT for prediction of gastric cancer survival and chemotherapeutic benefits. Theranostics. 2018;8(21):5915-5928.PubMedPubMedCentralCrossRef
37.
go back to reference Liu HH, Zhang CY, Wang LJ, et al. MRI radiomics analysis for predicting preoperative synchronous distant metastasis in patients with rectal cancer. Eur Radiol. 2019;29(8):4418-4426.PubMedCrossRef Liu HH, Zhang CY, Wang LJ, et al. MRI radiomics analysis for predicting preoperative synchronous distant metastasis in patients with rectal cancer. Eur Radiol. 2019;29(8):4418-4426.PubMedCrossRef
38.
go back to reference Meng XC, Xia W, Xie PY, et al. Preoperative radiomic signature based on multiparametric magnetic resonance imaging for noninvasive evaluation of biological characteristics in rectal cancer. Eur Radiol. 2019;29(6):3200-3209.PubMedCrossRef Meng XC, Xia W, Xie PY, et al. Preoperative radiomic signature based on multiparametric magnetic resonance imaging for noninvasive evaluation of biological characteristics in rectal cancer. Eur Radiol. 2019;29(6):3200-3209.PubMedCrossRef
39.
go back to reference Park YW, Oh JM, You SC, et al. Radiomics and machine learning may accurately predict the grade and histological subtype in meningiomas using conventional and diffusion tensor imaging. Eur Radiol. 2019;29(8):4068-4076.PubMedCrossRef Park YW, Oh JM, You SC, et al. Radiomics and machine learning may accurately predict the grade and histological subtype in meningiomas using conventional and diffusion tensor imaging. Eur Radiol. 2019;29(8):4068-4076.PubMedCrossRef
40.
go back to reference Yan PF, Yan L, Hu TT, et al. The Potential Value of Preoperative MRI Texture and Shape Analysis in Grading Meningiomas: A Preliminary Investigation. Transl Oncol. 2017;10(4):570-577.PubMedPubMedCentralCrossRef Yan PF, Yan L, Hu TT, et al. The Potential Value of Preoperative MRI Texture and Shape Analysis in Grading Meningiomas: A Preliminary Investigation. Transl Oncol. 2017;10(4):570-577.PubMedPubMedCentralCrossRef
41.
go back to reference Zhou M, Scott J, Chaudhury B, et al. Radiomics in Brain Tumor: Image Assessment, Quantitative Feature Descriptors, and Machine-Learning Approaches. AJNR Am J Neuroradiol. 2018;39(2):208-216.PubMedPubMedCentralCrossRef Zhou M, Scott J, Chaudhury B, et al. Radiomics in Brain Tumor: Image Assessment, Quantitative Feature Descriptors, and Machine-Learning Approaches. AJNR Am J Neuroradiol. 2018;39(2):208-216.PubMedPubMedCentralCrossRef
42.
go back to reference Wang QY, Li QN, Mi R, et al. Radiomics Nomogram Building From Multiparametric MRI to Predict Grade in Patients With Glioma: A Cohort Study. J Magn Reson Imaging. 2019;49(3):825-833.PubMedCrossRef Wang QY, Li QN, Mi R, et al. Radiomics Nomogram Building From Multiparametric MRI to Predict Grade in Patients With Glioma: A Cohort Study. J Magn Reson Imaging. 2019;49(3):825-833.PubMedCrossRef
43.
go back to reference Tang L, Zhou XHJ. Diffusion MRI of cancer: From low to high b-values. J Magn Reson Imaging. 2019;49(1):23-40.PubMedCrossRef Tang L, Zhou XHJ. Diffusion MRI of cancer: From low to high b-values. J Magn Reson Imaging. 2019;49(1):23-40.PubMedCrossRef
44.
go back to reference Kiselev VG. Microstructure with diffusion MRI: what scale we are sensitive to? J Neurosci Methods. 2021;347:108910.PubMedCrossRef Kiselev VG. Microstructure with diffusion MRI: what scale we are sensitive to? J Neurosci Methods. 2021;347:108910.PubMedCrossRef
45.
go back to reference Shu ZY, Mao DW, Song QW, et al. Multiparameter MRI-based radiomics for preoperative prediction of extramural venous invasion in rectal cancer. Eur Radiol. 2022;32(2):1002-1013.PubMedCrossRef Shu ZY, Mao DW, Song QW, et al. Multiparameter MRI-based radiomics for preoperative prediction of extramural venous invasion in rectal cancer. Eur Radiol. 2022;32(2):1002-1013.PubMedCrossRef
46.
go back to reference Peng H, Huo JH, Li B, et al. Predicting Isocitrate Dehydrogenase (IDH) Mutation Status in Gliomas Using Multiparameter MRI Radiomics Features. J Magn Reson Imaging. 2021;53(5):1399-1407.PubMedCrossRef Peng H, Huo JH, Li B, et al. Predicting Isocitrate Dehydrogenase (IDH) Mutation Status in Gliomas Using Multiparameter MRI Radiomics Features. J Magn Reson Imaging. 2021;53(5):1399-1407.PubMedCrossRef
47.
go back to reference Li HX, Liu ZL, Li FY, et al. Preoperatively Predicting Ki67 Expression in Pituitary Adenomas Using Deep Segmentation Network and Radiomics Analysis Based on Multiparameter MRI. Acad Radiol. 2023. Li HX, Liu ZL, Li FY, et al. Preoperatively Predicting Ki67 Expression in Pituitary Adenomas Using Deep Segmentation Network and Radiomics Analysis Based on Multiparameter MRI. Acad Radiol. 2023.
48.
go back to reference Laukamp KR, Shakirin G, Baeβler B, et al. Accuracy of Radiomics-Based Feature Analysis on Multiparametric Magnetic Resonance Images for Noninvasive Meningioma Grading. World Neurosurg. 2019;132:e366-e390.PubMedCrossRef Laukamp KR, Shakirin G, Baeβler B, et al. Accuracy of Radiomics-Based Feature Analysis on Multiparametric Magnetic Resonance Images for Noninvasive Meningioma Grading. World Neurosurg. 2019;132:e366-e390.PubMedCrossRef
49.
go back to reference Wang J, Hu Y, Zhou XJ, et al. A radiomics model based on DCE-MRI and DWI may improve the prediction of estimating IDH1 mutation and angiogenesis in gliomas. Eur J Radiol. 2022;147:110141.PubMedCrossRef Wang J, Hu Y, Zhou XJ, et al. A radiomics model based on DCE-MRI and DWI may improve the prediction of estimating IDH1 mutation and angiogenesis in gliomas. Eur J Radiol. 2022;147:110141.PubMedCrossRef
Metadata
Title
MRI- and DWI-Based Radiomics Features for Preoperatively Predicting Meningioma Sinus Invasion
Authors
Yuan Gui
Fen Chen
Jialiang Ren
Limei Wang
Kuntao Chen
Jing Zhang
Publication date
13-02-2024
Publisher
Springer International Publishing
Published in
Journal of Imaging Informatics in Medicine / Issue 3/2024
Print ISSN: 2948-2925
Electronic ISSN: 2948-2933
DOI
https://doi.org/10.1007/s10278-024-01024-x