Skip to main content
Top
Published in: BMC Medical Informatics and Decision Making 1/2020

01-12-2020 | Glioma | Research article

Machine learning assisted DSC-MRI radiomics as a tool for glioma classification by grade and mutation status

Authors: Carole H. Sudre, Jasmina Panovska-Griffiths, Eser Sanverdi, Sebastian Brandner, Vasileios K. Katsaros, George Stranjalis, Francesca B. Pizzini, Claudio Ghimenton, Katarina Surlan-Popovic, Jernej Avsenik, Maria Vittoria Spampinato, Mario Nigro, Arindam R. Chatterjee, Arnaud Attye, Sylvie Grand, Alexandre Krainik, Nicoletta Anzalone, Gian Marco Conte, Valeria Romeo, Lorenzo Ugga, Andrea Elefante, Elisa Francesca Ciceri, Elia Guadagno, Eftychia Kapsalaki, Diana Roettger, Javier Gonzalez, Timothé Boutelier, M. Jorge Cardoso, Sotirios Bisdas

Published in: BMC Medical Informatics and Decision Making | Issue 1/2020

Login to get access

Abstract

Background

Combining MRI techniques with machine learning methodology is rapidly gaining attention as a promising method for staging of brain gliomas. This study assesses the diagnostic value of such a framework applied to dynamic susceptibility contrast (DSC)-MRI in classifying treatment-naïve gliomas from a multi-center patients into WHO grades II-IV and across their isocitrate dehydrogenase (IDH) mutation status.

Methods

Three hundred thirty-three patients from 6 tertiary centres, diagnosed histologically and molecularly with primary gliomas (IDH-mutant = 151 or IDH-wildtype = 182) were retrospectively identified. Raw DSC-MRI data was post-processed for normalised leakage-corrected relative cerebral blood volume (rCBV) maps. Shape, intensity distribution (histogram) and rotational invariant Haralick texture features over the tumour mask were extracted. Differences in extracted features across glioma grades and mutation status were tested using the Wilcoxon two-sample test. A random-forest algorithm was employed (2-fold cross-validation, 250 repeats) to predict grades or mutation status using the extracted features.

Results

Shape, distribution and texture features showed significant differences across mutation status. WHO grade II-III differentiation was mostly driven by shape features while texture and intensity feature were more relevant for the III-IV separation. Increased number of features became significant when differentiating grades further apart from one another. Gliomas were correctly stratified by mutation status in 71% and by grade in 53% of the cases (87% of the gliomas grades predicted with distance less than 1).

Conclusions

Despite large heterogeneity in the multi-center dataset, machine learning assisted DSC-MRI radiomics hold potential to address the inherent variability and presents a promising approach for non-invasive glioma molecular subtyping and grading.
Appendix
Available only for authorised users
Literature
2.
go back to reference Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK. And others. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–20.PubMedCrossRef Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK. And others. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–20.PubMedCrossRef
3.
go back to reference Shirahata M, Ono T, Stichel D, et al. Novel, improved grading system(s) for IDH-mutant astrocytic gliomas. Acta Neuropathol. 2018;136(1):153–66.PubMedCrossRef Shirahata M, Ono T, Stichel D, et al. Novel, improved grading system(s) for IDH-mutant astrocytic gliomas. Acta Neuropathol. 2018;136(1):153–66.PubMedCrossRef
4.
go back to reference Chamberlain MC, Murovic JA, Levin VA. Absence of contrast enhancement on CT brain scans of patients with supratentorial malignant gliomas. Neurology. 1988;38(9):1371.PubMedCrossRef Chamberlain MC, Murovic JA, Levin VA. Absence of contrast enhancement on CT brain scans of patients with supratentorial malignant gliomas. Neurology. 1988;38(9):1371.PubMedCrossRef
5.
go back to reference Scott JN, Pma B, Sevick RJ, Rewcastle NB, PA. F. How Often Are Nonenhancing Supratentorial Gliomas Malignant? A Population Study. Neurology. 2002;59(6):947–9.PubMedCrossRef Scott JN, Pma B, Sevick RJ, Rewcastle NB, PA. F. How Often Are Nonenhancing Supratentorial Gliomas Malignant? A Population Study. Neurology. 2002;59(6):947–9.PubMedCrossRef
6.
go back to reference Santarosa C, Castellano A, Conte GM, et al. Dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging for Glioma grading: preliminary comparison of vessel compartment and permeability parameters using hotspot and histogram analysis. Eur J Radiol. 2016;85(6):1147–56.PubMedCrossRef Santarosa C, Castellano A, Conte GM, et al. Dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging for Glioma grading: preliminary comparison of vessel compartment and permeability parameters using hotspot and histogram analysis. Eur J Radiol. 2016;85(6):1147–56.PubMedCrossRef
7.
go back to reference Anzalone N, Castellano A, Cadioli M, et al. Brain Gliomas: Multicenter Standardized Assessment of Dynamic Contrast-enhanced and Dynamic Susceptibility Contrast MR Images. Radiology. 2018;1703:62. Anzalone N, Castellano A, Cadioli M, et al. Brain Gliomas: Multicenter Standardized Assessment of Dynamic Contrast-enhanced and Dynamic Susceptibility Contrast MR Images. Radiology. 2018;1703:62.
8.
go back to reference Kickingereder P, Bonekamp D, Nowosielski M, et al. Radiogenomics of Glioblastoma: machine learning-based classification of molecular characteristics by using multiparametric and multiregional MR imaging features. Radiology. 2016;281(3):907–18.PubMedCrossRef Kickingereder P, Bonekamp D, Nowosielski M, et al. Radiogenomics of Glioblastoma: machine learning-based classification of molecular characteristics by using multiparametric and multiregional MR imaging features. Radiology. 2016;281(3):907–18.PubMedCrossRef
9.
go back to reference Hu LS, Kelm Z, Korfiatis P, et al. Impact of software modeling on the accuracy of perfusion MRI in Glioma. AJNR Am J Neuroradiol. 2015;36(12):2242–9.PubMedPubMedCentralCrossRef Hu LS, Kelm Z, Korfiatis P, et al. Impact of software modeling on the accuracy of perfusion MRI in Glioma. AJNR Am J Neuroradiol. 2015;36(12):2242–9.PubMedPubMedCentralCrossRef
10.
go back to reference Kelm ZS, Korfiatis PD, Lingineni RK, et al. Variability and accuracy of different software packages for dynamic susceptibility contrast magnetic resonance imaging for distinguishing glioblastoma progression from pseudoprogression. J Med Imaging. 2015;2:2.CrossRef Kelm ZS, Korfiatis PD, Lingineni RK, et al. Variability and accuracy of different software packages for dynamic susceptibility contrast magnetic resonance imaging for distinguishing glioblastoma progression from pseudoprogression. J Med Imaging. 2015;2:2.CrossRef
11.
go back to reference Conte GM, Castellano A, Altabella L, et al. Reproducibility of dynamic contrast-enhanced MRI and dynamic susceptibility contrast MRI in the study of brain gliomas: a comparison of data obtained using different commercial software. Radiol Med. 2017;122(4):294–302.PubMedCrossRef Conte GM, Castellano A, Altabella L, et al. Reproducibility of dynamic contrast-enhanced MRI and dynamic susceptibility contrast MRI in the study of brain gliomas: a comparison of data obtained using different commercial software. Radiol Med. 2017;122(4):294–302.PubMedCrossRef
12.
go back to reference Welker K, Boxerman J, Kalnin A, et al. ASFNR recommendations for clinical performance of MR dynamic susceptibility contrast perfusion imaging of the brain. AJNR Am J Neuroradiol. 2015;36(6):E41–51.PubMedPubMedCentralCrossRef Welker K, Boxerman J, Kalnin A, et al. ASFNR recommendations for clinical performance of MR dynamic susceptibility contrast perfusion imaging of the brain. AJNR Am J Neuroradiol. 2015;36(6):E41–51.PubMedPubMedCentralCrossRef
14.
go back to reference Bisdas S, Shen H, Thust S, et al. Texture analysis- and support vector machine-assisted diffusional kurtosis imaging may allow in vivo gliomas grading and IDH-mutation status prediction: a preliminary study. Sci Rep. 2018;8:1.CrossRef Bisdas S, Shen H, Thust S, et al. Texture analysis- and support vector machine-assisted diffusional kurtosis imaging may allow in vivo gliomas grading and IDH-mutation status prediction: a preliminary study. Sci Rep. 2018;8:1.CrossRef
20.
go back to reference Ertosun MG, Rubin DL. Automated grading of Gliomas using deep learning in digital pathology images: a modular approach with ensemble of convolutional neural networks. AMIA. Annu Symp proceedings AMIA Symp. 2015;2015:1899–908. Ertosun MG, Rubin DL. Automated grading of Gliomas using deep learning in digital pathology images: a modular approach with ensemble of convolutional neural networks. AMIA. Annu Symp proceedings AMIA Symp. 2015;2015:1899–908.
22.
go back to reference Lu CF, Hsu FT, Hsieh KL, et al. Machine learning-based Radiomics for molecular subtyping of Gliomas. Clin Cancer Res. 2018;24(18):4429–36.PubMedCrossRef Lu CF, Hsu FT, Hsieh KL, et al. Machine learning-based Radiomics for molecular subtyping of Gliomas. Clin Cancer Res. 2018;24(18):4429–36.PubMedCrossRef
23.
go back to reference Hartmann C, Meyer J, Balss J, et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol. 2009;118(4):469–74.PubMedCrossRef Hartmann C, Meyer J, Balss J, et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol. 2009;118(4):469–74.PubMedCrossRef
24.
go back to reference Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A. And others. International society of neuropathology--Haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol. 2014;24(5):429–35.PubMedCrossRefPubMedCentral Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A. And others. International society of neuropathology--Haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol. 2014;24(5):429–35.PubMedCrossRefPubMedCentral
25.
go back to reference Balss J, Meyer J, Mueller W, Korshunov A, Hartmann C, von Deimling A. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol. 2008;116(6):597–602.PubMedCrossRef Balss J, Meyer J, Mueller W, Korshunov A, Hartmann C, von Deimling A. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol. 2008;116(6):597–602.PubMedCrossRef
26.
go back to reference Brandner S, von Deimling A. Diagnostic. Prognostic and predictive relevance of molecular markers in gliomas. Neuropathol Appl Neurobiol. 2015;41(6):694–720.PubMedCrossRef Brandner S, von Deimling A. Diagnostic. Prognostic and predictive relevance of molecular markers in gliomas. Neuropathol Appl Neurobiol. 2015;41(6):694–720.PubMedCrossRef
27.
go back to reference Jaunmuktane Z, Capper D, Dtw J, et al. Methylation array profiling of adult brain tumours: diagnostic outcomes in a large, single Centre. Acta Neuropathol Commun. 2019;7:1.CrossRef Jaunmuktane Z, Capper D, Dtw J, et al. Methylation array profiling of adult brain tumours: diagnostic outcomes in a large, single Centre. Acta Neuropathol Commun. 2019;7:1.CrossRef
28.
go back to reference Yushkevich PA, Piven J, Hazlett HC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31(3):1116–28.PubMedCrossRef Yushkevich PA, Piven J, Hazlett HC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31(3):1116–28.PubMedCrossRef
30.
go back to reference Boxerman JL, Paulson ES, Prah MA, Schmainda KM. The effect of pulse sequence parameters and contrast agent dose on percentage signal recovery in DSC-MRI: implications for clinical applications. AJNR Am J Neuroradiol. 2013;34(7):1364–9.PubMedPubMedCentralCrossRef Boxerman JL, Paulson ES, Prah MA, Schmainda KM. The effect of pulse sequence parameters and contrast agent dose on percentage signal recovery in DSC-MRI: implications for clinical applications. AJNR Am J Neuroradiol. 2013;34(7):1364–9.PubMedPubMedCentralCrossRef
31.
go back to reference Boxerman JL, Schmainda KM, Weisskoff RM. Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol. 2006;34(7):1364–9.CrossRef Boxerman JL, Schmainda KM, Weisskoff RM. Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol. 2006;34(7):1364–9.CrossRef
32.
go back to reference Modat M, Cash DM, Daga P, Winston GP, Duncan JS, Ourselin S. Global image registration using a symmetric block-matching approach. J Med Imaging. 2014;1(2):024003.CrossRef Modat M, Cash DM, Daga P, Winston GP, Duncan JS, Ourselin S. Global image registration using a symmetric block-matching approach. J Med Imaging. 2014;1(2):024003.CrossRef
34.
go back to reference Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern Part B. 1973;SMC-3(6):610–21.CrossRef Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern Part B. 1973;SMC-3(6):610–21.CrossRef
35.
go back to reference Breiman L. Statistical modeling: the two cultures. Stat Sci. 2001;16(3):199–215.CrossRef Breiman L. Statistical modeling: the two cultures. Stat Sci. 2001;16(3):199–215.CrossRef
36.
go back to reference Catalaa I, Henry R, Dillon WP, et al. Perfusion, diffusion and spectroscopy values in newly diagnosed cerebral gliomas. NMR Biomed. 2006;19(4):463–75.PubMedCrossRef Catalaa I, Henry R, Dillon WP, et al. Perfusion, diffusion and spectroscopy values in newly diagnosed cerebral gliomas. NMR Biomed. 2006;19(4):463–75.PubMedCrossRef
37.
go back to reference Kim H, Choi SH, Kim JH, et al. Gliomas: application of cumulative histogram analysis of normalized cerebral blood volume on 3 T MRI to tumor grading. PLoS One. 2013;8:5.CrossRef Kim H, Choi SH, Kim JH, et al. Gliomas: application of cumulative histogram analysis of normalized cerebral blood volume on 3 T MRI to tumor grading. PLoS One. 2013;8:5.CrossRef
38.
go back to reference Falk A, Fahlstrom M, Rostrup E, et al. Discrimination between glioma grades II and III in suspected low-grade gliomas using dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging: a histogram analysis approach. Neuroradiology. 2014;56(12):1031–8.PubMedCrossRef Falk A, Fahlstrom M, Rostrup E, et al. Discrimination between glioma grades II and III in suspected low-grade gliomas using dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging: a histogram analysis approach. Neuroradiology. 2014;56(12):1031–8.PubMedCrossRef
39.
go back to reference Hempel JM, Schittenhelm J, Bisdas S, et al. In vivo assessment of tumor heterogeneity in WHO 2016 glioma grades using diffusion kurtosis imaging: diagnostic performance and improvement of feasibility in routine clinical practice. J Neuroradiol. 2018;45(1):32–40.PubMedCrossRef Hempel JM, Schittenhelm J, Bisdas S, et al. In vivo assessment of tumor heterogeneity in WHO 2016 glioma grades using diffusion kurtosis imaging: diagnostic performance and improvement of feasibility in routine clinical practice. J Neuroradiol. 2018;45(1):32–40.PubMedCrossRef
40.
go back to reference Zöllner FG, Emblem KE, Schad LR. Support vector machines in DSC-based glioma imaging: suggestions for optimal characterization. Magn Reson Med. 2010;64:1230–6.PubMedCrossRef Zöllner FG, Emblem KE, Schad LR. Support vector machines in DSC-based glioma imaging: suggestions for optimal characterization. Magn Reson Med. 2010;64:1230–6.PubMedCrossRef
41.
go back to reference Emblem KE, Due-Tonnessen P, Hald JK, Bjornerud A, Pinho MC, Scheie D, et al. Machine learning in preoperative glioma MRI: survival associations by perfusion-based support vector machine outperforms traditional MRI. J Magn Reson Imaging. 2014;40(1):47–54.PubMedCrossRef Emblem KE, Due-Tonnessen P, Hald JK, Bjornerud A, Pinho MC, Scheie D, et al. Machine learning in preoperative glioma MRI: survival associations by perfusion-based support vector machine outperforms traditional MRI. J Magn Reson Imaging. 2014;40(1):47–54.PubMedCrossRef
42.
go back to reference Emblem KE, Pinho MC, Zollner FG, Due-Tonnessen P, Hald JK, Schad LR, et al. A generic support vector machine model for preoperative glioma survival associations. Radiology. 2015;275(1):228–34.PubMedCrossRef Emblem KE, Pinho MC, Zollner FG, Due-Tonnessen P, Hald JK, Schad LR, et al. A generic support vector machine model for preoperative glioma survival associations. Radiology. 2015;275(1):228–34.PubMedCrossRef
43.
go back to reference Citak-Er F, Firat Z, Kovanlikaya I, Ture U, Ozturk-Isik E. Machine-learning in grading of gliomas based on multi-parametric magnetic resonance imaging at 3T. Comput Biol Med. 2018;99:154–60.PubMedCrossRef Citak-Er F, Firat Z, Kovanlikaya I, Ture U, Ozturk-Isik E. Machine-learning in grading of gliomas based on multi-parametric magnetic resonance imaging at 3T. Comput Biol Med. 2018;99:154–60.PubMedCrossRef
45.
go back to reference Boxerman JL, Rosen BR, Weisskoff RM. Signal-to-noise analysis of cerebral blood volume maps from dynamic NMR imaging studies. J Magn Reson Imaging. 1997;7(3):528–37.PubMedCrossRef Boxerman JL, Rosen BR, Weisskoff RM. Signal-to-noise analysis of cerebral blood volume maps from dynamic NMR imaging studies. J Magn Reson Imaging. 1997;7(3):528–37.PubMedCrossRef
Metadata
Title
Machine learning assisted DSC-MRI radiomics as a tool for glioma classification by grade and mutation status
Authors
Carole H. Sudre
Jasmina Panovska-Griffiths
Eser Sanverdi
Sebastian Brandner
Vasileios K. Katsaros
George Stranjalis
Francesca B. Pizzini
Claudio Ghimenton
Katarina Surlan-Popovic
Jernej Avsenik
Maria Vittoria Spampinato
Mario Nigro
Arindam R. Chatterjee
Arnaud Attye
Sylvie Grand
Alexandre Krainik
Nicoletta Anzalone
Gian Marco Conte
Valeria Romeo
Lorenzo Ugga
Andrea Elefante
Elisa Francesca Ciceri
Elia Guadagno
Eftychia Kapsalaki
Diana Roettger
Javier Gonzalez
Timothé Boutelier
M. Jorge Cardoso
Sotirios Bisdas
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Medical Informatics and Decision Making / Issue 1/2020
Electronic ISSN: 1472-6947
DOI
https://doi.org/10.1186/s12911-020-01163-5

Other articles of this Issue 1/2020

BMC Medical Informatics and Decision Making 1/2020 Go to the issue