Abstract
The grading of glioma has clinical significance in determining a treatment strategy and evaluating prognosis to investigate a novel set of radiomic features extracted from the fractional anisotropy (FA) and mean diffusivity (MD) maps of brain diffusion tensor imaging (DTI) sequences for computer-aided grading of gliomas. This retrospective study included 108 patients who had pathologically confirmed brain gliomas and DTI scanned during 2012–2018. This cohort included 43 low-grade gliomas (LGGs; all grade II) and 65 high-grade gliomas (HGGs; grade III or IV). We extracted a set of radiomic features, including traditional texture, morphological, and novel deep features derived from pre-trained convolutional neural network models, in the manually-delineated tumor regions. We employed support vector machine and these radiomic features for two classification tasks: LGGs vs HGGs, and grade III vs IV. The area under the receiver operating characteristic (ROC) curve (AUC), accuracy, sensitivity, and specificity was reported as the performance metrics using the leave-one-out cross-validation method. When combining FA+MD, AUC = 0.93, accuracy = 0.94, sensitivity = 0.98, and specificity = 0.86 in classifying LGGs from HGGs, while AUC = 0.99, accuracy = 0.98, sensitivity = 0.98, and specificity = 1.00 in classifying grade III from IV. The AUC and accuracy remain close when features were extracted from only the solid tumor or additionally including necrosis, cyst, and peritumoral edema. Still, the effects in terms of sensitivity and specificity are mixed. Deep radiomic features derived from pre-trained convolutional neural networks showed higher prediction ability than the traditional texture and shape features in both classification experiments. Radiomic features extracted on the FA and MD maps of brain DTI images are useful for noninvasively classification/grading of LGGs vs HGGs, and grade III vs IV.
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Ostrom QT, Gittleman H, Liao P, Rouse C, Chen Y, Dowling J, Wolinsky Y, Kruchko C, Barnholtz-Sloan J: CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007–2011. Neuro Oncol 16(Suppl 4):iv1–i63, 2014. https://doi.org/10.1093/neuonc/nou223
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW: The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820, 2016. https://doi.org/10.1007/s00401-016-1545-1
Weller M, van den Bent M, Tonn JC, Stupp R, Preusser M, Cohen-Jonathan-Moyal E, Henriksson R, Rhun EL, Balana C, Chinot O, Bendszus M, Reijneveld JC, Dhermain F, French P, Marosi C, Watts C, Oberg I, Pilkington G, Baumert BG, Taphoorn MJB, Hegi M, Westphal M, Reifenberger G, Soffietti R, Wick W, European Association for Neuro-Oncology (EANO) Task Force on Gliomas: European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol 18:e315–315e329, 2017. https://doi.org/10.1016/S1470-2045(17)30194-8
Omuro A, DeAngelis LM: Glioblastoma and other malignant gliomas: a clinical review. JAMA 310:1842–1850, 2013. https://doi.org/10.1001/jama.2013.280319
Johnson DR, Guerin JB, Giannini C, Morris JM, Eckel LJ, Kaufmann TJ: 2016 updates to the WHO brain tumor classification system: what the radiologist needs to know. Radiographics 37:2164–2180, 2017. https://doi.org/10.1148/rg.2017170037
Bai Y, Lin Y, Tian J, Shi D, Cheng J, Haacke EM, Hong X, Ma B, Zhou J, Wang M: Grading of gliomas by using monoexponential, biexponential, and stretched exponential diffusion-weighted MR imaging and diffusion kurtosis MR imaging. Radiology 278:496–504, 2016. https://doi.org/10.1148/radiol.2015142173
Smits M, van den Bent MJ: Imaging correlates of adult glioma genotypes. Radiology 284:316–331, 2017. https://doi.org/10.1148/radiol.2017151930
Caulo M, Panara V, Tortora D, Mattei PA, Briganti C, Pravatà E, Salice S, Cotroneo AR, Tartaro A: Data-driven grading of brain gliomas: a multiparametric MR imaging study. Radiology 272:494–503, 2014. https://doi.org/10.1148/radiol.14132040
Liu X, Tian W, Kolar B, Yeaney GA, Qiu X, Johnson MD, Ekholm S: MR diffusion tensor and perfusion-weighted imaging in preoperative grading of supratentorial nonenhancing gliomas. Neuro Oncol 13:447–455, 2011. https://doi.org/10.1093/neuonc/noq197
White ML, Zhang Y, Yu F, Jaffar Kazmi SA: Diffusion tensor MR imaging of cerebral gliomas: evaluating fractional anisotropy characteristics. AJNR Am J Neuroradiol 32:374–381, 2011. https://doi.org/10.3174/ajnr.A2267
Wang Q, Zhang J, Xu X, Chen X, Xu B: Diagnostic performance of apparent diffusion coefficient parameters for glioma grading. J Neurooncol 139:61–68, 2018. https://doi.org/10.1007/s11060-018-2841-5
Jakab A, Molnár P, Emri M, Berényi E: Glioma grade assessment by using histogram analysis of diffusion tensor imaging-derived maps. Neuroradiology 53:483–491, 2011. https://doi.org/10.1007/s00234-010-0769-3
Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout R, Granton P, Zegers CM, Gillies R, Boellard R, Dekker A, Aerts HJ: Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446, 2012. https://doi.org/10.1016/j.ejca.2011.11.036
Gillies RJ, Kinahan PE, Hricak H: Radiomics: images are more than pictures, they are data. Radiology 278:563–577, 2016. https://doi.org/10.1148/radiol.2015151169
Lambin P, Leijenaar RTH, Deist TM, Peerlings J, de Jong EEC, van Timmeren J, Sanduleanu S, Larue RTHM, Even AJG, Jochems A, van Wijk Y, Woodruff H, van Soest J, Lustberg T, Roelofs E, van Elmpt W, Dekker A, Mottaghy FM, Wildberger JE, Walsh S: Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 14:749–762, 2017. https://doi.org/10.1038/nrclinonc.2017.141
Aerts HJ et al.: Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006, 2014. https://doi.org/10.1038/ncomms5006
Tian Q et al.: Radiomics strategy for glioma grading using texture features from multiparametric MRI. J Magn Reson Imaging, 2018. https://doi.org/10.1002/jmri.26010
Skogen K, Schulz A, Dormagen JB, Ganeshan B, Helseth E, Server A: Diagnostic performance of texture analysis on MRI in grading cerebral gliomas. Eur J Radiol 85:824–829, 2016. https://doi.org/10.1016/j.ejrad.2016.01.013
Ryu YJ, Choi SH, Park SJ, Yun TJ, Kim JH, Sohn CH: Glioma: application of whole-tumor texture analysis of diffusion-weighted imaging for the evaluation of tumor heterogeneity. PLoS One 9:e108335, 2014. https://doi.org/10.1371/journal.pone.0108335
Tajbakhsh N, Shin JY, Gurudu SR, Hurst RT, Kendall CB, Gotway MB, Liang J: Convolutional neural networks for medical image analysis: full training or fine tuning. IEEE Trans Med Imaging 35:1299–1312, 2016. https://doi.org/10.1109/TMI.2016.2535302
Mori S, Zhang J: Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539, 2006. https://doi.org/10.1016/j.neuron.2006.08.012
Zacharaki EI, Wang S, Chawla S, Soo Yoo D, Wolf R, Melhem ER, Davatzikos C: Classification of brain tumor type and grade using MRI texture and shape in a machine learning scheme. Magn Reson Med 62:1609–1618, 2009. https://doi.org/10.1002/mrm.22147
Vedaldi A, Lenc K. MatConvNet: convolutional neural networks for MATLAB. Proceedings of the 23rd ACM International Conference on Multimedia. 2807412:ACM. 689–692. https://doi.org/10.1145/2733373.2807412.
Litjens G, Kooi T, Bejnordi BE, Setio A, Ciompi F, Ghafoorian M, van der Laak J, van Ginneken B, Sánchez CI: A survey on deep learning in medical image analysis. Med Image Anal 42:60–88, 2017. https://doi.org/10.1016/j.media.2017.07.005
Oktay O, Bai W, Lee M, Guerrero R, Kamnitsas K, Caballero J, de Marvao A, Cook S, O 'regan D, Rueckert D. Multi-input Cardiac Image Super-resolution using Convolutional Neural Networks. 2016. 246–254. https://doi.org/10.1007/978-3-319-46726-9_29
Antropova N, Huynh B, Giger M: SU-D-207B-06: predicting breast cancer malignancy on DCE-MRI data using pre-trained convolutional neural networks. Med Phys 43:3349–3350, 2016. https://doi.org/10.1007/978-3-319-46726-9_29
Chatfield K, Simonyan K, Vedaldi A, Zisserman A. Return of the devil in the details: delving deep into convolutional nets. 2014. https://doi.org/10.5244/C.28.6
Paul R, Hawkins SH, Schabath MB, Gillies RJ, Hall LO, Goldgof DB: Predicting malignant nodules by fusing deep features with classical radiomics features. J Med Imaging (Bellingham) 5:011021, 2018. https://doi.org/10.1117/1.JMI.5.1.011021
Franklin J: The elements of statistical learning: data mining, inference and prediction. Publ Am Stat Assoc 99:567–567, 2010. https://doi.org/10.1007/BF02985802
Jiang L, Xiao CY, Xu Q, Sun J, Chen H, Chen YC, Yin X: Analysis of DTI-derived tensor metrics in differential diagnosis between low-grade and high-grade gliomas. Front Aging Neurosci 9:271, 2017. https://doi.org/10.3389/fnagi.2017.00271
Server A, Graff BA, Josefsen R, Orheim TE, Schellhorn T, Nordhøy W, Nakstad PH: Analysis of diffusion tensor imaging metrics for gliomas grading at 3 T. Eur J Radiol 83:e156–e165, 2014. https://doi.org/10.1016/j.ejrad.2013.12.023
Raja R, Sinha N, Saini J, Mahadevan A, Rao KN, Swaminathan A: Assessment of tissue heterogeneity using diffusion tensor and diffusion kurtosis imaging for grading gliomas. Neuroradiology 58:1217–1231, 2016. https://doi.org/10.1007/s00234-016-1758-y
Cho HH, Lee SH, Kim J, Park H: Classification of the glioma grading using radiomics analysis. PeerJ 6:e5982, 2018. https://doi.org/10.7717/peerj.5982
Qin JB, Liu Z, Zhang H, Shen C, Wang XC, Tan Y, Wang S, Wu XF, Tian J: Grading of gliomas by using radiomic features on multiple magnetic resonance imaging (MRI) sequences. Med Sci Monit 23:2168–2178, 2017. https://doi.org/10.12659/MSM.901270
Rodriguez Gutierrez D, Awwad A, Meijer L, Manita M, Jaspan T, Dineen RA, Grundy RG, Auer DP: Metrics and textural features of MRI diffusion to improve classification of pediatric posterior fossa tumors. AJNR Am J Neuroradiol 35:1009–1015, 2014. https://doi.org/10.3174/ajnr.A3784
Brynolfsson P, Nilsson D, Henriksson R, Hauksson J, Karlsson M, Garpebring A, Birgander R, Trygg J, Nyholm T, Asklund T: ADC texture--an imaging biomarker for high-grade glioma. Med Phys 41:101903, 2014. https://doi.org/10.1118/1.4894812
Kang D, Park JE, Kim YH, Kim JH, Oh JY, Kim J, Kim Y, Kim ST, Kim HS: Diffusion radiomics as a diagnostic model for atypical manifestation of primary central nervous system lymphoma: development and multicenter external validation. Neuro Oncol, 2018. https://doi.org/10.1093/neuonc/noy021
Yang F, Dogan N, Stoyanova R, Ford JC: Evaluation of radiomic texture feature error due to MRI acquisition and reconstruction: a simulation study utilizing ground truth. Phys Med 50:26–36, 2018. https://doi.org/10.1016/j.ejmp.2018.05.017
Chang P, Grinband J, Weinberg BD, Bardis M, Khy M, Cadena G, Su MY, Cha S, Filippi CG, Bota D, Baldi P, Poisson LM, Jain R, Chow D: Deep-learning convolutional neural networks accurately classify genetic mutations in gliomas. AJNR Am J Neuroradiol 39:1201–1207, 2018. https://doi.org/10.3174/ajnr.A5667
Korfiatis P, Kline TL, Lachance DH, Parney IF, Buckner JC, Erickson BJ: Residual deep convolutional neural network predicts MGMT methylation status. J Digit Imaging 30:622–628, 2017. https://doi.org/10.1007/s10278-017-0009-z
Zhou H, Chang K, Bai HX, Xiao B, Su C, Bi WL, Zhang PJ, Senders JT, Vallières M, Kavouridis VK, Boaro A, Arnaout O, Yang L, Huang RY: Machine learning reveals multimodal MRI patterns predictive of isocitrate dehydrogenase and 1p/19q status in diffuse low- and high-grade gliomas. J Neurooncol 142:299–307, 2019. https://doi.org/10.1007/s11060-019-03096-0
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This work was partially supported by the National Key Research and Development Plan of China (NO. 2016YFC0103100) and the National Natural Science Foundation of China (No. 61701506).
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Zhang, Z., Xiao, J., Wu, S. et al. Deep Convolutional Radiomic Features on Diffusion Tensor Images for Classification of Glioma Grades. J Digit Imaging 33, 826–837 (2020). https://doi.org/10.1007/s10278-020-00322-4
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DOI: https://doi.org/10.1007/s10278-020-00322-4