Abstract
Glioma constitutes \(80\%\) of malignant primary brain tumors in adults, and is usually classified as high-grade glioma (HGG) and low-grade glioma (LGG). The LGG tumors are less aggressive, with slower growth rate as compared to HGG, and are responsive to therapy. Tumor biopsy being challenging for brain tumor patients, noninvasive imaging techniques like magnetic resonance imaging (MRI) have been extensively employed in diagnosing brain tumors. Therefore, development of automated systems for the detection and prediction of the grade of tumors based on MRI data becomes necessary for assisting doctors in the framework of augmented intelligence. In this paper, we thoroughly investigate the power of deep convolutional neural networks (ConvNets) for classification of brain tumors using multi-sequence MR images. We propose novel ConvNet models, which are trained from scratch, on MRI patches, slices, and multi-planar volumetric slices. The suitability of transfer learning for the task is next studied by applying two existing ConvNets models (VGGNet and ResNet) trained on ImageNet dataset, through fine-tuning of the last few layers. Leave-one-patient-out testing, and testing on the holdout dataset are used to evaluate the performance of the ConvNets. The results demonstrate that the proposed ConvNets achieve better accuracy in all cases where the model is trained on the multi-planar volumetric dataset. Unlike conventional models, it obtains a testing accuracy of \(95\%\) for the low/high grade glioma classification problem. A score of \(97\%\) is generated for classification of LGG with/without 1p/19q codeletion, without any additional effort toward extraction and selection of features. We study the properties of self-learned kernels/ filters in different layers, through visualization of the intermediate layer outputs. We also compare the results with that of state-of-the-art methods, demonstrating a maximum improvement of \(7\%\) on the grading performance of ConvNets and \(9\%\) on the prediction of 1p/19q codeletion status.
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References
Akkus Z, Ali I, et al. Predicting deletion of chromosomal arms 1p/19q in low-grade gliomas from mr images using machine intelligence. J Digit Imaging. 2017;30(4):469–76.
Bakas S, Akbari H, et al. Advancing the cancer genome atlas glioma MRI collections with expert segmentation labels and radiomic features. Sci Data. 2017;4:170117.
Banerjee S, Mitra S, Shankar BU, Synergetic neuro-fuzzy feature selection and classification of brain tumors. In: Proceedings of IEEE international conference on fuzzy systems (FUZZ-IEEE); 2017. pp. 1–6
Banerjee S, Mitra S, Sharma A, Uma Shankar, B, A CADe system for gliomas in brain MRI using convolutional neural networks; 2018. arXiv preprint arXiv:1806.07589
Banerjee S, Mitra S, Uma Shankar B. Single seed delineation of brain tumor using multi-thresholding. Inf Sci. 2016;330:88–103.
Banerjee S, Mitra S, Uma Shankar B. Automated 3D segmentation of brain tumor using visual saliency. Inf Sci. 2018;424:337–53.
Banerjee S, Mitra S, Uma Shankar B, Hayashi Y. A novel GBM saliency detection model using multi-channel MRI. PLOS ONE. 2016;11(1):e0146388.
Cha S. Update on brain tumor imaging: from anatomy to physiology. Am J Neuroradiol. 2006;27(3):475–87.
Chandrasoma PT, Smith MM, Apuzzo MLJ. Stereotactic biopsy in the diagnosis of brain masses: comparison of results of biopsy and resected surgical specimen. Neurosurgery. 1989;24(2):160–5.
Chekhun V, Sherban S, Savtsova Z. Tumor cell heterogeneity. Exp Oncol. 2013;35:154–62.
Cho HH, Lee SH, Kim J, Park H. Classification of the glioma grading using radiomics analysis. PeerJ. 2018;6:e5982.
Clark K, Vendt B, Smith K, et al. The Cancer Imaging Archive (TCIA): maintaining and operating a public information repository. J Digit Imaging. 2013;26:1045–57.
Coroller T, Bi W, et al. Early grade classification in meningioma patients combining radiomics and semantics data. Med Phys. 2016;43:3348–9.
DeAngelis LM. Brain tumors. New Engl J Med. 2001;344(2):114–23.
Erickson B, Akkus Z, Data from LGG-1p19q deletion; 2017. https://doi.org/10.7937/K9/TCIA.2017.dwehtz9v. The Cancer Imaging Archive
Field M, Witham TF, Flickinger JC, Kondziolka D, Lunsford LD. Comprehensive assessment of hemorrhage risks and outcomes after stereotactic brain biopsy. J Neurosurg. 2001;94(4):545–51.
Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology. 2015;278:563–77.
Glantz MJ, Burger PC, et al. Influence of the type of surgery on the histologic diagnosis in patients with anaplastic gliomas. Neurology. 1991;41(11):1741.
Glorot X, Bordes A, Bengio Y, Deep sparse rectifier neural networks. In: Proceedings of the fourteenth international conference on artificial intelligence and statistics, 2011; pp. 315–323
Goodfellow I, Bengio Y, Courville A. Deep learning. Cambridge: MIT Press; 2016.
Greenspan H, van Ginneken B, Summers RM. Deep learning in medical imaging: overview and future promise of an exciting new technique. IEEE Trans Med Imaging. 2016;35:1153–9.
Havaei M, Davy A, et al. Brain tumor segmentation with deep neural networks. Med Image Anal. 2017;35:18–31.
He K, Zhang X, Ren S, Sun J, Deep residual learning for image recognition. In: Proceedings of the IEEE conference on computer vision and pattern recognition, 2016; pp. 770–778
Ioffe S, Szegedy C, Batch normalization: Accelerating deep network training by reducing internal covariate shift. In: Proceedings of international conference on machine learning, 2015; pp. 448–456
Jackson RJ, Fuller GN, et al. Limitations of stereotactic biopsy in the initial management of gliomas. Neuro-Oncology. 2001;3(3):193–200.
Kamnitsas K, Ledig C, et al. Efficient multi-scale 3D CNN with fully connected CRF for accurate brain lesion segmentation. Med Image Anal. 2017;36:61–78.
LeCun Y, Bengio Y, Hinton G. Deep learning. Nature. 2015;521(7553):436–44.
Li Y, Wang D, et al., Distinct genomics aberrations between low-grade and high-grade gliomas of Chinese patients. PLOS ONE; 2013. https://doi.org/10.1371/journal.pone.0057168
Louis DN, Perry A, Reifenberger G, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131:803–20.
Lyksborg M, Puonti O, et al. An ensemble of 2D convolutional neural networks for tumor segmentation. Image analysis. New York: Springer; 2015. p. 201–11.
McGirt MJ, Woodworth GF, et al. Independent predictors of morbidity after image-guided stereotactic brain biopsy: a risk assessment of 270 cases. J Neurosurg. 2005;102(5):897–901.
Menze BH, Jakab A, Bauer S, Kalpathy-Cramer J, Farahani K, Kirby J, Burren Y, Porz N, Slotboom J, Wiest R, et al. The multimodal Brain Tumor image Segmentation benchmark (BraTS). IEEE Trans Med Imaging. 2015;34:1993–2024.
Mitra S, Banerjee S, Hayashi Y. Volumetric brain tumour detection from MRI using visual saliency. PLOS ONE. 2017;12:1–14.
Mitra S, Uma Shankar B. Integrating radio imaging with gene expressions toward a personalized management of cancer. IEEE Trans Hum Mach Syst. 2014;44(5):664–77.
Mitra S, Uma Shankar B. Medical image analysis for cancer management in natural computing framework. Inf Sci. 2015;306:111–31.
Mousavi HS, Monga V, Rao G, Rao AUK. Automated discrimination of lower and higher grade gliomas based on histopathological image analysis. J Pathol Inform. 2015;6:15.
Oquab M, Bottou L, Laptev I, Sivic J, Learning and transferring mid-level image representations using convolutional neural networks. In: Proceedings of IEEE conference on computer vision and pattern recognition, 2014; pp. 1717–1724
Patel SH, Poisson LM, Brat DJ, et al., \(T2-FLAIR\) mismatch, an imaging biomarker for \(IDH\) and \(1p/19q\) status in lower grade gliomas: a TCGA/TCIA project. American Association for Cancer Research; 2017. https://doi.org/10.1158/1078-0432.CCR-17-0560
Pedano N, Flanders A, Scarpace L, et al., Radiology data from The Cancer Genome Atlas Low Grade Glioma [TCGA-LGG] collection. Cancer Imaging Archive, 2016
Pereira S, Pinto A, Alves V, Silva CA. Brain tumor segmentation using convolutional neural networks in MRI images. IEEE Trans Med Imaging. 2016;35:1240–51.
Phan HTH, Kumar A, Kim J, Feng D, Transfer learning of a convolutional neural network for hep-2 cell image classification. In: Proceedings of IEEE 13th international symposium on biomedical imaging (ISBI); 2016. pp. 1208–1211
Scarpace L, Mikkelsen T, et al., Radiology data from The Cancer Genome Atlas Glioblastoma Multiforme [TCGA-GBM] collection. The Cancer Imaging Archive. https://doi.org/10.7937/K9/TCIA.2016.RNYFUYE9
Simonyan K, Zisserman A, Very deep convolutional networks for large-scale image recognition; 2014. arXiv preprint arXiv:1409.1556
Srivastava N, Hinton GE, Krizhevsky A, Sutskever I, Salakhutdinov R. Dropout: a simple way to prevent neural networks from overfitting. J Mach Learn Res. 2014;15(1):1929–58.
Szegedy C, Liu W, et al., Going deeper with convolutions. In: Proceedings of the IEEE conference on computer vision and pattern recognition; 2015. pp. 1–9
Tajbakhsh N, Shin JY, et al. Convolutional neural networks for medical image analysis: full training or fine tuning? IEEE Trans Med Imaging. 2016;35(5):1299–312.
Urban G, Bendszus M, Hamprecht FA, Kleesiek J, Multi-modal brain tumor segmentation using deep convolutional neural networks. In: Proceedings of MICCAI-BRATS (Winning Contribution); 2014. pp. 1–5
Van den Bent MJ, Brandes AA, et al. Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol. 2012;31:344–50.
Yang Y, Yan LF, et al. Glioma grading on conventional MR images: a deep learning study with transfer learning. Front Neurosci. 2018;12:804. https://doi.org/10.3389/fnins.2018.00804.
Zacharaki EI, Wang S, et al. Classification of brain tumor type and grade using MRI texture and shape in a machine learning scheme. Magn Reson Med. 2009;62:1609–18.
Zhao F, Ahlawat S, et al. Can MR imaging be used to predict tumor grade in soft-tissue sarcoma? Radiology. 2014;272(1):192–201.
Zhou M, Scott J, et al. Radiomics in brain tumor: image assessment, quantitative feature descriptors, and machine-learning approaches. Am J Neuroradiol. 2017;39:208–16.
Zikic D, Ioannou Y, et al., Segmentation of brain tumor tissues with convolutional neural networks; 2014. pp. 36–39
Acknowledgements
This research is supported by the IEEE Computational Intelligence Society Graduate Student Research Grant 2017. Banerjee acknowledges the support provided to him by the Intel Corporation, through the Intel AI Student Ambassador Program. Mitra acknowledges the support provided to her by the Indian National Academy of Engineering, through the INAE Chair Professorship. This publication is an outcome of the R&D work undertaken in a project with the Visvesvaraya PhD Scheme of Ministry of Electronics & Information Technology, Government of India, being implemented by Digital India Corporation.
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This article is part of the topical collection “Computational Biology and Biomedical Informatics” guest edited by Dhruba Kr Bhattacharyya, Sushmita Mitra and Jugal Kr Kalita.
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Banerjee, S., Mitra, S., Masulli, F. et al. Glioma Classification Using Deep Radiomics. SN COMPUT. SCI. 1, 209 (2020). https://doi.org/10.1007/s42979-020-00214-y
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DOI: https://doi.org/10.1007/s42979-020-00214-y