Texture analysis- and support vector machine-assisted diffusional kurtosis imaging may allow in vivo gliomas grading and IDH-mutation status prediction: a preliminary study

We sought to investigate, whether texture analysis of diffusional kurtosis imaging (DKI) enhanced by support vector machine (SVM) analysis may provide biomarkers for gliomas staging and detection of the IDH mutation. First-order statistics and texture feature extraction were performed in 37 patients on both conventional (FLAIR) and mean diffusional kurtosis (MDK) images and recursive feature elimination (RFE) methodology based on SVM was employed to select the most discriminative diagnostic biomarkers. The first-order statistics demonstrated significantly lower MDK values in the IDH-mutant tumors. This resulted in 81.1% accuracy (sensitivity = 0.96, specificity = 0.45, AUC 0.59) for IDH mutation diagnosis. There were non-significant differences in average MDK and skewness among the different tumour grades. When texture analysis and SVM were utilized, the grading accuracy achieved by DKI biomarkers was 78.1% (sensitivity 0.77, specificity 0.79, AUC 0.79); the prediction accuracy for IDH mutation reached 83.8% (sensitivity 0.96, specificity 0.55, AUC 0.87). For the IDH mutation task, DKI outperformed significantly the FLAIR imaging. When using selected biomarkers after RFE, the prediction accuracy achieved 83.8% (sensitivity 0.92, specificity 0.64, AUC 0.88). These findings demonstrate the superiority of DKI enhanced by texture analysis and SVM, compared to conventional imaging, for gliomas staging and prediction of IDH mutational status.

[1]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[2]  D. Geng,et al.  Combination of diffusion tensor imaging and conventional MRI correlates with isocitrate dehydrogenase 1/2 mutations but not 1p/19q genotyping in oligodendroglial tumours , 2016, European Radiology.

[3]  Johan Trygg,et al.  ADC texture--an imaging biomarker for high-grade glioma? , 2014, Medical physics.

[4]  J. Hanley,et al.  A method of comparing the areas under receiver operating characteristic curves derived from the same cases. , 1983, Radiology.

[5]  D. Busam,et al.  An Integrated Genomic Analysis of Human Glioblastoma Multiforme , 2008, Science.

[6]  Tej D. Azad,et al.  Magnetic resonance image features identify glioblastoma phenotypic subtypes with distinct molecular pathway activities , 2015, Science Translational Medicine.

[7]  Eric Achten,et al.  Optimal Experimental Design for Diffusion Kurtosis Imaging , 2010, IEEE Transactions on Medical Imaging.

[8]  Xiaohong Joe Zhou,et al.  Differentiation of Low- and High-Grade Gliomas Using High b-Value Diffusion Imaging with a Non-Gaussian Diffusion Model , 2016, American Journal of Neuroradiology.

[9]  Valerij G Kiselev,et al.  Effect of impermeable boundaries on diffusion-attenuated MR signal. , 2006, Journal of magnetic resonance.

[10]  T E Lund,et al.  Mean Diffusional Kurtosis in Patients with Glioma: Initial Results with a Fast Imaging Method in a Clinical Setting , 2015, American Journal of Neuroradiology.

[11]  J. E. Tanner Transient diffusion in a system partitioned by permeable barriers. Application to NMR measurements with a pulsed field gradient , 1978 .

[12]  J. Helpern,et al.  Three‐dimensional characterization of non‐gaussian water diffusion in humans using diffusion kurtosis imaging , 2006, NMR in biomedicine.

[13]  P. LaViolette,et al.  Precise ex vivo histological validation of heightened cellularity and diffusion-restricted necrosis in regions of dark apparent diffusion coefficient in 7 cases of high-grade glioma. , 2014, Neuro-oncology.

[14]  U. Klose,et al.  Histogram analysis of diffusion kurtosis imaging estimates for in vivo assessment of 2016 WHO glioma grades: A cross-sectional observational study. , 2017, European journal of radiology.

[15]  [World Health Organization classification of tumours of the central nervous system: a summary]. , 2016, Zhonghua bing li xue za zhi = Chinese journal of pathology.

[16]  Andrew Zisserman,et al.  A Statistical Approach to Texture Classification from Single Images , 2004, International Journal of Computer Vision.

[17]  P. Basser Inferring microstructural features and the physiological state of tissues from diffusion‐weighted images , 1995, NMR in biomedicine.

[18]  A. Deimling,et al.  Diagnostic, prognostic and predictive relevance of molecular markers in gliomas , 2015, Neuropathology and applied neurobiology.

[19]  Geoffrey J McLachlan,et al.  Selection bias in gene extraction on the basis of microarray gene-expression data , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Camel Tanougast,et al.  Extracted magnetic resonance texture features discriminate between phenotypes and are associated with overall survival in glioblastoma multiforme patients , 2016, Medical & Biological Engineering & Computing.

[21]  Mitchel S. Berger,et al.  Magnetic Resonance of 2-Hydroxyglutarate in IDH1-Mutated Low-Grade Gliomas , 2012, Science Translational Medicine.

[22]  A. Rao,et al.  Texture Feature Ratios from Relative CBV Maps of Perfusion MRI Are Associated with Patient Survival in Glioblastoma , 2016, American Journal of Neuroradiology.

[23]  Wenzhen Zhu,et al.  Diffusion kurtosis imaging can efficiently assess the glioma grade and cellular proliferation , 2015, Oncotarget.

[24]  Ed X. Wu,et al.  Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis , 2008, NeuroImage.

[25]  Bjoern H Menze,et al.  Diffusion tensor image features predict IDH genotype in newly diagnosed WHO grade II/III gliomas , 2017, Scientific Reports.

[26]  Aixia Guo,et al.  Gene Selection for Cancer Classification using Support Vector Machines , 2014 .

[27]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[28]  Pieter Wesseling,et al.  International Society of Neuropathology‐Haarlem Consensus Guidelines for Nervous System Tumor Classification and Grading , 2014, Brain pathology.

[29]  M. Moseley,et al.  Magnetic Resonance in Medicine 51:924–937 (2004) Characterizing Non-Gaussian Diffusion by Using Generalized Diffusion Tensors , 2022 .

[30]  B. Scheithauer,et al.  The 2007 WHO classification of tumours of the central nervous system , 2007, Acta Neuropathologica.

[31]  M. J. D. Mallett,et al.  Exact analytic solutions for diffusion impeded by an infinite array of partially permeable barriers , 1992, Proceedings of the Royal Society of London. Series A: Mathematical and Physical Sciences.

[32]  Sohil H. Patel,et al.  T2–FLAIR Mismatch, an Imaging Biomarker for IDH and 1p/19q Status in Lower-grade Gliomas: A TCGA/TCIA Project , 2017, Clinical Cancer Research.

[33]  H. Lanfermann,et al.  Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. , 2010, Radiology.

[34]  Salvador Castaneda Vega,et al.  In vivo molecular profiling of human glioma using diffusion kurtosis imaging , 2016, Journal of Neuro-Oncology.

[35]  Sabine Van Huffel,et al.  Integrating diffusion kurtosis imaging, dynamic susceptibility-weighted contrast-enhanced MRI, and short echo time chemical shift imaging for grading gliomas. , 2014, Neuro-oncology.

[36]  G. Reifenberger,et al.  The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary , 2016, Acta Neuropathologica.

[37]  J. Helpern,et al.  MRI quantification of non‐Gaussian water diffusion by kurtosis analysis , 2010, NMR in biomedicine.

[38]  Jan Sijbers,et al.  Gliomas: diffusion kurtosis MR imaging in grading. , 2012, Radiology.

[39]  David T. W. Jones,et al.  ATRX and IDH1-R132H immunohistochemistry with subsequent copy number analysis and IDH sequencing as a basis for an “integrated” diagnostic approach for adult astrocytoma, oligodendroglioma and glioblastoma , 2014, Acta Neuropathologica.

[40]  David J Collins,et al.  Technology Insight: water diffusion MRI—a potential new biomarker of response to cancer therapy , 2008, Nature Clinical Practice Oncology.

[41]  J. Sneep,et al.  With a summary , 1945 .

[42]  M. Fujiki,et al.  Comparison of Multiple Parameters Obtained on 3T Pulsed Arterial Spin-Labeling, Diffusion Tensor Imaging, and MRS and the Ki-67 Labeling Index in Evaluating Glioma Grading , 2014, American Journal of Neuroradiology.

[43]  Jong-Hee Chang,et al.  Prediction of IDH1-Mutation and 1p/19q-Codeletion Status Using Preoperative MR Imaging Phenotypes in Lower Grade Gliomas , 2018, American Journal of Neuroradiology.

[44]  B. Ardekani,et al.  Estimation of tensors and tensor‐derived measures in diffusional kurtosis imaging , 2011, Magnetic resonance in medicine.

[45]  Bachir Taouli,et al.  Body diffusion kurtosis imaging: Basic principles, applications, and considerations for clinical practice , 2015, Journal of magnetic resonance imaging : JMRI.