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Research Article| Volume 84, P127-134, July 2018

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Voxel-based automated detection of focal cortical dysplasia lesions using diffusion tensor imaging and T2-weighted MRI data

      Highlights

      • Gray–white matter lesions are detected by combining GPML with multimodal features.
      • Classifier modeled using DTI indexes can increase the sensitivity of detection.
      • GPML is robust to unbalanced datasets and performs better than conventional SVM.
      • Accurate detection may contribute to successful surgery and lower surgical risk.

      Abstract

      The aim of this study was to automatically detect focal cortical dysplasia (FCD) lesions in patients with extratemporal lobe epilepsy by relying on diffusion tensor imaging (DTI) and T2-weighted magnetic resonance imaging (MRI) data. We implemented an automated classifier using voxel-based multimodal features to identify gray and white matter abnormalities of FCD in patient cohorts. In addition to the commonly used T2-weighted image intensity feature, DTI-based features were also utilized. A Gaussian processes for machine learning (GPML) classifier was tested on 12 patients with FCD (8 with histologically confirmed FCD) scanned at 1.5 T and cross-validated using a leave-one-out strategy. Moreover, we compared the multimodal GPML paradigm's performance with that of single modal GPML and classical support vector machine (SVM). Our results demonstrated that the GPML performance on DTI-based features (mean AUC = 0.63) matches with the GPML performance on T2-weighted image intensity feature (mean AUC = 0.64). More promisingly, GPML yielded significantly improved performance (mean AUC = 0.76) when applying DTI-based features to multimodal paradigm. Based on the results, it can also be clearly stated that the proposed GPML strategy performed better and is robust to unbalanced dataset contrary to SVM that performed poorly (AUC = 0.69). Therefore, the GPML paradigm using multimodal MRI data containing DTI modality has promising result towards detection of the FCD lesions and provides an effective direction for future researches.

      Keywords

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      References

        • Bernasconi A.
        • Bernasconi N.
        • Bernhardt B.C.
        • Schrader D.
        Advances in MRI for ‘cryptogenic’ epilepsies.
        Nat Rev Neurol. 2011; 7: 99-108
        • Lerner J.T.
        • Salamon N.
        • Hauptman J.S.
        • Velasco T.R.
        • Hemb M.
        • Wu J.Y.
        • et al.
        Assessment and surgical outcomes for mild type I and severe type II cortical dysplasia: a critical review and the UCLA experience.
        Epilepsia. 2009; 50: 1310-1335
        • Kuzniecky R.I.
        • Barkovich A.J.
        Malformations of cortical development and epilepsy.
        Brain Dev. 2001; 23: 2-11
        • Engel J.
        • Wiebe S.
        • French J.
        • Sperling M.
        • Williamson P.
        • Spencer D.
        • et al.
        Practice parameter: temporal lobe and localized neocortical resections for epilepsy—report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons.
        Neurology. 2003; 60: 538-547
        • Tellez-Zenteno J.F.
        • Dhar R.
        • Hernandez-Ronquillo L.
        • Wiebe S.
        Long-term outcomes in epilepsy surgery: antiepileptic drugs, mortality, cognitive and psychosocial aspects.
        Brain. 2007; 130: 334-345
        • Cossu M.
        • Lo Russo G.
        • Francione S.
        • Mai R.
        • Nobili L.
        • Sartori I.
        • et al.
        Epilepsy surgery in children: results and predictors of outcome on seizures.
        Epilepsia. 2008; 49: 65-72
        • Mosewich R.K.
        • So E.L.
        • O'Brien T.J.
        • Cascino G.D.
        • Sharbrough F.W.
        • Marsh W.R.
        • et al.
        Factors predictive of the outcome of frontal lobe epilepsy surgery.
        Epilepsia. 2000; 41: 843-849
        • Widdess-Walsh P.
        • Jeha L.
        • Nair D.
        • Kotagal P.
        • Bingaman W.
        • Najm I.
        Subdural electrode analysis in focal cortical dysplasia—predictors of surgical outcome.
        Neurology. 2007; 69: 660-667
        • Jeha L.E.
        • Najm I.
        • Bingaman W.
        • Dinner D.
        • Widdess-Walsh P.
        • Luders H.
        Surgical outcome and prognostic factors of frontal lobe epilepsy surgery.
        Brain. 2007; 130: 574-584
        • Palmini A.
        • Najm I.
        • Avanzini G.
        • Babb T.
        • Guerrini R.
        • Foldvary-Schaefer N.
        • et al.
        Terminology and classification of the cortical dysplasias.
        Neurology. 2004; 62: S2-S8
        • Wagner J.
        • Weber B.
        • Urbach H.
        • Elger C.E.
        • Huppertz H.J.
        Morphometric MRI analysis improves detection of focal cortical dysplasia type II.
        Brain. 2011; 134: 2844-2854
        • Wang Z.I.
        • Alexopoulos A.V.
        • Jones S.E.
        • Jaisani Z.
        • Najm I.M.
        • Prayson R.A.
        The pathology of magnetic-resonance-imaging-negative epilepsy.
        Mod Pathol. 2013; 26: 1051-1058
        • Bernasconi A.
        • Antel S.B.
        • Collins D.L.
        • Bernasconi N.
        • Olivier A.
        • Dubeau F.
        • et al.
        Texture analysis and morphological processing of magnetic resonance imaging assist detection of focal cortical dysplasia in extra-temporal partial epilepsy.
        Ann Neurol. 2001; 49: 770-775
        • Antel S.B.
        • Bernasconi A.
        • Bernasconi N.
        • Collins D.L.
        • Kearney R.E.
        • Shinghal R.
        • et al.
        Computational models of MRI characteristics of focal cortical dysplasia improve lesion detection.
        Neuroimage. 2002; 17: 1755-1760
        • Antel S.B.
        • Collins D.L.
        • Bernasconi N.
        • Andermann F.
        • Shinghal R.
        • Kearney R.E.
        • et al.
        Automated detection of focal cortical dysplasia lesions using computational models of their MRI characteristics and texture analysis.
        Neuroimage. 2003; 19: 1748-1759
        • Thesen T.
        • Quinn B.T.
        • Carlson C.
        • Devinsky O.
        • DuBois J.
        • McDonald C.R.
        • et al.
        Detection of epileptogenic cortical malformations with surface-based MRI morphometry.
        Plos One. 2011; 6: 10
        • Hong S.J.
        • Kim H.
        • Schrader D.
        • Bernasconi N.
        • Bernhardt B.C.
        • Bernasconi A.
        Automated detection of cortical dysplasia type II in MRI-negative epilepsy.
        Neurology. 2014; 83: 48-55
        • Besson P.
        • Bernasconi N.
        • Colliot O.
        • Evans A.
        • Bornasconi A.
        Surface-based texture and morphological analysis detects subtle cortical dysplasia.
        in: Medical image computing and computer-assisted intervention—MICCAI 2008, pt I, proceedings. 5241. 2008: 645 ([-+])
        • Ahmed B.
        • Brodley C.E.
        • Blackmon K.E.
        • Kuzniecky R.
        • Barash G.
        • Carlson C.
        • et al.
        Cortical feature analysis and machine learning improves detection of “MRI-negative” focal cortical dysplasia.
        Epilepsy Behav. 2015; 48: 21-28
        • Adler S.
        • Wagstyl K.
        • Gunny R.
        • Ronan L.
        • Carmichael D.
        • Cross J.H.
        • et al.
        Novel surface features for automated detection of focal cortical dysplasias in paediatric epilepsy.
        Neuroimage Clin. 2017; 14: 18-27
        • Basser P.J.
        • Mattiello J.
        • Lebihan D.
        Mr diffusion tensor spectroscopy and imaging.
        Biophys J. 1994; 66: 259-267
        • Barth P.G.
        Disorders of neuronal migration.
        Can J Neurol Sci. 1987; 14: 1-16
        • Thom M.
        • Harding B.N.
        • Lin W.R.
        • Martinian L.
        • Cross H.
        • Sisodiya S.M.
        Cajal–Retzius cells, inhibitory interneuronal populations and neuropeptide Y expression in focal cortical dysplasia and microdysgenesis.
        Acta Neuropathol. 2003; 105: 561-569
        • Andres M.
        • Andre V.M.
        • Nguyen S.
        • Salamon N.
        • Cepeda C.
        • Levine M.S.
        • et al.
        Human cortical dysplasia and epilepsy: an ontogenetic hypothesis based on volumetric MRI and NeuN neuronal density and size measurements.
        Cereb Cortex. 2005; 15: 194-210
        • Sisodiya S.M.
        • Fauser S.
        • Cross J.H.
        • Thom M.
        Focal cortical dysplasia type II: biological features and clinical perspectives.
        Lancet Neurol. 2009; 8: 830-843
        • Eriksson S.H.
        • Rugg-Gunn E.J.
        • Symms M.R.
        • Barker G.J.
        • Duncan J.S.
        Diffusion tensor imaging in patients with epilepsy and malformations of cortical development.
        Brain. 2001; 124: 617-626
        • Sotak C.H.
        The role of diffusion tensor imaging in the evaluation of ischemic brain injury—a review.
        NMR Biomed. 2002; 15: 561-569
        • Gass A.
        • Niendorf T.
        • Hirsch J.
        Acute and chronic changes of the apparent diffusion coefficient in neurological disorders—biophysical mechanisms and possible underlying histopathology.
        J Neurol Sci. 2001; 186: S15-S23
        • Basser P.J.
        • Pierpaoli C.
        Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI.
        J Magn Reson B. 1996; 111: 209-219
        • Pierpaoli C.
        • Jezzard P.
        • Basser P.J.
        • Barnett A.
        • Di Chiro G.
        Diffusion tensor MR imaging of the human brain.
        Radiology. 1996; 201: 637-648
        • Widjaja E.
        • Blaser S.
        • Miller E.
        • Kassner A.
        • Shannon P.
        • Chuang S.H.
        • et al.
        Evaluation of subcortical white matter and deep white matter tracts in malformations of cortical development.
        Epilepsia. 2007; 48: 1460-1469
        • de la Roque A.D.
        • Oppenheim C.
        • Chassoux F.
        • Rodrigo S.
        • Beuvon F.
        • Daumas-Duport C.
        • et al.
        Diffusion tensor imaging of partial intractable epilepsy.
        Eur Radiol. 2005; 15: 279-285
        • Gross D.W.
        • Bastos A.
        • Beaulieu C.
        Diffusion tensor imaging abnormalities in focal cortical dysplasia.
        Can J Neurol Sci. 2005; 32: 477-482
        • Lee S.K.
        • Kim D.I.
        • Mori S.
        • Kim J.
        • Kim H.D.
        • Heo K.
        • et al.
        Diffusion tensor MRI visualizes decreased subcortical fiber connectivity in focal cortical dysplasia.
        Neuroimage. 2004; 22: 1826-1829
        • Widjaja E.
        • Mahmoodabadi S.Z.
        • Otsubo H.
        • Snead O.C.
        • Holowka S.
        • Bells S.
        • et al.
        Subcortical alterations in tissue microstructure adjacent to focal cortical dysplasia: detection at diffusion-tensor MR imaging by using magnetoencephalographic dipole cluster localization.
        Radiology. 2009; 251: 206-215
        • Guye M.
        • Ranjeva J.P.
        • Bartolomei F.
        • Confort-Gouny S.
        • McGonigal A.
        • Regis J.
        • et al.
        What is the significance of interictal water diffusion changes in frontal lobe epilepsies?.
        Neuroimage. 2007; 35: 28-37
        • Rugg-Gunn F.J.
        • Eriksson S.H.
        • Symms M.R.
        • Barker G.J.
        • Duncan J.S.
        Diffusion tensor imaging of cryptogenic and acquired partial epilepsies.
        Brain. 2001; 124: 627-636
        • Thivard L.
        • Adam C.
        • Hasboun D.
        • Clemenceau S.
        • Dezamis E.
        • Lehericy S.
        • et al.
        Interictal diffusion MRI in partial epilepsies explored with intracerebral electrodes.
        Brain. 2006; 129: 375-385
        • Hong S.-J.
        • Bernhardt B.C.
        • Caldairou B.
        • Hall J.A.
        • Guiot M.C.
        • Schrader D.
        • et al.
        Multimodal MRI profiling of focal cortical dysplasia type II.
        Neurology. 2017; 88: 734-742
        • Japkowicz N.
        • Stephen S.
        The class imbalance problem: a systematic study.
        Intell Data Anal. 2002; 6: 429-449
        • Woolrich M.W.
        • Jbabdi S.
        • Patenaude B.
        • Chappell M.
        • Makni S.
        • Behrens T.
        • et al.
        Bayesian analysis of neuroimaging data in FSL.
        Neuroimage. 2009; 45: S173-S186
        • Greve D.N.
        • Fischl B.
        Accurate and robust brain image alignment using boundary-based registration.
        Neuroimage. 2009; 48: 63-72
        • Zhang Y.Y.
        • Brady M.
        • Smith S.
        Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm.
        IEEE Trans Med Imaging. 2001; 20: 45-57
        • Le Bihan D.
        • Mangin J.F.
        • Poupon C.
        • Clark C.A.
        • Pappata S.
        • Molko N.
        • et al.
        Diffusion tensor imaging: concepts and applications.
        J Magn Reson Imaging. 2001; 13: 534-546
        • Colliot O.
        • Bernasconi N.
        • Khalili N.
        • Antel S.B.
        • Naessens V.
        • Bernasconi A.
        Individual voxel-based analysis of gray matter in focal cortical dysplasia.
        Neuroimage. 2006; 29: 162-171
        • Tuch D.S.
        • Reese T.G.
        • Wiegell M.R.
        • Wedeen V.J.
        Diffusion MRI of complex neural architecture.
        Neuron. 2003; 40: 885-895
        • Tuch D.S.
        • Reese T.G.
        • Wiegell M.R.
        • Makris N.
        • Belliveau J.W.
        • Wedeen V.J.
        High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity.
        Magn Reson Med. 2002; 48: 577-582
        • Behrens T.E.J.
        • Johansen-Berg H.
        • Woolrich M.W.
        • Smith S.M.
        • Wheeler-Kingshott C.A.M.
        • Boulby P.A.
        • et al.
        Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging.
        Nat Neurosci. 2003; 6: 750-757
        • Krsek P.
        • Maton B.
        • Korman B.
        • Pacheco-Jacome E.
        • Jayakar P.
        • Dunoyer C.
        • et al.
        Different features of histopathological subtypes of pediatric focal cortical dysplasia.
        Ann Neurol. 2008; 63: 758-769
        • Lawson J.A.
        • Birchansky S.
        • Pacheco E.
        • Jayakar P.
        • Resnick T.J.
        • Dean P.
        • et al.
        Distinct clinicopathologic subtypes of cortical dysplasia of Taylor.
        Neurology. 2005; 64: 55-61
        • Urbach H.
        • Scheffler B.
        • Heinrichsmeier T.
        • von Oertzen J.
        • Kral T.
        • Wellmer J.
        • et al.
        Focal cortical dysplasia of Taylor's balloon cell type: a clinicopathological entity with characteristic neuroimaging and histopathological features, and favorable postsurgical outcome.
        Epilepsia. 2002; 43: 33-40
        • Matsuda K.
        • Mihara T.
        • Tottori T.
        • Otubo T.
        • Usui N.
        • Baba K.
        • et al.
        Neuroradiologic findings in focal cortical dysplasia: histologic correlation with surgically resected specimens.
        Epilepsia. 2001; 42: 29-36
        • Cohen-Gadol A.A.
        • Ozduman K.
        • Bronen R.A.
        • Kim J.H.
        • Spencer D.D.
        Long-term outcome after epilepsy surgery for focal cortical dysplasia.
        J Neurosurg. 2004; 101: 55-65
        • Colombo N.
        • Tassi L.
        • Galli C.
        • Citterio A.
        • Lo Russo G.
        • Scialfa G.
        • et al.
        Focal cortical dysplasias: MR imaging, histopathologic, and clinical correlations in surgically treated patients with epilepsy.
        Am J Neuroradiol. 2003; 24: 724-733

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