Sulcus-Based MR Analysis of Focal Cortical Dysplasia Located in the Central Region

Objective Focal cortical dysplasias (FCDs) are mainly located in the frontal region, with a particular tropism for the central sulcus. Up to 30% of lesions are undetected (magnetic resonance [MR]-negative FCD patients) or belatedly diagnosed by visual analysis of MR images. We propose an automated sulcus-based method to analyze abnormal sulcal patterns associated with central FCD, taking into account the normal interindividual sulcal variability. Methods We retrospectively studied 29 right-handed patients with FCD in the central region (including 12 MR negative histologically-confirmed cases) and 29 right-handed controls. The analysis of sulcal abnormalities from T1-weighted MR imaging (MRI) was performed using a graph-based representation of the cortical folds and an automated sulci recognition system, providing a new quantitative criterion to describe sulcal patterns, termed sulcus energy. Results Group analysis showed that the central sulcus in the hemisphere ipsilateral to the FCD exhibited an abnormal sulcal pattern compared with controls (p = 0.032). FCDs were associated with abnormal patterns of the central sulci compared with controls (p = 0.006), a result that remained significant when MR-negative and MR-positive patients were considered separately, while the effects of sex, age and MR-field were not significant. At the individual level, sulcus energy alone failed to detect the FCD lesion. We found, however, a significant association between maximum z-scores and the site of FCD (p = 0.0046) which remained significant in MR-negative (p = 0.024) but not in MR-positive patients (p = 0.058). The maximum z-score pointed to an FCD sulcus in four MR-negative and five MR-positive patients. Conclusions We identified abnormal sulcal patterns in patients with FCD of the central region compared with healthy controls. The abnormal sulcal patterns ipsilateral to the FCD and the link between sulcus energy and the FCD location strengthen the interest of sulcal abnormalities in FCD patients.

[1]  P. Merlet,et al.  FDG-PET improves surgical outcome in negative MRI Taylor-type focal cortical dysplasias , 2010, Neurology.

[2]  D. Louis Collins,et al.  Object-based morphometry of the cerebral cortex , 2004, IEEE Transactions on Medical Imaging.

[3]  Paul M. Thompson,et al.  Measuring brain variability by extrapolating sparse tensor fields measured on sulcal lines , 2007, NeuroImage.

[4]  A. Barkovich,et al.  Neuroimaging in disorders of cortical development. , 2004, Neuroimaging clinics of North America.

[5]  K. Kannan,et al.  Focal Cortical Dysplasia (FCD) lesion analysis with complex diffusion approach , 2009, Comput. Medical Imaging Graph..

[6]  Itzhak Fried,et al.  Assessment and surgical outcomes for mild type I and severe type II cortical dysplasia: A critical review and the UCLA experience , 2009, Epilepsia.

[7]  J. Lefévre,et al.  A reaction-diffusion model of the human brain development , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[8]  C. Chung,et al.  Predictors of surgical outcome and pathologic considerations in focal cortical dysplasia , 2009, Neurology.

[9]  Bertrand Devaux,et al.  3T MRI improves the detection of transmantle sign in type 2 focal cortical dysplasia , 2014, Epilepsia.

[10]  Eleonora Aronica,et al.  Detection of human papillomavirus in human focal cortical dysplasia type IIB , 2012, Annals of neurology.

[11]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[12]  Jean-Francois Mangin,et al.  Automatic recognition of cortical sulci of the human brain using a congregation of neural networks , 2002, Medical Image Anal..

[13]  C. Daumas-Duport,et al.  Optimizing MR Imaging Detection of Type 2 Focal Cortical Dysplasia: Best Criteria for Clinical Practice , 2012, American Journal of Neuroradiology.

[14]  A. Razek,et al.  Disorders of Cortical Formation: MR Imaging Features , 2008, American Journal of Neuroradiology.

[15]  Horst Urbach,et al.  Characteristics and surgical outcomes of patients with refractory magnetic resonance imaging-negative epilepsies. , 2009, Archives of neurology.

[16]  Arnaud Cachia,et al.  The power button sign: a newly described central sulcal pattern on surface rendering MR images of type 2 focal cortical dysplasia. , 2015, Radiology.

[17]  H. Huppertz,et al.  Comparison of morphometric analysis based on T1- and T2-weighted MRI data for visualization of focal cortical dysplasia , 2013, Epilepsy Research.

[18]  Hui Zhang,et al.  Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy☆ , 2014, Epilepsy Research.

[19]  D. Louis Collins,et al.  Automated detection of focal cortical dysplasia lesions using computational models of their MRI characteristics and texture analysis , 2003, NeuroImage.

[20]  Orrin Devinsky,et al.  Detection of Epileptogenic Cortical Malformations with Surface-Based MRI Morphometry , 2011, PloS one.

[21]  Eileen Luders,et al.  Gender differences in cortical complexity , 2004, Nature Neuroscience.

[22]  Jean-Francois Mangin,et al.  Cortical sulci recognition and spatial normalization , 2011, Medical Image Anal..

[23]  Jerry L Prince,et al.  Cross-sectional and longitudinal analyses of anatomical sulcal changes associated with aging. , 2005, Cerebral cortex.

[24]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[25]  Jean-Francois Mangin,et al.  The effect of handedness on the shape of the central sulcus , 2012, NeuroImage.

[26]  Nadia Colombo,et al.  Imaging of malformations of cortical development. , 2009, Epileptic disorders : international epilepsy journal with videotape.

[27]  Jan Kassubek,et al.  Detection and Localization of Focal Cortical Dysplasia by Voxel‐based 3‐D MRI Analysis , 2002, Epilepsia.

[28]  Jean-Francois Mangin,et al.  Classification Based on Cortical Folding Patterns , 2007, IEEE Transactions on Medical Imaging.

[29]  R. Kuzniecky,et al.  A developmental and genetic classification for malformations of cortical development: update 2012 , 2012, Brain : a journal of neurology.

[30]  Andrea Bernasconi,et al.  Small focal cortical dysplasia lesions are located at the bottom of a deep sulcus. , 2008, Brain : a journal of neurology.

[31]  Christian E Elger,et al.  Morphometric MRI analysis improves detection of focal cortical dysplasia type II. , 2011, Brain : a journal of neurology.

[32]  Neda Bernasconi,et al.  Automated detection of cortical dysplasia type II in MRI-negative epilepsy , 2014, Neurology.

[33]  Neda Bernasconi,et al.  Individual voxel-based analysis of gray matter in focal cortical dysplasia , 2006, NeuroImage.

[34]  Nadia Colombo,et al.  Focal cortical dysplasia type IIa and IIb: MRI aspects in 118 cases proven by histopathology , 2012, Neuroradiology.

[35]  G. Cosgrove,et al.  Identifying subtle cortical gyral abnormalities as a predictor of focal cortical dysplasia and a cure for epilepsy. , 2012, Archives of neurology.

[36]  Denis Rivière,et al.  Subclinical Abnormal Gyration Pattern, a Potential Anatomic Marker of Epileptogenic Zone in Patients With Magnetic Resonance Imaging–Negative Frontal Lobe Epilepsy , 2011, Neurosurgery.

[37]  G. B. Pike,et al.  Texture analysis and morphological processing of magnetic resonance imaging assist detection of focal cortical dysplasia in extra‐temporal partial epilepsy , 2001, Annals of neurology.

[38]  Y. Burnod,et al.  A morphogenetic model for the development of cortical convolutions. , 2005, Cerebral cortex.

[39]  R. Kuzniecky,et al.  A developmental and genetic classification for malformations of cortical development , 2005, Neurology.

[40]  E. Duchesnay,et al.  A framework to study the cortical folding patterns , 2004, NeuroImage.

[41]  Luiz Eduardo Betting,et al.  White Matter Abnormalities in Patients with Focal Cortical Dysplasia Revealed by Diffusion Tensor Imaging Analysis in a Voxelwise Approach , 2012, Front. Neur..

[42]  D. V. Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system , 1997, Nature.

[43]  R K Fulbright,et al.  Cerebrospinal fluid cleft with cortical dimple: MR imaging marker for focal cortical dysgenesis. , 2000, Radiology.