Robust skull stripping using multiple MR image contrasts insensitive to pathology

Abstract Automatic skull‐stripping or brain extraction of magnetic resonance (MR) images is often a fundamental step in many neuroimage processing pipelines. The accuracy of subsequent image processing relies on the accuracy of the skull‐stripping. Although many automated stripping methods have been proposed in the past, it is still an active area of research particularly in the context of brain pathology. Most stripping methods are validated on T1‐w MR images of normal brains, especially because high resolution T1‐w sequences are widely acquired and ground truth manual brain mask segmentations are publicly available for normal brains. However, different MR acquisition protocols can provide complementary information about the brain tissues, which can be exploited for better distinction between brain, cerebrospinal fluid, and unwanted tissues such as skull, dura, marrow, or fat. This is especially true in the presence of pathology, where hemorrhages or other types of lesions can have similar intensities as skull in a T1‐w image. In this paper, we propose a sparse patch based Multi‐cONtrast brain STRipping method (MONSTR),2 where non‐local patch information from one or more atlases, which contain multiple MR sequences and reference delineations of brain masks, are combined to generate a target brain mask. We compared MONSTR with four state‐of‐the‐art, publicly available methods: BEaST, SPECTRE, ROBEX, and OptiBET. We evaluated the performance of these methods on 6 datasets consisting of both healthy subjects and patients with various pathologies. Three datasets (ADNI, MRBrainS, NAMIC) are publicly available, consisting of 44 healthy volunteers and 10 patients with schizophrenia. Other three in‐house datasets, comprising 87 subjects in total, consisted of patients with mild to severe traumatic brain injury, brain tumors, and various movement disorders. A combination of T1‐w, T2‐w were used to skull‐strip these datasets. We show significant improvement in stripping over the competing methods on both healthy and pathological brains. We also show that our multi‐contrast framework is robust and maintains accurate performance across different types of acquisitions and scanners, even when using normal brains as atlases to strip pathological brains, demonstrating that our algorithm is applicable even when reference segmentations of pathological brains are not available to be used as atlases. HighlightsA novel multi‐contrast patch‐based MR brain skullstripping algorithm is proposed.It is validated on 6 datasets, including subjects with traumatic brain injuries and tumors.It outperforms 4 state‐of‐the art methods, both on normal and pathological brains.

[1]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[2]  Snehashis Roy,et al.  Longitudinal Patch-Based Segmentation of Multiple Sclerosis White Matter Lesions , 2015, MLMI.

[3]  Jeffrey N. Chiang,et al.  Optimized Brain Extraction for Pathological Brains (optiBET) , 2014, PloS one.

[4]  Jean-Michel Morel,et al.  A non-local algorithm for image denoising , 2005, 2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR'05).

[5]  Yaozong Gao,et al.  Integration of sparse multi-modality representation and anatomical constraint for isointense infant brain MR image segmentation , 2014, NeuroImage.

[6]  G. Hagemann,et al.  Fast, accurate, and reproducible automatic segmentation of the brain in T1‐weighted volume MRI data , 1999, Magnetic resonance in medicine.

[7]  Arthur W. Toga,et al.  A meta-algorithm for brain extraction in MRI , 2004, NeuroImage.

[8]  Claudio A. Perez,et al.  An accurate skull stripping method based on simplex meshes and histogram analysis for magnetic resonance images , 2012, Journal of Neuroscience Methods.

[9]  Snehashis Roy,et al.  Subject-Specific Sparse Dictionary Learning for Atlas-Based Brain MRI Segmentation , 2015, IEEE Journal of Biomedical and Health Informatics.

[10]  Peter A. Calabresi,et al.  Longitudinal intensity normalization in the presence of multiple sclerosis lesions , 2013, 2013 IEEE 10th International Symposium on Biomedical Imaging.

[11]  Sébastien Ourselin,et al.  Brain MAPS: An automated, accurate and robust brain extraction technique using a template library , 2011, NeuroImage.

[12]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[13]  H. Zou,et al.  Regularization and variable selection via the elastic net , 2005 .

[14]  Olivier Clatz,et al.  Spatial decision forests for MS lesion segmentation in multi-channel magnetic resonance images , 2011, NeuroImage.

[15]  François Rousseau,et al.  Brain Hallucination , 2008, ECCV.

[16]  Snehashis Roy,et al.  Example based lesion segmentation , 2014, Medical Imaging.

[17]  Pierrick Coupé,et al.  Nonlocal regularization for active appearance model: Application to medial temporal lobe segmentation , 2014, Human brain mapping.

[18]  Snehashis Roy,et al.  MR contrast synthesis for lesion segmentation , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[19]  Paul A. Yushkevich,et al.  Multi-atlas segmentation with joint label fusion and corrective learning—an open source implementation , 2013, Front. Neuroinform..

[20]  Colin Studholme,et al.  A Supervised Patch-Based Approach for Human Brain Labeling , 2011, IEEE Transactions on Medical Imaging.

[21]  Dinggang Shen,et al.  Robust Deformable-Surface-Based Skull-Stripping for Large-Scale Studies , 2011, MICCAI.

[22]  Snehashis Roy,et al.  MR image synthesis by contrast learning on neighborhood ensembles , 2015, Medical Image Anal..

[23]  Klaus H. Maier-Hein,et al.  Deep MRI brain extraction: A 3D convolutional neural network for skull stripping , 2016, NeuroImage.

[24]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[25]  Jean Ponce,et al.  Sparse Modeling for Image and Vision Processing , 2014, Found. Trends Comput. Graph. Vis..

[26]  Bilwaj Gaonkar,et al.  Multi-atlas skull-stripping. , 2013, Academic radiology.

[27]  C. Jack,et al.  Alzheimer's Disease Neuroimaging Initiative , 2008 .

[28]  Daniel Rueckert,et al.  Automatic anatomical brain MRI segmentation combining label propagation and decision fusion , 2006, NeuroImage.

[29]  Heinz-Otto Peitgen,et al.  The Skull Stripping Problem in MRI Solved by a Single 3D Watershed Transform , 2000, MICCAI.

[30]  Jerry L Prince,et al.  PET Attenuation Correction Using Synthetic CT from Ultrashort Echo-Time MR Imaging , 2014, The Journal of Nuclear Medicine.

[31]  Guang H. Yue,et al.  Automated Histogram-Based Brain Segmentation in T1-Weighted Three-Dimensional Magnetic Resonance Head Images , 2002, NeuroImage.

[32]  Dinggang Shen,et al.  LABEL: Pediatric brain extraction using learning-based meta-algorithm , 2012, NeuroImage.

[33]  Aaron Carass,et al.  Simple paradigm for extra-cerebral tissue removal: Algorithm and analysis , 2011, NeuroImage.

[34]  Snehashis Roy,et al.  MR to CT registration of brains using image synthesis , 2014, Medical Imaging.

[35]  Amod Jog,et al.  Effects of spatial resolution on image registration , 2016, SPIE Medical Imaging.

[36]  Ben Glocker,et al.  Is Synthesizing MRI Contrast Useful for Inter-modality Analysis? , 2013, MICCAI.

[37]  Snehashis Roy,et al.  Magnetic Resonance Image Example-Based Contrast Synthesis , 2013, IEEE Transactions on Medical Imaging.

[38]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.

[39]  Ninon Burgos,et al.  Attenuation Correction Synthesis for Hybrid PET-MR Scanners: Application to Brain Studies , 2014, IEEE Transactions on Medical Imaging.

[40]  D. Louis Collins,et al.  BEaST: Brain extraction based on nonlocal segmentation technique , 2012, NeuroImage.

[41]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[42]  André J. W. van der Kouwe,et al.  Brain morphometry with multiecho MPRAGE , 2008, NeuroImage.

[43]  Michael W. L. Chee,et al.  Skull stripping using graph cuts , 2010, NeuroImage.

[44]  David A. Rottenberg,et al.  Putting our heads together: a consensus approach to brain/non-brain segmentation in T1-weighted MR volumes , 2004, NeuroImage.

[45]  Mark Meyer,et al.  Implicit fairing of irregular meshes using diffusion and curvature flow , 1999, SIGGRAPH.

[46]  Jennifer L. Whitwell,et al.  Accurate automatic estimation of total intracranial volume: A nuisance variable with less nuisance , 2015, NeuroImage.

[47]  Amir Alansary,et al.  MRBrainS Challenge: Online Evaluation Framework for Brain Image Segmentation in 3T MRI Scans , 2015, Comput. Intell. Neurosci..

[48]  Marleen de Bruijne,et al.  Why Does Synthesized Data Improve Multi-sequence Classification? , 2015, MICCAI.

[49]  Henry Rusinek,et al.  Fully automatic segmentation of the brain from T1‐weighted MRI using Bridge Burner algorithm , 2008, Journal of magnetic resonance imaging : JMRI.

[50]  Snehashis Roy,et al.  Pulse sequence based multi-acquisition MR intensity normalization , 2013, Medical Imaging.

[51]  Aaron Carass,et al.  A JOINT REGISTRATION AND SEGMENTATION APPROACH TO SKULL STRIPPING , 2007, 2007 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[52]  D. Louis Collins,et al.  Simultaneous segmentation and grading of anatomical structures for patient's classification: Application to Alzheimer's disease , 2012, NeuroImage.

[53]  Snehashis Roy,et al.  Synthesizing MR contrast and resolution through a patch matching technique , 2010, Medical Imaging.

[54]  Paul A. Yushkevich,et al.  Multi-Atlas Segmentation with Joint Label Fusion , 2013, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[55]  Chulhee Lee,et al.  Skull stripping based on region growing for magnetic resonance brain images , 2009, NeuroImage.

[56]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[57]  Jyrki Lötjönen,et al.  Robust whole-brain segmentation: Application to traumatic brain injury , 2015, Medical Image Anal..

[58]  Jerry L. Prince,et al.  Adaptive fuzzy segmentation of magnetic resonance images , 1999, IEEE Transactions on Medical Imaging.

[59]  David A. Rottenberg,et al.  Quantitative comparison of four brain extraction algorithms , 2004, NeuroImage.

[60]  D. Louis Collins,et al.  MRI Superresolution Using Self-Similarity and Image Priors , 2010, Int. J. Biomed. Imaging.

[61]  D. Donoho For most large underdetermined systems of equations, the minimal 𝓁1‐norm near‐solution approximates the sparsest near‐solution , 2006 .

[62]  William M. Wells,et al.  Simultaneous truth and performance level estimation (STAPLE): an algorithm for the validation of image segmentation , 2004, IEEE Transactions on Medical Imaging.

[63]  Alex Rovira,et al.  MARGA: Multispectral Adaptive Region Growing Algorithm for brain extraction on axial MRI , 2014, Comput. Methods Programs Biomed..

[64]  Ahmed Serag,et al.  Accurate Learning with Few Atlases (ALFA): an algorithm for MRI neonatal brain extraction and comparison with 11 publicly available methods , 2016, Scientific Reports.

[65]  Victoria Arango,et al.  Computerized Three-Dimensional Reconstruction Reveals Cerebrovascular Regulatory Subregions in Rat Brain Stem , 1993, NeuroImage.

[66]  D. Selkoe Alzheimer's disease. , 2011, Cold Spring Harbor perspectives in biology.

[67]  D. Louis Collins,et al.  Rotation-invariant multi-contrast non-local means for MS lesion segmentation , 2015, NeuroImage: Clinical.

[68]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[69]  R. Leahy,et al.  Magnetic Resonance Image Tissue Classification Using a Partial Volume Model , 2001, NeuroImage.

[70]  Arthur W. Toga,et al.  Skull-stripping magnetic resonance brain images using a model-based level set , 2006, NeuroImage.

[71]  Paul M. Thompson,et al.  Robust Brain Extraction Across Datasets and Comparison With Publicly Available Methods , 2011, IEEE Transactions on Medical Imaging.