Accurate and Fully Automatic Hippocampus Segmentation Using Subject-Specific 3D Optimal Local Maps Into a Hybrid Active Contour Model

Assessing the structural integrity of the hippocampus (HC) is an essential step toward prevention, diagnosis, and follow-up of various brain disorders due to the implication of the structural changes of the HC in those disorders. In this respect, the development of automatic segmentation methods that can accurately, reliably, and reproducibly segment the HC has attracted considerable attention over the past decades. This paper presents an innovative 3-D fully automatic method to be used on top of the multiatlas concept for the HC segmentation. The method is based on a subject-specific set of 3-D optimal local maps (OLMs) that locally control the influence of each energy term of a hybrid active contour model (ACM). The complete set of the OLMs for a set of training images is defined simultaneously via an optimization scheme. At the same time, the optimal ACM parameters are also calculated. Therefore, heuristic parameter fine-tuning is not required. Training OLMs are subsequently combined, by applying an extended multiatlas concept, to produce the OLMs that are anatomically more suitable to the test image. The proposed algorithm was tested on three different and publicly available data sets. Its accuracy was compared with that of state-of-the-art methods demonstrating the efficacy and robustness of the proposed method.

[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]  Bennett A Landman,et al.  Non-local statistical label fusion for multi-atlas segmentation , 2013, Medical Image Anal..

[3]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[4]  Anant Madabhushi,et al.  Multifeature Landmark-Free Active Appearance Models: Application to Prostate MRI Segmentation , 2012, IEEE Transactions on Medical Imaging.

[5]  内村 圭一,et al.  Active Appearance Modelを用いた作成表情画像による顔認証 , 2013 .

[6]  Olivier D. Faugeras,et al.  Statistical shape influence in geodesic active contours , 2000, Proceedings IEEE Conference on Computer Vision and Pattern Recognition. CVPR 2000 (Cat. No.PR00662).

[7]  Daniel Rueckert,et al.  LEAP: Learning embeddings for atlas propagation , 2010, NeuroImage.

[8]  N. Schuff,et al.  Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease , 2001, Journal of neurology, neurosurgery, and psychiatry.

[9]  C R Jack,et al.  MRI-based hippocampal volumetrics: data acquisition, normal ranges, and optimal protocol. , 1995, Magnetic resonance imaging.

[10]  M. Tsolaki,et al.  Correlation of dementia, neuropsychological and MRI findings in multiple sclerosis. , 1994, Dementia.

[11]  D. Mumford,et al.  Optimal approximations by piecewise smooth functions and associated variational problems , 1989 .

[12]  Jia Pei Active Appearance Model , 2010 .

[13]  Nicolas Cherbuin,et al.  Optimal weights for local multi-atlas fusion using supervised learning and dynamic information (SuperDyn): Validation on hippocampus segmentation , 2011, NeuroImage.

[14]  Michaël Sdika,et al.  Combining atlas based segmentation and intensity classification with nearest neighbor transform and accuracy weighted vote , 2010, Medical Image Anal..

[15]  G. Chételat,et al.  Hippocampal subfield volumetry in mild cognitive impairment, Alzheimer's disease and semantic dementia☆ , 2013, NeuroImage: Clinical.

[16]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[17]  Arthur W. Toga,et al.  Defining the human hippocampus in cerebral magnetic resonance images—An overview of current segmentation protocols , 2009, NeuroImage.

[18]  L.-K. Shark,et al.  Medical Image Segmentation Using New Hybrid Level-Set Method , 2008, 2008 Fifth International Conference BioMedical Visualization: Information Visualization in Medical and Biomedical Informatics.

[19]  J. Os,et al.  The size and burden of mental disorders and other disorders of the brain in Europe 2010 , 2011, European Neuropsychopharmacology.

[20]  C. Daumas-Duport,et al.  Dementia in two histologically confirmed cases of multiple sclerosis: one case with isolated dementia and one case associated with psychiatric symptoms. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[21]  D. Louis Collins,et al.  Appearance-based modeling for segmentation of hippocampus and amygdala using multi-contrast MR imaging , 2011, NeuroImage.

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

[23]  Arthur W Toga,et al.  Medial temporal lobe in childhood-onset schizophrenia , 2001, Psychiatry Research: Neuroimaging.

[24]  M. Mallar Chakravarty,et al.  A novel in vivo atlas of human hippocampal subfields using high-resolution 3T magnetic resonance imaging , 2013, NeuroImage.

[25]  Guido Gerig,et al.  Valmet: A New Validation Tool for Assessing and Improving 3D Object Segmentation , 2001, MICCAI.

[26]  Paul M. Thompson,et al.  Regional specificity of hippocampal volume reductions in first-episode schizophrenia , 2004, NeuroImage.

[27]  Olga Veksler,et al.  Fast approximate energy minimization via graph cuts , 2001, Proceedings of the Seventh IEEE International Conference on Computer Vision.

[28]  Theo G. M. van Erp,et al.  A Twin Study of Genetic Contributions to Hippocampal Morphology in Schizophrenia , 2002, Neurobiology of Disease.

[29]  Vladimir Kolmogorov,et al.  An experimental comparison of min-cut/max- flow algorithms for energy minimization in vision , 2001, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[30]  Shiyan Hu,et al.  Validation of appearance-model based segmentation with patch-based refinement on medial temporal lobe structures , 2011 .

[31]  D. Louis Collins,et al.  Nonlocal Patch-Based Label Fusion for Hippocampus Segmentation , 2010, MICCAI.

[32]  A. Toga,et al.  Three-dimensional mapping of temporo-limbic regions and the lateral ventricles in schizophrenia: gender effects , 2001, Biological Psychiatry.

[33]  C. Jack,et al.  Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease , 1997, Neurology.

[34]  James S. Duncan,et al.  Neighbor-constrained segmentation with level set based 3-D deformable models , 2004, IEEE Transactions on Medical Imaging.

[35]  R. Buchanan,et al.  Brain morphology and schizophrenia. A magnetic resonance imaging study of limbic, prefrontal cortex, and caudate structures. , 1992, Archives of general psychiatry.

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

[37]  Vladimir Kolmogorov,et al.  An Experimental Comparison of Min-Cut/Max-Flow Algorithms for Energy Minimization in Vision , 2004, IEEE Trans. Pattern Anal. Mach. Intell..

[38]  Mark Jenkinson,et al.  Evaluation of Hippocampal Segmentation Methods for Healthy and Pathological Subjects , 2010, VCBM.

[39]  Paul A. Yushkevich,et al.  Spatial bias in multi-atlas based segmentation , 2012, 2012 IEEE Conference on Computer Vision and Pattern Recognition.

[40]  Sebastien Ourselin,et al.  Automated hippocampal segmentation in patients with epilepsy: Available free online , 2013, Epilepsia.

[41]  J. Gore,et al.  Amygdala and hippocampal volumes in adolescents and adults with bipolar disorder. , 2003, Archives of general psychiatry.

[42]  Alan C. Evans,et al.  Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. , 2000, Cerebral cortex.

[43]  Rasmus Larsen,et al.  Multi-band modelling of appearance , 2003, Image Vis. Comput..

[44]  N. Decarolis,et al.  Hippocampal neurogenesis as a target for the treatment of mental illness: A critical evaluation , 2010, Neuropharmacology.

[45]  Juha Koikkalainen,et al.  Fast and robust multi-atlas segmentation of brain magnetic resonance images , 2010, NeuroImage.

[46]  J. Lieberman,et al.  Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia , 1990, Psychiatry Research: Neuroimaging.

[47]  Paolo Brambilla,et al.  Limbic changes identified by imaging in bipolar patients , 2008, Current psychiatry reports.

[48]  Nicos Maglaveras,et al.  Hippocampus Segmentation using a Local Prior Model on its Boundary , 2011 .

[49]  D. Louis Collins,et al.  Patch-based segmentation using expert priors: Application to hippocampus and ventricle segmentation , 2011, NeuroImage.

[50]  Stephen M. Smith,et al.  A Bayesian model of shape and appearance for subcortical brain segmentation , 2011, NeuroImage.

[51]  Moo K. Chung,et al.  Robust Atlas-Based Brain Segmentation Using Multi-structure Confidence-Weighted Registration , 2009, MICCAI.

[52]  Nicolette Marshall,et al.  Temporal lobe abnormalities in first-episode psychosis. , 2002, The American journal of psychiatry.

[53]  Ronen Basri,et al.  Prior Knowledge Driven Multiscale Segmentation of Brain MRI , 2007, MICCAI.

[54]  Daniel Rueckert,et al.  Multi-atlas based segmentation of brain images: Atlas selection and its effect on accuracy , 2009, NeuroImage.

[55]  Tony F. Chan,et al.  Active contours without edges , 2001, IEEE Trans. Image Process..

[56]  N C Andreasen,et al.  A new method for the in vivo volumetric measurement of the human hippocampus with high neuroanatomical accuracy , 2000, Hippocampus.

[57]  Satrajit S. Ghosh,et al.  Evaluation of volume-based and surface-based brain image registration methods , 2010, NeuroImage.

[58]  Patricia Desmond,et al.  Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. , 2006, Archives of general psychiatry.

[59]  Jingyu Liu,et al.  A Genome-Wide Association Study Suggests Novel Loci Associated with a Schizophrenia-Related Brain-Based Phenotype , 2013, PloS one.

[60]  Paul M. Thompson,et al.  Atlas-based hippocampus segmentation in Alzheimer's disease and mild cognitive impairment , 2005, NeuroImage.

[61]  C. Jack,et al.  Harmonization of magnetic resonance-based manual hippocampal segmentation: A mandatory step for wide clinical use , 2011, Alzheimer's & Dementia.

[62]  Timothy F. Cootes,et al.  Using parts and geometry models to initialise Active Appearance Models for automated segmentation of 3D medical images , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[63]  C. Mcdonald,et al.  Neurobiological trait abnormalities in bipolar disorder , 2009, Molecular Psychiatry.

[64]  D. Louis Collins,et al.  Towards accurate, automatic segmentation of the hippocampus and amygdala from MRI by augmenting ANIMAL with a template library and label fusion , 2010, NeuroImage.

[65]  John G. Csernansky,et al.  Open Access Series of Imaging Studies (OASIS): Cross-sectional MRI Data in Young, Middle Aged, Nondemented, and Demented Older Adults , 2007, Journal of Cognitive Neuroscience.

[66]  Keith A. Johnson,et al.  Steps to standardization and validation of hippocampal volumetry as a biomarker in clinical trials and diagnostic criterion for Alzheimer’s disease , 2011, Alzheimer's & Dementia.

[67]  Jens C. Pruessner,et al.  Operationalizing protocol differences for EADC-ADNI manual hippocampal segmentation , 2015, Alzheimer's & Dementia.

[68]  Carlos Ortiz-de-Solorzano,et al.  Combination Strategies in Multi-Atlas Image Segmentation: Application to Brain MR Data , 2009, IEEE Transactions on Medical Imaging.

[69]  D. Louis Collins,et al.  Joint level-set shape modeling and appearance modeling for brain structure segmentation , 2007, NeuroImage.

[70]  Nicos Maglaveras,et al.  Hippocampus segmentation by optimizing the local contribution of image and prior terms, through graph cuts and multi-atlas , 2012, 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI).

[71]  Ronald Fedkiw,et al.  Level set methods and dynamic implicit surfaces , 2002, Applied mathematical sciences.

[72]  Timothy F. Cootes,et al.  Interpreting face images using active appearance models , 1998, Proceedings Third IEEE International Conference on Automatic Face and Gesture Recognition.

[73]  Guillermo Sapiro,et al.  Geodesic Active Contours , 1995, International Journal of Computer Vision.

[74]  Timothy F. Cootes,et al.  Active Shape Models-Their Training and Application , 1995, Comput. Vis. Image Underst..

[75]  Barry Horwitz,et al.  Relation of corpus callosum and hippocampal size to age in nondemented adults with Down's syndrome. , 2003, The American journal of psychiatry.

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

[77]  Timothy F. Cootes,et al.  Active Appearance Models , 1998, ECCV.

[78]  Qualification opinion of low hippocampal volume ( atrophy ) by MRI for use in regulatory clinical trials-in pre-dementia stage of Alzheimer ’ s disease , 2011 .