Multimodal Hippocampal Subfield Grading For Alzheimer’s Disease Classification

Numerous studies have proposed biomarkers based on magnetic resonance imaging (MRI) to detect and predict the risk of evolution toward Alzheimer’s disease (AD). While anatomical MRI captures structural alterations, studies demonstrated the ability of diffusion MRI to capture microstructural modifications at an earlier stage. Several methods have focused on hippocampus structure to detect AD. To date, the patch-based grading framework provides the best biomarker based on the hippocampus. However, this structure is complex since the hippocampus is divided into several heterogeneous subfields not equally impacted by AD. Former in-vivo imaging studies only investigated structural alterations of these subfields using volumetric measurements and microstructural modifications with mean diffusivity measurements. The aim of our work is to study the efficiency of hippocampal subfields compared to the whole hippocampus structure with a multimodal patch-based framework that enables to capture subtler structural and microstructural alterations. To this end, we analyze the significance of the different hippocampal subfields for AD diagnosis and prognosis with volumetric, diffusivity measurements and a novel multimodal patch-based grading framework that combines structural and diffusion MRI. The experiments conducted in this work showed that the whole hippocampus provides the most discriminant biomarkers for advanced AD detection while biomarkers applied into subiculum obtain the best results for AD prediction, improving by 2% the accuracy compared to the whole hippocampus.

[1]  Igor Yakushev,et al.  Diffusion tensor imaging of the hippocampus in MCI and early Alzheimer's disease. , 2011, Journal of Alzheimer's disease : JAD.

[2]  C. Jack,et al.  Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging☆ , 2013, NeuroImage: Clinical.

[3]  Martha Brumfield,et al.  Coalition Against Major Diseases/European Medicines Agency biomarker qualification of hippocampal volume for enrichment of clinical trials in predementia stages of Alzheimer's disease , 2014, Alzheimer's & Dementia.

[4]  N. Schuff,et al.  Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T , 2007, Neurobiology of Aging.

[5]  Karl J. Friston,et al.  Automatic Differentiation of Anatomical Patterns in the Human Brain: Validation with Studies of Degenerative Dementias , 2002, NeuroImage.

[6]  G. Kerchner,et al.  Hippocampal CA1 apical neuropil atrophy in mild Alzheimer disease visualized with 7-T MRI , 2010, Neurology.

[7]  H. Braak,et al.  Staging of alzheimer's disease-related neurofibrillary changes , 1995, Neurobiology of Aging.

[8]  K. Kaida,et al.  Alzheimer's disease with asymmetric parietal lobe atrophy: A case report , 1998, Journal of the Neurological Sciences.

[9]  A. Gutiérrez,et al.  Early neuronal loss and axonal/presynaptic damage is associated with accelerated amyloid-β accumulation in AβPP/PS1 Alzheimer's disease mice subiculum. , 2014, Journal of Alzheimer's disease : JAD.

[10]  H. Keselman,et al.  Multiple Comparison Procedures , 2005 .

[11]  Shantanu H. Joshi,et al.  Brain connectivity and novel network measures for Alzheimer's disease classification , 2015, Neurobiology of Aging.

[12]  Takashi Asada,et al.  Voxel-based morphometry to discriminate early Alzheimer's disease from controls , 2005, Neuroscience Letters.

[13]  Vince D. Calhoun,et al.  Single subject prediction of brain disorders in neuroimaging: Promises and pitfalls , 2017, NeuroImage.

[14]  Juha Koikkalainen,et al.  Differential diagnosis of neurodegenerative diseases using structural MRI data , 2016, NeuroImage: Clinical.

[15]  Nick C. Fox,et al.  Global and local gray matter loss in mild cognitive impairment and Alzheimer's disease , 2004, NeuroImage.

[16]  Daoqiang Zhang,et al.  Ensemble sparse classification of Alzheimer's disease , 2012, NeuroImage.

[17]  M. Filippi,et al.  Robust Automated Detection of Microstructural White Matter Degeneration in Alzheimer’s Disease Using Machine Learning Classification of Multicenter DTI Data , 2013, PloS one.

[18]  Manojkumar Saranathan,et al.  Hippocampal CA1 apical neuropil atrophy and memory performance in Alzheimer's disease , 2012, NeuroImage.

[19]  Daniel Rueckert,et al.  Multiple instance learning for classification of dementia in brain MRI , 2013, Medical Image Anal..

[20]  S. Rose,et al.  Gray and white matter changes in Alzheimer's disease: A diffusion tensor imaging study , 2008, Journal of magnetic resonance imaging : JMRI.

[21]  D. Louis Collins,et al.  An Optimized PatchMatch for multi-scale and multi-feature label fusion , 2016, NeuroImage.

[22]  Kiralee M. Hayashi,et al.  Conversion of mild cognitive impairment to Alzheimer disease predicted by hippocampal atrophy maps. , 2006, Archives of neurology.

[23]  C. Jack,et al.  DWI predicts future progression to Alzheimer disease in amnestic mild cognitive impairment , 2005, Neurology.

[24]  G. Busatto,et al.  Neurostructural predictors of Alzheimer's disease: A meta-analysis of VBM studies , 2011, Neurobiology of Aging.

[25]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  A. Nappi,et al.  Alzheimer ' s Disease : Cell-Specific Pathology Isolates the Hippocampal Formation , 2022 .

[27]  Yadi Li,et al.  Discriminative Analysis of Mild Alzheimer’s Disease and Normal Aging Using Volume of Hippocampal Subfields and Hippocampal Mean Diffusivity , 2013, American journal of Alzheimer's disease and other dementias.

[28]  U. Rüb,et al.  Alzheimer-Related τ-Pathology in the Perforant Path Target Zone and in the Hippocampal Stratum Oriens and Radiatum Correlates with Onset and Degree of Dementia , 2000, Experimental Neurology.

[29]  Shantanu H. Joshi,et al.  Diffusion weighted imaging-based maximum density path analysis and classification of Alzheimer's disease , 2015, Neurobiology of Aging.

[30]  Pierrick Coupé,et al.  High Resolution Hippocampus Subfield Segmentation Using Multispectral Multiatlas Patch-Based Label Fusion , 2016, Patch-MI@MICCAI.

[31]  D. Louis Collins,et al.  Nonlocal Intracranial Cavity Extraction , 2014, Int. J. Biomed. Imaging.

[32]  Pierrick Coupé,et al.  NICE: Non-local Intracranial Cavity Extraction , 2014 .

[33]  A. Tamhane,et al.  Multiple Comparison Procedures , 1989 .

[34]  Nick C Fox,et al.  The Alzheimer's disease neuroimaging initiative (ADNI): MRI methods , 2008, Journal of magnetic resonance imaging : JMRI.

[35]  Paul M. Thompson,et al.  Diffusion tensor imaging in seven minutes: Determining trade-offs between spatial and directional resolution , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[36]  H. Braak,et al.  Alzheimer’s disease: transiently developing dendritic changes in pyramidal cells of sector CA1 of the Ammon’s horn , 1997, Acta Neuropathologica.

[37]  Pierrick Coupé,et al.  volBrain: An Online MRI Brain Volumetry System , 2015, Front. Neuroinform..

[38]  Pierrick Coupé,et al.  Patch-Based DTI Grading: Application to Alzheimer's Disease Classification , 2016, Patch-MI@MICCAI.

[39]  D. Rueckert,et al.  Multi-Method Analysis of MRI Images in Early Diagnostics of Alzheimer's Disease , 2011, PloS one.

[40]  N. Amoroso,et al.  DTI measurements for Alzheimer’s classification , 2017, Physics in medicine and biology.

[41]  D. Prvulovic,et al.  Using Support Vector Machines with Multiple Indices of Diffusion for Automated Classification of Mild Cognitive Impairment , 2012, PloS one.

[42]  Adam Finkelstein,et al.  PatchMatch: a randomized correspondence algorithm for structural image editing , 2009, SIGGRAPH 2009.

[43]  J. Morris,et al.  Current concepts in mild cognitive impairment. , 2001, Archives of neurology.

[44]  J. Dukart,et al.  Age Correction in Dementia – Matching to a Healthy Brain , 2011, PloS one.

[45]  Thomas Kirste,et al.  Predicting Prodromal Alzheimer's Disease in Subjects with Mild Cognitive Impairment Using Machine Learning Classification of Multimodal Multicenter Diffusion‐Tensor and Magnetic Resonance Imaging Data , 2015, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[46]  D. Louis Collins,et al.  Diffusion Weighted Image Denoising Using Overcomplete Local PCA , 2013, PloS one.

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

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

[49]  Jean-François Aujol,et al.  Adaptive Regularization of the NL-Means: Application to Image and Video Denoising , 2014, IEEE Transactions on Image Processing.

[50]  Daniel Rueckert,et al.  A Novel Grading Biomarker for the Prediction of Conversion From Mild Cognitive Impairment to Alzheimer's Disease , 2017, IEEE Transactions on Biomedical Engineering.

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

[52]  H. Braak,et al.  Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry , 2006, Acta Neuropathologica.

[53]  Daoqiang Zhang,et al.  Identification of MCI individuals using structural and functional connectivity networks , 2012, NeuroImage.

[54]  J. Troncoso,et al.  Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease , 1994, The Lancet.

[55]  Pierrick Coupé,et al.  Author manuscript, published in "Journal of Magnetic Resonance Imaging 2010;31(1):192-203" DOI: 10.1002/jmri.22003 Adaptive Non-Local Means Denoising of MR Images with Spatially Varying Noise Levels , 2010 .

[56]  J. Morris,et al.  Clinical core of the Alzheimer's disease neuroimaging initiative: Progress and plans , 2010, Alzheimer's & Dementia.

[57]  Vladimir Fonov,et al.  Standardized evaluation of algorithms for computer-aided diagnosis of dementia based on structural MRI: The CADDementia challenge , 2015, NeuroImage.

[58]  Tao Liu,et al.  Automated detection of amnestic mild cognitive impairment in community-dwelling elderly adults: A combined spatial atrophy and white matter alteration approach , 2012, NeuroImage.

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

[60]  Nick C Fox,et al.  Normalization of cerebral volumes by use of intracranial volume: implications for longitudinal quantitative MR imaging. , 2001, AJNR. American journal of neuroradiology.

[61]  J. Morris,et al.  Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease , 1996, The Journal of Neuroscience.

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

[63]  C. Igel,et al.  Differential diagnosis of mild cognitive impairment and Alzheimer's disease using structural MRI cortical thickness, hippocampal shape, hippocampal texture, and volumetry* , 2016, NeuroImage: Clinical.

[64]  Maxime Descoteaux,et al.  Collaborative patch-based super-resolution for diffusion-weighted images , 2013, NeuroImage.

[65]  Wiro J Niessen,et al.  Hippocampal shape is predictive for the development of dementia in a normal, elderly population , 2014, Human brain mapping.

[66]  Nick C Fox,et al.  Automatic classification of MR scans in Alzheimer's disease. , 2008, Brain : a journal of neurology.

[67]  D. Collins,et al.  Scoring by nonlocal image patch estimator for early detection of Alzheimer's disease☆ , 2012, NeuroImage: Clinical.

[68]  Nick C Fox,et al.  The clinical use of structural MRI in Alzheimer disease , 2010, Nature Reviews Neurology.

[69]  Pierrick Coupé,et al.  HIPS: A new hippocampus subfield segmentation method , 2017, NeuroImage.

[70]  Hilkka Soininen,et al.  Diffusion tensor imaging and Tract-Based Spatial Statistics in Alzheimer's disease and mild cognitive impairment , 2011, Neurobiology of Aging.

[71]  Peter Stoeter,et al.  Functional implications of hippocampal volume and diffusivity in mild cognitive impairment , 2005, NeuroImage.

[72]  Fei Gao,et al.  Discriminative analysis of multivariate features from structural MRI and diffusion tensor images. , 2014, Magnetic resonance imaging.

[73]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[74]  M. Mallar Chakravarty,et al.  Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol , 2015, NeuroImage.

[75]  Carlo Caltagirone,et al.  Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease , 2015, Alzheimer's & dementia.

[76]  Qing X. Yang,et al.  Interhemispheric Functional and Structural Disconnection in Alzheimer’s Disease: A Combined Resting-State fMRI and DTI Study , 2015, PloS one.

[77]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[78]  K Patterson,et al.  Progressive biparietal atrophy: an atypical presentation of Alzheimer's disease. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[79]  Marie Chupin,et al.  Multidimensional classification of hippocampal shape features discriminates Alzheimer's disease and mild cognitive impairment from normal aging , 2009, NeuroImage.

[80]  Michèle Allard,et al.  Detection of Alzheimer's disease signature in MR images seven years before conversion to dementia: Toward an early individual prognosis , 2015, Human brain mapping.

[81]  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.

[82]  Paul M. Thompson,et al.  Hippocampal shape analysis in Alzheimer’s disease: A population-based study , 2007, NeuroImage.

[83]  Vladimir Fonov,et al.  Prediction of Alzheimer's disease in subjects with mild cognitive impairment from the ADNI cohort using patterns of cortical thinning , 2013, NeuroImage.

[84]  Matthias J. Müller,et al.  Predicting conversion to dementia in mild cognitive impairment by volumetric and diffusivity measurements of the hippocampus , 2006, Psychiatry Research: Neuroimaging.

[85]  C. Jack,et al.  Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade , 2010, The Lancet Neurology.

[86]  C. Jack,et al.  MR‐based hippocampal volumetry in the diagnosis of Alzheimer's disease , 1992, Neurology.

[87]  Maxime Descoteaux,et al.  Dipy, a library for the analysis of diffusion MRI data , 2014, Front. Neuroinform..