Discriminative analysis of early-stage Alzheimer’s disease and normal aging with automatic segmentation technique in subcortical gray matter structures: a multicenter in vivo MRI volumetric and DTI study

Background Previous studies have revealed that amyloid depositions exist in not only the hippocampus but in other subcortical gray matter structures as well. Diffusion-tensor imaging (DTI) parameters might be more sensitive measures of early degeneration in Alzheimer’s disease (AD) than conventional magnetic resonance imaging (MRI) techniques. Purpose To evaluate the significance of the volumes and the mean diffusivity (MD) values of subcortical gray matter structures in discrimination between early-stage AD and normal subjects using the Integrated Registration and Segmentation Tool in FMRIB’s Software Library. Material and Methods Fifty-three cases of early-stage AD and 30 normal aging volunteers from two hospitals were scanned with 3D-FSPGRIR and SSSE-EPI sequences using two similar 1.5T MR systems. The mean relative volumes and mean MD values of subcortical gray matter structures were compared between early-stage AD and control groups. Binary logistic regression analysis and receiver-operating characteristic (ROC) curves were applied to assess the diagnostic significance of every structure’s relative volume, MD value, and combination of both. Results The relative volumes of the left hippocampus, right amygdala, bilateral thalamus, right caudate, left putamen, and bilateral pallidum were significantly lower in the early-stage AD group than in the control group (P < 0.05). The MD values of the bilateral hippocampus and pallidum, and of the right thalamus and caudate were significantly elevated in the early-stage AD group (P < 0.05). In binary logistic regression analysis, the relative volume of left hippocampus and age entered the final model of volumetric analysis. The MD values of bilateral hippocampi and pallidums entered the final model of MD analysis. The MD values of bilateral hippocampi and pallidums, and the relative volume of left pallidum, entered the final model of combination analysis. The accuracy of three models was 84.7%, 88.9%, and 93.1%, respectively. Conclusion Pathological changes takes place in the hippocampus and other subcortical gray matter structures in early-stage AD. Diffusive imaging has great diagnostic significance in early-stage AD. The combination of both imaging modalities can lead to better discrimination between early-stage AD and normal aging.

[1]  Scott H Faro,et al.  Diffusion tensor imaging of the hippocampal formation in temporal lobe epilepsy. , 2003, AJNR. American journal of neuroradiology.

[2]  R. Petersen.  Mild cognitive impairment as a diagnostic entity , 2004, Journal of internal medicine.

[3]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease , 1984, Neurology.

[4]  J. Becker,et al.  Differential cortical atrophy in subgroups of mild cognitive impairment. , 2005, Archives of neurology.

[5]  Anders M. Fjell,et al.  Multimodal imaging in mild cognitive impairment: Metabolism, morphometry and diffusion of the temporal–parietal memory network , 2009, NeuroImage.

[6]  Brian Patenaude,et al.  Bayesian statistical models of shape and appearance for subcortical brain segmentation , 2007 .

[7]  R. Coleman,et al.  Neuroimaging and early diagnosis of Alzheimer disease: a look to the future. , 2003, Radiology.

[8]  H. Braak,et al.  Neuropathological stageing of Alzheimer-related changes , 2004, Acta Neuropathologica.

[9]  W. D. Ehmann,et al.  Imbalances of trace elements related to oxidative damage in Alzheimer's disease brain. , 1998, Neurotoxicology.

[10]  Stephen M. Smith,et al.  Accurate, Robust, and Automated Longitudinal and Cross-Sectional Brain Change Analysis , 2002, NeuroImage.

[11]  Majaz Moonis,et al.  Amyloid Deposition Begins in the Striatum of Presenilin-1 Mutation Carriers from Two Unrelated Pedigrees , 2007, The Journal of Neuroscience.

[12]  Shu-Wei Sun,et al.  Detection of age-dependent brain injury in a mouse model of brain amyloidosis associated with Alzheimer's disease using magnetic resonance diffusion tensor imaging , 2005, Experimental Neurology.

[13]  J. Baron,et al.  In Vivo Mapping of Gray Matter Loss with Voxel-Based Morphometry in Mild Alzheimer's Disease , 2001, NeuroImage.

[14]  Y. Zou,et al.  Diffusion tensor imaging of the brain in patients with Alzheimer’s disease and cerebrovascular lesions , 2007, Journal of Zhejiang University SCIENCE B.

[15]  Matthias J. Müller,et al.  Ultrastructural Hippocampal and White Matter Alterations in Mild Cognitive Impairment: A Diffusion Tensor Imaging Study , 2004, Dementia and Geriatric Cognitive Disorders.

[16]  C. Jack,et al.  Mild cognitive impairment and Alzheimer disease: regional diffusivity of water. , 2001, Radiology.

[17]  H. Soininen,et al.  Volumes of hippocampus, amygdala and frontal lobes in the MRI-based diagnosis of early Alzheimer's disease: Correlation with memory functions , 1995, Journal of neural transmission. Parkinson's disease and dementia section.

[18]  M. Ball,et al.  Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia , 1977, Acta Neuropathologica.

[19]  Jim Mintz,et al.  Brain ferritin iron as a risk factor for age at onset in neurodegenerative diseases , 2005, Alzheimer's & Dementia.

[20]  A. Levey,et al.  Alterations in Cortical Thickness and White Matter Integrity in Mild Cognitive Impairment Measured by Whole-Brain Cortical Thickness Mapping and Diffusion Tensor Imaging , 2009, American Journal of Neuroradiology.

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

[22]  Rossana Ganzola,et al.  Mapping local hippocampal changes in Alzheimer's disease and normal ageing with MRI at 3 Tesla. , 2008, Brain : a journal of neurology.

[23]  J. Morris,et al.  Amygdala atrophy is prominent in early Alzheimer's disease and relates to symptom severity , 2011, Psychiatry Research: Neuroimaging.

[24]  J B Poline,et al.  Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. , 2007, Brain : a journal of neurology.

[25]  P. Scheltens,et al.  Early diagnostic indices for the prevention of Alzheimer's disease. , 1998, Annals of medicine.

[26]  J. Baron,et al.  Mapping gray matter loss with voxel-based morphometry in mild cognitive impairment , 2002, Neuroreport.

[27]  Yong He,et al.  Discriminative analysis of early Alzheimer's disease using multi-modal imaging and multi-level characterization with multi-classifier (M3) , 2012, NeuroImage.

[28]  B. Dubois,et al.  Is the HM story only a ‘remote memory’? Some facts about hippocampus and memory in humans , 2001, Behavioural Brain Research.

[29]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[30]  I. Veer,et al.  Strongly reduced volumes of putamen and thalamus in Alzheimer's disease: an MRI study , 2008, Brain : a journal of neurology.

[31]  S. Lehéricy,et al.  Cholinergic neuronal loss in the globus pallidus of Alzheimer disease patients , 1991, Neuroscience Letters.

[32]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[33]  Zhengyang Zhou,et al.  Evaluation of apparent diffusion coefficient mappings in amnestic mild cognitive impairment using an image analysis software brain search , 2011, Acta radiologica.

[34]  Sang Won Seo,et al.  Volume reduction in subcortical regions according to severity of Alzheimer’s disease , 2011, Journal of Neurology.

[35]  I. McKeith,et al.  MRI Study of Caudate Nucleus Volume in Parkinson’s Disease with and without Dementia with Lewy Bodies and Alzheimer’s Disease , 2003, Dementia and Geriatric Cognitive Disorders.

[36]  Dong Young Lee,et al.  Discrimination of normal aging, MCI and AD with multimodal imaging measures on the medial temporal lobe , 2010, Psychiatry Research: Neuroimaging.

[37]  Maija Pihlajamäki,et al.  Structural and functional MRI in mild cognitive impairment. , 2009, Current Alzheimer research.

[38]  H. Braak,et al.  Alzheimer's Disease: Striatal Amyloid Deposits and Neurofibrillary Changes , 1990, Journal of neuropathology and experimental neurology.