Particulate matter and episodic memory decline mediated by early neuroanatomic biomarkers of Alzheimer's disease.

Evidence suggests exposure to particulate matter with aerodynamic diameter <2.5 μm (PM2.5) may increase the risk for Alzheimer's disease and related dementias. Whether PM2.5 alters brain structure and accelerates the preclinical neuropsychological processes remains unknown. Early decline of episodic memory is detectable in preclinical Alzheimer's disease. Therefore, we conducted a longitudinal study to examine whether PM2.5 affects the episodic memory decline, and also explored the potential mediating role of increased neuroanatomic risk of Alzheimer's disease associated with exposure. Participants included older females (n = 998; aged 73-87) enrolled in both the Women's Health Initiative Study of Cognitive Aging and the Women's Health Initiative Memory Study of Magnetic Resonance Imaging, with annual (1999-2010) episodic memory assessment by the California Verbal Learning Test, including measures of immediate free recall/new learning (List A Trials 1-3; List B) and delayed free recall (short- and long-delay), and up to two brain scans (MRI-1: 2005-06; MRI-2: 2009-10). Subjects were assigned Alzheimer's disease pattern similarity scores (a brain-MRI measured neuroanatomical risk for Alzheimer's disease), developed by supervised machine learning and validated with data from the Alzheimer's Disease Neuroimaging Initiative. Based on residential histories and environmental data on air monitoring and simulated atmospheric chemistry, we used a spatiotemporal model to estimate 3-year average PM2.5 exposure preceding MRI-1. In multilevel structural equation models, PM2.5 was associated with greater declines in immediate recall and new learning, but no association was found with decline in delayed-recall or composite scores. For each interquartile increment (2.81 μg/m3) of PM2.5, the annual decline rate was significantly accelerated by 19.3% [95% confidence interval (CI) = 1.9% to 36.2%] for Trials 1-3 and 14.8% (4.4% to 24.9%) for List B performance, adjusting for multiple potential confounders. Long-term PM2.5 exposure was associated with increased Alzheimer's disease pattern similarity scores, which accounted for 22.6% (95% CI: 1% to 68.9%) and 10.7% (95% CI: 1.0% to 30.3%) of the total adverse PM2.5 effects on Trials 1-3 and List B, respectively. The observed associations remained after excluding incident cases of dementia and stroke during the follow-up, or further adjusting for small-vessel ischaemic disease volumes. Our findings illustrate the continuum of PM2.5 neurotoxicity that contributes to early decline of immediate free recall/new learning at the preclinical stage, which is mediated by progressive atrophy of grey matter indicative of increased Alzheimer's disease risk, independent of cerebrovascular damage.

[1]  P. Snyder,et al.  Cognitive impairment and decline in cognitively normal older adults with high amyloid-b: A meta-analysis , 2020 .

[2]  B. Dickerson,et al.  Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer's disease , 2019, Neuropsychologia.

[3]  Ying Han,et al.  Trajectories of the Hippocampal Subfields Atrophy in the Alzheimer’s Disease: A Structural Imaging Study , 2019, Front. Neuroinform..

[4]  A. Booth,et al.  Air Pollution and Dementia: A Systematic Review , 2019, Journal of Alzheimer's disease : JAD.

[5]  Theresa M. Harrison,et al.  Longitudinal tau accumulation and atrophy in aging and alzheimer disease , 2019, Annals of neurology.

[6]  Owen Carmichael,et al.  Vascular Burden Score Impacts Cognition Independent of Amyloid PET and MRI Measures of Alzheimer's Disease and Vascular Brain Injury. , 2019, Journal of Alzheimer's disease : JAD.

[7]  Susan M. Resnick,et al.  Using high-dimensional machine learning methods to estimate an anatomical risk factor for Alzheimer's disease across imaging databases , 2018, NeuroImage.

[8]  W. Jagust Imaging the evolution and pathophysiology of Alzheimer disease , 2018, Nature Reviews Neuroscience.

[9]  Reneé C. Wurth,et al.  Fine particle sources and cognitive function in an older Puerto Rican cohort in Greater Boston , 2018, Environmental epidemiology.

[10]  D. Strachan,et al.  Are noise and air pollution related to the incidence of dementia? A cohort study in London, England , 2018, BMJ Open.

[11]  Ramon Casanova,et al.  Trajectories of Relative Performance with 2 Measures of Global Cognitive Function , 2018, Journal of the American Geriatrics Society.

[12]  Hui-ming Li,et al.  Particulate Matter Triggers Depressive-Like Response Associated With Modulation of Inflammatory Cytokine Homeostasis and Brain-Derived Neurotrophic Factor Signaling Pathway in Mice , 2018, Toxicological sciences : an official journal of the Society of Toxicology.

[13]  B. Forsberg,et al.  Association between air pollution from residential wood burning and dementia incidence in a longitudinal study in Northern Sweden , 2018, PloS one.

[14]  The Lancet Neurology Air pollution and brain health: an emerging issue , 2018, The Lancet Neurology.

[15]  C. Jack,et al.  The Association of Long-Term Exposure to Particulate Matter Air Pollution with Brain MRI Findings: The ARIC Study , 2018, Environmental health perspectives.

[16]  Joshua F. Wiley,et al.  MplusAutomation: An R Package for Facilitating Large-Scale Latent Variable Analyses in Mplus , 2018, Structural equation modeling : a multidisciplinary journal.

[17]  Daniel R. Schonhaut,et al.  Tau pathology and neurodegeneration contribute to cognitive impairment in Alzheimer’s disease , 2017, Brain : a journal of neurology.

[18]  B. Forsberg,et al.  Is Long-term Exposure to Air Pollution Associated with Episodic Memory? A Longitudinal Study from Northern Sweden , 2017, Scientific Reports.

[19]  Diesel engine exhaust accelerates plaque formation in a mouse model of Alzheimer’s disease , 2017, Particle and Fibre Toxicology.

[20]  Wei Yan,et al.  NF-κB-regulated microRNA-574-5p underlies synaptic and cognitive impairment in response to atmospheric PM2.5 aspiration , 2017, Particle and Fibre Toxicology.

[21]  Roy W Jones,et al.  On the path to 2025: understanding the Alzheimer’s disease continuum , 2017, Alzheimer's Research & Therapy.

[22]  R. Sacco,et al.  Long-Term Exposure to Ambient Air Pollution and Subclinical Cerebrovascular Disease in NOMAS (the Northern Manhattan Study) , 2017, Stroke.

[23]  T. Morgan,et al.  Traffic-related air pollution impact on mouse brain accelerates myelin and neuritic aging changes with specificity for CA1 neurons , 2017, Neurobiology of Aging.

[24]  Chetwyn C. H. Chan,et al.  PM2.5 Exposure Suppresses Dendritic Maturation in Subgranular Zone in Aged Rats , 2017, Neurotoxicity Research.

[25]  R. Burnett,et al.  Living near major roads and the incidence of dementia, Parkinson's disease, and multiple sclerosis: a population-based cohort study , 2017, The Lancet.

[26]  Emily Underwood,et al.  The polluted brain. , 2017, Science.

[27]  R. Lipton,et al.  Roles of hippocampal subfields in verbal and visual episodic memory , 2017, Behavioural Brain Research.

[28]  S. Resnick,et al.  Particulate air pollutants, APOE alleles and their contributions to cognitive impairment in older women and to amyloidogenesis in experimental models , 2017, Translational Psychiatry.

[29]  P. Snyder,et al.  Cognitive impairment and decline in cognitively normal older adults with high amyloid-β: A meta-analysis , 2016, Alzheimer's & dementia.

[30]  W. Vizuete,et al.  Regionalized PM2.5 Community Multiscale Air Quality model performance evaluation across a continuous spatiotemporal domain. , 2017, Atmospheric environment.

[31]  S. Resnick,et al.  A Voxel-Based Morphometry Study Reveals Local Brain Structural Alterations Associated with Ambient Fine Particles in Older Women , 2016, Front. Hum. Neurosci..

[32]  B. Forsberg,et al.  Traffic-Related Air Pollution and Dementia Incidence in Northern Sweden: A Longitudinal Study , 2015, Environmental health perspectives.

[33]  J. Schwartz,et al.  Fine Particulate Matter, Residential Proximity to Major Roads, and Markers of Small Vessel Disease in a Memory Study Population. , 2016, Journal of Alzheimer's Disease.

[34]  Ramon Casanova,et al.  Ambient air pollution and neurotoxicity on brain structure: Evidence from women's health initiative memory study , 2015, Annals of neurology.

[35]  Colin K. Combs,et al.  A Pilot Study to Assess Effects of Long-Term Inhalation of Airborne Particulate Matter on Early Alzheimer-Like Changes in the Mouse Brain , 2015, PloS one.

[36]  L. Nyberg,et al.  Free Recall Episodic Memory Performance Predicts Dementia Ten Years prior to Clinical Diagnosis: Findings from the Betula Longitudinal Study , 2015, Dementia and Geriatric Cognitive Disorders Extra.

[37]  J. Trojanowski,et al.  Spreading of pathology in neurodegenerative diseases: a focus on human studies , 2015, Nature Reviews Neuroscience.

[38]  Itai Kloog,et al.  Long-Term Exposure to Fine Particulate Matter, Residential Proximity to Major Roads and Measures of Brain Structure , 2014, Stroke.

[39]  B. Hwang,et al.  Ozone, particulate matter, and newly diagnosed Alzheimer's disease: a population-based cohort study in Taiwan. , 2015, Journal of Alzheimer's disease : JAD.

[40]  Susan M. Resnick,et al.  Trajectories of Alzheimer disease-related cognitive measures in a longitudinal sample , 2014, Alzheimer's & Dementia.

[41]  Arno Klein,et al.  Large-scale evaluation of ANTs and FreeSurfer cortical thickness measurements , 2014, NeuroImage.

[42]  S. Beevers,et al.  Traffic-related Air Pollution in Relation to Cognitive Function in Older Adults , 2014, Epidemiology.

[43]  Christos Davatzikos,et al.  Change in brain and lesion volumes after CEE therapies , 2014, Neurology.

[44]  S. Resnick,et al.  Alzheimer's Disease Risk Assessment Using Large-Scale Machine Learning Methods , 2013, PloS one.

[45]  G. Akopian,et al.  Urban air pollutants reduce synaptic function of CA1 neurons via an NMDA/NȮ pathway in vitro , 2013, Journal of neurochemistry.

[46]  Cindee M. Madison,et al.  The aging brain and cognition: contribution of vascular injury and aβ to mild cognitive dysfunction. , 2013, JAMA neurology.

[47]  D. Mungas,et al.  Advanced psychometric analysis and the Alzheimer’s Disease Neuroimaging Initiative: reports from the 2011 Friday Harbor conference , 2012, Brain Imaging and Behavior.

[48]  B. Howard,et al.  Relationship between diabetes risk and admixture in postmenopausal African-American and Hispanic-American women , 2012, Diabetologia.

[49]  Joel Schwartz,et al.  Exposure to particulate air pollution and cognitive decline in older women. , 2011, Archives of internal medicine.

[50]  M. Gallagher,et al.  Episodic Memory on the Path to Alzheimer's Disease This Review Comes from a Themed Issue on Neurobiology of Disease Edited , 2022 .

[51]  Ramon Casanova,et al.  High Dimensional Classification of Structural MRI Alzheimer’s Disease Data Based on Large Scale Regularization , 2011, Front. Neuroinform..

[52]  S. Rajagopalan,et al.  Air pollution impairs cognition, provokes depressive-like behaviors and alters hippocampal cytokine expression and morphology , 2011, Molecular Psychiatry.

[53]  R. Killiany,et al.  Alzheimer-signature MRI biomarker predicts AD dementia in cognitively normal adults , 2011, Neurology.

[54]  Brian B. Avants,et al.  An Open Source Multivariate Framework for n-Tissue Segmentation with Evaluation on Public Data , 2011, Neuroinformatics.

[55]  Bradford C. Dickerson,et al.  Fractionating verbal episodic memory in Alzheimer's disease , 2011, NeuroImage.

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

[57]  Trevor Hastie,et al.  Regularization Paths for Generalized Linear Models via Coordinate Descent. , 2010, Journal of statistical software.

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

[59]  H. Eichenbaum,et al.  The Episodic Memory System: Neurocircuitry and Disorders , 2010, Neuropsychopharmacology.

[60]  R. Castellani,et al.  Alzheimer disease. , 2010, Disease-a-month : DM.

[61]  C Davatzikos,et al.  Postmenopausal hormone therapy and regional brain volumes , 2009, Neurology.

[62]  Jennifer G. Robinson,et al.  Validity of diabetes self-reports in the Women's Health Initiative: comparison with medication inventories and fasting glucose measurements , 2008, Clinical trials.

[63]  Christos Davatzikos,et al.  Computer-assisted Segmentation of White Matter Lesions in 3d Mr Images Using Support Vector Machine 1 , 2022 .

[64]  C. Rock,et al.  Validation of the WHI brief physical activity questionnaire among women diagnosed with breast cancer. , 2007, American journal of health behavior.

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

[66]  C. Kooperberg,et al.  Comparison of self-report, hospital discharge codes, and adjudication of cardiovascular events in the Women's Health Initiative. , 2004, American journal of epidemiology.

[67]  Duanping Liao,et al.  Accuracy and repeatability of commercial geocoding. , 2004, American journal of epidemiology.

[68]  L. Thal,et al.  Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study , 2004, JAMA.

[69]  R. Maronpot,et al.  DNA Damage in Nasal and Brain Tissues of Canines Exposed to Air Pollutants Is Associated with Evidence of Chronic Brain Inflammation and Neurodegeneration , 2003, Toxicologic pathology.

[70]  David P Mackinnon,et al.  Investigation of Mediational Processes Using Parallel Process Latent Growth Curve Modeling , 2003, Structural equation modeling : a multidisciplinary journal.

[71]  S. West,et al.  A comparison of methods to test mediation and other intervening variable effects. , 2002, Psychological methods.

[72]  C D Frith,et al.  The functional roles of prefrontal cortex in episodic memory. II. Retrieval. , 1998, Brain : a journal of neurology.

[73]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.