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Apolipoprotein E ε4 allele, AD pathology, and the clinical expression of Alzheimer’s disease
Abstract
Objective To test the hypothesis that the APOE epsilon4 allele is associated with the clinical manifestations of AD through an association with the pathologic hallmarks of disease. Methods Participants were older Catholic nuns, priests, and brothers who agreed to annual neurologic and neuropsychological evaluation for AD and other common neurologic conditions and brain autopsy at the time of death. There were 77 persons without dementia and 51 with probable AD; 38 participants had one or more epsilon4 alleles. Results In logistic regression analyses, controlling for age, sex, and education, the epsilon4 allele was strongly associated with the likelihood of clinical AD (odds = 3.46, 95% CI = 1.44 to 8.33). However, controlling for the effect of AD pathology, the association of the epsilon allele with clinical AD was reduced by >50% and was no longer significant (odds = 1.58, 95% CI = 0.56 to 4.43). Similarly, in linear regression analyses, controlling for age, sex, and education, the epsilon4 allele was strongly associated with level of cognitive function proximate to death (regression coefficient = -0.477, p = 0.005). However, after controlling for the effect of AD pathology, the association of the epsilon4 allele with level of cognition was reduced by >80% and was no longer significant (regression coefficient = -0.093). Similar results were found in analyses using separate measures of neuritic plaques, diffuse plaques, and neurofibrillary tangles, and in analyses of five dif…
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“In our previous study, we found that the inter-rater reliability of the counts of AD pathologic indices were from 0.89 to 0.93, supporting reproducibility of these measures [13].”
From Sex differences in Alzheimer’s disease and common neuropathologies of aging (2018) · cites this paper as [13]
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“In our previous study, we showed that the regional standardized scores were highly correlated with the global AD pathology score (r range: 0.47–0.73, median r = 0.67) and the Chronbach α coefficient was 0.90, indicating high internal consistency and supporting use of the global AD pathology score [13].”
From Sex differences in Alzheimer’s disease and common neuropathologies of aging (2018) · cites this paper as [13]
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Apolipoprotein E: Implications for AD neurobiology, epidemiology and risk assessment
Schipper, H. M. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.04.021 · Cited by 113
Cognitive reserve, presynaptic proteins, and dementia in the elderly
Honer, W. G., Barr, A. M., Sawada, K., Thornton, A. E., Morris, M. C., Leurgans, S. E., Schneider, J. A., & Bennett, D. A. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.38 · Cited by 100
Self-citationArvanitakis, Z., Fleischman, D. A., Arfanakis, K., Leurgans, S. E., Barnes, L. L., & Bennett, D. A. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1034-7 · Cited by 104
Self-citationAmyloid mediates the association of apolipoprotein E e4 allele to cognitive function in older people
Bennett, D. A. (2005) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.2004.054445 · Cited by 99
Self-citationWang, H., Gustafson, D., Kivipelto, M., Pedersen, N. L., Skoog, I. G., Windblad, B., & Fratiglioni, L. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.10.003 · Cited by 104
Kaneshwaran, K., Olah, M., Tasaki, S., Yu, L., Bradshaw, E. M., Schneider, J. A., Buchman, A. S., Bennett, D. A., Jager, P. L. D., & Lim, A. S. P. (2019) · Science Advances · doi:10.1126/sciadv.aax7331 · Cited by 107
Self-citationGenetic Heterogeneity in Alzheimer Disease and Implications for Treatment Strategies
Dominantly Inherited Alzheimer Network, Ringman, J. M., Goate, A., Masters, C. L., Cairns, N. J., Danek, A., Graff-Radford, N., Ghetti, B., & Morris, J. C. (2014) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-014-0499-8 · Cited by 96
den Heijer, T., Vermeer, S. E., van Dijk, E. J., Prins, N. D., Koudstaal, P. J., van Duijn, C. M., Albert Hofman, D., & Breteler, M. M. B. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.4.992 · Cited by 96
Tremblay, C., St‐Amour, I., Schneider, J. A., Bennett, D. A., & Calon, F. (2011) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31822c62cf · Cited by 98
Self-citationSchneider, J. A., Bienias, J. L., Wilson, R. S., Berry‐Kravis, E., Evans, D. A., & Bennett, D. A. (2005) · Stroke · doi:10.1161/01.str.0000160747.27470.2a · Cited by 96
Self-citationNeuropathologic intermediate phenotypes enhance association to Alzheimer susceptibility alleles
Bennett, D. A., De Jager, P. L., Leurgans, S. E., & Schneider, J. A. (2009) · Neurology · doi:10.1212/wnl.0b013e3181a2e87d · Cited by 93
Self-citationSleep fragmentation and Parkinson's disease pathology in older adults without Parkinson's disease
Sohail, S., Yu, L., Schneider, J. A., Bennett, D. A., Buchman, A. S., & Lim, A. S. P. (2017) · Movement Disorders · doi:10.1002/mds.27200 · Cited by 97
Self-citationMIND Diet, Common Brain Pathologies, and Cognition in Community-Dwelling Older Adults
Dhana, K., James, B. D., Agarwal, P., Aggarwal, N. T., Cherian, L. J., Leurgans, S. E., Barnes, L. L., Bennett, D. A., & Schneider, J. A. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210107 · Cited by 98
Self-citationYuan, C., Chen, H., Wang, Y., Schneider, J. A., Willett, W. C., & Morris, M. C. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa303 · Cited by 94
Self-citationA coding variant in CR1 interacts with APOE-ɛ4 to influence cognitive decline
Keenan, B. T., Shulman, J. M., Chibnik, L. B., Raj, T., Tran, D., Sabuncu, M. R., Initiative, T. A. D. N., Allen, A. N., Corneveaux, J. J., Hardy, J., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds054 · Cited by 97
Self-citationKleiman, T., Zdanys, K. F., Black, B. T., Rightmer, T., Grey, M. A., Garman, K. S., MacAvoy, M. G., Gelernter, J. E., & van Dyck, C. H. (2006) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000093316 · Cited by 90
Oveisgharan, S., Wilson, R. S., Yu, L., Schneider, J. A., & Bennett, D. A. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2020.1941 · Cited by 88
Self-citationChang, Y., Bondi, M. W., Fennema‐Notestine, C., McEvoy, L. K., Hagler, D. J., Jacobson, M. W., & Dale, A. M. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.12.024 · Cited by 92
Boyle, P. A., Buchman, A. S., Wilson, R. S., Kelly, J. F., & Bennett, D. A. (2009) · Neuroepidemiology · doi:10.1159/000256662 · Cited by 88
Self-citationNegash, S., Wilson, R. S., Leurgans, S. E., Wolk, D. A., Schneider, J. S., Buchman, A. S., Bennett, D., & Arnold, S. E. (2013) · Current Alzheimer Research · doi:10.2174/15672050113109990157 · Cited by 88
Self-citationNeltner, J. H., Abner, E. L., Schmitt, F. A., Denison, S. K., Anderson, S., Patel, E., & Nelson, P. T. (2012) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3182768de4 · Cited by 85
Amyloid-beta and Alzheimer’s disease: the role of neprilysin-2 in amyloid-beta clearance
Marr, R. A., & Hafez, D. M. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00187 · Cited by 84
Etiology and Pathogenesis of Late-Onset Alzheimer’s Disease
Balin, B. J., & Hudson, A. P. (2014) · Current Allergy and Asthma Reports · doi:10.1007/s11882-013-0417-1 · Cited by 86
Hippocampal atrophy and disconnection in incipient and mild Alzheimer's disease
deToledo‐Morrell, L., Stoub, T. R., & Wang, C. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63040-4 · Cited by 84
Tremblay, C., Pilote, M., Phivilay, A., Émond, V., Bennett, D. A., & Calon, F. (2007) · Journal of Alzheimer s Disease · doi:10.3233/jad-2007-12411 · Cited by 78
Self-citationFunctional Screening of Alzheimer Pathology Genome-wide Association Signals in Drosophila
Shulman, J. M., Chipendo, P. I., Chibnik, L. B., Aubin, C., Tran, D., Keenan, B. T., Kramer, P. L., Schneider, J. A., Bennett, D., Feany, M. Β., et al. (2011) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.01.006 · Cited by 84
Self-citationNegash, S., Bennett, D. A., Wilson, R. S., Schneider, J. A., & Arnold, S. E. (2011) · Current Alzheimer Research · doi:10.2174/156720511795745302 · Cited by 79
Self-citationSingle cell gene expression profiling in Alzheimer’s disease
Ginsberg, S. D., Che, S., Counts, S., & Mufson, E. J. (2006) · NeuroRx · doi:10.1016/j.nurx.2006.05.007 · Cited by 76
Metadata
- Authors
- Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Aggarwal, N. T., Arnold, S. E., Cochran, E. J., Berry-Kravis, E., & Bienias, J. L.
- Affiliations
- From the Rush Alzheimer’s Disease Center and Rush Institute for Healthy Aging (Drs. Bennett, Wilson, Schneider, Evans, Aggarwal, and Bienias); Department of Neurological Sciences (Drs. Bennett, Wilson, Schneider, Evans, Aggarwal, Cochran, and Berry-Kravis); Department of Psychology (Dr. Wilson); Department of Pathology (Drs. Schneider and Cochran); Department of Internal Medicine (Drs. Evans and Bienias), Department of Pediatrics (Dr. Berry-Kravis), Rush Presbyterian-St. Luke’s Medical Center,...
- Venue
- Neurology
- Published
- 2003-01-28
- Volume
- 60
- Issue
- 2
- Pages
- 246-252
- ISSN
- 0028-3878 (ISSN-L)
- 1526-632X
- OpenAlex
- W2005578478
- Cited by
- 282
- References
- 64
- Citations by year
- 2026: 10 · 2025: 13 · 2024: 11 · 2023: 10 · 2022: 9 · 2021: 15 · 2020: 9 · 2019: 11 · 2018: 10 · 2017: 13 · 2016: 10 · 2015: 10 · 2014: 8 · 2013: 9 · 2012: 15
- FWCI
- 12.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG-15819, AG 10161, P30AG010161)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- APOE ε4, Alzheimer's disease, neuropathology, neuritic plaques, neurofibrillary tangles, cognitive function, episodic memory, semantic memory, working memory, perceptual speed, visuospatial ability, women religious, brain autopsy
- MeSH terms
- Age Factors, Aged, Aged, 80 and over, Alleles, Alzheimer Disease, Apolipoproteins E, Brain, Cognition Disorders, Educational Status, Female, Humans, Longitudinal Studies, Male, Memory Disorders, Neuropsychological Tests, Risk Factors, Linear Models, Logistic Models, Odds Ratio, Disease Progression, Genetic Predisposition to Disease, Apolipoprotein E4
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