Apolipoprotein E ε4 allele, AD pathology, and the clinical expression of Alzheimer’s disease

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.

doi:10.1212/01.wnl.0000042478.08543.f7

Cited by 282Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Apolipoprotein E ε4 allele, AD pathology, and the clinical expression of Alzheimer’s disease

Bennett, D.A., Wilson, R.S., Schneider, J.A., Evans, D.A., Aggarwal, N.T., Arnold, S.E., Cochran, E.J., Berry-Kravis, E. +1 more·2003·Neurology

DOI 10.1212/01.wnl.0000042478.08543.f7

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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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The inter-rater reliability of the counts of AD pathologic indices was 0.89 to 0.93, supporting reproducibility.
“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]
The regional standardized scores were highly correlated with the global AD pathology score (r range 0.47-0.73, median 0.67) and Chronbach α 0.90, supporting use of the global AD pathology score.
“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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Education modifies the relation of AD pathology to level of cognitive function in older persons
Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Mendes de Leon, C. F., Arnold, S. E., Barnes, L. L., & Bienias, J. L. (2003) · Neurology · doi:10.1212/01.wnl.0000069923.64550.9f · Cited by 549 · see citing works
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Mild cognitive impairment is related to Alzheimer disease pathology and cerebral infarctions
Bennett, D. A., Schneider, J. A., Bienias, J. L., Evans, D. A., & Wilson, R. S. (2005) · Neurology · doi:10.1212/01.wnl.0000152982.47274.9e · Cited by 537 · see citing works
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Neurofibrillary tangles mediate the association of amyloid load with clinical Alzheimer disease and level of cognitive function
Bennett, D. A., Schneider, J. A., Wilson, R. S., Bienias, J. L., & Arnold, S. E. (2004) · Archives of Neurology · doi:10.1001/archneur.61.3.378 · Cited by 526 · see citing works
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Human microglial state dynamics in Alzheimer’s disease progression
Sun, N., Victor, M. B., Park, Y. P., Xiong, X., Scannail, A. N., Leary, N., Prosper, S., Viswanathan, S., Luna, X., Boix, C. A., et al. (2023) · Cell · doi:10.1016/j.cell.2023.08.037 · Cited by 462 · see citing works
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Sirtuin 1 Reduction Parallels the Accumulation of Tau in Alzheimer Disease
Julien, C., Tremblay, C., Émond, V., Lebbadi, M., Salem, N., Bennett, D. A., & Calon, F. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181922348 · Cited by 467 · see citing works
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Epigenetic age of the pre-frontal cortex is associated with neuritic plaques, amyloid load, and Alzheimer’s disease related cognitive functioning
Levine, M. E., Lu, A. T., Bennett, D. A., & Horvath, S. (2015) · Aging · doi:10.18632/aging.100864 · Cited by 455 · see citing works
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Cognitive Impairment Associated With Chemotherapy for Cancer: Report of a Workshop
Tannock, I. F., Ahles, T. A., Ganz, P. A., & van Dam, F. S. A. M. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.08.094 · Cited by 455 · see citing works
Age at surgical menopause influences cognitive decline and Alzheimer pathology in older women
Bove, R., Secor, E., Chibnik, L. B., Barnes, L. L., Schneider, J. A., Bennett, D. A., & De Jager, P. L. (2014) · Neurology · doi:10.1212/wnl.0000000000000033 · Cited by 437 · see citing works
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Cerebral infarctions and the likelihood of dementia from Alzheimer disease pathology
Schneider, J. A., Wilson, R. S., Bienias, J. L., Evans, D. A., & Bennett, D. A. (2004) · Neurology · doi:10.1212/01.wnl.0000118211.78503.f5 · Cited by 436 · see citing works
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Proneness to psychological distress is associated with risk of Alzheimer’s disease
Wilson, R. S., Evans, D. A., Bienias, J. L., Mendes de Leon, C. F., Schneider, J. A., & Bennett, D. A. (2003) · Neurology · doi:10.1212/01.wnl.0000096167.56734.59 · Cited by 428 · see citing works
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Brain amyloid-β oligomers in ageing and Alzheimer’s disease
Lesné, S., Sherman, M. A., Grant, M. K. O., Kuskowski, M. A., Schneider, J. A., Bennett, D. A., & Ashe, K. H. (2013) · Brain · doi:10.1093/brain/awt062 · Cited by 407 · see citing works
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The Rush Memory and Aging Project: Study Design and Baseline Characteristics of the Study Cohort
Bennett, D. A., Schneider, J. A., Buchman, A. S., de Leon, C. F. M., Bienias, J. L., & Wilson, R. S. (2005) · Neuroepidemiology · doi:10.1159/000087446 · Cited by 405 · see citing works
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Microinfarct Pathology, Dementia, and Cognitive Systems
Arvanitakis, Z., Leurgans, S. E., Barnes, L. L., Bennett, D. A., & Schneider, J. A. (2011) · Stroke · doi:10.1161/strokeaha.110.595082 · Cited by 404 · see citing works
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The natural history of cognitive decline in Alzheimer's disease.
Wilson, R. S., Segawa, E., Boyle, P. A., Anagnos, S. E., Hizel, L. P., & Bennett, D. A. (2012) · Psychology and Aging · doi:10.1037/a0029857 · Cited by 386 · see citing works
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Cerebral amyloid angiopathy pathology and cognitive domains in older persons
Arvanitakis, Z., Leurgans, S. E., Wang, Z., Wilson, R. S., Bennett, D. A., & Schneider, J. A. (2011) · Annals of Neurology · doi:10.1002/ana.22112 · Cited by 383 · see citing works
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Alzheimer’s disease is not “brain aging”: neuropathological, genetic, and epidemiological human studies
Nelson, P. T., Head, E., Schmitt, F. A., Davis, P. R., Neltner, J. H., Jicha, G. A., Abner, E. L., Smith, C. D., Van Eldik, L. J., Kryscio, R. J., et al. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0826-y · Cited by 365 · see citing works
Genes and the parsing of cognitive processes
Goldberg, T. E., & Weinberger, D. R. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.05.011 · Cited by 356 · see citing works
Sex differences in Alzheimer’s disease and common neuropathologies of aging
Oveisgharan, S., Arvanitakis, Z., Yu, L., Farfel, J., Schneider, J. A., & Bennett, D. A. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1920-1 · Cited by 330 · see citing works
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Investigation of frailty as a moderator of the relationship between neuropathology and dementia in Alzheimer's disease: a cross-sectional analysis of data from the Rush Memory and Aging Project
Wallace, L. M. K., Theou, O., Godin, J., Andrew, M. K., Bennett, D. A., & Rockwood, K. (2019) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30371-5 · Cited by 310 · see citing works
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Incidence and risk factors for mild cognitive impairment: A population-based three-year follow-up study of cognitively healthy elderly subjects
Tervo, S., Kivipelto, M., Hänninen, T., Vanhanen, M., Hallikainen, M., Mannermaa, A., & Soininen, H. (2004) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000076356 · Cited by 298 · see citing works
Diabetes is related to cerebral infarction but not to AD pathology in older persons
Arvanitakis, Z., Schneider, J. A., Wilson, R. S., Li, Y., Arnold, S. E., Wang, Z., & Bennett, D. A. (2006) · Neurology · doi:10.1212/01.wnl.0000247053.45483.4e · Cited by 280 · see citing works
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Cognitive impairment, decline and fluctuations in older community-dwelling subjects with Lewy bodies
Schneider, J. A., Arvanitakis, Z., Yu, L., Boyle, P. A., Leurgans, S. E., & Bennett, D. A. (2012) · Brain · doi:10.1093/brain/aws234 · Cited by 273 · see citing works
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Better Memory and Neural Efficiency in Young Apolipoprotein E 4 Carriers
Mondadori, C. R. A., de Quervain, D. J. ‐., Buchmann, A., Mustovic, H., Wollmer, M. A., Schmidt, C. F., Boesiger, P., Hock, C., Nitsch, R. M., Papassotiropoulos, A., et al. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl103 · Cited by 265 · see citing works
Modification of the Relationship of the Apolipoprotein E ε4 Allele to the Risk of Alzheimer Disease and Neurofibrillary Tangle Density by Sleep
Lim, A. S. P., Yu, L., Kowgier, M. E., Schneider, J. A., Buchman, A. S., & Bennett, D. A. (2013) · JAMA Neurology · doi:10.1001/jamaneurol.2013.4215 · Cited by 260 · see citing works
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Cognitive Phenotypes in Alzheimer's Disease and Genetic Risk
Snowden, J. S., Stopford, C. L., Julien, C. L., Thompson, J. C., Davidson, Y., Gibbons, L., Pritchard, A., Lendon, C. L., Richardson, A. M., Varma, A., et al. (2007) · Cortex · doi:10.1016/s0010-9452(08)70683-x · Cited by 254 · see citing works
Effect ofAPOEgenotype on amyloid plaque load and gray matter volume in Alzheimer disease
Drzezga, A., Grimmer, T., Henriksen, G., Mühlau, M., Perneczky, R., Miederer, I., Praus, C., Sorg, C., Wohlschläger, A., Riemenschneider, M., et al. (2009) · Neurology · doi:10.1212/wnl.0b013e3181a2e8d0 · Cited by 248 · see citing works
Higher brain BDNF gene expression is associated with slower cognitive decline in older adults
Buchman, A. S., Yu, L., Boyle, P. A., Schneider, J. A., De Jager, P. L., & Bennett, D. A. (2016) · Neurology · doi:10.1212/wnl.0000000000002387 · Cited by 239 · see citing works
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Increased proNGF Levels in Subjects with Mild Cognitive Impairment and Mild Alzheimer Disease
Peng, S., Wuu, J., Mufson, E. J., & Fahnestock, M. L. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.6.641 · Cited by 236 · see citing works
Clinical predictors of progression to Alzheimer disease in amnestic mild cognitive impairment
Fleisher, A., Sowell, B. B., Taylor, C., Gamst, A. C., Petersen, R. C., & Thal, L. J. (2007) · Neurology · doi:10.1212/01.wnl.0000258542.58725.4c · Cited by 230 · see citing works
Fourteen‐year longitudinal study of vascular risk factors, APOE genotype, and cognition: The ARIC MRI Study
Knopman, D. S., Mosley, T. H., Catellier, D., Coker, L. H., & Study, A. R. I. C. S. B. M. (2009) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2009.01.027 · Cited by 229 · see citing works
Impact of APOE genotype on neuropathologic and neurochemical markers of Alzheimer disease
Tiraboschi, P., Hansen, L. A., Masliah, E., Alford, M., Thal, L. J., & Corey-Bloom, J. (2004) · Neurology · doi:10.1212/01.wnl.0000128091.92139.0f · Cited by 226 · see citing works
Dietary fat composition and dementia risk
Morris, M. C., & Tangney, C. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.03.038 · Cited by 222 · see citing works
Relation of neuropathology to cognition in persons without cognitive impairment
Bennett, D. A., Wilson, R. S., Boyle, P. A., Buchman, A. S., & Schneider, J. A. (2012) · Annals of Neurology · doi:10.1002/ana.23654 · Cited by 220 · see citing works
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Combined neuropathological pathways account for age‐related risk of dementia
Power, M. C., Mormino, E. C., Soldan, A., James, B. D., Yu, L., Armstrong, N. M., Bangen, K. J., Delano‐Wood, L., Lamar, M., Lim, Y. Y., et al. (2018) · Annals of Neurology · doi:10.1002/ana.25246 · Cited by 215 · see citing works
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APOE alleles predict the rate of cognitive decline in Alzheimer disease: A nonlinear model
Martins, C. A. R., Oulhaj, A., de Jager, C. A., & Williams, J. H. (2005) · Neurology · doi:10.1212/01.wnl.0000188871.74093.12 · Cited by 205 · see citing works
Impact of APOE in mild cognitive impairment
Farlow, M., He, Y., Tekin, S., Xu, J., Lane, R., & Charles, H. (2004) · Neurology · doi:10.1212/01.wnl.0000144279.21502.b7 · Cited by 217 · see citing works
Statins, incident Alzheimer disease, change in cognitive function, and neuropathology
Arvanitakis, Z., Schneider, J. A., Wilson, R. S., Bienias, J. L., Kelly, J. F., Evans, D. A., & Bennett, D. A. (2008) · Neurology · doi:10.1212/01.wnl.0000288181.00826.63 · Cited by 199 · see citing works
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Glial heme oxygenase-1 expression in Alzheimer disease and mild cognitive impairment
Schipper, H. M., BENNETT, D., Liberman, A., Bienias, J. L., Schneider, J. A., Kelly, J. W., & Arvanitakis, Z. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.01.016 · Cited by 197 · see citing works
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Alzheimer's Disease: Redox Dysregulation As a Common Denominator for Diverse Pathogenic Mechanisms
Rommy von Bernhardi, M., & Eugenín, J. L. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4082 · Cited by 189 · see citing works
Nutritional determinants of cognitive aging and dementia
Morris, M. C. (2011) · Proceedings of The Nutrition Society · doi:10.1017/s0029665111003296 · Cited by 185 · see citing works
MRI predictors of risk of incident Alzheimer disease
Stoub, T. R., Bulgakova, M., Leurgans, S. E., Bennett, D. A., Fleischman, D. A., Turner, D. A., & deToledo‐Morrell, L. (2005) · Neurology · doi:10.1212/01.wnl.0000160089.43264.1a · Cited by 188 · see citing works
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Chlamydophila (Chlamydia) pneumoniaein the Alzheimer's brain
GÃ©rard, H. C., Dreses-Werringloer, U., Wildt, K. S., Deka, S., Oszust, C., Balin, B. J., Frey, W. H., Bordayo, E. Z., Whittum-Hudson, J. A., & Hudson, A. P. (2006) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2006.00154.x · Cited by 186 · see citing works
Lipid homeostasis and apolipoprotein E in the development and progression of Alzheimer's disease Published, JLR Papers in Press, February 16, 2005. DOI 10.1194/jlr.M400486-JLR200
Lane, R., & Farlow, M. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m400486-jlr200 · Cited by 184 · see citing works
What did you do yesterday? A meta-analysis of sex differences in episodic memory.
Asperholm, M., Högman, N., Rafi, J., & Herlitz, A. (2019) · Psychological Bulletin · doi:10.1037/bul0000197 · Cited by 182 · see citing works
CR1 is associated with amyloid plaque burden and age‐related cognitive decline
Chibnik, L. B., Shulman, J. M., Leurgans, S. E., Schneider, J. A., Wilson, R. S., Tran, D., Aubin, C., Buchman, A. S., Heward, C. B., Myers, A. J., et al. (2011) · Annals of Neurology · doi:10.1002/ana.22277 · Cited by 174 · see citing works
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PET amyloid-beta imaging in preclinical Alzheimer's disease
Vlassenko, A. G., Benzinger, T. L. S., & Morris, J. C. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.11.005 · Cited by 173 · see citing works
Single-nucleus multiregion transcriptomic analysis of brain vasculature in Alzheimer’s disease
Sun, N., Akay, L. A., Murdock, M. H., Park, Y., Galiana-Melendez, F., Bubnys, A., Galani, K., Mathys, H., Jiang, X., Ng, A. P., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01334-3 · Cited by 177 · see citing works
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Abnormal brain cholesterol homeostasis in Alzheimer’s disease-a targeted metabolomic and transcriptomic study
Varma, V. R., Büşra Lüleci, H., Oommen, A. M., Varma, S., Blackshear, C. T., Griswold, M. E., An, Y., Roberts, J. A., O’Brien, R., Pletnikova, O., et al. (2021) · npj Aging and Mechanisms of Disease · doi:10.1038/s41514-021-00064-9 · Cited by 153 · see citing works
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Identification of the Genetic Basis for Complex Disorders by Use of Pooling-Based Genomewide Single-Nucleotide–Polymorphism Association Studies
Pearson, J. V., Huentelman, M. J., Halperin, R. F., Tembe, W., Melquist, S., Homer, N., Brun, M., Szelinger, S., Coon, K. D., Zismann, V., et al. (2006) · The American Journal of Human Genetics · doi:10.1086/510686 · Cited by 152 · see citing works
Implicit memory and Alzheimer's disease neuropathology
Fleischman, D. A., Wilson, R. S., Gabrieli, J. D. E., Schneider, J. A., Bienias, J. L., & Bennett, D. A. (2005) · Brain · doi:10.1093/brain/awh559 · Cited by 148 · see citing works
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Paradoxical Upregulation of Glutamatergic Presynaptic Boutons during Mild Cognitive Impairment
Bell, K. F. S., Bennett, D. A., & Cuello, A. C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3269-07.2007 · Cited by 145 · see citing works
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Cognitive functioning after adjuvant chemotherapy and/or radiotherapy for early‐stage breast carcinoma
Donovan, K. A., Small, B. J., Andrykowski, M. A., Schmitt, F. A., Münster, P. N., & Jacobsen, P. B. (2005) · Cancer · doi:10.1002/cncr.21482 · Cited by 130 · see citing works
NMNAT2:HSP90 Complex Mediates Proteostasis in Proteinopathies
Ali, Y., Allen, H. M., Yu, L., Li‐Kroeger, D., Bakhshizadehmahmoudi, D., Hatcher, A., Aubin, C., Xu, J., Bjorklund, N. L., Taglialatela, G., et al. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002472 · Cited by 128 · see citing works
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Progressive parkinsonism in older adults is related to the burden of mixed brain pathologies
Buchman, A. S., Yu, L., Wilson, R. S., Leurgans, S. E., Nag, S., Shulman, J. M., Barnes, L. L., Schneider, J. A., & Bennett, D. A. (2019) · Neurology · doi:10.1212/wnl.0000000000007315 · Cited by 125 · see citing works
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Terminal Cognitive Decline: Accelerated Loss of Cognition in the Last Years of Life
Wilson, R. S., Beck, T. L., Bienias, J. L., & Bennett, D. A. (2007) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31803130ae · Cited by 117 · see citing works
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Relation of NSAIDs to incident AD, change in cognitive function, and AD pathology
Arvanitakis, Z., Grodstein, F., Bienias, J. L., Schneider, J. A., Wilson, R. S., Kelly, J. F., Evans, D. A., & Bennett, D. A. (2008) · Neurology · doi:10.1212/01.wnl.0000313813.48505.86 · Cited by 116 · see citing works
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Cerebral glucose metabolism in patients with AD and different APOE genotypes
Drzezga, A., Riemenschneider, M., Strassner, B., Grimmer, T., Peller, M., Knoll, A., Wagenpfeil, S., Minoshima, S., Schwaiger, M., & Kurz, A. (2005) · Neurology · doi:10.1212/01.wnl.0000148478.39691.d3 · Cited by 116 · see citing works
Cerebrovascular insulin receptors are defective in Alzheimer’s disease
Leclerc, M., Bourassa, P., Tremblay, C., Caron, V., Sugère, C., Émond, V., Bennett, D. A., & Calon, F. (2022) · Brain · doi:10.1093/brain/awac309 · Cited by 110 · see citing works
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Differential effect of APOE genotype on amyloid load and glucose metabolism in AD dementia
Ossenkoppele, R., van der Flier, W. M., Zwan, M. D., Adriaanse, S. F., Boellaard, R., Windhorst, A. D., Barkhof, F., Lammertsma, A. A., Scheltens, P., & van Berckel, B. N. M. (2013) · Neurology · doi:10.1212/wnl.0b013e31827f0889 · Cited by 112 · see citing works
A genome‐wide profiling of brain DNA hydroxymethylation in Alzheimer's disease
Zhao, J., Zhu, Y., Yang, J., Lin, L., Wu, H., Jager, P. L. D., Jin, P., & Bennett, D. A. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2016.10.004 · Cited by 111 · see citing works
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Depressive symptoms, clinical AD, and cortical plaques and tangles in older persons
Wilson, R. S., Schneider, J. A., Bienias, J. L., Arnold, S. E., Evans, D. A., & Bennett, D. A. (2003) · Neurology · doi:10.1212/01.wnl.0000092914.04345.97 · Cited by 109 · see citing works
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Level of Executive Function Influences Verbal Memory in Amnestic Mild Cognitive Impairment and Predicts Prefrontal and Posterior Cingulate Thickness
Chang, Y.-L., Jacobson, M. W., Fennema-Notestine, C., Hagler, D. J., Jennings, R. G., Dale, A. M., McEvoy, L. K., & Initiative, A. A. D. N. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp192 · Cited by 130 · see citing works
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 105 · see citing works
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 · see citing works
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Association of white matter hyperintensities and gray matter volume with cognition in older individuals without cognitive impairment
Arvanitakis, 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 99 · see citing works
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Amyloid 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 · see citing works
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Education halves the risk of dementia due to apolipoprotein ε4 allele: a collaborative study from the Swedish Brain Power initiative
Wang, 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 99 · see citing works
Sleep fragmentation, microglial aging, and cognitive impairment in adults with and without Alzheimer’s dementia
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 101 · see citing works
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Genetic 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 · see citing works
Alcohol intake in relation to brain magnetic resonance imaging findings in older persons without dementia
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 · see citing works
Accumulation of Transactive Response DNA Binding Protein 43 in Mild Cognitive Impairment and Alzheimer Disease
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 93 · see citing works
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The Apolipoprotein E ε4 Allele Increases the Odds of Chronic Cerebral Infarction Detected at Autopsy in Older Persons
Schneider, 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 94 · see citing works
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Neuropathologic 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 · see citing works
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Sleep 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 92 · see citing works
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MIND 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 95 · see citing works
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Dietary carotenoids related to risk of incident Alzheimer dementia (AD) and brain AD neuropathology: a community-based cohort of older adults
Yuan, 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 91 · see citing works
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A 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 93 · see citing works
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Apolipoprotein E ε4 Allele Is Unrelated to Cognitive or Functional Decline in Alzheimer’s Disease: Retrospective and Prospective Analysis
Kleiman, 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 · see citing works
Association of Early-Life Cognitive Enrichment With Alzheimer Disease Pathological Changes and Cognitive Decline
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 · see citing works
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Brain substrates of learning and retention in mild cognitive impairment diagnosis and progression to Alzheimer's disease
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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,...
ORCID: Bennett, D.A.
Schneider, J.A.
Evans, D.A.
Aggarwal, N.T.
Arnold, S.E.
Cochran, E.J.
Venue: Neurology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2003-01-28
Volume: 60
Issue: 2
Pages: 246-252
ISSN: 0028-3878 (ISSN-L)
1526-632X
DOI: 10.1212/01.wnl.0000042478.08543.f7
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: Health Sciences › Medicine › Physiology › 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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Apolipoprotein E ε4 allele, AD pathology, and the clinical expression of Alzheimer’s disease

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