Clinicopathologic Studies in Cognitively Healthy Aging and Alzheimer Disease: Relation of Histologic Markers to Dementia Severity, Age, Sex, and Apolipoprotein E Genotype

Berg, Leonard; McKeel, Daniel W.; Miller, J. Philip; Storandt, Martha; Rubin, Eugene H.; Morris, John C.; Baty, Jack; Coats, Mary; Norton, Joanne; Goate, Alison M.; Price, Joseph L.; Gearing, Marla; Mirra, Suzanne S.; Saunders, Ann M.

doi:10.1001/archneur.55.3.326

Cited by 657Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsNeuroinflammation and Neurodegeneration Mechanisms

Clinicopathologic Studies in Cognitively Healthy Aging and Alzheimer Disease: Relation of Histologic Markers to Dementia Severity, Age, Sex, and Apolipoprotein E Genotype

Berg, Leonard, McKeel, Daniel W., Miller, J. Philip, Storandt, Martha, Rubin, Eugene H., Morris, John C., Baty, Jack, Coats, Mary +6 more·1998·Archives of Neurology

DOI 10.1001/archneur.55.3.326

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Abstract

OBJECTIVE: To study differences between subjects with Alzheimer disease (AD) and cognitively intact control subjects, with respect to brain histologic markers of AD, and the relationship of those markers in the AD group to severity of dementia, age at death, sex, and apolipoprotein E genotype. SETTING: Washington University Alzheimer's Disease Research Center, St Louis, Mo. DESIGN AND SUBJECTS: Consecutive neuropathologic series of 224 prospectively studied volunteer research subjects, 186 with dementia of the Alzheimer type (DAT) or "incipient" DAT and confirmed to have AD by postmortem examination and 13 cognitively intact subjects, confirmed to lack postmortem findings of AD. MAIN OUTCOME MEASURES: Brain densities (number per square millimeter) of senile plaques and neurofibrillary tangles, extent of cerebral amyloid angiopathy, cortical Lewy bodies, and apolipoprotein E genotype. RESULTS: Neocortical neurofibrillary tangle densities were substantially correlated with dementia severity, and to a greater degree than was true for senile plaque densities. When infarcts, hemorrhages, and Parkinson disease changes coexisted with AD, neurofibrillary tangle and senile plaque densities were lower. Plaque-predominant AD was found in a greater proportion of subjects with milder than more severe dementia. Entorhinal cortical Lewy bodies were no more frequent in plaque-predominant AD than in the remaining AD cases. Increasing age at death was negatively correlated with dementia severity and densities of senile plaques and neurofibrillary tangles. The apolipoprotein E epsilon4 allele frequency was greater in AD than in control subjects but decreased with increasing age. After controlling for dementia severity, senile plaque densities were only weakly related to epsilon4 allele frequency, and only in hippocampus. However, the degree of cerebral amyloid angiopathy was clearly related to epsilon4 allele frequency. Among subjects diagnosed during life as having DAT or incipient DAT, only 7% were found to have a neuropathologic disorder other than AD causing their dementia. CONCLUSIONS: (1) The order of the strength of relationships between densities of histologic markers and dementia severity in AD is neurofibrillary tangles greater than cored senile plaques greater than total senile plaques. (2) Advanced age at death is associated with somewhat less severe dementia and fewer senile plaques and neurofibrillary tangles. (3) Plaque-predominant AD may represent a developmental stage in AD. (4) Despite a substantial effect of apolipoprotein E epsilon4 as a risk factor for AD, on decreasing the age at AD onset, and increasing the amount of cerebral amyloid angiopathy, its effect on senile plaque densities is variable and complex, being confounded with age, dementia severity, and methodologic differences. (5) Stringent clinical diagnostic criteria for DAT, even in the very mild stage, and senile plaque-based neuropathologic criteria for AD are highly accurate.

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The conjecture that excess temporal neocortex metabolic reduction in E4 carriers is related to increased β-amyloid deposition is supported by the increased predilection in early AD for β-amyloid to accumulate in the neocortex rather than the hippocampal formation and by reductions in METglu observed in transgenic mouse models overproducing amyloid.
“This conjecture is supported further by the increased predilection in early AD for β-amyloid to accumulate in the neocortex rather than the hippocampal formation (2, 6) and by reductions in METglu observed in transgenic mouse models overproducing amyloid (44).”
From Prediction of cognitive decline in normal elderly subjects with 2-[ 18 F]fluoro-2-deoxy- <scp>d</scp> -glucose/positron-emission tomography (FDG/PET) (2001) · cites this paper as [2]

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Corey‐Bloom, J., Sabbagh, M. N., Bondi, M. W., Hansen, L., Alford, M. F., Masliah, E., & Thal, L. J. (1997) · Neurology · doi:10.1212/wnl.48.1.154 · Cited by 110 · see citing works
The Consortium to Establish a Registry for Alzheimer's Disease (CERAD)
Hulette, C., Mirra, S. S., Wilkinson, W. E., Heyman, A., Fillenbaum, G. G., & Clark, C. (1995) · Neurology · doi:10.1212/wnl.45.11.1991 · Cited by 98 · see citing works
Self-citation
Age and Histopathologic Heterogeneity in Alzheimer's Disease
Bondareff, W. (1987) · Archives of General Psychiatry · doi:10.1001/archpsyc.1987.01800170026005 · Cited by 94 · see citing works
Accuracy of Clinical Diagnosis of Alzheimer Disease and Clinical Features of Patients with Non-Alzheimer Disease Neuropathology
Rasmusson, D. X., Brandt, J., Steele, C., Hedreen, J. C., Troncoso, J. C., & Folstein, M. F. (1996) · Alzheimer Disease & Associated Disorders · doi:10.1097/00002093-199601040-00002 · Cited by 93 · see citing works
Differential correlation between neurochemical deficits, neuropathology, and cognitive status in Alzheimer's disease
Dournaud, P., Delaère, P., Hauw, J., & Epelbaum, J. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00086-t · Cited by 83 · see citing works
Lewy bodies are located preferentially in limbic areas in diffuse Lewy body disease
Rezaie, P., Cairns, N. J., Chadwick, A. J., & Lantos, P. L. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12775-0 · Cited by 80 · see citing works
Retrospective Postmortem Dementia Assessment
Davis, P. B. (1991) · Archives of Neurology · doi:10.1001/archneur.1991.00530180069019 · Cited by 74 · see citing works
Alzheimer's disease with and without coexisting Parkinson's disease changes
Gearing, M., Schneider, J. A., Rebeck, G. W., Hyman, B. T., & Mirra, S. S. (1995) · Neurology · doi:10.1212/wnl.45.11.1985 · Cited by 66 · see citing works
Self-citation
The apolipoprotein E allele epsilon 4 does not correlate with the number of senile plaques or neurofibrillary tangles in patients with Alzheimer's disease.
Landén, M., Thorsell, A., Wallin, A., & Blennow, K. (1996) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.61.4.352 · Cited by 54 · see citing works
Alzheimer pathology of patients carrying apoliprotein E ε4 allele
Heinonen, O. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00076-q · Cited by 52 · see citing works
Polymorphism in AACT gene may lower age of onset of Alzheimerʼs disease
Talbot, C. J., Houlden, H., Craddock, N. J., et al. (1996) · Neuroreport · doi:10.1097/00001756-199601310-00038 · Cited by 52 · see citing works
An extensive network of PHFτ‐rich dystrophic neurites permeates neocortex and nearly all neuritic and diffuse amyloid plaques in Alzheimer disease
Schmidt, M. L., Didario, A. G., Lee, V. M. ‐., & Trojanowski, J. Q. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00259-2 · Cited by 47 · see citing works
Mesolimbocortical dementia. A clinicopathologic case study of a putative disorder.
Torack, R., & Morris, J. C. (1986) · Archives of Neurology · doi:10.1001/archneur.1986.00520100078018 · Cited by 47 · see citing works
Self-citation
Effect of apolipoprotein E genotype on Alzheimer's disease neuropathology in a cohort of elderly Norwegians
Morris, C. M., Benjamin, R., Leake, A., McArthur, F. K., Candy, J. M., Ince, P. G., Torvik, A., Bjertness, E., & Edwardson, J. A. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(94)12126-b · Cited by 38 · see citing works
Apolipoprotein E genotype and amyloid load in Alzheimer disease and control brains
Pirttilä, T., Soininen, H. S., Mehta, P. D., Heinonen, O., Lehtimäki, T. J., Bogdanović, N., Paljärvi, L., Kim, K. S., Kosunen, O., Winblad, B. G., et al. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(96)00204-7 · Cited by 33 · see citing works
APOE alleles in Alzheimer's disease and vascular dementia in a population aged 85+
Sulkava, R. O., Kainulainen, K., Verkkoniemi, A., Niinistö, L., Sobel, E. L., Davanipour, Z., Polvikoski, T. M., Haltia, M., & KONTULA, K. K. (1996) · Neurobiology of Aging · doi:10.1016/0197-4580(96)00023-1 · Cited by 33 · see citing works
βAP deposition and head trauma
Adle‐Biassette, H., Duyckaerts, C. J., Wasowicz, M., He, Y., Fornés, P., Foncin, J. F., Lecomte, D., & Hauw, J. (1996) · Neurobiology of Aging · doi:10.1016/0197-4580(96)00029-2 · Cited by 19 · see citing works
Psychometric Discrimination of Moderate Senile Dementia of the Alzheimer Type
Hill, R. D., Storandt, M., & LaBarge, E. (1992) · Archives of Neurology · doi:10.1001/archneur.1992.00530280065023 · Cited by 18 · see citing works
Self-citation
Selective silver impregnation of senile plaques: a method useful for computer imaging
Hedreen, J. C., Raskin, L. S., Struble, R. G., & Price, D. L. (1988) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(88)90153-7 · Cited by 18 · see citing works
Tangles and plaques in healthy aging and Alzheimer's disease: independence or interaction?
Price, J. L. (1994) · Seminars in Neuroscience · doi:10.1006/smns.1994.1051 · Cited by 17 · see citing works
Self-citation
Automated identification and quantitative morphometry of the senile plaques of Alzheimer's disease.
Hibbard, L., & Dw, M. (1997) · PubMed · Cited by 14 · see citing works
Alzheimer's disease and apolipoprotein E genotype in Western Australia: an autopsy‐verified series
Fabian, V. A., Jones, T. M., Wilton, S. D., Dench, J. E., Davis, M. R., Lim, L., & Kakulas, B. A. (1996) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.1996.tb124852.x · Cited by 11 · see citing works

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Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound‐B
Klunk, W. E., Engler, H., Nordberg, A., Wang, Y., Blomqvist, G., Holt, D. P., Bergström, M., Savitcheva, I., Huang, G., Estrada, S., et al. (2004) · Annals of Neurology · doi:10.1002/ana.20009 · Cited by 4,496 · see citing works
Self-citation
Silent Brain Infarcts and the Risk of Dementia and Cognitive Decline
Vermeer, S. E., Prins, N. D., den Heijer, T., Hofman, A., Koudstaal, P. J., & Breteler, M. M. B. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa022066 · Cited by 2,313 · see citing works
Open Access Series of Imaging Studies (OASIS): Cross-sectional MRI Data in Young, Middle Aged, Nondemented, and Demented Older Adults
Marcus, D. S., Wang, T. H., Parker, J., Csernansky, J. G., Morris, J. C., & Buckner, R. L. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.9.1498 · Cited by 2,163 · see citing works
Self-citation
Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory
Buckner, R. L., Snyder, A. Z., Shannon, B. J., LaRossa, G., Sachs, R., Fotenos, A. F., Sheline, Y. I., Klunk, W. E., Mathis, C. A., Morris, J. C., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2177-05.2005 · Cited by 2,140 · see citing works
Self-citation
Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature
Nelson, P. T., Alafuzoff, I., Bigio, E. H., Bouras, C., Braak, H., Cairns, N. J., Castellani, R. J., Crain, B. J., Davies, P., Tredici, K. D., et al. (2012) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31825018f7 · Cited by 2,050 · see citing works
Self-citation
Thinning of the Cerebral Cortex in Aging
Salat, D. H. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh032 · Cited by 1,851 · see citing works
Primary age-related tauopathy (PART): a common pathology associated with human aging
Crary, J. F., Trojanowski, J. Q., Schneider, J. A., Abisambra, J. F., Abner, E. L., Alafuzoff, I., Arnold, S. E., Attems, J., Beach, T. G., Bigio, E. H., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1349-0 · Cited by 1,467 · see citing works
Self-citation
Practice parameter: Diagnosis of dementia (an evidence-based review): Report of the Quality Standards Subcommittee of the American Academy of Neurology
Knopman, D. S., DeKosky, S. T., Cummings, J. L., Chui, H., Corey–Bloom, J., Relkin, N., Small, G. W., Miller, B., & Stevens, J. C. (2001) · Neurology · doi:10.1212/wnl.56.9.1143 · Cited by 1,410 · see citing works
The Cortical Signature of Alzheimer's Disease: Regionally Specific Cortical Thinning Relates to Symptom Severity in Very Mild to Mild AD Dementia and is Detectable in Asymptomatic Amyloid-Positive Individuals
Dickerson, B. C., Bakkour, A., Salat, D. H., Feczko, E., Pacheco, J., Greve, D. N., Grodstein, F., Wright, C. I., Blacker, D., Rosas, H. D., et al. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn113 · Cited by 1,153 · see citing works
Self-citation
[ 11 C]PIB in a nondemented population: Potential antecedent marker of Alzheimer disease
Mintun, M. A., LaRossa, G. N., Sheline, Y. I., Dence, C. S., Lee, S. Y., Mach, R. H., Klunk, W. E., Mathis, C. A., DeKosky, S. T., & Morris, J. C. (2006) · Neurology · doi:10.1212/01.wnl.0000228230.26044.a4 · Cited by 1,036 · see citing works
Self-citation
Classification and basic pathology of Alzheimer disease
Duyckaerts, C., Delatour, B., & Potier, M.-C. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0532-1 · Cited by 1,031 · see citing works
The neuropathology of probable Alzheimer disease and mild cognitive impairment
Schneider, J. A., Arvanitakis, Z., Leurgans, S. E., & Bennett, D. A. (2009) · Annals of Neurology · doi:10.1002/ana.21706 · Cited by 935 · see citing works
Cerebrospinal Fluid tau/β-Amyloid42 Ratio as a Prediction of Cognitive Decline in Nondemented Older Adults
Fagan, A. M., Roe, C. M., Xiong, C., Mintun, M. A., Morris, J. C., & Holtzman, D. M. (2007) · Archives of Neurology · doi:10.1001/archneur.64.3.noc60123 · Cited by 897 · see citing works
Self-citation
Age, Neuropathology, and Dementia
Savva, G. M., Wharton, S. B., Ince, P. G., Forster, G., Matthews, F. E., & Brayne, C. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0806142 · Cited by 900 · see citing works
APOE predicts amyloid‐beta but not tau Alzheimer pathology in cognitively normal aging
Morris, J. C., Roe, C. M., Xiong, C., Fagan, A. M., Goate, A. M., Holtzman, D. M., & Mintun, M. A. (2010) · Annals of Neurology · doi:10.1002/ana.21843 · Cited by 830 · see citing works
Self-citation
Using mice to model Alzheimer's dementia: an overview of the clinical disease and the preclinical behavioral changes in 10 mouse models
Webster, S. J., Bachstetter, A. D., Nelson, P. T., Schmitt, F. A., & Van Eldik, L. J. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00088 · Cited by 755 · see citing works
“…to correlate amyloid plaques with the cognitive deﬁcits seen in AD (Blessed et al., 1968; Tomlinson et al., 1970; Duyckaerts et al., 1990, 1998; Berg et al., 1998; Gold et al., 2000; Mungas et al., 2001; Tiraboschi et al., 2002, 2004; Guillozet et al., 2003; Kraybill et al., 2005; Holtzer et…”
Background
Neuropathology of Cognitively Normal Elderly
Knopman, D. S., Parisi, J. E., Salviati, A., Floriach-Robert, M., Boeve, B. F., Ivnik, R. J., Smith, G. E., Dickson, D. W., Johnson, K. A., Petersen, L. E., et al. (2003) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/62.11.1087 · Cited by 674 · see citing works
Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease
Price, J. L., McKeel, D. W., Buckles, V. D., Roe, C. M., Xiong, C., Grundman, M., Hansen, L. A., Petersen, R. C., Parisi, J. E., Dickson, D. W., et al. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.04.002 · Cited by 661 · see citing works
Self-citation
Tau and tauopathies
Arendt, T., Stieler, J. T., & Holzer, M. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.08.018 · Cited by 609 · see citing works
Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: Evidence from diffusion tensor imaging.
Head, D. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh003 · Cited by 645 · see citing works
Neuropathology and Cognitive Impairment in Alzheimer Disease: A Complex but Coherent Relationship
Nelson, P. T., Braak, H., & Markesbery, W. R. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181919a48 · Cited by 643 · see citing works
Organ aging signatures in the plasma proteome track health and disease
Oh, H. S.-H., Rutledge, J., Nachun, D., Pálovics, R., Abiose, O., Moran-Losada, P., Channappa, D., Urey, D. Y., Kim, K., Sung, Y. J., et al. (2023) · Nature · doi:10.1038/s41586-023-06802-1 · Cited by 634 · see citing works
Prediction of cognitive decline in normal elderly subjects with 2-[ 18 F]fluoro-2-deoxy- <scp>d</scp> -glucose/positron-emission tomography (FDG/PET)
de Leon, M. J., Convit, A., Wolf, O. T., Tarshish, C. Y., DeSanti, S., Rusinek, H., Tsui, W., Kandil, E., Scherer, A. J., Roche, A., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191044198 · Cited by 629 · see citing works
Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis
Han, X., M. Holtzman, D., W. McKeel, D., Kelley, J., & Morris, J. C. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00997.x · Cited by 626 · see citing works
Self-citation
Neuron Number in the Entorhinal Cortex and CA1 in Preclinical Alzheimer Disease
Price, J. L., Ko, A. I., Wade, M. J., Tsou, S. K., McKeel, D. W., & Morris, J. C. (2001) · Archives of Neurology · doi:10.1001/archneur.58.9.1395 · Cited by 596 · see citing works
Self-citation
CSF phosphorylated tau protein correlates with neocortical neurofibrillary pathology in Alzheimer's disease
Buerger, K., Ewers, M., Pirttila, T., Zinkowski, R., Alafuzoff, I., Teipel, S. J., DeBernardis, J., Kerkman, D., McCulloch, C., Soininen, H., et al. (2006) · Brain · doi:10.1093/brain/awl269 · Cited by 586 · see citing works
Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD
Fotenos, A. F., Snyder, A. Z., Girton, L. E., Morris, J. C., & Buckner, R. L. (2005) · Neurology · doi:10.1212/01.wnl.0000154530.72969.11 · Cited by 579 · see citing works
Self-citation
Preclinical Alzheimer's disease and its outcome: a longitudinal cohort study
Vos, S. J., Xiong, C., Visser, P. J., Jasielec, M. S., Hassenstab, J., Grant, E. A., Cairns, N. J., Morris, J. C., Holtzman, D. M., & Fagan, A. M. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70194-7 · Cited by 564 · see citing works
Self-citation
Amyloid, hypometabolism, and cognition in Alzheimer disease: An [11C]PIB and [18F]FDG PET study
Edison, P., Archer, H. A., Hinz, R., Hammers, A., Pavese, N., Tai, Y. F., Hotton, G., Cutler, D., Fox, N., Kennedy, A., et al. (2007) · Neurology · doi:10.1212/01.wnl.0000244749.20056.d4 · Cited by 518 · see citing works
Pathologic Correlates of Nondemented Aging, Mild Cognitive Impairment, and Early-Stage Alzheimer's Disease
Morris, J. C., & Price, J. L. (2001) · Journal of Molecular Neuroscience · doi:10.1385/jmn:17:2:101 · Cited by 513 · see citing works
Self-citation
The importance of neuritic plaques and tangles to the development and evolution of AD
Tiraboschi, P., Hansen, L. A., Thal, L. J., & Corey-Bloom, J. (2004) · Neurology · doi:10.1212/01.wnl.0000129697.01779.0a · Cited by 477 · see citing works
Pittsburgh compound B imaging and prediction of progression from cognitive normality to symptomatic Alzheimer disease
Morris, J. C., Roe, C. M., Grant, E. A., Head, D., Storandt, M., Goate, A. M., Fagan, A. M., Holtzman, D. M., & Mintun, M. A. (2009) · Archives of Neurology · doi:10.1001/archneurol.2009.269 · Cited by 476 · see citing works
Self-citation
Variants in the ATP-Binding Cassette Transporter (ABCA7), Apolipoprotein E ϵ4, and the Risk of Late-Onset Alzheimer Disease in African Americans
Reitz, C., Jun, G., Naj, A., Rajbhandary, R., Vardarajan, B. N., Wang, L.-S., Valladares, O., Lin, C.-F., Larson, E. B., Graff-Radford, N. R., et al. (2013) · JAMA · doi:10.1001/jama.2013.2973 · Cited by 431 · see citing works
Self-citation
“Preclinical” AD revisited: Neuropathology of cognitively normal older adults
Schmitt, F. A., Davis, D. G., Wekstein, D. R., Smith, C. D., Ashford, J. W., & Markesbery, W. R. (2000) · Neurology · doi:10.1212/wnl.55.3.370 · Cited by 369 · see citing works
Cardiorespiratory fitness and brain atrophy in early Alzheimer disease.
Burns, J. M., Cronk, B. B., Anderson, H. S., Donnelly, J. E., Thomas, G. P., Harsha, A., Brooks, W. M., & Swerdlow, R. H. (2008) · Neurology · doi:10.1212/01.wnl.0000317094.86209.cb · Cited by 363 · see citing works
Cerebrospinal fluid tau and ptau181 increase with cortical amyloid deposition in cognitively normal individuals: Implications for future clinical trials of Alzheimer's disease
Fagan, A. M., Mintun, M. A., Shah, A. R., Aldea, P., Roe, C. M., Mach, R. H., Marcus, D., Morris, J. C., & Holtzman, D. M. (2009) · EMBO Molecular Medicine · doi:10.1002/emmm.200900048 · Cited by 353 · see citing works
Self-citation
Preclinical detection of Alzheimer’s disease: hippocampal shape and volume predict dementia onset in the elderly
Csernansky, J. G., Wang, L., Swank, J., Miller, J. P., Gado, M., McKeel, D., Miller, M. I., & Morris, J. C. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.036 · Cited by 328 · see citing works
Self-citation
Decreased cerebrospinal fluid Aβ 42 correlates with brain atrophy in cognitively normal elderly
Fagan, A. M., Head, D., Shah, A. R., Marcus, D., Mintun, M., Morris, J. C., & Holtzman, D. M. (2009) · Annals of Neurology · doi:10.1002/ana.21559 · Cited by 327 · see citing works
“Cognitive status was determined annually in accordance with standard protocols and criteria.(18,19) A Clinical Dementia Rating (CDR)(20) of 0 (n 69) indicated no dementia, whereas CDRs of 0.”
MethodSelf-citation
PIB is a non-specific imaging marker of amyloid-beta (A ) peptide-related cerebral amyloidosis
Lockhart, A., Lamb, J. R., Osredkar, T., Sue, L. I., Joyce, J. N., Ye, L., Libri, V., Leppert, D., & Beach, T. G. (2007) · Brain · doi:10.1093/brain/awm191 · Cited by 302 · see citing works
Apolipoprotein E–dependent accumulation of Alzheimer disease–related lesions begins in middle age
Kok, E., Haikonen, S., Luoto, T., Huhtala, H., Goebeler, S., Haapasalo, H., & Karhunen, P. J. (2009) · Annals of Neurology · doi:10.1002/ana.21696 · Cited by 299 · see citing works
Clinicopathologic Correlations in a Large Alzheimer Disease Center Autopsy Cohort: Neuritic Plaques and Neurofibrillary Tangles "Do Count" When Staging Disease Severity
Nelson, P. T., Jicha, G. A., Schmitt, F. A., Liu, H., Davis, D. G., Mendiondo, M. S., Abner, E. L., & Markesbery, W. R. (2007) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/nen.0b013e31815c5efb · Cited by 292 · see citing works
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. (2003) · Neurology · doi:10.1212/01.wnl.0000042478.08543.f7 · Cited by 282 · see citing works
A multicentre longitudinal study of flortaucipir (18F) in normal ageing, mild cognitive impairment and Alzheimer’s disease dementia
Pontecorvo, M. J., Devous, M. D., Kennedy, I., Navitsky, M., Lu, M., Galante, N., Salloway, S., Doraiswamy, P. M., Southekal, S., Arora, A. K., et al. (2019) · Brain · doi:10.1093/brain/awz090 · Cited by 249 · see citing works
Changes in hippocampal volume and shape across time distinguish dementia of the Alzheimer type from healthy aging
Wang, L., Swank, J. S., Glick, I. E., Gado, M. H., Miller, M. I., Morris, J. C., & Csernansky, J. G. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00361-6 · Cited by 263 · see citing works
Self-citation
The cause of neuronal degeneration in Alzheimer’s disease
Vickers, J. (2000) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00023-4 · 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
Modeling the Association between 43 Different Clinical and Pathological Variables and the Severity of Cognitive Impairment in a Large Autopsy Cohort of Elderly Persons
Nelson, P. T., Abner, E. L., Schmitt, F. A., Kryscio, R. J., Jicha, G. A., Smith, C. D., Davis, D. G., Poduska, J. W., Patel, E., Mendiondo, M. S., et al. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00244.x · Cited by 239 · see citing works
Survival and mortality differences between dementia with Lewy bodies vs Alzheimer disease
Williams, M. M., Xiong, C., Morris, J. C., & Galvin, J. E. (2006) · Neurology · doi:10.1212/01.wnl.0000247041.63081.98 · Cited by 239 · see citing works
Self-citation
Analyzing dendritic spine pathology in Alzheimer’s disease: Problems and opportunities
Dorostkar, M. M., Zou, C., Blazquez-Llorca, L., & Herms, J. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1449-5 · Cited by 235 · see citing works
Diabetes is associated with cerebrovascular but not Alzheimer's disease neuropathology
Abner, E. L., Nelson, P. T., Kryscio, R. J., Schmitt, F. A., Fardo, D. W., Woltjer, R. L., Cairns, N. J., Yu, L., Dodge, H. H., Xiong, C., et al. (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2015.12.006 · Cited by 233 · see citing works
AD lesions and infarcts in demented and non‐demented Japanese‐American men
Petrovitch, H., Ross, G. W., Steinhorn, S. C., Abbott, R. D., Markesbery, W., Davis, D., Nelson, J., Hardman, J., Masaki, K., Vogt, M. R., et al. (2005) · Annals of Neurology · doi:10.1002/ana.20318 · Cited by 230 · see citing works
Amyloid imaging and CSF biomarkers in predicting cognitive impairment up to 7.5 years later
Roe, C. M., Fagan, A. M., Grant, E. A., Hassenstab, J., Moulder, K. L., Maue Dreyfus, D., Sutphen, C. L., Benzinger, T. L. S., Mintun, M. A., Holtzman, D. M., et al. (2013) · Neurology · doi:10.1212/wnl.0b013e3182918ca6 · Cited by 222 · see citing works
Self-citation
Mixed Dementia—the Most Common Cause of Dementia
KORCZYN, A. D. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04807.x · Cited by 219 · see citing works
Dendritic Spine Pathology in Neurodegenerative Diseases
Herms, J., & Dorostkar, M. M. (2016) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044216 · Cited by 201 · see citing works
Cerebrospinal fluid APOE levels: an endophenotype for genetic studies for Alzheimer's disease
Cruchaga, C., Kauwe, J. S. K., Nowotny, P., Bales, K., Pickering, E. H., Mayo, K., Bertelsen, S., Hinrichs, A., Fagan, A. M., Holtzman, D. M., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds296 · Cited by 207 · see citing works
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Authors: Berg, L., McKeel, D. W., Miller, J. P., Storandt, M., Rubin, E. H., Morris, J. C., Baty, J., Coats, M., Norton, J., Goate, A. M., Price, J. L., Gearing, M., Mirra, S. S., & Saunders, A. M.
Affiliations: Washington University in St. Louis (US)
ORCID: Miller, J. Philip
Morris, John C.
Goate, Alison M.
Gearing, Marla
Saunders, Ann M.
Venue: Archives of Neurology
Publisher: American Medical Association (AMA)
Published: 1998-03-01
Volume: 55
Issue: 3
Pages: 326
ISSN: 0003-9942 (ISSN-L)
DOI: 10.1001/archneur.55.3.326
OpenAlex: W1972340735
Semantic Scholar: d2f7c7a3c16b4b289f3c3ff65621f74384dd4be5
Cited by: 657
References: 93
Citations by year: 2026: 9 · 2025: 13 · 2024: 10 · 2023: 6 · 2022: 14 · 2021: 12 · 2020: 10 · 2019: 11 · 2018: 8 · 2017: 18 · 2016: 18 · 2015: 26 · 2014: 36 · 2013: 30 · 2012: 33
FWCI: 15.75
Type: journal article
Language: en
Open access: closed
Locations: Archives of Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (AG03991, AG 05681, AG-00634, P50AG005681, P01AG003991)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: Alzheimer's disease, amyloid plaques, neurofibrillary tangles, cerebral amyloid angiopathy, Lewy bodies, APOE ε4, dementia severity, age at death, hippocampus, entorhinal cortex, Parkinson's disease, neuropathology, cognitive aging, postmortem brain examination, apolipoprotein E
MeSH terms: Aged, Aged, 80 and over, Aging, Alzheimer Disease, Apolipoproteins E, Brain, Cognition, Female, Genotype, Humans, Longitudinal Studies, Male, Organ Size, Prospective Studies, Neurofibrillary Tangles, Apolipoprotein E4, Plaque, Amyloid

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Clinicopathologic Studies in Cognitively Healthy Aging and Alzheimer Disease: Relation of Histologic Markers to Dementia Severity, Age, Sex, and Apolipoprotein E Genotype

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