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Stages of the Pathologic Process in Alzheimer Disease: Age Categories From 1 to 100 Years
Abstract
Two thousand three hundred and thirty two nonselected brains from 1- to 100-year-old individuals were examined using immunocytochemistry (AT8) and Gallyas silver staining for abnormal tau; immunocytochemistry (4G8) and Campbell-Switzer staining were used for the detection ofβ-amyloid. A total of 342 cases was negative in the Gallyas stain but when restaged for AT8 only 10 were immunonegative. Fifty-eight cases had subcortical tau predominantly in the locus coeruleus, but there was no abnormal cortical tau (subcortical Stages a-c). Cortical involvement (abnormal tau in neurites) was identified first in the transentorhinal region (Stage 1a, 38 cases). Transentorhinal pyramidal cells displayed pretangle material (Stage 1b, 236 cases). Pretangles gradually became argyrophilic neurofibrillary tangles (NFTs) that progressed in parallel with NFT Stages I to VI. Pretangles restricted to subcortical sites were seen chiefly at younger ages. Of the total cases, 1,031 (44.2%) had β-amyloid plaques. The first plaques occurred in the neocortex after the onset of tauopathy in the brainstem. Plaques generally developed in the 40s in 4% of all cases, culminating in their tenth decade (75%). β-amyloid plaques and NFTs were significantly correlated (p < 0.0001). These data suggest that tauopathy associated with sporadic Alzheimer disease may begin earlier than previously thought and possibly in the lower brainstem rather than in the transentorhinal region.
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“Up to 60% of CU individuals over age 80 years have AD neuropathologic changes at autopsy or by biomarkers [60,152,212–214].”
From NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease (2018) · cites this paper as [213]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“screening revealed low rates of Braak 1–2 NFT stages in all three groups (Table 2), consistent with literature-based norms [3].”
From Tuberous sclerosis complex is associated with a novel human tauopathy (2023) · cites this paper as [3]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“It should be noted that tau aggregation in the brain is associated with older age and is generally uncommon in healthy young adults (Braak et al., 2011; Crary et al., 2014).”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Braak et al., 2011
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“It is expected that many persons die with brains that exhibit AD neuropathologic change in the preclinical phase of AD; indeed, data support the modeled expectations (44, 142).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
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“Medial temporal and brainstem neurofibrillary changes were observed in our older TSC subjects, as expected, but at a rate comparable to that observed in the epilepsy and non-neurological control groups and age-based norms [3].”
From Tuberous sclerosis complex is associated with a novel human tauopathy (2023) · cites this paper as [3]
In the citing paper
“In individuals with autosomal dominant mutations in genes coding for amyloid precursor protein (APP) or Presenilin 119 , alterations in Aβ generation that result in early deposition of plaque initiate the disease and patients invariably develop the full spectrum of tau pathology 120,121 .”
From The amyloid hypothesis in Alzheimer disease: new insights from new therapeutics (2022) · cites this paper as [121]
In the citing paper
“NFTs first appear in layer II of the entorhinal cortex (EC) during AD onset.”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [231]
In the citing paper
“NFTs subsequently appear in interconnected anatomical regions within the brain, including the hippocampus and neocortex during neurodegenerative progression [229–231].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [231]
In the citing paper
“Furthermore, it impairs adult hippocampal neurogenesis in mice and affects cortical thickness, brain activity, and mitochondrial function well before significant Aβ accumulation in the human brains [74–76].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [76]
In the citing paper
“Most of all, this binary threshold does not reflect the reality of amyloid β and tau pathology, which is continuous and present at a minimal extent in almost all people older than 70 years,17 with important discrepancies between pathology burden and clinical symptoms at intermediate extents (panel 2).”
From Clinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group (2021) · cites this paper as [17]
In the citing paper
“For tau biomarkers, there is also a strong discrepancy between neuropathological identification (in post-mortem studies, the presence of tau Braak stages I–II is almost universal after age 70 years)17,19 and in-vivo measures of tau aggregates on PET (36% of individuals are tau positive after the age of 70 years23).”
From Clinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group (2021) · cites this paper as [17]
In the citing paper
“The concordance of genetics and Aβ deposition is aligned with CPC studies that indicate that AβPs may be a temporally “upstream” feature of the neocortical disease, with the caveats that brainstem and medial temporal lobe pretangles and NFTs are seen in subjects without Aβ deposition in all age categories (33, 39, 44).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
In the citing paper
“In contrast to NFTs, AβPs are extracellular (45, 46) and are found in a high proportion of all elderly persons but are not universal (44, 47, 48).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
In the citing paper
“Recently, it has been reported that NFTs are also very common in certain brainstem nuclei in subjects without dementia (39-44).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
In the citing paper
“Neurofibrillary pathology is observed in the human brain long before Aβ plaques develop (39, 44, 300).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
In the citing paper
“Neuritic plaques seem to develop after diffuse AβPs and NFTs (44).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
In the citing paper
“At 40 years, all individuals studied by Braak and Del Tredici (39) and Braak et al (44) exhibited at least initial neurofibrillary pathology in the brainstem (Fig. 5).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [44]
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KGen: a knowledge graph generator from biomedical scientific literature
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Thal, D. R., von Arnim, C. A. F., Griffin, W. S. T., Mrak, R. E., Walker, L., Attems, J., & Arzberger, T. (2015) · Journal of Neural Transmission · doi:10.1007/s00702-014-1360-6 · Cited by 67
Self-citationConnections Between Insomnia and Cognitive Aging
Sexton, C. E., Sykara, K., Karageorgiou, E., Zitser, J., Rosa, T. D., Yaffe, K. S., & Leng, Y. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-019-00401-9 · Cited by 67
Mechanisms of Intranasal Deferoxamine in Neurodegenerative and Neurovascular Disease
Kosyakovsky, J., Fine, J. M., Frey, W. H., & Hanson, L. R. (2021) · Pharmaceuticals · doi:10.3390/ph14020095 · Cited by 67
A conformal TOF–DOI Prism‐PET prototype scanner for high‐resolution quantitative neuroimaging
Zeng, X., Wang, Z., Tan, W., Petersen, E. W., Cao, X., LaBella, A., Boccia, A., Franceschi, D., de Leon, M. J., Chiang, G. C.-Y., et al. (2023) · Medical Physics · doi:10.1002/mp.16223 · Cited by 67
Dahl, M. J., Kulesza, A., Werkle‐Bergner, M., & Mather, M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105358 · Cited by 67
Audiovisual gamma stimulation for the treatment of neurodegeneration
Blanco‐Duque, C., Chan, D., Kahn, M. C., Murdock, M. H., & Tsai, L. (2023) · Journal of Internal Medicine · doi:10.1111/joim.13755 · Cited by 67
The substantia nigra and ventral tegmental dopaminergic neurons from development to degeneration
Fu, Y., Paxinos, G., WATSON, C. R. R., & Halliday, G. M. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2016.02.001 · Cited by 67
Von Economo neurons of the anterior cingulate across the lifespan and in Alzheimer's disease
Gefen, T. D., Papastefan, S. T., Rezvanian, A., Bigio, E. H., Weıntraub, S., Rogalski, E. J., Mesulam, M. M., & Geula, C. (2017) · Cortex · doi:10.1016/j.cortex.2017.10.015 · Cited by 67
Early vs late age at onset frontotemporal dementia and frontotemporal lobar degeneration
Seo, S. W., Thibodeau, M., Perry, D. C., Hua, A. Y., Sidhu, M., Sible, I. J., Vargas, J. N. S., Gaus, S. E., Rabinovici, G. D., Rankin, K. D., et al. (2018) · Neurology · doi:10.1212/wnl.0000000000005163 · Cited by 67
Ludwig, M., Wienke, C., Betts, M. J., Zaehle, T., & Hämmerer, D. (2021) · Autonomic Neuroscience · doi:10.1016/j.autneu.2021.102900 · Cited by 66
Intracellular and Extracellular Roles for Tau in Neurodegenerative Disease
Hanger, D. P., Lau, D. H. W., Phillips, E. C., Bondulich, M. K., Guo, T., Woodward, B. W., Pooler, A. M., & Noble, W. J. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-132054 · Cited by 66
Franciotti, R., Falasca, N. W., Arnaldi, D., Famà, F., Babiloni, C., ONOFRJ, M. C., Nobili, F. M., & Bonanni, L. (2018) · Brain Topography · doi:10.1007/s10548-018-0674-3 · Cited by 66
Sleep–wake regulation and the hallmarks of the pathogenesis of Alzheimer’s disease
Egroo, M. V., Narbutas, J., Chylinski, D., González, P. V., Maquet, P., Salmon, É., Bastin, C., Collette, F., & Vandewalle, G. (2019) · SLEEP · doi:10.1093/sleep/zsz017 · Cited by 66
Lu, J., Testa, N., Jordan, R., Elyan, R., Kanekar, S. G., Wang, J., Eslinger, P. J., Yang, Q. X., Zhang, B., & Karunanayaka, P. (2019) · Brain Sciences · doi:10.3390/brainsci9120338 · Cited by 66
Sex Differences in Healthspan Predict Lifespan in the 3xTg-AD Mouse Model of Alzheimer’s Disease
Kane, A. E., Shin, S., Wong, A. A., Fertan, E., Faustova, N. S., Howlett, S. E., & Brown, R. E. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00172 · Cited by 65
Lee, J., Weerasinghe-Mudiyanselage, P. D. E., Kim, B., Kang, S., Kim, J., & Moon, C. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.115565 · Cited by 65
Correlations between cortical and subcortical tau pathology
Attems, J., Thomas, A. J., & Jellinger, K. A. (2011) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2011.01244.x · Cited by 65
Osorio, R. S., Ducca, E. L., Wohlleber, M. E., Tanzi, E. B., Gumb, T., Twumasi, A., Tweardy, S., Lewis, C., Fischer, E., Koushyk, V., et al. (2016) · SLEEP · doi:10.5665/sleep.5846 · Cited by 65
Dementia Pugilistica Revisited
Castellani, R. J., & Perry, G. L. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170669 · Cited by 65
Locus coeruleus in memory formation and Alzheimer's disease
James, T., Kula, B., Choi, S., Khan, S. S., Bekar, L. K., & Smith, N. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15045 · Cited by 65
Haque, R., Watson, C. M., Liu, J., Carter, E. K., Duong, D. M., Lah, J. J., Wingo, A. P., Roberts, B. R., Johnson, E. C. B., Saykin, A. J., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adg4122 · Cited by 64
Fan, L., Tzen, K., Chen, Y., Chen, T., Lai, Y., Yen, R., Huang, Y.-Y., Shiue, C., Yang, S., & Chiu, M. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00175 · Cited by 64
Alber, J., Bouwman, F. H., den Haan, J., Rissman, R. A., Groef, L. D., Koronyo‐Hamaoui, M., Lengyel, I., & Thal, D. R. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.13529 · Cited by 64
Self-citationHigh plasticity of axonal pathology in Alzheimer’s disease mouse models
Blázquez‐Llorca, L., Valero-Freitag, S., Rodrigues, E. F., Merchán-Pérez, Á., Rodríguez, J., Dorostkar, M. M., DeFelipe, J., & Herms, J. W. (2017) · Acta Neuropathologica Communications · doi:10.1186/s40478-017-0415-y · Cited by 64
Sleep and hippocampal neurogenesis: Implications for Alzheimer’s disease
Kent, B. A., & Mistlberger, R. E. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.02.004 · Cited by 64
PET imaging of tau protein targets: a methodology perspective
Lois, C., González, I., Johnson, K. A., & Price, J. C. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9847-7 · Cited by 64
Koga, S., Sanchez‐Contreras, M., Josephs, K. A., Uitti, R. J., Graff‐Radford, N., van Gerpen, J. A., Cheshire, W. P., Wszolek, Z. K., Rademakers, R., & Dickson, D. W. (2017) · Movement Disorders · doi:10.1002/mds.26809 · Cited by 63
Locus Coeruleus Modulates Neuroinflammation in Parkinsonism and Dementia
Giorgi, F. S., Biagioni, F., Galgani, A., Pavese, N., Lazzeri, G., & Fornai, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228630 · Cited by 63
Goodman, A. M., Langner, B. M., Jackson, N. L., Alex, C., & McMahon, L. L. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0119-21.2021 · Cited by 63
Dammer, E. B., Shantaraman, A., Ping, L., Duong, D. M., Gerasimov, E. S., Ravindran, S. P., Guðmundsdóttir, V., Frick, E. A., Gómez, G., Walker, K. A., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adn3504 · Cited by 63
Mastroeni, D., Delvaux, E., Nolz, J., Tan, Y., Grover, A., Oddo, S., & Coleman, P. D. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.08.017 · Cited by 63
Cognitive decline associated with pathological burden in primary age‐related tauopathy
Jefferson‐George, K., Wolk, D. A., Lee, E. B., & McMillan, C. T. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2017.01.028 · Cited by 63
Ross, J. A., Gliebus, G. P., & Bockstaele, E. J. V. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.08.004 · Cited by 63
The Neuroanatomy of the Reticular Nucleus Locus Coeruleus in Alzheimer’s Disease
Giorgi, F. S., Ryskalin, L., Ruffoli, R., Biagioni, F., Limanaqi, F., Ferrucci, M., Busceti, C. L., Bonuccelli, U., & Fornai, F. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00080 · Cited by 63
Prevention and Treatment of Alzheimer’s Disease: Biological Mechanisms of Exercise
McGurran, H., Glenn, J. M., Madero, E. N., & Bott, N. T. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-180958 · Cited by 63
(ADNI), A. D. N. I., Kleineidam, L., Chouraki, V., Próchnicki, T., van der Lee, S. J., Madrid-Márquez, L., Wagner-Thelen, H., Karaca, I., Weinhold, L., Wolfsgruber, S., et al. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02138-6 · Cited by 62
In Vivo Comparison of Tau Radioligands 18F-THK-5351 and 18F-THK-5317
Betthauser, T. J., Lao, P. J., Murali, D., Barnhart, T. E., Furumoto, S., Okamura, N., Stone, C. K., Johnson, S. C., & Christian, B. T. (2016) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.182980 · Cited by 62
Nicastro, N., Malpetti, M., Cope, T., Bevan-Jones, W. R., Mak, E., Passamonti, L., Rowe, J. B., & O'Brien, J. T. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200246 · Cited by 62
Sex is a defining feature of neuroimaging phenotypes in major brain disorders
Salminen, L. E., Tubi, M. A., Bright, J. K., Thomopoulos, S. I., Wieand, A., & Thompson, P. M. (2021) · Human Brain Mapping · doi:10.1002/hbm.25438 · Cited by 61
Ferrer, I., Andrés‐Benito, P., Ausín, K., Pamplona, R., del Río, J. A., Fernández‐Irigoyen, J., & Santamaría, E. (2021) · Brain Pathology · doi:10.1111/bpa.12996 · Cited by 61
Metadata
- Authors
- Braak, H., Thal, D. R., Ghebremedhin, E., & Del Tredici, K.
- Affiliations
- The University of Queensland (AU)
- Corresponding author
- Braak, Heiko
- Venue
- Journal of Neuropathology & Experimental Neurology
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-11
- Volume
- 70
- Issue
- 11
- Pages
- 960-969
- ISSN
- 0022-3069 (ISSN-L)
- 1554-6578
- OpenAlex
- W1993023011
- Cited by
- 2,194
- References
- 75
- Citations by year
- 2026: 152 · 2025: 192 · 2024: 260 · 2023: 233 · 2022: 192 · 2021: 235 · 2020: 182 · 2019: 144 · 2018: 121 · 2017: 110 · 2016: 100 · 2015: 85 · 2014: 78 · 2013: 65 · 2012: 42
- FWCI
- 41.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuropathology & Experimental Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alzheimer Forschung Initiative (10810)
- Deutsche Forschungsgemeinschaft (TH624 4–1)
- 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
- Alzheimer's disease, pathological staging, tauopathy, neurofibrillary tangles, amyloid plaques, locus coeruleus, brainstem, sporadic Alzheimer's disease, AT8 antibody
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Alzheimer Disease, Brain, Child, Child, Preschool, Female, Humans, Infant, Male, Middle Aged, Neurons, Cohort Studies, Amyloid beta-Peptides, Silver Staining, Neurofibrillary Tangles, tau Proteins, Disease Progression, Statistics, Nonparametric, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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