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Aging-related tau astrogliopathy (ARTAG): harmonized evaluation strategy
Open accessAbstract
Pathological accumulation of abnormally phosphorylated tau protein in astrocytes is a frequent, but poorly characterized feature of the aging brain. Its etiology is uncertain, but its presence is sufficiently ubiquitous to merit further characterization and classification, which may stimulate clinicopathological studies and research into its pathobiology. This paper aims to harmonize evaluation and nomenclature of aging-related tau astrogliopathy (ARTAG), a term that refers to a morphological spectrum of astroglial pathology detected by tau immunohistochemistry, especially with phosphorylation-dependent and 4R isoform-specific antibodies. ARTAG occurs mainly, but not exclusively, in individuals over 60 years of age. Tau-immunoreactive astrocytes in ARTAG include thorn-shaped astrocytes at the glia limitans and in white matter, as well as solitary or clustered astrocytes with perinuclear cytoplasmic tau immunoreactivity that extends into the astroglial processes as fine fibrillar or granular immunopositivity, typically in gray matter. Various forms of ARTAG may coexist in the same brain and might reflect different pathogenic processes. Based on morphology and anatomical distribution, ARTAG can be distinguished from primary tauopathies, but may be concurrent with primary tauopathies or other disorders. We recommend four steps for evaluation of ARTAG: (1) identification of five types based on the location of either morphologies of tau astrogliopathy: subpial, subependymal, perivascular, white matter, gray matter; (2) documentation of the regional involvement: medial temporal lobe, lobar (frontal, parietal, occipital, lateral temporal), subcortical, brainstem; (3) documentation of the severity of tau astrogliopathy; and (4) description of subregional involvement. Some types of ARTAG may underlie neurological symptoms; however, the clinical significance of ARTAG is currently uncertain and awaits further studies. The goal of this proposal is to raise awareness of astroglial tau pathology in the aged brain, facilitating communication among neuropathologists and researchers, and informing interpretation of clinical biomarkers and imaging studies that focus on tau-related indicators.
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“Primary age-related tauopathy (PART) and aging-related tau astrogliopathy (ARTAG) are independent tau pathologies commonly observed in patients over 80 years of age, and PART may account for a proportion of the misdiagnosed clinical AD cases in the elderly [130, 141, 142].”
From The neuropathological diagnosis of Alzheimer's disease (2019) · cites this paper as [141]
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“Perivascular, subpial, and periventricular p-tau immunoreactive NFTs and astrocytic tangles in the neocortex have been reported to be characteristic of both primary age-related tauopathy (PART) [35] and age-related tau astrogliopathy (ARTAG) [36].”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [36]
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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“PART refers to neuronal tau pathology and ARTAG is characterized by astrocytic tau pathology, although they are not mutually exclusive, and appear to be more a manifestation of age than a subtype of neurodegenerative disease.”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [36]
Experimental — accuracy not yet measuredIn the citing paper
“Another exemplary phenomenon is age-related tau astrogliopathy (ARTAG), in which p-tau accumulates in astrocytes of various brain regions [79].”
From DNA repair deficiency and senescence in concussed professional athletes involved in contact sports (2019) · cites this paper as [79]
In the citing paper
“The panel did not ultimately accept all of the a priori criteria for CTE; they did not include pathology known to be associated with aging (i.e.primary age-related tauopathy [PART] [16] and aging-related tau astrogliopathy [ARTAG] [17]).”
From Mild Chronic Traumatic Encephalopathy Neuropathology in People With No Known Participation in Contact Sports or History of Repetitive Neurotrauma (2019) · cites this paper as [17]
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Citations
Cites
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on behalf of the MRC Cognitive Function and Ageing Neuropathology Study Group, Wharton, S. B., Minett, T., Drew, D., Forster, G., Matthews, F. E., Brayne, C., & Ince, P. G. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0275-x · Cited by 61
“Astroglial tau pathology is common in this aged cohort, most commonly TSA which, as one of the major constituent subtypes of ARTAG, are suggested to be an age-related tauopathy rather than disease-specific.”
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“Tau also accumulates in microglia and astrocytes in several of these conditions (Buée and Delacourte, 1999; Kovacs et al., 2016; Ferrer et al., 2018).”
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“The granular or fuzzy astrocytes seen in the present cases were similar to those reported in agingrelated tau astrogliopathy.(20) The appearance of many ghost tangles and granular or fuzzy astrocytes has been recognized to be characteristic of very old brains.”
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Multisite Assessment of Aging-Related Tau Astrogliopathy (ARTAG)
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“on a birds-eye view), AT8immunoreactive astrocytes ought to be interpreted as occasional or numerous/widespread as required by the original scoring system (8) when they occurred along the cortical ribbon with a 500–2000 mm distance between them.”
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“…as NFT, coiled bodies, granular fuzzy astrocytes in argyro-philic grain disease (31), thorn-shaped astrocytes in aging-related tau astrogliopathy (32), and globular astrocytic inclusions in globular glial tauopathy (GGT) (33) should be included to develop a more versatile model to assist in…”
BackgroundThe Delayed Neuropathological Consequences of Traumatic Brain Injury in a Community-Based Sample
Postupna, N. O., Rose, S. E., Gibbons, L. E., Coleman, N., Hellstern, L. L., Ritchie, K., Wilson, A. M., Cudaback, E., Li, X., Melief, E. J., et al. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.624696 · Cited by 51
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BackgroundMethodInfluentialAstrocytic 4R tau expression drives astrocyte reactivity and dysfunction
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“Granular/fuzzy astrocytes (GFAs) are a subtype of aging-related tau astrogliopathy (ARTAG), seen in the aging brain [18].”
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“The ageing-related TAU astrogliopa-thy (ARTAG) is rarely an isolated finding, but rather a co-pathology in ageing, with pathologic accumulation of abnormally phosphorylated 4R-TAU in astrocytes [24].”
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Kovács, G. G., Yousef, A., Kaindl, S., Lee, V. M., & Trojanowski, J. Q. (2017) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12427 · Cited by 40
Schwab, N., Wennberg, R. A., Grenier, K., Tartaglia, M. C., Tator, C. H., & Hazrati, L. (2021) · Neurology · doi:10.1212/wnl.0000000000011668 · Cited by 42
“Similarly, it has been suggested that some cases of CTE may simply be misdiagnosed cases of ARTAG,(31) a neuropathologic condition marked by an age-related accumulation of p-tau in astrocytes, particularly in the subpial, subependymal, and perivascular white and gray matter regions.(32) These features overlap signific…”
BackgroundBouvier, D. S., Fixemer, S., Heurtaux, T., Jeannelle, F., Frauenknecht, K. B. M., & Mittelbronn, M. G. A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.814889 · Cited by 43
Modelling human pathology of traumatic brain injury in animal models
Risling, M., Smith, D. H., Stein, T. D., Thelin, E. P., Zanier, E. R., Ankarcrona, M., & Nilsson, P. (2019) · Journal of Internal Medicine · doi:10.1111/joim.12909 · Cited by 45
Blood-brain barrier and innate immunity in the pathogenesis of Alzheimer's disease
Šimić, G., Španić, E., Horvat, L. L., & Hof, P. R. (2019) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2019.06.003 · Cited by 40
Pires, G., McElligott, S., Drusinsky, S., Halliday, G. M., Potier, M., Wısnıewskı, T., & Drummond, E. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0848-6 · Cited by 41
Tisdall, M. D., Ohm, D. T., Lobrovich, R., Das, S. R., Mizsei, G., Prabhakaran, K., Ittyerah, R., Lim, S., McMillan, C. T., Wolk, D. A., et al. (2021) · NeuroImage Clinical · doi:10.1016/j.nicl.2021.102913 · Cited by 41
“…examination identified tau-positive Pick bodies in neurons and tau-positive astrocytes in a ramified morphology typical for tau immunostaining (Kovacs et al., 2016) throughout the cortical layers and associated with severe neuronal loss typical for Pick ’ s disease in the OFC, IPFC, and…”
Neocortical Lewy Body Pathology Parallels Parkinson's Dementia, but Not Always
Martin, W. R. W., Younce, J. R., Campbell, M. C., Racette, B. A., Norris, S. A., Ushe, M., Criswell, S. R., Davis, A. A., Alfradique‐Dunham, I., Maiti, B., et al. (2022) · Annals of Neurology · doi:10.1002/ana.26542 · Cited by 44
“Other neuropathological findings in our patients included ARTAG, a recently described neuropathological entity characterized by astroglial tau pathology in the aged brain.(19) The clinical significance is uncertain.”
BackgroundYoshida, K., Hata, Y., Ichimata, S., Okada, K., & Nishida, N. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00352-2 · Cited by 38
Uchihara, T., Endo, K., Kondo, H., Okabayashi, S., Shimozawa, N., Yasutomi, Y., Adachi, E., & Kimura, N. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0385-5 · Cited by 40
Emerging Diagnostic and Therapeutic Strategies for Tauopathies
Coughlin, D. G., & Irwin, D. J. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0779-1 · Cited by 42
Modeling the Long-Term Consequences of Repeated Blast-Induced Mild Traumatic Brain Injuries
Agoston, D. V. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.5317 · Cited by 40
Spectrum of tau pathologies in Huntington's disease
Baskota, S. U., López, O. L., Greenamyre, J. T., & Kofler, J. (2018) · Laboratory Investigation · doi:10.1038/s41374-018-0166-9 · Cited by 38
“newly defined criteria for PART and ARTAG in the context of HD [28, 29].”
InfluentialNeuropathological comorbidity associated with argyrophilic grain disease
Yokota, O., Miki, T., Ikeda, C., Nagao, S., Takenoshita, S., Ishizu, H., Haraguchi, T., Kuroda, S., Terada, S., & Yamada, N. (2018) · Neuropathology · doi:10.1111/neup.12429 · Cited by 38
“Recently, a classification of the major tau-positive astrocytic lesions in degenerative diseases has been proposed.(33) In the consensus paper, it was noted that disease-specific tau-positive astrocytic lesions are tufted astrocytes in PSP, astrocytic plaques in CBD, globular astroglial inclusions in globular glial ta…”
InfluentialPrimary retinal tauopathy: A tauopathy with a distinct molecular pattern
Walkiewicz, G., Ronisz, A., Ginderdeuren, R. V., Lemmens, S., Bouwman, F. H., Hoozemans, J. J. M., Morrema, T. H. J., Rozemüller, A. J. M., de Ruyter, F. J. H., Groef, L. D., et al. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.13424 · Cited by 34
α-Synuclein pathology in post-mortem retina and optic nerve is specific for α-synucleinopathies
de Ruyter, F. J. H., Morrema, T. H. J., den Haan, J., Gase, G., Twisk, J. W. R., de Boer, J. F., Scheltens, P., Bouwman, F. H., Verbraak, F. D., Rozemüller, A. J. M., et al. (2023) · npj Parkinson s Disease · doi:10.1038/s41531-023-00570-5 · Cited by 37
“…to clinicopathological diagnosis in Parkinson ’ s disease (and dementia) 40,41 ( n = 21), dementia with Lewy bodies ( n = 5) 42 , Multiple system atrophy ( n = 7), Alzheimer ’ s disease 37 ( n = 19), other neurodegenerative diseases 43 – 45 ( n = 22) and non-neurological controls ( n = 25).”
A Conserved Cytoskeletal Signaling Cascade Mediates Neurotoxicity of FTDP-17 Tau Mutations In Vivo
Bardai, F. H., Wang, L., Mutreja, Y., Yenjerla, M., Gamblin, T. C., & Feany, M. B. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1550-17.2017 · Cited by 37
“However, when we express human tau in Drosophila glia using the pan-glial driver repo-GAL4, we observe numerous inclusions comprised of filamentous tau at the electron microscopic level (Colodner and Feany, 2010), as can be seen in human glial tauopathies (Feany and Dickson, 1995, 1996; Kovacs et al., 2016).”
BackgroundMethodMcAleese, K. E., Graham, S., Dey, M., Walker, L., Erskine, D., Johnson, M. A., Johnston, E., Thomas, A. J., McKeith, I. G., DeCarli, C. S., et al. (2018) · Brain Pathology · doi:10.1111/bpa.12685 · Cited by 38
ARTAG in the basal forebrain: widening the constellation of astrocytic tau pathology
Liu, A. K. L., Goldfinger, M., Questari, H. E., Pearce, R. K. B., & Gentleman, S. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0330-7 · Cited by 38
“This unique astroglial tau pathology has been termed aging-related tau astrogliopathy (ARTAG) [6].”
InfluentialChronic Traumatic Encephalopathy: Is Latency in Symptom Onset Explained by Tau Propagation?Preprint
Kriegel, J., Papadopoulos, Z., & McKee, A. C. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a024059 · Cited by 38
“The panel found that CTE was reliably distinguished from other tauopathies (including aging-related tau astrogliopathy [ARTAG]) (Kovacs et al. 2016) by the diagnostic criteria (McKee et al.”
BackgroundRelevance of host tau in tau seeding and spreading in tauopathies
Ferrer, I., Zelaya, M. V., Aguiló, M., Carmona, M., López‐González, I., Andrés‐Benito, P., Lidón, L., Gavı́n, R., Garcia‐Esparcia, P., & del Rı́o, J. A. (2019) · Brain Pathology · doi:10.1111/bpa.12778 · Cited by 37
TDP-43 Proteinopathy and Tauopathy: Do They Have Pathomechanistic Links?
Riku, Y., Yoshida, M., Iwasaki, Y., Sobue, G., Katsuno, M., & Ishigaki, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232415755 · Cited by 36
“ARTAG is a 4R tauopathy.”
BackgroundInfluentialAstrocytic changes with aging and Alzheimer's disease‐type pathology in chimpanzees
Munger, E. L., Edler, M. K., Hopkins, W. D., Ely, J. J., ERWIN, J. M., Perl, D. P., Mufson, E. J., Hof, P. R., Sherwood, C. C., & Raghanti, M. A. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24610 · Cited by 37
“The term aging-related tau astrogliopathy (ARTAG) was recently applied to describe astroglial pathology detected using tau immunohistochemical markers (Kovacs et al., 2016; Kovacs et al., 2018).”
BackgroundLanguage and spatial dysfunction in Alzheimer disease with white matter thorn-shaped astrocytes
Resende, E. D. P. F., Nolan, A., Petersen, C., Ehrenberg, A. J., Spina, S., Allen, I. E., Rosen, H. J., Kramer, J. H., Miller, B. L., Seeley, W. W., et al. (2020) · Neurology · doi:10.1212/wnl.0000000000008937 · Cited by 37
“However, this feature has been mostly neglected in neurodegenerative evaluations of the brain until recently when an international group of pathologists proposed a harmonizing strategy for classifying tau inclusions in astroglia collectively called ARTAG.9 A small but growing number of clinicopathologic studies have b…”
BackgroundInfluentialGenome-wide association study and functional validation implicates JADE1 in tauopathy
Farrell, K. W., Kim, S., Han, N., Iida, M. A., Gonzalez, E. M., Otero‐García, M., Walker, J. M., Richardson, T. E., Renton, A. E., Andrews, S. J., et al. (2021) · Acta Neuropathologica · doi:10.1007/s00401-021-02379-z · Cited by 36
Association of glial tau pathology and LATE-NC in the ageing brain
Forrest, S. L., Wagner, S., Kim, A., & Kovács, G. G. (2022) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2022.07.010 · Cited by 35
Giannini, L., Ohm, D. T., Rozemüller, A. J. M., Dratch, L., Suh, E. R., Deerlin, V. M. V., Trojanowski, J. Q., Lee, E. B., Swieten, J. C. V., Grossman, M., et al. (2022) · Acta Neuropathologica · doi:10.1007/s00401-022-02487-4 · Cited by 34
Tau pathology associates with in vivo cortical thinning in Lewy body disorders
Spotorno, N., Coughlin, D. G., Olm, C. A., Wolk, D. A., Vaishnavi, S., Shaw, L. M. J., Dahodwala, N. A., Morley, J. F., Duda, J. E., Deik, A., et al. (2020) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51183 · Cited by 34
“While AD CSF biomarkers are more established in AD,(8) a portion of our AD reference group could harbor some degree of alphasynuclein,(57,58) TDP-43,(59,60) or other age-related copathologies.(61,62) These pathologies are largely focused in the medial temporal lobe in AD(2,59) while our focus was largely on cortical t…”
ResultAmeen‐Ali, K. E., Bretzin, A. C., Lee, E. B., Folkerth, R. D., Hazrati, L., Iacono, D., Keene, C. D., Kofler, J., Kovács, G. G., Nolan, A., et al. (2022) · Acta Neuropathologica Communications · doi:10.1186/s40478-022-01353-4 · Cited by 34
Neuropathology of supercentenarians - four autopsy case studies
Takao, M., Hirose, N., Arai, Y., Mihara, B., & Mimura, M. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0368-6 · Cited by 33
“ARTAG was recently determined to be a pathological astrocytic condition involving tau accumulation [14].”
InfluentialMock, C., Teylan, M., Beecham, G. W., Besser, L. M., Cairns, N. J., Crary, J. F., Katsumata, Y., Nelson, P. T., & Kukull, W. A. (2020) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0000000000000380 · Cited by 34
Pharmacological Modulators of Tau Aggregation and Spreading
Dominguez‐Meijide, A., Vasili, E., & Outeiro, T. F. (2020) · Brain Sciences · doi:10.3390/brainsci10110858 · Cited by 36
Ygland, E., van Westen, D., Englund, E. M., Rademakers, R., Wszołek, Z. K., Nilsson, K. H., Nilsson, C., Waldö, M. L., Alafuzoff, I. I., Hansson, O., et al. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-017-0330-2 · Cited by 32
“The pathological picture in the Swedish family was reminiscent of PSP also in aspects other than 4R predominance: (1) the presence of neuronal NFTs and, albeit scarce, of tufted astrocytes and occasional coiled bodies [22, 23]; (2) prominent tau white matter pathology, and (3) marked involvement of the brainstem and c…”
Pathology of neurodegenerative disease for the general neurologist
Cullinane, P. W., Wrigley, S., Parmera, J. B., Valério, F., Millner, T. O., Shaw, K., Pablo‐Fernández, E. D., Warner, T. T., & Jaunmuktane, Z. (2023) · Practical Neurology · doi:10.1136/pn-2023-003988 · Cited by 37
“37 It may coexist with other primary tauopathies There is severe atrophy of the hippocampus, reduction in bulk of the thalamus (A1, purple arrow), and less prominent atrophy of the frontal lobe (A1).”
BackgroundProgressive Supranuclear Palsy and Corticobasal Degeneration
Coughlin, D. G., Dickson, D. W., Josephs, K. A., & Litvan, I. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-51140-1_11 · Cited by 33
Lee, B. G., Leavitt, M. J., Bernick, C. B., Léger, G. C., Rabinovici, G. D., & Banks, S. J. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2017.5558 · Cited by 34
Early-Onset Dementia in War Veterans: Brain Polypathology and Clinicopathologic Complexity
Iacono, D., Lee, P. J., Edlow, B. L., Gray, N., Fischl, B. R., Kenney, K., Lew, H. L., Lozanoff, S., Liacouras, P. C., Lichtenberger, J. P., et al. (2019) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlz122 · Cited by 32
“In addition, frequent pTau-glia cells of fuzzy type in the WM and gray matter (GM) as per aging-related tau astrogliopathy (ARTAG) were observed (12).”
BackgroundJiang, Y., Huang, H., Abner, E. L., Broster, L. S., Jicha, G. A., Schmitt, F. A., Kryscio, R. J., Andersen, A. H., Powell, D. K., Eldik, L. J. V., et al. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00015 · Cited by 32
“, 2013), cortical Aβ-negative individuals can also have neurodegeneration (as tracked by tau biomarkers; Dickerson and Wolk, 2012; Crary et al., 2014; Kovacs et al., 2016).”
BackgroundMixed TDP-43 proteinopathy and tauopathy in frontotemporal lobar degeneration: nine case series
Kim, E., Brown, J. A., Deng, J., Hwang, J., Spina, S., Miller, Z., DeMay, M. G., Valcour, V., Karydas, A., Ramos, E. M., et al. (2018) · Journal of Neurology · doi:10.1007/s00415-018-9086-2 · Cited by 31
Forrest, S. L., Kril, J. J., & Kovács, G. G. (2021) · JAMA Neurology · doi:10.1001/jamaneurol.2021.1813 · Cited by 31
Distribution Patterns of Astrocyte Populations in the Human Cortex
Forrest, S. L., Kim, J. H., Crockford, D. R., Huynh, K., Cheong, R., Knott, S., Kane, M. A., Ittner, L. M., Halliday, G. M., & Kril, J. J. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03700-2 · Cited by 34
Conte, C., Ingrassia, A. M. T., Brevé, J. J. P., Bol, J. G. J. M., Huisman, E., van Dam, A., Beccari, T., & van de Berg, W. D. J. (2023) · Cells · doi:10.3390/cells12101368 · Cited by 33
“Braak neurofibrillary tangle (NFT) stages [37], CERAD neuritic plaque scores [39] and levels of AD-type pathology were determined according to NIA-AA consensus criteria [40] Additionally, the presence of aging-related tau astrogliopathy (ARTAG) [41] microvascular lesions and hippocampal sclerosis was assessed.”
MethodMcKee, A. C., Stein, T. D., Crary, J. F., Bieniek, K. F., Cantu, R. C., & Kovács, G. G. (2020) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlaa047 · Cited by 31
Concurrent tau pathologies in frontotemporal lobar degeneration with TDP‐43 pathology
Koga, S., Zhou, X., Murakami, A., Fernandez De Castro, C., Baker, M. C., Rademakers, R., & Dickson, D. W. (2022) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12778 · Cited by 30
Self-citationRisk of Misdiagnosing Chronic Traumatic Encephalopathy in Men With Depression
Iverson, G. L., & Gardner, A. J. (2019) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.19010021 · Cited by 30
Arena, J. D., Johnson, V. E., Lee, E. B., Gibbons, G. S., Smith, D. H., Trojanowski, J. Q., & Stewart, W. B., Jr. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa210 · Cited by 31
“Ageingrelated tau astrogliopathy (ARTAG) is increasingly recognized in the brains of older individuals and as a co-morbidity in a variety of neurodegenerative diseases (Kovacs et al., 2016; Kovacs et al., 2017), with its presence suggested to correlate with a greater degree of cognitive impairment (Robinson et al.”
BackgroundInfluentialZhao, X., Zeng, W., Xu, H. W., Sun, Z., Hu, Y., Peng, B., McBride, J. D., Duan, J., Deng, J., Zhang, B., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.abo6889 · Cited by 31
Walker, L., McAleese, K. E., Johnson, M. A., Khundakar, A. A., Erskine, D., Thomas, A. J., McKeith, I. G., & Attems, J. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1702-2 · Cited by 29
Metadata
- Authors
- Kovacs, G. G., Ferrer, I., Grinberg, L. T., Alafuzoff, I., Attems, J., Budka, H., Cairns, N. J., Crary, J. F., Duyckaerts, C., Ghetti, B., Halliday, G. M., Ironside, J. W., Love, S., Mackenzie, I. R., Munoz, D. G., Murray, M. E., Nelson, P. T., Takahashi, H., Trojanowski, J. Q., Ansorge, O., Arzberger, T., Baborie, A., Beach, T. G., Bieniek, K. F., Bigio, E. H., Bodi, I., Dugger, B. N., Feany, M., Gelpi, E., Gentleman, S. M., Giaccone, G., Hatanpaa, K. J., Heale, R., Hof, P. R., Hofer, M., Hortobágyi, T., Jellinger, K., Jicha, G. A., Ince, P., Kofler, J., Kövari, E., Kril, J. J., Mann, D. M., Matej, R., McKee, A. C., McLean, C., Milenkovic, I., Montine, T. J., Murayama, S., Lee, E. B., Rahimi, J., Rodriguez, R. D., Rozemüller, A., Schneider, J. A., Schultz, C., Seeley, W., Seilhean, D., Smith, C., Tagliavini, F., Takao, M., Thal, D. R., Toledo, J. B., Tolnay, M., Troncoso, J. C., Vinters, H. V., Weis, S., Wharton, S. B., White, C. L., Wisniewski, T., Woulfe, J. M., Yamada, M., & Dickson, D. W.
- Affiliations
- Universidade de São Paulo (BR)
- Uppsala University (SE)
- Newcastle University (GB)
- University Hospital Zurich (CH)
- Washington University in St. Louis (US)
- Icahn School of Medicine at Mount Sinai (US)
- Sorbonne Université (FR)
- Indiana University School of Medicine (US)
- UNSW Sydney (AU)
- University of Edinburgh (GB)
- Southmead Hospital (GB)
- University of British Columbia (CA)
- Mayo Clinic (US)
- University of Kentucky (US)
- Brain Research Institute, Niigata University (JP)
- University of Pennsylvania (US)
- John Radcliffe Hospital (GB)
- Institut für Neuropathologie (DE)
- Walton Centre (GB)
- Banner Sun Health Research Institute (US)
- Northwestern University (US)
- University of California, San Francisco (US)
- Brigham and Women's Hospital (US)
- Imperial College London (GB)
- Fondazione IRCCS Istituto Neurologico Carlo Besta (IT)
- The University of Texas Southwestern Medical Center (US)
- University of Debrecen (HU)
- University of Sheffield (GB)
- University of Pittsburgh (US)
- The University of Sydney (AU)
- University of Manchester (GB)
- Boston University (US)
- The Alfred Hospital (AU)
- University of Washington (US)
- Tokyo Metropolitan Institute of Gerontology (JP)
- Vienna General Hospital (AT)
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Rush University Medical Center (US)
- Heidelberg University (DE)
- Saitama International Medical Center (JP)
- Universität Ulm (DE)
- University Hospital of Basel (CH)
- Johns Hopkins University (US)
- University of California, Los Angeles (US)
- Johannes Kepler University of Linz (AT)
- University of Ottawa (CA)
- Kanazawa University (JP)
- Corresponding author
- Dickson, Dennis W.
- ORCID
- Grinberg, Lea T.
- Alafuzoff, Irina
- Attems, Johannes
- Budka, Herbert
- Cairns, Nigel J.
- Crary, John F.
- Duyckaerts, Charles
- Ghetti, Bernardino
- Halliday, Glenda M.
- Ironside, James W.
- Love, Seth
- Mackenzie, Ian R.
- Murray, Melissa E.
- Nelson, Peter T.
- Takahashi, Hitoshi
- Trojanowski, John Q.
- Ansorge, Olaf
- Arzberger, Thomas
- Beach, Thomas G.
- Bieniek, Kevin F.
- Bigio, Eileen H.
- Dugger, Brittany N.
- Feany, Mel
- Giaccone, Giorgio
- Hatanpaa, Kimmo J.
- Heale, Richard
- Hof, Patrick R.
- Hofer, Monika
- Hortobágyi, Tibor
- Jellinger, Kurt
- Jicha, Gregory A.
- Ince, Paul
- Kofler, Julia
- Kril, Jillian J.
- Mann, David M.
- McKee, Ann C.
- McLean, Catriona
- Montine, Thomas J.
- Murayama, Shigeo
- Lee, Edward B.
- Rodriguez, Roberta D.
- Rozemüller, Annemieke
- Schneider, Julie A.
- Schultz, Christian
- Seeley, William
- Seilhean, Danielle
- Smith, Colin
- Tagliavini, Fabrizio
- Takao, Masaki
- Thal, Dietmar Rudolf
- Toledo, Jon B.
- Tolnay, Markus
- Troncoso, Juan C.
- Vinters, Harry V.
- Weis, Serge
- Wharton, Stephen B.
- White, Charles L.
- Woulfe, John M.
- Yamada, Masahito
- Dickson, Dennis W.
- Venue
- Acta Neuropathologica
- Published
- 2015-12-10
- Volume
- 131
- Issue
- 1
- Pages
- 87-102
- ISSN
- 0001-6322 (ISSN-L)
- 1432-0533
- PMC
- PMC4879001
- OpenAlex
- W2195527239
- Cited by
- 532
- References
- 69
- Citations by year
- 2026: 37 · 2025: 49 · 2024: 66 · 2023: 48 · 2022: 57 · 2021: 56 · 2020: 54 · 2019: 51 · 2018: 49 · 2017: 38 · 2016: 25 · 2015: 1
- FWCI
- 27.47
- Type
- journal article
- Language
- en
- Open access
- green
- pure.amsterdamumc.nl
- Licence
- Locations
- Acta Neuropathologica (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Explore Bristol Research (publishedVersion, other-oa)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Bristol Research (University of Bristol) (submittedVersion, other-oa)
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- Lirias (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- IUScholarWorks (Indiana University) (submittedVersion)
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- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- FP7 EU Project (Develage No. 278486)
- National Institutes of Health (NIH P30 AG10133, R01 AG040311, P01 AG019724-03, P50 AG023501, AG010124, AG017586, P50 AG005138, AG028383, P50AG05146, grants P50 AG05136 and P50 NS062684, P50 AG016574 and P50 NS072187)
- NIA Grant (P50 AG05681, P01 AG03991)
- Nelson Family Foundation
- Alzheimer’s Research UK
- Alzheimer's Society, National Institute for Health Research
- Medical Research Council (G0400074, MR/L016400/1, MR/L016400/1 Edinburgh Brain Bank)
- National Health and Medical Research Council of Australia (Senior Principal Research Fellow (#630434))
- Grant Agency of Ministry of Health of Czech Republic (IGA NT12094-5)
- NIA P50 (P50 AG005133)
- National Institute of Neurological Disorders and Stroke (1U01NS086659-01)
- National Institute of Aging Boston University Alzheimer’s Disease Center (P30AG13846; supplement 0572063345–5)
- MRC (MC-PC-13044)
- National Brain Research Program, Hungary (KTIA_13_NAP-A-II/7)
- Grant-in-Aid (KAKEN 26250017)
- NIH (P30AG12300)
- DFG Grant (SFB 1134/A03)
- Alzheimer's Disease Core Center (P30AG008051-26)
- Grant (AG13854)
- JSPS KAKENHI (26430060)
- Italian Ministry of Health
- Vienna KIN-Neurobiobank and VITA–study
- France Alzheimer, France Parkinson, Fondacion ARSEP and CSC (GIE NeuroCEB)
- Neuroscience Research Australia and the University of New South Wales (Sydney Brain Bank)
- Sheffield and Cambridge Brain Banks (Brain Banks)
- Parkinson's UK (Parkinson's UK Tissue Bank at Imperial College)
- 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
- tau phosphorylation, astrocytes, glia limitans, white matter, gray matter, primary tauopathies, nomenclature, brain aging, clinical biomarkers
- MeSH terms
- Aging, Animals, Astrocytes, Brain, Humans, Neuroglia, tau Proteins, Tauopathies
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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