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Cited by 71Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsMedical Imaging Techniques and Applications

Staging tau pathology with tau PET in Alzheimer’s disease: a longitudinal study

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Chen, Shi-Dong, Lu, Jia-Ying, Li, Hong-Qi, Yang, Yu-Xiang, Jiang, Jie-Hui, Cui, Mei, Zuo, Chuan-Tao, Tan, Lan +482 more·2021·Translational Psychiatry
DOI 10.1038/s41398-021-01602-5PMC PMC8449785
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Abstract

A biological research framework to define Alzheimer’ disease with dichotomized biomarker measurement was proposed by National Institute on Aging–Alzheimer’s Association (NIA–AA). However, it cannot characterize the hierarchy spreading pattern of tau pathology. To reflect in vivo tau progression using biomarker, we constructed a refined topographic 18 F-AV-1451 tau PET staging scheme with longitudinal clinical validation. Seven hundred and thirty-four participants with baseline 18 F-AV-1451 tau PET (baseline age 73.9 ± 7.7 years, 375 female) were stratified into five stages by a topographic PET staging scheme. Cognitive trajectories and clinical progression were compared across stages with or without further dichotomy of amyloid status, using linear mixed-effect models and Cox proportional hazard models. Significant cognitive decline was first observed in stage 1 when tau levels only increased in transentorhinal regions. Rates of cognitive decline and clinical progression accelerated from stage 2 to stage 3 and stage 4. Higher stages were also associated with greater CSF phosphorylated tau and total tau concentrations from stage 1. Abnormal tau accumulation did not appear with normal β-amyloid in neocortical regions but prompt cognitive decline by interacting with β-amyloid in temporal regions. Highly accumulated tau in temporal regions independently led to cognitive deterioration. Topographic PET staging scheme have potentials in early diagnosis, predicting disease progression, and studying disease mechanism. Characteristic tau spreading pattern in Alzheimer’s disease could be illustrated with biomarker measurement under NIA–AA framework. Clinical–neuroimaging–neuropathological studies in other cohorts are needed to validate these findings.

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  • The middle temporal gyrus is a transition zone between aging-related or preclinical AD-related medial temporal lobe pTau and more advanced stages of AD, where neocortical pTau extends across the brain and is strongly correlated with dementia.

    “Many studies, from the histopathology of Braak and Braak4 to longitudinal studies of Tau positron emission tomography imaging27,28, demonstrate that MTG is a transition zone between aging-related or preclinical AD-related medial temporal lobe pTau and more advanced stages of AD, where neocortical pTau extends across the brain and is strongly correlated with dementia4,29–31.”

    From Integrated multimodal cell atlas of Alzheimer’s disease (2024) · cites this paper as [28]

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Authors
Chen, S.-D., Lu, J.-Y., Li, H.-Q., Yang, Y.-X., Jiang, J.-H., Cui, M., Zuo, C.-T., Tan, L., Dong, Q., Yu, J.-T., Initiative, F. T. A. D. N., Weiner, M. W., Aisen, P., Petersen, R., Jack, C. R., Jagust, W., Trojanowki, J. Q., Toga, A. W., Beckett, L., Green, R. C., Saykin, A. J., Morris, J. C., Perrin, R. J., Shaw, L. M., Carrillo, M., Potter, W., Barnes, L., Bernard, M., González, H., Ho, C., Hsiao, J. K., Jackson, J., Masliah, E., Masterman, D., Okonkwo, O., Perrin, R., Ryan, L., Silverberg, N., Fleisher, A., Sacrey, D. T., Fockler, J., Conti, C., Veitch, D., Neuhaus, J., Jin, C., Nosheny, R., Ashford, M., Flenniken, D., Kormos, A., Rafii, M., Raman, R., Jimenez, G., Donohue, M., Gessert, D., Salazar, J., Zimmerman, C., Cabrera, Y., Walter, S., Miller, G., Coker, G., Clanton, T., Hergesheimer, L., Smith, S., Adegoke, O., Mahboubi, P., Moore, S., Pizzola, J., Shaffer, E., Sloan, B., Harvey, D., Forghanian-Arani, A., Borowski, B., Ward, C., Schwarz, C., Jones, D., Gunter, J., Kantarci, K., Senjem, M., Vemuri, P., Reid, R., Fox, N. C., Malone, I., Thompson, P., Thomopoulos, S. I., Nir, T. M., Jahanshad, N., DeCarli, C., Knaack, A., Fletcher, E., Tosun-Turgut, D., Chen, S. R., Choe, M., Crawford, K., Yushkevich, P. A., Das, S., Koeppe, R. A., Reiman, E. M., Chen, K., Mathis, C., Landau, S., Cairns, N. J., Householder, E., Franklin, E., Bernhardt, H., Taylor-Reinwald, L., Shaw, L. M., Trojanowki, J. Q., Korecka, M., Figurski, M., Crawford, K., Neu, S., Saykin, A. J., Nho, K., Risacher, S. L., Apostolova, L. G., Shen, L., Foroud, T. M., Nudelman, K., Faber, K., Wilmes, K., Thal, L., Khachaturian, Z., Hsiao, J. K., Silbert, L. C., Lind, B., Crissey, R., Kaye, J. A., Carter, R., Dolen, S., Quinn, J., Schneider, L. S., Pawluczyk, S., Becerra, M., Teodoro, L., Dagerman, K., Spann, B. M., Brewer, J., Vanderswag, H., Fleisher, A., Ziolkowski, J., Heidebrink, J. L., Zbizek-Nulph, L., Lord, J. L., Mason, S. S., Albers, C. S., Knopman, D., Johnson, K., Villanueva-Meyer, J., Pavlik, V., Pacini, N., Lamb, A., Kass, J. S., Doody, R. S., Shibley, V., Chowdhury, M., Rountree, S., Dang, M., Stern, Y., Honig, L. S., Mintz, A., Ances, B., Winkfield, D., Carroll, M., Stobbs-Cucchi, G., Oliver, A., Creech, M. L., Mintun, M. A., Schneider, S., Geldmacher, D., Love, M. N., Griffith, R., Clark, D., Brockington, J., Marson, D., Grossman, H., Goldstein, M. A., Greenberg, J., Mitsis, E., Shah, R. C., Lamar, M., Samuels, P., Duara, R., Greig-Custo, M. T., Rodriguez, R., Albert, M., Onyike, C., Farrington, L., Rudow, S., Brichko, R., Kielb, S., Smith, A., Raj, B. A., Fargher, K., Sadowski, M., Wisniewski, T., Shulman, M., Faustin, A., Rao, J., Castro, K. M., Ulysse, A., Chen, S., Sheikh, M. O., Singleton-Garvin, J., Doraiswamy, P. M., Petrella, J. R., James, O., Wong, T. Z., Borges-Neto, S., Karlawish, J. H., Wolk, D. A., Vaishnavi, S., Clark, C. M., Arnold, S. E., Smith, C. D., Jicha, G. A., El Khouli, R., Raslau, F. D., Lopez, O. L., Oakley, M., Simpson, D. M., Porsteinsson, A. P., Martin, K., Kowalski, N., Keltz, M., Goldstein, B. S., Makino, K. M., Ismail, M. S., Brand, C., Thai, G., Pierce, A., Yanez, B., Sosa, E., Witbracht, M., Kelley, B., Nguyen, T., Womack, K., Mathews, D., Quiceno, M., Levey, A. I., Lah, J. J., Hajjar, I., Cellar, J. S., Burns, J. M., Swerdlow, R. H., Brooks, W. M., Silverman, D. H. S., Kremen, S., Apostolova, L., Tingus, K., Lu, P. H., Bartzokis, G., Woo, E., Teng, E., Graff-Radford, N. R., Parfitt, F., Poki-Walker, K., Farlow, M. R., Hake, A. M., Matthews, B. R., Brosch, J. R., Herring, S., van Dyck, C. H., Mecca, A. P., Good, S. P., MacAvoy, M. G., Carson, R. E., Varma, P., Chertkow, H., Vaitekunis, S., Hosein, C., Black, S., Stefanovic, B., Heyn, C., Hsiung, G.-Y. R., Kim, E., Mudge, B., Sossi, V., Feldman, H., Assaly, M., Finger, E., Pasternak, S., Rachinsky, I., Kertesz, A., Drost, D., Rogers, J., Grant, I., Muse, B., Rogalski, E., Robson, J., Mesulam, M.-M., Kerwin, D., Wu, C.-K., Johnson, N., Lipowski, K., Weintraub, S., Bonakdarpour, B., Pomara, N., Hernando, R., Sarrael, A., Rosen, H. J., Miller, B. L., Perry, D., Turner, R. S., Johnson, K., Reynolds, B., MCCann, K., Poe, J., Sperling, R. A., Johnson, K. A., Marshall, G. A., Belden, C. M., Atri, A., Spann, B. M., Clark, K. A., Zamrini, E., Sabbagh, M., Killiany, R., Stern, R., Mez, J., Kowall, N., Budson, A. E., Obisesan, T. O., Ntekim, O. E., Wolday, S., Khan, J. I., Nwulia, E., Nadarajah, S., Lerner, A., Ogrocki, P., Tatsuoka, C., Fatica, P., Fletcher, E., Maillard, P., Olichney, J., DeCarli, C., Carmichael, O., Bates, V., Capote, H., Rainka, M., Borrie, M., Lee, T.-Y., Bartha, R., Johnson, S., Asthana, S., Carlsson, C. M., Perrin, A., Burke, A., Scharre, D. W., Kataki, M., Tarawneh, R., Kelley, B., Hart, D., Zimmerman, E. A., Celmins, D., Miller, D. D., Boles Ponto, L. L., Smith, K. E., Koleva, H., Shim, H., Nam, K. W., Schultz, S. K., Williamson, J. D., Craft, S., Cleveland, J., Yang, M., Sink, K. M., Ott, B. R., Drake, J., Tremont, G., Daiello, L. A., Drake, J. D., Sabbagh, M., Ritter, A., Bernick, C., Munic, D., Mintz, A., O’Connelll, A., Mintzer, J., Wiliams, A., Masdeu, J., Shi, J., Garcia, A., Sabbagh, M., Newhouse, P., Potkin, S., Salloway, S., Malloy, P., Correia, S., Kittur, S., Pearlson, G. D., Blank, K., Anderson, K., Flashman, L. A., Seltzer, M., Hynes, M. L., Santulli, R. B., Relkin, N., Chiang, G., Lin, M., Ravdin, L., Lee, A., Petersen, R., Neylan, T., Grafman, J., Montine, T., Petersen, R., Hergesheimer, L., Danowski, S., Nguyen-Barrera, C., Hayes, J., Finley, S., Donohue, M., Bernstein, M., Senjem, M., Ward, C., Chen, S. R., Koeppe, R. A., Foster, N., Foroud, T. M., Potkin, S., Shen, L., Faber, K., Kim, S., Nho, K., Wilmes, K., Spann, B. M., Vanderswag, H., Fleisher, A., Sood, A., Blanchard, K. S., Fleischman, D., Arfanakis, K., Varon, D., Greig, M. T., Goldstein, B., Martin, K. S., Thai, G., Pierce, A., Reist, C., Yanez, B., Sosa, E., Witbracht, M., Sadowsky, C., Martinez, W., Villena, T., Rosen, H., Marshall, G., Nadarajah, S., Peskind, E. R., Petrie, E. C., Li, G., Yesavage, J., Taylor, J. L., Chao, S., Coleman, J., White, J. D., Lane, B., Rosen, A., Tinklenberg, J., Chiang, G., Mackin, S., Raman, R., Jimenez-Maggiora, G., Gessert, D., Salazar, J., Zimmerman, C., Walter, S., Adegoke, O., Mahboubi, P., Drake, E., Donohue, M., Nelson, C., Bickford, D., Butters, M., Zmuda, M., Borowski, B., Gunter, J., Senjem, M., Kantarci, K., Ward, C., Reyes, D., Faber, K. M., Nudelman, K. N., Au, Y. H., Scherer, K., Catalinotto, D., Stark, S., Ong, E., Fernandez, D., & Zmuda, M.
Affiliations
  • Shanghai Medical College of Fudan University (CN)
  • Qingdao University (CN)
  • University of Southern California (US)
  • Mayo Clinic (US)
  • University of Pennsylvania (US)
  • University of California, Davis (US)
  • Indiana University Bloomington (US)
  • Washington University in St. Louis (US)
  • National Institutes of Health (US)
  • University of California San Diego (US)
  • Biogen (United States) (US)
  • University of Wisconsin–Madison (US)
  • University of California, San Francisco (US)
  • Northern California Institute for Research and Education (US)
  • Mayo Clinic in Arizona (US)
  • University College London (GB)
  • University of Michigan (US)
  • Banner Alzheimer’s Institute (US)
  • University of Pittsburgh (US)
  • Indiana University School of Medicine (US)
  • Oregon Health & Science University (US)
  • Brigham and Women's Hospital (US)
  • Baylor College of Medicine (US)
  • Columbia University Irving Medical Center (US)
  • University of Alabama at Birmingham (US)
  • Icahn School of Medicine at Mount Sinai (US)
  • Rush University Medical Center (US)
  • Johns Hopkins University (US)
  • University of South Florida (US)
  • New York University (US)
  • Duke Medical Center (US)
  • University of Kentucky (US)
  • University of Rochester Medicine (US)
  • University of California, Irvine (US)
  • The University of Texas Southwestern Medical Center (US)
  • Emory University (US)
  • University of Kansas Medical Center (US)
  • University of California, Los Angeles (US)
  • Yale University (US)
  • Jewish General Hospital (CA)
  • Sunnybrook Health Science Centre (CA)
  • Northwestern University (US)
  • Nathan Kline Institute for Psychiatric Research (US)
  • Georgetown University Medical Center (US)
  • Banner Sun Health Research Institute (US)
  • Boston University (US)
  • Howard University (US)
  • Case Western Reserve University (US)
  • Dent Neurologic Institute (US)
  • Parkwood Institute (CA)
  • The Ohio State University (US)
  • Albany Medical College (US)
  • University of Iowa (US)
  • Wake Forest University Health Sciences (US)
  • Rhode Island Hospital (US)
  • Cleveland Clinic (US)
  • Roper St. Francis Healthcare (US)
  • Houston Methodist (US)
  • Barrow Neurological Institute (US)
  • Vanderbilt University Medical Center (US)
  • Butler Hospital (US)
  • Hartford Hospital (US)
  • Dartmouth–Hitchcock Medical Center (US)
  • Cornell University (US)
  • University of Utah (US)
  • Palm Beach Neurology (US)
  • University of Washington (US)
  • Stanford University (US)
Corresponding author
  • Tan, Lan
  • Dong, Qiang
  • Yu, Jin-Tai
ORCID
Venue
Translational Psychiatry
Publisher
Springer Science and Business Media LLC
Published
2021-09-18
Volume
11
Issue
1
Pages
483-483
ISSN
2158-3188 (ISSN-L)
DOI
10.1038/s41398-021-01602-5
PMC
PMC8449785
OpenAlex
W3201026716
Cited by
71
References
9
Citations by year
2026: 13 · 2025: 21 · 2024: 13 · 2023: 11 · 2022: 13
FWCI
6.64
Type
journal article
Language
en
Open access
Licence
Locations
  • Translational Psychiatry (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • IUScholarWorks (Indiana University) (submittedVersion, cc-by)
  • eScholarship (California Digital Library) (submittedVersion)
  • Civil War Book Review (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UCL Discovery (University College London) (submittedVersion)
  • Scholarship@Western (Western University) (submittedVersion)
Funders
  • U.S. Department of Defense (U01 AG024904, W81XWH, W81XWH-12-2-, W81XWH-12, W81XWH1220012, AG024904)
  • Foundation for the National Institutes of Health (W81XWH-12-2-0012, U01AG024904, Grant U01 AG024904, AG024904)
  • Alzheimer's Association (U01 AG024904, W81XWH-12-2-0012)
  • Bristol-Myers Squibb (U01 AG024904, AG024904, W81XWH-12-2-0012)
  • Eli Lilly and Company (U01 AG024904, AG024904, W81XWH-12-2-0012)
  • Pfizer (AG024904, W81XWH-12-2-0012, U01 AG024904)
  • Biogen (W81XWH-12-2-0012, U01 AG024904, AG024904)
  • University of Southern California (W81XWH-12-2-0012, U01 AG024904)
  • F. Hoffmann-La Roche (W81XWH-12-2-0012, AG024904, U01 AG024904)
  • Meso Scale Diagnostics (U01 AG024904, AG024904, W81XWH-12-2-0012)
  • Alzheimer's Disease Neuroimaging Initiative (W81XWH-12-2–0012, U01AG024904, AG024904, W81XWH-12-2-, Department of Defense award number W81XWH-12-2-0012)
  • BioClinica (U01 AG024904, W81XWH-12-2-0012, AG024904)
  • Novartis Pharmaceuticals Corporation (W81XWH-12-2-0012, U01 AG024904, AG024904)
  • Northern California Institute for Research and Education (U01 AG024904, W81XWH-12-2-0012)
  • National Natural Science Foundation of China (81771148, 2018YFC1314700, 91849126, U01 AG024904, W81XWH-12-2-0012, 2018SHZDZX01, 81571245)
  • Fudan University (2018SHZDZX01)
  • Eisai (W81XWH-12-2-0012, U01 AG024904, AG024904)
  • Servier (AG024904, W81XWH-12-2-0012, U01 AG024904)
  • H. Lundbeck A/S (U01 AG024904, AG024904, W81XWH-12-2-0012)
  • IXICO (AG024904, W81XWH-12-2-0012, U01 AG024904)
  • National Institutes of Health (3u01ag024904-10s2, UL1TR001422, W81XWH, W81XWH-12-2-0012, U01-AG024904, Grant U01 AG024904, AG024904)
  • Genentech (W81XWH-12-2-0012, AG024904, U01 AG024904)
  • Canadian Institutes of Health Research (U01 AG024904, W81XWH-12-2-0012)
  • National Institute on Aging (U01-AG-024904, P30AG066512, W81XWH-12-2–0012, AG 024904)
  • National Institute of Biomedical Imaging and Bioengineering (W81XWH-12-2-0012, U01 AG024904, AG024904)
  • National Center for Advancing Translational Sciences
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Medical Imaging Techniques and Applications
Keywords
Alzheimer's disease, tau PET, 18F-AV-1451, tau pathology, cognitive decline, amyloid, phosphorylated tau, cerebrospinal fluid biomarkers, temporal lobe, disease progression, NIA-AA criteria, early diagnosis
MeSH terms
Aged, Aged, 80 and over, Alzheimer Disease, Female, Humans, Longitudinal Studies, Male, Biomarkers, Amyloid beta-Peptides, tau Proteins, Positron-Emission Tomography, Cognitive Dysfunction

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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