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Prevalence of Cerebral Amyloid Pathology in Persons Without Dementia: A Meta-analysis
Open accessAbstract
IMPORTANCE: Cerebral amyloid-β aggregation is an early pathological event in Alzheimer disease (AD), starting decades before dementia onset. Estimates of the prevalence of amyloid pathology in persons without dementia are needed to understand the development of AD and to design prevention studies. OBJECTIVE: To use individual participant data meta-analysis to estimate the prevalence of amyloid pathology as measured with biomarkers in participants with normal cognition, subjective cognitive impairment (SCI), or mild cognitive impairment (MCI). DATA SOURCES: Relevant biomarker studies identified by searching studies published before April 2015 using the MEDLINE and Web of Science databases and through personal communication with investigators. STUDY SELECTION: Studies were included if they provided individual participant data for participants without dementia and used an a priori defined cutoff for amyloid positivity. DATA EXTRACTION AND SYNTHESIS: Individual records were provided for 2914 participants with normal cognition, 697 with SCI, and 3972 with MCI aged 18 to 100 years from 55 studies. MAIN OUTCOMES AND MEASURES: Prevalence of amyloid pathology on positron emission tomography or in cerebrospinal fluid according to AD risk factors (age, apolipoprotein E [APOE] genotype, sex, and education) estimated by generalized estimating equations. RESULTS: The prevalence of amyloid pathology increased from age 50 to 90 years from 10% (95% CI, 8%-13%) to 44% (95% CI, 37%-51%) among participants with normal cognition; from 12% (95% CI, 8%-18%) to 43% (95% CI, 32%-55%) among patients with SCI; and from 27% (95% CI, 23%-32%) to 71% (95% CI, 66%-76%) among patients with MCI. APOE-ε4 carriers had 2 to 3 times higher prevalence estimates than noncarriers. The age at which 15% of the participants with normal cognition were amyloid positive was approximately 40 years for APOE ε4ε4 carriers, 50 years for ε2ε4 carriers, 55 years for ε3ε4 carriers, 65 years for ε3ε3 carriers, and 95 years for ε2ε3 carriers. Amyloid positivity was more common in highly educated participants but not associated with sex or biomarker modality. CONCLUSIONS AND RELEVANCE: Among persons without dementia, the prevalence of cerebral amyloid pathology as determined by positron emission tomography or cerebrospinal fluid findings was associated with age, APOE genotype, and presence of cognitive impairment. These findings suggest a 20- to 30-year interval between first development of amyloid positivity and onset of dementia.
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“This possibility has remained unaddressed, because case–control studies without neuropathological or biomarker assessments of AD may have underestimated the impact of APOE genotypes on Alzheimer’s dementia ORs due to the confounding effects of APOE genotypes on the percentages of neuropathologically misclassified cases and controls8–10.”
From Exceptionally low likelihood of Alzheimer’s dementia in APOE2 homozygotes from a 5,000-person neuropathological study (2020) · cites this paper as [10]
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“Due to the prioritized ascertainment of those cases who met the clinical and neuropathological criteria for Alzheimer’s dementia and those unimpaired controls without AD, the number of misclassified cases and controls available through the AD Genetics Consortium12 is much smaller than our estimated number of neuropathologically misclassified cases and controls8–11, limiting our ability to clarify”
From Exceptionally low likelihood of Alzheimer’s dementia in APOE2 homozygotes from a 5,000-person neuropathological study (2020) · cites this paper as [10]
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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“the Aβ load, which has been our main target, correlates better with age than disease severity in AD [291,292,293]”
From Ageing, Cellular Senescence and Neurodegenerative Disease (2018) · cites this paper as [293]
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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 [60]
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“In epidemiological cohorts assessing patients without dementia using amyloid PET status or CSF profile, Aβ pathology was associated with APOE genotype, presence of cognitive impairment and suggested a 2- to 30- year interval between first development of Αβ positivity and onset of dementia [3, 169].”
From The use of neuroimaging techniques in the early and differential diagnosis of dementia (2023) · cites this paper as [169]
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“The association of the APOE4 isoform with amyloid deposition has been well established in human studies, where APOE4 carriers exhibit higher A β plaque burden and earlier onset of amyloid positivity compared with non-carriers 35 -37 .”
From APOE2 attenuates APOE4-associated amyloid pathology and related toxicity in a mouse model of Alzheimer’s disease (2026) · cites this paper as [35]
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“In addition, those with the e4 form are more likely to have beta-amyloid accumulation and Alzheimer's dementia at a younger age than those with the e2 or e3 forms of the APOE gene.76,77”
From 2023 Alzheimer's disease facts and figures (2023) · cites this paper as [76]
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“A meta-analysis reported a prevalence of amyloid pathology among individuals with SCD of 12%-43% [22].”
From Neuroimaging advances regarding subjective cognitive decline in preclinical Alzheimer's disease (2020) · cites this paper as [22]
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“Owing to the substantially higher prevalence of Aβ+ in APOE ε4 carriers18,19,28, plasma biomarkers had higher PPVs for brain amyloid-β, particularly in individuals with MCI.”
From Diagnosis of Alzheimer's disease using plasma biomarkers adjusted to clinical probability (2024) · cites this paper as [28]
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“and a similar proportion has abnormal amyloid biomarkers [33,53–55,60,70–73].”
From NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease (2018) · cites this paper as [60]
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In the citing paper
“In epidemiological cohorts assessing patients without dementia using amyloid PET status or CSF profile, Aβ pathology was associated with APOE genotype, presence of cognitive impairment and suggested a 2- to 30- year interval between first development of Αβ positivity and onset of dementia [3, 169].”
From The use of neuroimaging techniques in the early and differential diagnosis of dementia (2023) · cites this paper as [169]
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“In a previous autopsy study, we found that 25% of persons with the clinical diagnosis of mild-to-moderate Alzheimer’s dementia lacked at least moderately frequent neuritic plaques, one of the cardinal features of AD, including 37% of APOE4 non-carriers and 13% of carriers, findings that are consistent with those in living patients9,10.”
From Exceptionally low likelihood of Alzheimer’s dementia in APOE2 homozygotes from a 5,000-person neuropathological study (2020) · cites this paper as [10]
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“and a similar proportion has normal amyloid PET or CSF Aβ42 studies [53–62].”
From NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease (2018) · cites this paper as [60]
Experimental — accuracy not yet measuredIn the citing paper
“Substantial amyloid pathology is already present in the neocortex decades prior to overt AD symptomatology”
From The amyloid hypothesis in Alzheimer disease: new insights from new therapeutics (2022) · cites this paper as [17]
In the citing paper
“The trigger scenario can be discounted as the onset of amyloid deposition may occur ~20 years prior to cognitive alterations”
From The amyloid hypothesis in Alzheimer disease: new insights from new therapeutics (2022) · cites this paper as [17]
In the citing paper
“Between the appearance of amyloid plaques and neuronal tangles in the human brain, to the ultimate dementia in patients, up to twenty years may elapse (Bateman et al. , 2012; Villemagne et al. , 2013; Jansen et al. , 2015).”
From Spatial Transcriptomics and In Situ Sequencing to Study Alzheimer’s Disease (2020) · cites this paper as Jansen et al., 2015
In the citing paper
“Attempts to quantify the duration of AD should be age-specific, because age imposes the greatest risk for both dementia and mortality, and take into account APOE genotype, sex, and cerebrospinal fluid (CSF) tau levels [4, 6, 10-12].”
From Duration of preclinical, prodromal, and dementia stages of Alzheimer's disease in relation to age, sex, and APOE genotype (2019) · cites this paper as [4]
In the citing paper
“Accumulation of amyloid in the brain is believed to be the first sign of the disease and can precede a clinical diagnosis of dementia by up to 20 years [1, 4, 5].”
From Duration of preclinical, prodromal, and dementia stages of Alzheimer's disease in relation to age, sex, and APOE genotype (2019) · cites this paper as [4]
In the citing paper
“Among individuals who were cognitively unimpaired on objective cognitive testing, there was no difference in frequency of CSF Alzheimer’s disease profiles between people with and people without subjective cognitive decline.83”
From Clinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group (2021) · cites this paper as [83]
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Prevalence Estimates of Amyloid Abnormality Across the Alzheimer Disease Clinical Spectrum
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Self-citationNeuroimaging advances regarding subjective cognitive decline in preclinical Alzheimer's disease
Wang, X., Huang, W., Su, L., Xing, Y., Jessen, F., Sun, Y., Shu, N., & Han, Y. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00395-3 · Cited by 265
Borghammer, P. (2021) · Journal of Parkinson's Disease · doi:10.3233/jpd-202481 · Cited by 259
Recommendations of the 5th Canadian Consensus Conference on the diagnosis and treatment of dementia
Ismail, Z., Black, S. E., Camicioli, R., Chertkow, H., Herrmann, N., Laforce, R., Montero‐Odasso, M., Rockwood, K., Rosa‐Neto, P., Seitz, D., et al. (2020) · Alzheimer's & Dementia · doi:10.1002/alz.12105 · Cited by 245
Towards a future where Alzheimer’s disease pathology is stopped before the onset of dementia
van der Flier, W. M., de Vugt, M. E., Smets, E. M. A., Blom, M., & Teunissen, C. E. (2023) · Nature Aging · doi:10.1038/s43587-023-00404-2 · Cited by 220
Self-citationRoberts, R. O., Aakre, J. A., Kremers, W. K., Vassilaki, M., Knopman, D. S., Mielke, M. M., Alhurani, R., Geda, Y. E., Machulda, M. M., Coloma, P., et al. (2018) · JAMA Neurology · doi:10.1001/jamaneurol.2018.0629 · Cited by 223
Alzheimer’s Disease: Key Insights from Two Decades of Clinical Trial Failures
Kim, C. K., Lee, Y. R., Ong, L., Gold, M., Kalali, A., & Sarkar, J. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215699 · Cited by 241
Tau Protein Interaction Partners and Their Roles in Alzheimer’s Disease and Other Tauopathies
Sinsky, J., Pichlerova, K., & Hanes, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179207 · Cited by 220
Morris, G. P., Clark, I. A., & Vissel, B. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1918-8 · Cited by 212
Prevalence of amyloid‐β pathology in distinct variants of primary progressive aphasia
Bergeron, D., Gorno‐Tempini, M. L., Rabinovici, G. D., Santos‐Santos, M. A., Seeley, W., Miller, B. L., Pijnenburg, Y., Keulen, M. A., Groot, C., van Berckel, B. N. M., et al. (2018) · Annals of Neurology · doi:10.1002/ana.25333 · Cited by 203
Self-citationNeuroinflammation and neurogenesis in Alzheimer's disease and potential therapeutic approaches
Sung, P.-S., Lin, P.-Y., Liu, C.-H., Su, H.-C., & Tsai, K.-J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030701 · Cited by 193
Amyloid blood biomarker detects Alzheimer's disease
Nabers, A., Perna, L., Lange, J., Mons, U., Schartner, J., Güldenhaupt, J., Saum, K., Janelidze, S., Holleczek, B., Rujescu, D., et al. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201708763 · Cited by 185
The use of neuroimaging techniques in the early and differential diagnosis of dementia
Chouliaras, L., & O’Brien, J. T. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02215-8 · Cited by 221
“In epidemiological cohorts assessing patients without dementia using amyloid PET status or CSF pro fi le, A β pathology was associated with APOE genotype, presence of cognitive impairment and suggested a 2-to 30-year interval between fi rst development of Αβ positivity and onset of dementia [3, 169].”
BackgroundDuara, R., & Barker, W. (2022) · Neurotherapeutics · doi:10.1007/s13311-022-01185-z · Cited by 187
The pre-synaptic vesicle protein synaptotagmin is a novel biomarker for Alzheimer’s disease
Öhrfelt, A., Brinkmalm, A., Dumurgier, J., Brinkmalm, G., Hansson, O., Zetterberg, H., Bouaziz-Amar, E., Hugon, J., Paquet, C., & Blennow, K. (2016) · Alzheimer's Research & Therapy · doi:10.1186/s13195-016-0208-8 · Cited by 184
Self-citationDistinct 18F-AV-1451 tau PET retention patterns in early- and late-onset Alzheimer’s disease
Schöll, M., Ossenkoppele, R., Strandberg, O., Palmqvist, S., study, T. S. B., Jögi, J., Ohlsson, T., Smith, R., & Hansson, O. (2017) · Brain · doi:10.1093/brain/awx171 · Cited by 180
Self-citationAmyloid‐β immunotherapy for alzheimer disease: Is it now a long shot?
Panza, F., Lozupone, M., Seripa, D., & Imbimbo, B. P. (2019) · Annals of Neurology · doi:10.1002/ana.25410 · Cited by 178
The BACE‐1 inhibitor CNP520 for prevention trials in Alzheimer's disease
Neumann, U., Ufer, M., Jacobson, L. H., Rouzade‐Dominguez, M., Huledal, G., Kolly, C., Lüönd, R. M., Machauer, R., Veenstra, S. J., Hurth, K., et al. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201809316 · Cited by 177
“…with a biomarker signature for ongoing Ab deposition both in the APOE4 non-carrier and in the carrier group, but the proportion was higher in the carrier group, in line with reports documenting an increased risk of early Ab deposition in APOE4 carriers (Jansen et al, 2015; Hollands et al, 2017).”
ResultBrookmeyer, R., & Abdalla, N. (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.03.005 · Cited by 176
A second X chromosome contributes to resilience in a mouse model of Alzheimer’s disease
Davis, E. J., Broestl, L., Abdulai-Saiku, S., Worden, K., Bonham, L. W., Miñones-Moyano, E., Moreno, A. J., Wang, D., Chang, K., Williams, G., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aaz5677 · Cited by 176
Circadian disruption and sleep disorders in neurodegeneration
Shen, Y., Lv, Q.-K., Xie, W.-Y., Gong, S.-Y., Zhuang, S., Liu, J.-Y., Mao, C.-J., & Liu, C.-F. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00340-6 · Cited by 171
Local and distant relationships between amyloid, tau and neurodegeneration in Alzheimer's Disease
Iaccarino, L., Tammewar, G., Ayakta, N., Baker, S. L., Bejanin, A., Boxer, A. L., Gorno-Tempini, M. L., Janabi, M., Kramer, J. H., Lazaris, A., et al. (2018) · NeuroImage: Clinical · doi:10.1016/j.nicl.2017.09.016 · Cited by 165
Self-citationOssenkoppele, R., Lyoo, C. H., Jester-Broms, J., Sudre, C. H., Cho, H., Ryu, Y. H., Choi, J. Y., Smith, R., Strandberg, O., Palmqvist, S., et al. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2019.5154 · Cited by 161
Herbert, J., & Lucassen, P. J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.12.001 · Cited by 150
Markers of neuroinflammation associated with Alzheimer’s disease pathology in older adults
Popp, J., Oikonomidi, A., Tautvydaitė, D., Dayon, L., Bacher, M., Migliavacca, E., Henry, H., Kirkland, R., Severin, I., Wojcik, J., et al. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.01.020 · Cited by 136
Self-citationMahan, T. E., Wang, C., Bao, X., Choudhury, A., Ulrich, J. D., & Holtzman, D. M. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00516-0 · Cited by 134
Huynh, T.-P. V., Wang, C., Tran, A. C., Tabor, G. T., Mahan, T. E., Francis, C. M., Finn, M. B., Spellman, R., Manis, M., Tanzi, R. E., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0337-1 · Cited by 139
Utilizing the Centiloid scale in cross-sectional and longitudinal PiB PET studies
Su, Y., Flores, S., Hornbeck, R. C., Speidel, B., Vlassenko, A. G., Gordon, B. A., Koeppe, R. A., Klunk, W. E., Xiong, C., Morris, J. C., et al. (2018) · NeuroImage: Clinical · doi:10.1016/j.nicl.2018.04.022 · Cited by 126
Self-citationDESGESCO (Dementia Genetics Spanish Consortium), E. (. D. E. D. B., van der Lee, S. J., biobank), E. (. D. E. D., IFGC (International FTD-Genomics Consortium), I. (. I. P. D. G. C., IPDGC (The International Parkinson Disease Genomics Consortium), Dementia), R.-F. (. A. M. F. I. F.-T., (NBB), N. B. B., The GIFT (Genetic Investigation in Frontotemporal Dementia and Alzheimer’s Disease) Study Group, Conway, O. J., Jansen, I., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-02026-8 · Cited by 120
Self-citationThe implications of different approaches to define AT(N) in Alzheimer disease
Mattsson-Carlgren, N., Leuzy, A., Janelidze, S., Palmqvist, S., Stomrud, E., Strandberg, O., Smith, R., & Hansson, O. (2020) · Neurology · doi:10.1212/wnl.0000000000009485 · Cited by 114
Developing Effective Alzheimer’s Disease Therapies: Clinical Experience and Future Directions
Elmaleh, D. R., Farlow, M. R., Conti, P. S., Tompkins, R. G., Kundakovic, L., & Tanzi, R. E. (2019) · Journal of Alzheimer’s Disease · doi:10.3233/jad-190507 · Cited by 129
Jack, C. R., Therneau, T. M., Wiste, H. J., Weigand, S. D., Knopman, D. S., Lowe, V. J., Mielke, M. M., Vemuri, P., Roberts, R. O., Machulda, M. M., et al. (2016) · The Lancet Neurology · doi:10.1016/s1474-4422(15)00323-3 · Cited by 129
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Self-citationPredicting future rates of tau accumulation on PET
Jack, C. R., Wiste, H. J., Weigand, S. D., Therneau, T. M., Lowe, V. J., Knopman, D. S., Botha, H., Graff-Radford, J., Jones, D. T., Ferman, T. J., et al. (2020) · Brain · doi:10.1093/brain/awaa248 · Cited by 117
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Self-citationDiagnosis of Alzheimer's disease using plasma biomarkers adjusted to clinical probability
Therriault, J., Janelidze, S., Benedet, A. L., Ashton, N. J., Arranz Martínez, J., Gonzalez-Escalante, A., Bellaver, B., Alcolea, D., Vrillon, A., Karim, H., et al. (2024) · Nature Aging · doi:10.1038/s43587-024-00731-y · Cited by 131
“The results of our study used amyloid-β pathology prevalence estimates derived from the Amyloid Biomarker Study Group, an international multicenter study of more than 19,000 individuals 19,28 .”
InfluentialSelf-citationPET Neuroimaging of Alzheimer's Disease: Radiotracers and Their Utility in Clinical Research
Bao, W., Xie, F., Zuo, C., Guan, Y., & Huang, Y. H. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.624330 · Cited by 102
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BACE inhibitors in clinical development for the treatment of Alzheimer’s disease
Panza, F., Lozupone, M., Solfrizzi, V., Sardone, R., Piccininni, C., Dibello, V., Stallone, R., Giannelli, G., Bellomo, A., Greco, A., et al. (2018) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2018.1531706 · Cited by 92
Unbiased estimates of cerebrospinal fluid β-amyloid 1–42 cutoffs in a large memory clinic population
Bertens, D., Tijms, B. M., Scheltens, P., Teunissen, C. E., & Visser, P. J. (2017) · Alzheimer's Research & Therapy · doi:10.1186/s13195-016-0233-7 · Cited by 91
Self-citationMattsson, N., Groot, C., Jansen, W. J., Landau, S. M., Villemagne, V. L., Engelborghs, S., Mintun, M. M., Lleo, A., Molinuevo, J. L., Jagust, W. J., et al. (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.02.009 · Cited by 88
Self-citationMRI predictors of amyloid pathology: results from the EMIF-AD Multimodal Biomarker Discovery study
ten Kate, M., Redolfi, A., Peira, E., Bos, I., Vos, S. J., Vandenberghe, R., Gabel, S., Schaeverbeke, J., Scheltens, P., Blin, O., et al. (2018) · Alzheimer's Research & Therapy · doi:10.1186/s13195-018-0428-1 · Cited by 78
Self-citationHampel, H., Shaw, L. M., Aisen, P., Chen, C., Lleó, A., Iwatsubo, T., Iwata, A., Yamada, M., Ikeuchi, T., Jia, J., et al. (2022) · Alzheimer's & Dementia · doi:10.1002/alz.12372 · Cited by 77
Self-citationBiomarkers for Alzheimer’s Disease
Guzman-Martinez, L., Maccioni, R. B., Farías, G. A., Fuentes, P., & Navarrete, L. P. (2019) · Current Alzheimer Research · doi:10.2174/1567205016666190517121140 · Cited by 87
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Self-citationA 2-Step Cerebrospinal Algorithm for the Selection of Frontotemporal Lobar Degeneration Subtypes
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Self-citationPeet, B. T., Spina, S., Mundada, N., & La Joie, R. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01101-x · Cited by 74
APOE effects on regional tau in preclinical Alzheimer’s disease
Young, C. B., Johns, E., Kennedy, G., Belloy, M. E., Insel, P. S., Greicius, M. D., Sperling, R. A., Johnson, K. A., Poston, K. L., Mormino, E. C., et al. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00590-4 · Cited by 80
Bejanin, A., Iulita, M. F., Vilaplana, E., Carmona-Iragui, M., Benejam, B., Videla, L., Barroeta, I., Fernandez, S., Altuna, M., Pegueroles, J., et al. (2021) · JAMA Neurology · doi:10.1001/jamaneurol.2021.1893 · Cited by 76
Self-citation
Metadata
- Authors
- Jansen, W. J., Ossenkoppele, R., Knol, D. L., Tijms, B. M., Scheltens, P., Verhey, F. R. J., Visser, P. J., Aalten, P., Aarsland, D., Alcolea, D., Alexander, M., Almdahl, I. S., Arnold, S. E., Baldeiras, I., Barthel, H., van Berckel, B. N. M., Bibeau, K., Blennow, K., Brooks, D. J., van Buchem, M. A., Camus, V., Cavedo, E., Chen, K., Chetelat, G., Cohen, A. D., Drzezga, A., Engelborghs, S., Fagan, A. M., Fladby, T., Fleisher, A. S., van der Flier, W. M., Ford, L., Förster, S., Fortea, J., Foskett, N., Frederiksen, K. S., Freund-Levi, Y., Frisoni, G. B., Froelich, L., Gabryelewicz, T., Gill, K. D., Gkatzima, O., Gómez-Tortosa, E., Gordon, M. F., Grimmer, T., Hampel, H., Hausner, L., Hellwig, S., Herukka, S.-K., Hildebrandt, H., Ishihara, L., Ivanoiu, A., Jagust, W. J., Johannsen, P., Kandimalla, R., Kapaki, E., Klimkowicz-Mrowiec, A., Klunk, W. E., Köhler, S., Koglin, N., Kornhuber, J., Kramberger, M. G., Van Laere, K., Landau, S. M., Lee, D. Y., de Leon, M., Lisetti, V., Lleó, A., Madsen, K., Maier, W., Marcusson, J., Mattsson, N., de Mendonça, A., Meulenbroek, O., Meyer, P. T., Mintun, M. A., Mok, V., Molinuevo, J. L., Møllergård, H. M., Morris, J. C., Mroczko, B., Van der Mussele, S., Na, D. L., Newberg, A., Nordberg, A., Nordlund, A., Novak, G. P., Paraskevas, G. P., Parnetti, L., Perera, G., Peters, O., Popp, J., Prabhakar, S., Rabinovici, G. D., Ramakers, I. H. G. B., Rami, L., Resende de Oliveira, C., Rinne, J. O., Rodrigue, K. M., Rodríguez-Rodríguez, E., Roe, C. M., Rot, U., Rowe, C. C., Rüther, E., Sabri, O., Sanchez-Juan, P., Santana, I., Sarazin, M., Schröder, J., Schütte, C., Seo, S. W., Soetewey, F., Soininen, H., Spiru, L., Struyfs, H., Teunissen, C. E., Tsolaki, M., Vandenberghe, R., Verbeek, M. M., Villemagne, V. L., Vos, S. J. B., van Waalwijk van Doorn, L. J. C., Waldemar, G., Wallin, A., Wallin, Å. K., Wiltfang, J., Wolk, D. A., Zboch, M., & Zetterberg, H.
- Affiliations
- Maastricht University (NL)
- Amsterdam Neuroscience (NL)
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Stavanger University Hospital (NO)
- Hospital de Sant Pau (ES)
- Roche (United Kingdom) (GB)
- Akershus University Hospital (NO)
- University of Pennsylvania (US)
- Unidade Local de Saúde de Coimbra (PT)
- Leipzig University (DE)
- Department of Radiology and Nuclear Medicine, VU University Medical Center, Neuroscience Campus Amsterdam, Amsterdam, the Netherlands
- GlaxoSmithKline (United States) (US)
- University of Gothenburg (SE)
- Imperial College London (GB)
- Department of Radiology, Leiden University Medical Center, Leiden, the Netherlands
- Université de Tours (FR)
- Sorbonne Université (FR)
- Banner Alzheimer’s Institute (US)
- Institut National de la Santé et de la Recherche Médicale (Inserm), U1077, Caen, France
- University of Pittsburgh (US)
- University of Cologne (DE)
- University of Antwerp (BE)
- Washington University in St. Louis (US)
- University of California San Diego (US)
- Department of Neurology and Alzheimer Center, VU University Medical Center, Neuroscience Campus Amsterdam, Amsterdam, the Netherlands6Department of Epidemiology and Biostatistics, VU University Medical Center, Amsterdam, the Netherlands
- Janssen Research and Development, Titusville, New Jersey
- Technical University of Munich (DE)
- University of Copenhagen (DK)
- Department of Geriatrics, Institution of NVS, Section of Clinical Geriatrics, Karolinska Institutet, Stockholm, Sweden
- University of Geneva (CH)
- Heidelberg University (DE)
- Mossakowski Medical Research Institute, Polish Academy of Sciences (PL)
- Post Graduate Institute of Medical Education and Research (IN)
- Aristotle University of Thessaloniki (GR)
- Department of Neurology, Fundación Jiménez Díaz, Madrid, Spain
- Boehringer Ingelheim (United States) (US)
- TUM Klinikum (DE)
- Inserm (FR)
- University Medical Center Freiburg (DE)
- University of Eastern Finland (FI)
- Center for Neurology, Hospital of Bremen-Ost, Bremen, Germany
- GlaxoSmithKline (United Kingdom) (GB)
- Cliniques Universitaires Saint-Luc (BE)
- University of California, Berkeley (US)
- Rigshospitalet (DK)
- Emory University (US)
- National and Kapodistrian University of Athens (GR)
- Jagiellonian University College of Medicine, Krakow, Poland
- Piramal (Germany) (DE)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Ljubljana University Medical Centre (SI)
- Department of Imaging and Pathology, Catholic University Leuven, Leuven, Belgium
- Seoul National University (KR)
- School of Medicine, Center for Brain Health, New York University, New York
- University of Perugia (IT)
- Copenhagen University Hospital (DK)
- University of Bonn (DE)
- Linköping University (SE)
- Lund University (SE)
- Institute of Molecular Medicine and Faculty of Medicine, University of Lisbon, Portugal
- Radboud University Medical Center (NL)
- Avid Radiopharmaceuticals (United States) (US)
- Chinese University of Hong Kong (HK)
- Alzheimer’s Disease and Other Cognitive Disorders Unit, IDIBAPS, Clinic University Hospital, Barcelona, Spain
- Medical University of Białystok (PL)
- Reference Center for Biological Markers of Dementia (BIODEM), University of Antwerp, Antwerp, Belgium
- Samsung Medical Center (KR)
- Thomas Jefferson University (US)
- Karolinska University Hospital (SE)
- King's College London (GB)
- German Center for Neurodegenerative Diseases (DE)
- Centre Hospitalier Universitaire Vaudois (CH)
- University of California, San Francisco (US)
- Consorci Institut D'Investigacions Biomediques August Pi I Sunyer (ES)
- Center for Neuroscience and Cell Biology, Faculty of Medicine, Hospital Center University of Coimbra, Portugal
- University of Turku (FI)
- The University of Texas at Dallas (US)
- Neurology Service, Universitary Hospital Marqués de Valdecilla, IDIVAL, Santander, Spain
- Center for Cognitive Impairments, University Medical Centre Ljubljana, Ljubljana, Slovenia
- Austin Hospital (AU)
- Universitätsmedizin Göttingen (DE)
- Centre Hospitalier Sainte-Anne (FR)
- Carol Davila University of Medicine and Pharmacy (RO)
- KU Leuven (BE)
- Departments of Neurology and Laboratory Medicine, Donders Institute for Brain, Cognition and Behaviour, Radboud Alzheimer Center, Radboud University Medical Center, Nijmegen, the Netherlands
- Wroclaw Medical University (PL)
- National Hospital for Neurology and Neurosurgery (GB)
- ORCID
- Jansen, Willemijn J.
- Ossenkoppele, Rik
- Tijms, Betty M.
- Scheltens, Philip
- Verhey, Frans R. J.
- Visser, Pieter Jelle
- Aarsland, Dag
- Alcolea, Daniel
- Alexander, Myriam
- Almdahl, Ina S.
- Arnold, Steven E.
- Baldeiras, Inês
- Barthel, Henryk
- Bibeau, Kristen
- Blennow, Kaj
- Brooks, David J.
- Camus, Vincent
- Cavedo, Enrica
- Chen, Kewei
- Cohen, Ann D.
- Drzezga, Alexander
- Engelborghs, Sebastiaan
- Fagan, Anne M.
- Fladby, Tormod
- Fleisher, Adam S.
- Ford, Lisa
- Förster, Stefan
- Fortea, Juan
- Frederiksen, Kristian S.
- Frisoni, Giovanni B.
- Froelich, Lutz
- Gkatzima, Olymbia
- Gordon, Mark Forrest
- Grimmer, Timo
- Hampel, Harald
- Hausner, Lucrezia
- Hellwig, Sabine
- Herukka, Sanna-Kaisa
- Hildebrandt, Helmut
- Jagust, William J.
- Johannsen, Peter
- Kandimalla, Ramesh
- Klunk, William E.
- Köhler, Sebastian
- Koglin, Norman
- Kornhuber, Johannes
- Kramberger, Milica G.
- Landau, Susan M.
- Lee, Dong Young
- Lleó, Alberto
- Madsen, Karine
- Maier, Wolfgang
- Marcusson, Jan
- Mattsson, Niklas
- Meyer, Philipp T.
- Mok, Vincent
- Morris, John C.
- Mroczko, Barbara
- Na, Duk L.
- Newberg, Andrew
- Nordberg, Agneta
- Novak, Gerald P.
- Paraskevas, George P.
- Parnetti, Lucilla
- Perera, Gayan
- Peters, Oliver
- Popp, Julius
- Rabinovici, Gil D.
- Ramakers, Inez H. G. B.
- Rami, Lorena
- Rinne, Juha O.
- Rodrigue, Karen M.
- Roe, Catherine M.
- Rowe, Christopher C.
- Sabri, Osama
- Santana, Isabel
- Sarazin, Marie
- Schröder, Johannes
- Seo, Sang W.
- Soininen, Hilkka
- Spiru, Luiza
- Teunissen, Charlotte E.
- Tsolaki, Magda
- Vandenberghe, Rik
- Verbeek, Marcel M.
- Villemagne, Victor L.
- Vos, Stephanie J. B.
- Waldemar, Gunhild
- Wallin, Anders
- Wiltfang, Jens
- Wolk, David A.
- Zboch, Marzena
- Zetterberg, Henrik
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2015-05-19
- Volume
- 313
- Issue
- 19
- Pages
- 1924
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- PMC
- PMC4486209
- OpenAlex
- W2168357345
- Cited by
- 1,610
- References
- 51
- Citations by year
- 2026: 118 · 2025: 144 · 2024: 168 · 2023: 140 · 2022: 151 · 2021: 174 · 2020: 184 · 2019: 142 · 2018: 135 · 2017: 117 · 2016: 92 · 2015: 43
- FWCI
- 104.60
- Type
- journal article
- Language
- en
- Open access
- Licence
- other-oa
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- VU Research Portal (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- IRIS (submittedVersion)
- Homo Politicus (Academy of Humanities and Economics in Lodz) (submittedVersion, cc-by-nc-nd)
- Homo Politicus (Academy of Humanities and Economics in Lodz) (submittedVersion)
- Jagiellonian University Repository (Jagiellonian University) (submittedVersion, cc-by-nc-nd)
- Digital Access to Libraries (submittedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Lirias (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion, other-oa)
- mediaTUM (Technical University of Munich) (submittedVersion)
- GRO (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- National Science Foundation (P01AG003991,, P50AG005681, P01 AG026276, FP7/2007-2013, P50 AG005133, U01 AG024904)
- U.S. Department of Defense (U01 AG024904, W81XWH, W81XWH-12-2-, W81XWH1220012, AG024904)
- Foundation for the National Institutes of Health (P01AG026276, W81XWH-12-2-0012, U01AG024904, AG024904, P01AG003991)
- Alzheimer's Association (P01 AG003991, P50 AG005681, 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, 115372, U01 AG024904)
- AstraZeneca
- GlaxoSmithKline (P01AG026276)
- Biogen (W81XWH-12-2-0012, U01 AG024904, AG024904)
- University of Southern California (P01 AG003991, W81XWH-12-2-0012, P01 AG026276, U01 AG024904)
- University of Pennsylvania
- Emory University
- F. Hoffmann-La Roche (W81XWH-12-2-0012, AG024904, U01 AG024904)
- Medpace (U01 AG024904)
- Meso Scale Diagnostics (U01 AG024904, AG024904, W81XWH-12-2-0012)
- Synarc (U01 AG024904)
- Alzheimer's Disease Neuroimaging Initiative (P01AG026276, W81XWH-12-2–0012, U01AG024904, AG024904, W81XWH-12-2-)
- BioClinica (U01 AG024904, W81XWH-12-2-0012, AG024904)
- Itä-Suomen Yliopisto
- National Research Centre
- University of Pittsburgh (P50 AG005133)
- Sundhed og Sygdom, Det Frie Forskningsråd
- Thomas Jefferson University
- Science and Industry Endowment Fund
- Northern California Institute for Research and Education (U01 AG024904, W81XWH-12-2-0012)
- EU Joint Programme – Neurodegenerative Disease Research
- European Federation of Pharmaceutical Industries and Associations (FP7/20072013, ANR-10-IAIHU-06, 115372)
- Postgraduate Institute of Medical Education and Research, Chandigarh
- Lui Che Woo Institute of Innovative Medicine
- York University
- Imperial College London
- European Commission (37670, U01 AG024904, 601055, 2007–2013, FP7 2007-2013, LSHB-CT-2005-512146, FP7/2007, W81XWH-12-2-0012, QLRT-2001-2455, 115372)
- Bayer HealthCare
- Commonwealth Scientific and Industrial Research Organisation
- Indian Council of Medical Research
- Deutsche Forschungsgemeinschaft (HE 4560/1-2, DR 445/3-1, 115372, FP7/2007–2013, DR 445/4-1)
- Universität Heidelberg
- Agence Nationale de la Recherche (ANR-10-IAIHU06, 10-IAIHU-06, ANR-10)
- Institut National de la Santé et de la Recherche Médicale (ANR-10-IAIHU-06, INSERM U930)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (FP7/2007-2013, 37670)
- Universiteit Leiden
- Edith Cowan University
- ZonMw
- Universiteit van Amsterdam
- Radboud Universiteit
- Vrije Universiteit Amsterdam (FP7/2007-2013)
- AXA Research Fund (ANR-10-IAIHU-06)
- Academy of Finland (W81XWH-12-2-0012, 115372, U01 AG024904)
- Bundesministerium für Bildung und Forschung (01GI1007A, 01GI0420)
- Seoul National University (FP7/2007-2013)
- Sungkyunkwan University
- Belgian Federal Science Policy Office
- Gentofte Hospital
- Dementia Collaborative Research Centres, Australia
- Fonds Wetenschappelijk Onderzoek
- Ministero della Salute
- Lunds Universitet
- Lundbeckfonden
- Eisai (W81XWH-12-2-0012, U01 AG024904, AG024904)
- KU Leuven
- Karolinska Institutet
- Kuopion Yliopistollinen Sairaala
- Chinese University of Hong Kong
- Leids Universitair Medisch Centrum
- Rigshospitalet
- National and Kapodistrian University of Athens
- Deutsches Zentrum für Neurodegenerative Erkrankungen
- Turun Yliopisto
- Technische Universität München
- Universidade de Coimbra
- Université Pierre et Marie Curie (FP7/2007-2013)
- Göteborgs Universitet
- Universidade de Lisboa
- Center for Translational Molecular Medicine (02N-101)
- Radboud Universitair Medisch Centrum
- Université de Genève
- Aristotle University of Thessaloniki
- Universiteit Antwerpen (FP7/2007-2013)
- Universitatea de Medicină şi Farmacie "Carol Davila" Bucureşti
- Universität zu Köln
- Rheinische Friedrich-Wilhelms-Universität Bonn
- Uniwersytet Medyczny im. Piastów Slaskich we Wroclawiu
- Università degli Studi di Perugia (ANR-10-IAIHU-06)
- Innovative Medicines Initiative (#115372, FP7/2007‐2013)
- Servier (AG024904, W81XWH-12-2-0012, U01 AG024904)
- Turun Yliopistollinen Keskussairaala
- Vlaamse regering
- Merz Pharmaceuticals
- H. Lundbeck A/S (U01 AG024904, AG024904, W81XWH-12-2-0012)
- Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas
- IXICO (AG024904, W81XWH-12-2-0012, U01 AG024904)
- Région Normandie
- Instituto de Investigación Marqués de Valdecilla
- Sorbonne Université
- Fondation pour la Recherche sur Alzheimer (ANR-10-IAIHU-06)
- National Institutes of Health (3u01ag024904-10s2, FP7/2007-2013, W81XWH, W81XWH-12-2-0012, U01-AG024904, AG005133, R01 AG12101, AG008051, AG024904, AG005681, AG12101, AG025204, AG003991, AG026276, AG025516, ANR-10-IAIHU-06)
- Genentech (W81XWH-12-2-0012, AG024904, U01 AG024904)
- Samsung
- University of California, San Diego (P50 AG005133)
- Avid Radiopharmaceuticals
- Canadian Institutes of Health Research (U01 AG024904, W81XWH-12-2-0012)
- Charles F. and Joanne Knight Alzheimer Disease Research Center, Washington University in St. Louis (P01AG003991)
- Medical Research Council (U01 AG024904)
- Menzies Centre for Australian Studies, King's College London, University of London
- National Health and Medical Research Council
- Instituto de Salud Carlos III (PI11/, PI13/01532)
- Sahlgrenska Akademin
- European Regional Development Fund (FP7/2007‐2013, 2007 – 2013, 20/21)
- Krajowy Naukowy Osrodek Wiodacy
- National Institute on Aging (U01-AG-024904, AG008051, R01AG13616, AG022374, W81XWH-12-2–0012, P01AG025204, AG-005133, RF1AG025516, P50AG005133, AG 024904, R01AG022374, P30AG010124, AG 12101, AG003991, R01AG012101, P30AG008051, AG026276, P50AG005681, AG025204, P01AG003991, R01-AG-12101, U19AG032438, U19AG010483, R37AG025516, R01AG013616, AG005681, P01AG026276, R01AG025516, AG 13616)
- National Institute of Biomedical Imaging and Bioengineering (W81XWH-12-2-0012, U01 AG024904, AG024904)
- Janssen Research and Development
- Janssen Pharmaceuticals
- Cilag
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Oncology › Cancer-related cognitive impairment studies
- Keywords
- cerebral amyloid-beta, Alzheimer's disease, mild cognitive impairment, subjective cognitive impairment, normal cognition, APOE ε4 carriers, APOE genotype, positron emission tomography, cerebrospinal fluid biomarkers, sex differences, dementia prevention
- MeSH terms
- Adult, Age Factors, Aged, Aged, 80 and over, Brain, Cerebrospinal Fluid, Dementia, Female, Genotype, Humans, Male, Middle Aged, Risk Factors, Biomarkers, Prevalence, Amyloid beta-Peptides, Positron-Emission Tomography, Apolipoprotein E4, 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.
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