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February 16, 2021; 96 (7) ArticleOpen Access

Frequency of Biologically Defined Alzheimer Disease in Relation to Age, Sex, APOE ε4, and Cognitive Impairment

View ORCID ProfileJoseph Therriault, Tharick A. Pascoal, Andrea L. Benedet, Cecile Tissot, Melissa Savard, Mira Chamoun, Firoza Lussier, Min Su Kang, Gleb Berzgin, Tina Wang, Jaime Fernandes-Arias, Gassan Massarweh, Jean-Paul Soucy, View ORCID ProfilePaolo Vitali, Paramita Saha-Chaudhuri, Serge Gauthier, View ORCID ProfilePedro Rosa-Neto
First published December 21, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011416
Joseph Therriault
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Tharick A. Pascoal
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Andrea L. Benedet
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Cecile Tissot
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Melissa Savard
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Mira Chamoun
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Firoza Lussier
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Min Su Kang
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Gleb Berzgin
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Tina Wang
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Jaime Fernandes-Arias
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Gassan Massarweh
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Jean-Paul Soucy
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Paolo Vitali
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Paramita Saha-Chaudhuri
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Serge Gauthier
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Pedro Rosa-Neto
From the Translational Neuroimaging Laboratory, The McGill University Research Centre for Studies in Aging, Douglas Hospital (J.T., T.A.P., A.L.B., C.T., M.S., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., S.G., P.R.-N.), and the Departments of Neurology and Neurosurgery (J.T., T.A.P., A.L.B., C.T., M.C., F.L., M.S.K., G.B., T.W., J.F.-A., J.-P.S., P.V., S.G., P.R.-N.), Psychiatry (S.G., P.R.-N.), Radiochemistry (G.M.), and Epidemiology and Biostatistics (P.S.-C.), McGill University, Montreal; and Montreal Neurological Institute (J.T., T.A.P., A.L.B., C.T., F.L., M.S.K., G.B., T.W., J.F.-A., G.M., J.-P.S., P.R.-N.), Canada.
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Citation
Frequency of Biologically Defined Alzheimer Disease in Relation to Age, Sex, APOE ε4, and Cognitive Impairment
Joseph Therriault, Tharick A. Pascoal, Andrea L. Benedet, Cecile Tissot, Melissa Savard, Mira Chamoun, Firoza Lussier, Min Su Kang, Gleb Berzgin, Tina Wang, Jaime Fernandes-Arias, Gassan Massarweh, Jean-Paul Soucy, Paolo Vitali, Paramita Saha-Chaudhuri, Serge Gauthier, Pedro Rosa-Neto
Neurology Feb 2021, 96 (7) e975-e985; DOI: 10.1212/WNL.0000000000011416

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Abstract

Objective To assess the frequency of biologically defined Alzheimer disease (AD) in relation to age, sex, APOE ε4, and clinical diagnosis in a prospective cohort study evaluated with amyloid-PET and tau-PET.

Methods We assessed cognitively unimpaired (CU) elderly (n = 166), patients with amnestic mild cognitive impairment (n = 77), and patients with probable AD dementia (n = 62) who underwent evaluation by dementia specialists and neuropsychologists in addition to amyloid-PET with [18F]AZD4694 and tau-PET with [18F]MK6240. Individuals were grouped according to their AD biomarker profile. Positive predictive value for biologically defined AD was assessed in relation to clinical diagnosis. Frequency of AD biomarker profiles was assessed using logistic regressions with odds ratios (ORs) and 95% confidence intervals (CIs).

Results The clinical diagnosis of probable AD dementia demonstrated good agreement with biologically defined AD (positive predictive value 85.2%). A total of 7.88% of CU were positive for both amyloid-PET and tau-PET. Frequency of biologically defined AD increased with age (OR 1.14; p < 0.0001) and frequency of APOE ε4 allele carriers (single ε4: OR 3.82; p < 0.0001; double ε4: OR 17.55, p < 0.0001).

Conclusion Whereas we observed strong, but not complete, agreement between clinically defined probable AD dementia and biomarker positivity for both β-amyloid and tau, we also observed that biologically defined AD was not rare in CU elderly. Abnormal tau-PET was almost exclusively observed in individuals with abnormal amyloid-PET. Our results highlight that even in tertiary care memory clinics, detailed evaluation by dementia specialists systematically underestimates the frequency of biologically defined AD and related entities.

Classification of Evidence This study provides Class I evidence that biologically defined AD (abnormal amyloid PET and tau PET) was observed in 85.2% of people with clinically defined AD and 7.88% of CU elderly.

Glossary

Aβ=
β-amyloid;
AD=
Alzheimer disease;
aMCI=
amnestic mild cognitive impairment;
CDR=
Clinical Dementia Rating;
CI=
confidence interval;
CN=
cognitively normal;
CU=
cognitively unimpaired;
MCI=
mild cognitive impairment;
MMSE=
Mini-Mental State Examination;
OR=
odds ratio;
pAD=
probable Alzheimer disease;
PART=
primary age-related tauopathy;
ROI=
region of interest;
SUVR=
standardized uptake value ratio;
TRIAD=
Translational Biomarkers in Aging and Dementia;
VIF=
variance inflation factor;
WMH=
white matter hyperintensity

Footnotes

  • The Article Processing Charge was funded by Canadian Institutes of Health Research.

  • Go to Neurology.org/Nhttps://n.neurology.org/lookup/doi/10.1212/WNL.0000000000011416 for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 299

  • Class of Evidence: NPub.org/coe

  • Podcast: NPub.org/uemtq0

  • Received June 23, 2020.
  • Accepted in final form October 8, 2020.
  • Copyright © 2020 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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