Prevalence of amyloid‐β pathology in distinct variants of primary progressive aphasia
Open accessAbstract
Objective: To estimate the prevalence of amyloid positivity, defined by positron emission tomography (PET)/cerebrospinal fluid (CSF) biomarkers and/or neuropathological examination, in primary progressive aphasia (PPA) variants. Methods: We conducted a meta‐analysis with individual participant data from 1,251 patients diagnosed with PPA (including logopenic [lvPPA, n = 443], nonfluent [nfvPPA, n = 333], semantic [svPPA, n = 401], and mixed/unclassifiable [n = 74] variants of PPA) from 36 centers, with a measure of amyloid‐β pathology (CSF [n = 600], PET [n = 366], and/or autopsy [n = 378]) available. The estimated prevalence of amyloid positivity according to PPA variant, age, and apolipoprotein E (ApoE) ε4 status was determined using generalized estimating equation models. Results: Amyloid‐β positivity was more prevalent in lvPPA (86%) than in nfvPPA (20%) or svPPA (16%; p < 0.001). Prevalence of amyloid‐β positivity increased with age in nfvPPA (from 10% at age 50 years to 27% at age 80 years, p < 0.01) and svPPA (from 6% at age 50 years to 32% at age 80 years, p < 0.001), but not in lvPPA (p = 0.94). Across PPA variants, ApoE ε4 carriers were more often amyloid‐β positive (58.0%) than noncarriers (35.0%, p < 0.001). Autopsy data revealed Alzheimer disease pathology as the most common pathologic diagnosis in lvPPA (76%), frontotemporal lobar degeneration–TDP‐43 in svPPA (80%), and frontotemporal lobar degeneration–TDP‐43/tau in nfvPPA (64%). Interpretation: This study shows that the current PPA classification system helps to predict underlying pathology across different cohorts and clinical settings, and suggests that age and ApoE genotype should be considered when interpreting amyloid‐β biomarkers in PPA patients. Ann Neurol 2018;84:737–748
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ADNC is observed not only in individuals with the typical, amnestic clinical presentation but also in people with atypical, non-amnestic presentations.
“However, ADNC is observed not only in individuals with the typical, amnestic clinical presentation but also in people with atypical, non‐amnestic presentations.”
From Automatic classification of AD pathology in FTD phenotypes using natural speech (2024) · cites this paper as [13]
The Results (Autopsy Results in Distinct PPA Variants; page not provided) report primary AD pathology in patients with language-led, non-amnestic presentations, especially logopenic PPA. This supports the atypical-presentation part of the claim, but the paper does not assess people with typical amnestic presentations for comparison. (LLM, conf=0.82)
Experimental — accuracy not yet measuredAlzheimer-type lesions are frequently observed as copathology in post-mortem examination of people who had other neurodegenerative diseases.
“Alternatively, lesions of the Alzheimer type are frequently observed as copathology in post-mortem examination of people who had other neurodegenerative diseases.40,41,94,96”
From Clinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group (2021) · cites this paper as [94]
Other phenotypes, including the behavioural variant or dysexecutive variant, the corticobasal variant, and other variants of primary progressive aphasia, are less commonly related to Alzheimer's disease pathology.
“Other phenotypes, including the behavioural variant or dysexecutive variant,95,96 the corticobasal variant,97,98 and the other variants of primary progressive aphasia94,99 (appendix p 2), are less commonly related to Alzheimer’s disease pathology (uncommon Alzheimer’s disease phenotypes).”
From Clinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group (2021) · cites this paper as [94]
In behavioural or dysexecutive variants, corticobasal syndrome, and semantic or non-fluent variants of primary progressive aphasia, positive Alzheimer's disease biomarkers are particularly ambiguous and can be considered either as Alzheimer's disease copathology or atypical forms of Alzheimer's disease.
“This biomarker positivity is particularly ambiguous in the case of behavioural or dysexecutive variants, corticobasal syndrome, and semantic or non-fluent variants of primary progressive aphasia, in which the presence of positive Alzheimer’s disease biomarkers can be considered either as Alzheimer’s disease copathology or atypical forms of Alzheimer’s disease94,96,98,99 (appendix p 2).”
From Clinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group (2021) · cites this paper as [94]
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Self-citationAmyloid in dementia associated with familial FTLD: not an innocent bystander
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Self-citationConcordance Between 11 C-PIB-PET and Clinical Diagnosis in a Memory Clinic
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Self-citationClinical and MRI models predicting amyloid deposition in progressive aphasia and apraxia of speech
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Anomalous functional language lateralization in semantic variant PPA
Miller, Z., Hinkley, L. B. N., Herman, A., Honma, S. M., Findlay, A. M., Block, N., Ketelle, R., Rabinovici, G. D., Rosen, H. J., Nagarajan, S. S., et al. (2014) · Neurology · doi:10.1212/wnl.0000000000001131 · Cited by 10 · see citing works
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Knopman, D. S., Amieva, H., Petersen, R. C., Chételat, G., Holtzman, D. M., Hyman, B. T., Nixon, R. A., & Jones, D. T. (2021) · Nature Reviews Disease Primers · doi:10.1038/s41572-021-00269-y · Cited by 2,606 · see citing works
Self-citationClinical diagnosis of Alzheimer’s disease: Recommendations of the International Working Group
Dubois, B., Villain, N., Frisoni, G. B., Rabinovici, G. D., Sabbagh, M., Cappa, S., Bejanin, A., Bombois, S., Epelbaum, S., Teichmann, M., et al. (2021) · The Lancet Neurology · doi:10.1016/s1474-4422(21)00066-1 · Cited by 1,051 · see citing works
“Other phenotypes, including the behavioural/dysexecutive variant 70,71 , the cortico-basal variant 72,73 , and the other variants of primary progressive aphasia 69,74 (Supplementary Figure 1), are less commonly related to AD pathology (uncommon AD phenotypes).”
BackgroundInfluentialSelf-citationNew insights into atypical Alzheimer's disease in the era of biomarkers
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Self-citationBiomarker-based staging of Alzheimer disease: rationale and clinical applications
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Self-citationNew landscape of the diagnosis of Alzheimer’s disease
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Self-citationSpeech and language therapy approaches to managing primary progressive aphasia
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Self-citationPrimary progressive aphasia: a model for neurodegenerative disease
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Self-citationS1 guidelines “lumbar puncture and cerebrospinal fluid analysis” (abridged and translated version)
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Self-citationClinical Spectrum of Tauopathies
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The path to biomarker-based diagnostic criteria for the spectrum of neurodegenerative diseases
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Tau PET imaging with 18F-PI-2620 in aging and neurodegenerative diseases
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Primary Progressive Aphasia: Toward a Pathophysiological Synthesis
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Lexical and Acoustic Speech Features Relating to Alzheimer Disease Pathology
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Self-citationEstablishing two principal dimensions of cognitive variation in logopenic progressive aphasia
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Self-citationBreakdown of specific functional brain networks in clinical variants of Alzheimer’s disease
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Self-citationA syntax–lexicon trade-off in language production
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Self-citationPersonalized Repetitive Transcranial Magnetic Stimulation for Primary Progressive Aphasia
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Self-citationIncidence and Prevalence of Frontotemporal Dementia
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Primary Progressive Aphasia Associated With GRN Mutations
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Self-citationCognitive Phenotyping and Interpretation of Alzheimer Blood Biomarkers
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Self-citationAtypical Alzheimer Disease Variants
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Self-citationParkinsonism in frontotemporal dementias
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Self-citationThe course of primary progressive aphasia diagnosis: a cross-sectional study
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Brain changes underlying progression of speech motor programming impairment
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Self-citationResearch Progress on the Pathogenesis, Diagnosis, and Drug Therapy of Alzheimer’s Disease
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PET Neuroimaging in Dementia Conditions
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Cortical developmental abnormalities in logopenic variant primary progressive aphasia with dyslexia
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Self-citationBasal forebrain atrophy in frontotemporal dementia
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Self-citationPosterior Cingulate Cortex Hypometabolism in Non-Amnestic Variants of Alzheimer’s Disease
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Self-citationNeuroimaging in Frontotemporal Lobar Degeneration: Research and Clinical Utility
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Self-citationProgressive apraxia of speech: delays to diagnosis and rates of alternative diagnoses
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A systematic review of atypical Alzheimer's disease including behavioural and psychological symptoms
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Self-citationPoint of view: Challenges in implementation of new immunotherapies for Alzheimer's disease
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Self-citationMultimodality Imaging in Primary Progressive Aphasia
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Silent Pauses and Speech Indices as Biomarkers for Primary Progressive Aphasia
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Longitudinal Amyloid-β PET in Atypical Alzheimer’s Disease and Frontotemporal Lobar Degeneration
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Limb and face apraxias in frontotemporal dementia: A systematic scoping review
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Primary progressive aphasias associated with C9orf72 expansions: Another side of the story
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Self-citationWhite Matter Damage in the Semantic Variant of Primary Progressive Aphasia
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Self-citationConnected speech markers of amyloid burden in primary progressive aphasia
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Self-citationGenetic variation in APOE, GRN, and TP53 are phenotype modifiers in frontotemporal dementia
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Self-citationAutomatic classification of AD pathology in FTD phenotypes using natural speech
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“12,13 Atypical presentations of ADNC with predominant linguistic and behavioral changes can present a challenging differential diagnosis among subtypes of frontotemporal dementia (FTD) due to frontotemporal lobar degeneration (FTLD), where common presentations include behavioral variant FTD (bvFTD)…”
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Aphasic mild cognitive impairment in prodromal dementia with Lewy bodies
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Atypical Presentations of Alzheimer Disease
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- Authors
- 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., van der Flier, W. M., Scheltens, P., Rohrer, J. D., Warren, J. D., Schott, J. M., Fox, N. C., Sanchez‐Valle, R., Grau‐Rivera, O., Gelpi, E., Seelaar, H., Papma, J. M., van Swieten, J. C., Hodges, J. R., Leyton, C. E., Piguet, O., Rogalski, E. J., Mesulam, M. M., Koric, L., Kristensen, N., Pariente, J., Dickerson, B., Mackenzie, I. R., Hsiung, G. R., Belliard, S., Irwin, D. J., Wolk, D. A., Grossman, M., Jones, M., Harris, J., Mann, D., Snowden, J. S., Chrem‐Mendez, P., Calandri, I. L., Amengual, A. A., Miguet‐Alfonsi, C., Magnin, E., Magnani, G., Santangelo, R., Deramecourt, V., Pasquier, F., Mattsson, N., Nilsson, C., Hansson, O., Keith, J., Masellis, M., Black, S. E., Matías‐Guiu, J. A., Cabrera‐Martin, M., Paquet, C., Dumurgier, J., Teichmann, M., Sarazin, M., Bottlaender, M., Dubois, B., Rowe, C. C., Villemagne, V. L., Vandenberghe, R., Granadillo, E., Teng, E., Mendez, M., Meyer, P. T., Frings, L., Lleó, A., Blesa, R., Fortea, J., Seo, S. W., Diehl‐Schmid, J., Grimmer, T., Frederiksen, K. S., Sánchez‐Juan, P., Chételat, G., Jansen, W., Bouchard, R. W., Laforce, R. J., Visser, P. J., & Ossenkoppele, R.
- Affiliations
- Amsterdam Neuroscience (NL)
- University of California, San Francisco (US)
- Department of Radiology and Nuclear Medicine VU University Medical Center Amsterdam the Netherlands
- Alzheimer center Amsterdam Amsterdam UMC, Amsterdam Neuroscience, VU University Amsterdam the Netherlands
- UCL Queen Square Institute of Neurology (GB)
- Alzheimer's Disease and Other Cognitive Disorders Unit, August Pi i Sunyer Biomedical Research Institute Barcelona Spain
- Consorci Institut D'Investigacions Biomediques August Pi I Sunyer (ES)
- Erasmus MC (NL)
- Alzheimer Center, Department of Neurology Erasmus University Medical Center Rotterdam the Netherlands
- The University of Sydney (AU)
- Harvard University (US)
- Northwestern University (US)
- Hôpital de la Timone (FR)
- University of Toulouse, INSERM, Toulouse Neuroimaging Center Toulouse France
- University of British Columbia (CA)
- University of Pennsylvania (US)
- University of Manchester (GB)
- Center of Aging and Memory, Neurological Research Institute Buenos Aires Argentina
- Centre Hospitalier Universitaire de Besançon (FR)
- Department of Neurology, CHRU Besançon and Integrative and Clinical Neurosciences Laboratory, Regional Memory Center University of Bourgogne Franche‐Comté Besançon France
- Vita-Salute San Raffaele University (IT)
- Inserm (FR)
- Lund University (SE)
- Sunnybrook Health Science Centre (CA)
- Universidad Complutense de Madrid (ES)
- Department of Neurology and Nuclear Medicine, San Carlos Clinical Hospital, San Carlos Health Research Institute Complutense University of Madrid Madrid Spain
- Hôpital Fernand-Widal (FR)
- Assistance Publique – Hôpitaux de Paris (FR)
- Université Paris-Sud (FR)
- Pitié-Salpêtrière Hospital (FR)
- The University of Melbourne (AU)
- Universitair Ziekenhuis Leuven (BE)
- University of California, Los Angeles (US)
- VA West Los Angeles Medical Center (US)
- University of Freiburg (DE)
- Universitat Autònoma de Barcelona (ES)
- Samsung Medical Center (KR)
- Technical University of Munich (DE)
- Department of Neurology Danish Dementia Research Center Copenhagen Denmark
- Marqués de Valdecilla University Hospital (ES)
- Maastricht University (NL)
- Université Laval (CA)
- Universitat Internacional de Catalunya (ES)
- Corresponding author
- Bergeron, David
- ORCID
- Bergeron, David
- Gorno‐Tempini, Maria L.
- Rabinovici, Gil D.
- Santos‐Santos, Miguel A.
- Seeley, William
- Miller, Bruce L.
- Pijnenburg, Yolande
- Groot, Colin
- Scheltens, Philip
- Rohrer, Jonathan D.
- Warren, Jason D.
- Schott, Jonathan M.
- Fox, Nick C.
- Grau‐Rivera, Oriol
- Seelaar, Harro
- Papma, Janne M.
- Hodges, John R.
- Leyton, Cristian E.
- Piguet, Olivier
- Rogalski, Emily J.
- Mesulam, Marsel M.
- Koric, Lejla
- Dickerson, Bradford
- Mackenzie, Ian R.
- Hsiung, Ging‐Yuek R.
- Belliard, Serge
- Irwin, David J.
- Wolk, David A.
- Grossman, Murray
- Jones, Matthew
- Mann, David
- Snowden, Julie S.
- Calandri, Ismael L.
- Miguet‐Alfonsi, Carole
- Magnani, Giuseppe
- Santangelo, Roberto
- Deramecourt, Vincent
- Pasquier, Florence
- Mattsson, Niklas
- Nilsson, Christer
- Hansson, Oskar
- Keith, Julia
- Masellis, Mario
- Black, Sandra E.
- Matías‐Guiu, Jordi A.
- Paquet, Claire
- Dumurgier, Julien
- Teichmann, Marc
- Sarazin, Marie
- Bottlaender, Michel
- Dubois, Bruno
- Rowe, Christopher C.
- Villemagne, Victor L.
- Vandenberghe, Rik
- Granadillo, Elias
- Teng, Edmond
- Mendez, Mario
- Meyer, Philipp T.
- Frings, Lars
- Lleó, Alberto
- Blesa, Rafael
- Fortea, Juan
- Seo, Sang Won
- Diehl‐Schmid, Janine
- Grimmer, Timo
- Frederiksen, Kristian Steen
- Chételat, Gaël
- Jansen, Willemijn
- Laforce, Robert Jr.
- Visser, Pieter Jelle
- Ossenkoppele, Rik
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2018-11
- Volume
- 84
- Issue
- 5
- Pages
- 729-740
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- PMC
- PMC6354051
- OpenAlex
- W2894273961
- Cited by
- 203
- References
- 75
- Citations by year
- 2026: 20 · 2025: 29 · 2024: 25 · 2023: 24 · 2022: 33 · 2021: 32 · 2020: 28 · 2019: 12
- FWCI
- 2.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annals of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- HAL (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Minerva Access (University of Melbourne) (submittedVersion)
- Lirias (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- mediaTUM (Technical University of Munich) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Canadian Institutes of Health Research
- 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 › Neurology › Amyotrophic Lateral Sclerosis Research
- Keywords
- primary progressive aphasia, amyloid-beta pathology, logopenic variant, semantic variant, APOE ε4, Alzheimer's disease, frontotemporal lobar degeneration, TDP-43, tau protein, amyloid PET, cerebrospinal fluid biomarkers, neuropathology, individual patient data
- MeSH terms
- Age Factors, Aged, Aged, 80 and over, Apolipoproteins E, Brain, Female, Genotype, Humans, Male, Middle Aged, Prevalence, Amyloid beta-Peptides, Aphasia, Primary Progressive
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