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Semantic loss marks early Alzheimer's disease-related neurodegeneration in older adults without dementia

J. M. J. Vonk 1, 2 Vincent Bouteloup 3, 4 J. F. Mangin 5, 6 B. Dubois 7 F. Blanc 8 A. Gabelle 9, 10 Mathieu Ceccaldi 11 C. Annweiler 12 P. Krolak-Salmon 13 C. Belin 14 Thérèse Rivasseau-Jonveaux 15 A. Julian 16 F. Sellal 17 E. Magnin 18, 19 M. Chupin 6 M. O. Habert 6, 20, 21 Genevieve Chene 3 Carole Dufouil 3
1 Columbia University [New York]
2 University Medical Center [Utrecht]
3 BPH - Bordeaux population health
4 CHU Bordeaux [Bordeaux]
5 NEUROSPIN - Service NEUROSPIN
6 CATI - CATI Multicenter Neuroimaging Platform
7 IM2A - Institut de la Mémoire et de la Maladie d'Alzheimer [Paris]
8 ICube - Laboratoire des sciences de l'ingénieur, de l'informatique et de l'imagerie
9 Neuropsychiatrie : recherche épidémiologique et clinique
10 CMRR - Centres Mémoire de Ressources et de Recherche Montpellier
11 INS - Institut de Neurosciences des Systèmes
12 LPPL - Laboratoire de Psychologie des Pays de la Loire
13 UCBL - Université Claude Bernard Lyon 1
14 CHU Saint Louis [APHP]
15 2LPN - Laboratoire lorrain de psychologie et neurosciences de la dynamique des comportements
16 Hôpital de la Milétrie
17 Mécanismes Centraux et Périphériques de la Neurodégénérescence
18 CMRR - Centre Mémoire de Ressources et de Recherche [Besançon]
19 NEURO - Laboratoire de Neurosciences Intégratives et Cliniques - UFC (EA 481)
20 LIB - Laboratoire d'Imagerie Biomédicale
21 CHU Pitié-Salpêtrière [AP-HP]
Abstract : Objective: To assess progression of semantic loss in early stages of cognitive decline using semantic and letter fluency performance, and its relation with Alzheimer's disease (AD)‐specific neurodegeneration using longitudinal multimodal neuroimaging measures. Methods: Change in verbal fluency was analyzed among 2261 non‐demented individuals with a follow‐up diagnosis of no mild cognitive impairment (MCI), amnestic MCI (aMCI), non‐amnestic MCI (naMCI), or incident dementia, using linear mixed models across 4 years of follow‐up, and relations with magnetic resonance imaging (MRI; n = 1536) and 18F‐fluorodeoxyglucose brain positron emission tomography (18F‐FDG‐PET) imaging (n = 756) using linear regression models across 2 years of follow‐up. Results: Semantic fluency declined—fastest in those at higher risk for AD (apolipoprotein E [APOE] e4 carriers, Clinical Dementia Rating score of .5, aMCI, or incident dementia)—while letter fluency did not except for those with incident dementia. Lower baseline semantic fluency was associated with an increase in white matter hyperintensities and total mean cortical thinning over time, and regionally with less hippocampal volume as well as more cortical thinning and reduced 18F‐FDG‐PET uptake in the inferior parietal lobule, entorhinal cortex, isthmus cingulate, and precuneus–posterior cingulate area. In contrast, baseline letter fluency was not associated with change in total nor regional neurodegeneration. Whole‐brain neurodegeneration over time was associated with faster decline in both fluencies, while AD‐specific regions were associated with a faster rate of decline in semantic but not letter fluency. Interpretation: This study provides strong evidence of distinctive degeneration of semantic abilities early on in relation to both cognitive decline and AD‐specific neurodegeneration.
Keywords : amnestic Alzheimer’s disease biomarkers category fluency cognitive aging cohort studies letter fluency MCI neuroimaging semantic fluency verbal fluency
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Submitted on : Monday, February 22, 2021 - 3:08:39 PM
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LIB | CEA | UNIV-LORRAINE | CEA-UPSAY | NEUROSPIN | UNIV-LYON1 | INC-CNRS | JOLIOT | UNIV-MONTPELLIER | CEA-DRF | UNIV-NANTES | U1061 | UNIV-AMU | INSA-STRASBOURG | SORBONNE-UNIVERSITE | 2LPN-UL | INSA-GROUPE | UNIV-ANGERS | LPPL | CNRS | BS | SITE-ALSACE | LPPL-ANGERS | SU-SCIENCES | SU-TI | INSERM | SU-MEDECINE | UDL | UNIV-FCOMTE | U1219

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J. M. J. Vonk, Vincent Bouteloup, J. F. Mangin, B. Dubois, F. Blanc, et al.. Semantic loss marks early Alzheimer's disease-related neurodegeneration in older adults without dementia. Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring, Wiley, 2020, 12 (1), pp.e12066. ⟨10.1002/dad2.12066⟩. ⟨hal-03148797⟩

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