Plasma phosphorylated tau-217 exhibits sex-specific prognostication of cognitive decline and brain atrophy in cognitively unimpaired adults.
Alzheimer's disease
amyloid positron emission tomography
cognition
cognitively unimpaired
glial fibrillary acidic protein
medial temporal lobe
neurofilament light
phosphorylated tau217
plasma biomarkers
sex differences
verbal memory
Journal
Alzheimer's & dementia : the journal of the Alzheimer's Association
ISSN: 1552-5279
Titre abrégé: Alzheimers Dement
Pays: United States
ID NLM: 101231978
Informations de publication
Date de publication:
28 Aug 2023
28 Aug 2023
Historique:
revised:
04
08
2023
received:
28
06
2023
accepted:
07
08
2023
medline:
28
8
2023
pubmed:
28
8
2023
entrez:
28
8
2023
Statut:
aheadofprint
Résumé
Accumulating evidence indicates disproportionate tau burden and tau-related clinical progression in females. However, sex differences in plasma phosphorylated tau (p-tau)217 prediction of subclinical cognitive and brain changes are unknown. We measured baseline plasma p-tau217, glial fibrillary acidic protein (GFAP), and neurofilament light (NfL) in 163 participants (85 cognitively unimpaired [CU], 78 mild cognitive impairment [MCI]). In CU, linear mixed effects models examined sex differences in plasma biomarker prediction of longitudinal domain-specific cognitive decline and brain atrophy. Cognitive models were repeated in MCI. In CU females, baseline plasma p-tau217 predicted verbal memory and medial temporal lobe trajectories such that trajectories significantly declined once p-tau217 concentrations surpassed 0.053 pg/ml, a threshold that corresponded to early levels of cortical amyloid aggregation in secondary amyloid positron emission tomography analyses. CU males exhibited similar rates of cognitive decline and brain atrophy, but these trajectories were not dependent on plasma p-tau217. Plasma GFAP and NfL exhibited similar female-specific prediction of medial temporal lobe atrophy in CU. Plasma p-tau217 exhibited comparable prediction of cognitive decline across sex in MCI. Plasma p-tau217 may capture earlier Alzheimer's disease (AD)-related cognitive and brain atrophy hallmarks in females compared to males, possibly reflective of increased susceptibility to AD pathophysiology.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIA NIH HHS
ID : U19 AG063911
Pays : United States
Organisme : Alzheimer's Association
ID : AARF-23-1145318
Pays : United States
Organisme : Alzheimer's Association
ID : AARF-22-974065
Pays : United States
Informations de copyright
© 2023 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
Références
Hansson O, Edelmayer RM, Boxer AL, et al. The Alzheimer's association appropriate use recommendations for blood biomarkers in Alzheimer's disease. Alzheimer's & Dementia. 2022;18:2669-2686.
Palmqvist S, Janelidze S, Quiroz YT, et al. Discriminative accuracy of Plasma Phospho-tau217 for Alzheimer disease vs other neurodegenerative disorders. JAMA. 2020;324:772-781.
Gonzalez-Ortiz F, Kac PR, Brum WS, Zetterberg H, Blennow K, Karikari TK. Plasma phospho-tau in Alzheimer's disease: towards diagnostic and therapeutic trial applications. Mol Neurodegener. 2023;18:18.
Doré V, Doecke JD, Saad ZS, et al. Plasma p217+tau versus NAV4694 amyloid and MK6240 tau PET across the Alzheimer's continuum. Alzheimers Dement (Amst). 2022;14:e12307.
Asken BM, Tanner JA, VandeVrede L, et al. Plasma P-tau181 and P-tau217 in patients with traumatic encephalopathy syndrome with and without evidence of alzheimer disease pathology. Neurology. 2022;99:e594-e604.
Thijssen EH, La Joie R, Strom A, et al. Plasma phosphorylated tau 217 and phosphorylated tau 181 as biomarkers in Alzheimer's disease and frontotemporal lobar degeneration: a retrospective diagnostic performance study. Lancet Neurol. 2021;20:739-752.
Milà-Alomà M, Ashton NJ, Shekari M, et al. Plasma P-tau231 and P-tau217 as state markers of amyloid-β pathology in preclinical Alzheimer's disease. Nat Med. 2022;28:1797-1801.
Mattsson-Carlgren N, Janelidze S, Palmqvist S, et al. Longitudinal plasma P-tau217 is increased in early stages of Alzheimer's disease. Brain. 2020;143:3234-3241.
Janelidze S, Berron D, Smith R, et al. Associations of plasma phospho-Tau217 levels with tau positron emission tomography in early alzheimer disease. JAMA Neurol. 2021;78:149-156.
Mattsson-Carlgren N, Salvadó G, Ashton NJ, et al. Prediction of longitudinal cognitive decline in preclinical Alzheimer disease using plasma biomarkers. JAMA Neurol. 2023;80:360-369.
Jonaitis EM, Janelidze S, Cody KA, et al. Plasma phosphorylated tau 217 in preclinical Alzheimer's disease. Brain Commun. 2023;5:fcad057.
Ashton NJ, Janelidze S, Mattsson-Carlgren N, et al. Differential roles of Aβ42/40, P-tau231 and P-tau217 for Alzheimer's trial selection and disease monitoring. Nat Med. 2022;28:2555-2562.
Mielke MM. Consideration of sex differences in the measurement and interpretation of Alzheimer disease-related biofluid-based biomarkers. J Appl Lab Med. 2020;5:158-169.
Buckley RF, O'Donnell A, McGrath ER, et al. Menopause status moderates sex differences in tau burden: a framingham PET study. Ann Neurol. 2022;92:11-22.
Wisch JK, Meeker KL, Gordon BA, et al. Sex-related differences in tau positron emission tomography (PET) and the effects of hormone therapy (HT). Alzheimer Dis Assoc Disord. 2021;35:164-168.
Buckley RF, Mormino EC, Rabin JS, et al. Sex differences in the association of global amyloid and regional tau deposition measured by positron emission tomography in clinically normal older adults. JAMA Neurol. 2019;76:542-551.
Buckley RF, Scott MR, Jacobs HIL, et al. Sex mediates relationships between regional tau pathology and cognitive decline. Ann Neurol. 2020;88:921-932.
Koran MEI, Wagener M, Hohman TJ. Sex differences in the association between AD biomarkers and cognitive decline. Brain Imaging Behav. 2017;11:205-213.
Lindbergh CA, Casaletto KB, Staffaroni AM, et al. Sex-related differences in the relationship between β-amyloid and cognitive trajectories in older adults. Neuropsychology. 2020;34:835-850.
Levine DA, Gross AL, Briceño EM, et al. Sex differences in cognitive decline among US adults. JAMA Netw Open. 2021;4:e210169-e.
Albert MS, DeKosky ST, Dickson D, et al. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011;7:270-279.
Mielke MM, Dage JL, Frank RD, et al. Performance of plasma phosphorylated tau 181 and 217 in the community. Nat Med. 2022;28:1398-1405.
Berry K, Asken BM, Grab JD, et al. Hepatic and renal function impact concentrations of plasma biomarkers of neuropathology. Alzheimers Dement (Amst). 2022;14:e12321.
Groot C, Cicognola C, Bali D, et al. Diagnostic and prognostic performance to detect Alzheimer's disease and clinical progression of a novel assay for plasma P-tau217. Alzheimer's Research & Therapy. 2022;14:67.
Triana-Baltzer G, Moughadam S, Slemmon R, et al. Development and validation of a high-sensitivity assay for measuring p217+tau in plasma. Alzheimers Dement (Amst). 2021;13:e12204.
Kramer JH, Jurik J, Sha SJ, et al. Distinctive neuropsychological patterns in frontotemporal dementia, semantic dementia, and Alzheimer disease. Cogn Behav Neurol. 2003;16.
Asken BM, VandeVrede L, Rojas JC, et al. Lower white matter volume and worse executive functioning reflected in higher levels of plasma GFAP among older adults with and without cognitive impairment. J Int Neuropsychol Soc. 2022;28:588-599.
Saloner R, Fonseca C, Paolillo EW, et al. Combined effects of synaptic and axonal integrity on longitudinal gray matter atrophy in cognitively unimpaired adults. Neurology. 2022. 10.1212/WNL.0000000000201165
Ashburner J, Friston KJ. Unified segmentation. Neuroimage. 2005;26:839-851.
Desikan RS, Ségonne F, Fischl B, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968-980.
Rabinovici GD, Furst AJ, Alkalay A, et al. Increased metabolic vulnerability in early-onset Alzheimer's disease is not related to amyloid burden. Brain. 2010;133:512-528.
Klunk WE, Koeppe RA, Price JC, et al. The centiloid project: standardizing quantitative amyloid plaque estimation by PET. Alzheimers Dement. 2015;11:1-15. e1-4.
Salvadó G, Molinuevo JL, Brugulat-Serrat A, et al. Centiloid cut-off values for optimal agreement between PET and CSF core AD biomarkers. Alzheimer's Research & Therapy. 2019;11:27.
Syrjanen JA, Campbell MR, Algeciras-Schimnich A, et al. Associations of amyloid and neurodegeneration plasma biomarkers with comorbidities. Alzheimer's & Dementia. 2022;18:1128-1140.
Johnson PO, Neyman J. Tests of certain linear hypotheses and their application to some educational problems. Statistical research memoirs. 1936;1:57-93. https://psycnet.apa.org/record/1936-05538-001
Preacher KJ, Curran PJ, Bauer DJ. Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of educational and behavioral statistics. 2006;31:437-448.
Sohn D, Shpanskaya K, Lucas JE, et al. Sex differences in cognitive decline in subjects with high likelihood of mild cognitive impairment due to Alzheimer's disease. Sci Rep. 2018;8:7490.
Banks SJ, Andrews MJ, Digma L, et al. Sex differences in Alzheimer's disease: do differences in tau explain the verbal memory gap? Neurobiol Aging. 2021;107:70-77.
Tsiknia AA, Edland SD, Sundermann EE, et al. Sex differences in plasma P-tau181 associations with Alzheimer's disease biomarkers, cognitive decline, and clinical progression. Mol Psychiatry. 2022;27:4314-4322.
Saloner R, Paolillo EW, Wojta KJ, et al. Sex-specific effects of SNAP-25 genotype on verbal memory and Alzheimer's disease biomarkers in clinically normal older adults. Alzheimer's & Dementia. 2023;n/a.
Sundermann EE, Maki P, Biegon A, et al. Sex-specific norms for verbal memory tests may improve diagnostic accuracy of amnestic MCI. Neurology. 2019;93:e1881.
Pauls F, Petermann F, Lepach AC. Gender differences in episodic memory and visual working memory including the effects of age. Memory. 2013;21:857-874.
Caldwell JZK, Cummings JL, Banks SJ, Palmqvist S, Hansson O. Cognitively normal women with Alzheimer's disease proteinopathy show relative preservation of memory but not of hippocampal volume. Alzheimer's Research & Therapy. 2019;11:109.
Digma LA, Madsen JR, Rissman RA, Jacobs DM, Brewer JB, Banks SJ. Women can bear a bigger burden: ante- and post-mortem evidence for reserve in the face of tau. Brain Commun. 2020;2:fcaa025.
Edwards L, La Joie R, Iaccarino L, et al. Multimodal neuroimaging of sex differences in cognitively impaired patients on the Alzheimer's continuum: greater tau-PET retention in females. Neurobiol Aging. 2021;105:86-98.
Sundermann EE, Maki PM, Rubin LH, et al. Female advantage in verbal memory: evidence of sex-specific cognitive reserve. Neurology. 2016;87:1916-1924.
Bocancea DI, Svenningsson AL, van Loenhoud AC, et al. Determinants of cognitive and brain resilience to tau pathology: a longitudinal analysis. Brain. 2023.
Lin KA, Choudhury KR, Rathakrishnan BG, Marks DM, Petrella JR, Doraiswamy PM. Marked gender differences in progression of mild cognitive impairment over 8 years. Alzheimer's & Dementia: Translational Research & Clinical Interventions. 2015;1:103-110.
Brickman AM, Manly JJ, Honig LS, et al. Plasma P-tau181, P-tau217, and other blood-based Alzheimer's disease biomarkers in a multi-ethnic, community study. Alzheimers Dement. 2021;17:1353-1364.
Therriault J, Vermeiren M, Servaes S, et al. Association of phosphorylated tau biomarkers with amyloid positron emission tomography vs tau positron emission tomography. JAMA Neurol. 2023;80:188-199.
Casaletto KB, Nichols E, Aslanyan V, et al. Sex-specific effects of microglial activation on Alzheimer's disease proteinopathy in older adults. Brain. 2022;145:3536-3545.
Falcon C, Grau-Rivera O, Suárez-Calvet M, et al. Sex differences of longitudinal brain changes in cognitively unimpaired adults. J Alzheimers Dis. 2020;76:1413-1422.
Benedet AL, Milà-Alomà M, Vrillon A, et al. Differences between plasma and cerebrospinal fluid glial fibrillary acidic protein levels across the Alzheimer disease continuum. JAMA Neurol. 2021;78:1471-1483.
Milà-Alomà M, Brinkmalm A, Ashton NJ, et al. CSF synaptic biomarkers in the preclinical stage of Alzheimer disease and their association with MRI and PET: a cross-sectional study. Neurology. 2021. 10.1212/WNL.0000000000012853.
Jansen WJ, Janssen O, Tijms BM, et al. Prevalence estimates of amyloid abnormality across the Alzheimer disease clinical spectrum. JAMA Neurol. 2022;79:228-243.
Davis EJ, Broestl L, Abdulai-Saiku S, et al. A second X chromosome contributes to resilience in a mouse model of Alzheimer's disease. Sci Transl Med. 2020:12.
Sundermann EE, Panizzon MS, Chen X, Andrews M, Galasko D, Banks SJ. Sex differences in Alzheimer's-related tau biomarkers and a mediating effect of testosterone. Biol Sex Differ. 2020;11:33.
Davis EJ, Solsberg CW, White CC, et al. Sex-specific association of the X chromosome with cognitive change and tau pathology in aging and Alzheimer disease. JAMA Neurol. 2021;78:1249-1254.