Investigation of sex differences in mutation carriers of the Dominantly Inherited Alzheimer Network.
cognition
dominantly inherited Alzheimer's disease
gender
presymptomatic Alzheimer's disease
sex
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:
23 Sep 2023
23 Sep 2023
Historique:
revised:
10
08
2023
received:
16
05
2023
accepted:
13
08
2023
medline:
23
9
2023
pubmed:
23
9
2023
entrez:
23
9
2023
Statut:
aheadofprint
Résumé
Studies suggest distinct differences in the development, presentation, progression, and response to treatment of Alzheimer's disease (AD) between females and males. We investigated sex differences in cognition, neuroimaging, and fluid biomarkers in dominantly inherited AD (DIAD). Three hundred twenty-five mutation carriers (55% female) and one hundred eighty-six non-carriers (58% female) of the Dominantly Inherited Alzheimer Network Observational Study were analyzed. Linear mixed models and Spearman's correlation explored cross-sectional sex differences in cognition, cerebrospinal fluid (CSF) biomarkers, Pittsburgh compound B positron emission tomography ( Female carriers performed better than males on delayed recall and processing speed despite similar hippocampal volumes. As the disease progressed, symptomatic females revealed higher increases in MRI markers of neurodegeneration and memory impairment. PiB PET and established CSF AD markers revealed no sex differences. Our findings suggest an initial cognitive reserve in female carriers followed by a pronounced increase in neurodegeneration coupled with worse performance on delayed recall at later stages of DIAD.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIA NIH HHS
ID : U19 AG032438
Pays : United States
Organisme : NIA NIH HHS
ID : UF1 AG032438
Pays : United States
Organisme : NIA NIH HHS
ID : U19AG032438
Pays : United States
Informations de copyright
© 2023 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
Références
Cao Q, Tan CC, Xu W, et al. The Prevalence of dementia: A systematic review and meta-analysis. J Alzheimers Dis. 2020;73(3):1157-1166. doi:10.3233/JAD-191092. Zhu LQ, ed.
Mielke MM, Aggarwal NT, Vila-Castelar C, et al. Consideration of sex and gender in Alzheimer's disease and related disorders from a global perspective. Alzheimers Dement. doi:10.1002/alz.12662. Published online April 8, 2022:alz.12662.
Seshadri S, Wolf PA, Beiser A, et al. Lifetime risk of dementia and Alzheimer's disease: The impact of mortality on risk estimates in the Framingham Study. Neurology. 1997;49(6):1498-1504. doi:10.1212/WNL.49.6.1498
Snyder HM, Asthana S, Bain L, et al. Sex biology contributions to vulnerability to Alzheimer's disease: A think tank convened by the women's Alzheimer's research initiative. Alzheimers Dement. 2016;12(11):1186-1196. doi:10.1016/j.jalz.2016.08.004
Hebert LE, Scherr PA, McCann JJ, Beckett LA, Evans DA. Is the risk of developing Alzheimer's disease greater for women than for men? Am J Epidemiol. 2001;153(2):132-136. doi:10.1093/aje/153.2.132
Barnes LL, Wilson RS, Bienias JL, Schneider JA, Evans DA, Bennett DA. Sex differences in the clinical manifestations of Alzheimer disease pathology. Arch Gen Psychiatry. 2005;62(6):685. doi:10.1001/archpsyc.62.6.685
Buckley RF, Mormino EC, Amariglio RE, et al. Sex, amyloid, and APOE ε4 and risk of cognitive decline in preclinical Alzheimer's disease: Findings from three well-characterized cohorts. Alzheimers Dement. 2018;14(9):1193-1203. doi:10.1016/j.jalz.2018.04.010
Jack CR, Wiste HJ, Weigand SD, et al. Age, sex, and APOE ε4 effects on memory, brain structure, and β-amyloid across the adult life span. JAMA Neurol. 2015;72(5):511. doi:10.1001/jamaneurol.2014.4821
Filon JR, Intorcia AJ, Sue LI, et al. Gender differences in Alzheimer disease: Brain atrophy, histopathology burden, and cognition. J Neuropathol Exp Neurol. 2016;75(8):748-754. doi:10.1093/jnen/nlw047
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(5):542. doi:10.1001/jamaneurol.2018.4693
Buckley RF, Scott MR, Jacobs HIL, et al. Sex mediates relationships between regional tau pathology and cognitive decline. Ann Neurol. 2020;88(5):921-932. doi:10.1002/ana.25878
Skup M, Zhu H, Wang Y, et al. Sex differences in grey matter atrophy patterns among AD and aMCI patients: Results from ADNI. NeuroImage. 2011;56(3):890-906. doi:10.1016/j.neuroimage.2011.02.060
Ardekani BA, Convit A, Bachman AH. Analysis of the MIRIAD data shows sex differences in hippocampal atrophy progression. J Alzheimers Dis. 2016;50(3):847-857. doi:10.3233/JAD-150780
Hohman TJ, Dumitrescu L, Barnes LL, et al. Sex-specific association of apolipoprotein E with cerebrospinal fluid levels of tau. JAMA Neurol. 2018;75(8):989. doi:10.1001/jamaneurol.2018.0821
Sundermann EE, Biegon A, Rubin LH, et al. Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy. Neurology. 2016;86(15):1368-1376. doi:10.1212/WNL.0000000000002570
Digma LA, Madsen JR, Rissman RA, et al. Women can bear a bigger burden: ante- and post-mortem evidence for reserve in the face of tau. Brain Commun. 2020;2(1):fcaa025. doi:10.1093/braincomms/fcaa025
Holland D, Desikan RS, Dale AM, McEvoy LK. Higher rates of decline for women and apolipoprotein E ε4 carriers. Am J Neuroradiol. 2013;34(12):2287-2293. doi:10.3174/ajnr.A3601
Koran MEI, Wagener M, Hohman TJ. Sex differences in the association between AD biomarkers and cognitive decline. Brain Imaging Behav. 2017;11(1):205-213. doi:10.1007/s11682-016-9523-8
Irvine K, Laws KR, Gale TM, Kondel TK. Greater cognitive deterioration in women than men with Alzheimer's disease: A meta analysis. J Clin Exp Neuropsychol. 2012;34(9):989-998. doi:10.1080/13803395.2012.712676
Eikelboom WS, Pan M, Ossenkoppele R, et al. Sex differences in neuropsychiatric symptoms in Alzheimer's disease dementia: a meta-analysis. Alzheimers Res Ther. 2022;14(1):48. doi:10.1186/s13195-022-00991-z
Bertram L, McQueen MB, Mullin K, Blacker D, Tanzi RE. Systematic meta-analyses of Alzheimer disease genetic association studies: The AlzGene database. Nat Genet. 2007;39(1):17-23. doi:10.1038/ng1934
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. doi:10.1016/j.neurobiolaging.2021.05.013
Wang YTT, Pascoal TA, Therriault J, et al. Interactive rather than independent effect of APOE and sex potentiates tau deposition in women. Brain Commun. 2021;3(2):fcab126. doi:10.1093/braincomms/fcab126
Liu M, Paranjpe MD, Zhou X, et al. Sex modulates the ApoE ε4 effect on brain tau deposition measured by 18F-AV-1451 PET in individuals with mild cognitive impairment. Theranostics. 2019;9(17):4959-4970. doi:10.7150/thno.35366
Altmann A, Tian L, Henderson VW, Greicius MD. Alzheimer's disease neuroimaging initiative investigators. Sex modifies the APOE -related risk of developing Alzheimer disease: Sex and APOE -Related AD Risk. Ann Neurol. 2014;75(4):563-573. doi:10.1002/ana.24135
Polsinelli AJ, Logan PE, Lane KA, et al. APOE ε4 carrier status and sex differentiate rates of cognitive decline in early- and late-onset Alzheimer's disease. Alzheimers Dement. 2022;19(5):1983-1993. doi:10.1002/alz.12831
Bekris LM, Yu CE, Bird TD, Tsuang DW. Genetics of Alzheimer Disease. J Geriatr Psychiatry Neurol. 2010;23(4):213-227. doi:10.1177/0891988710383571
Vila-Castelar C, Guzmán-Vélez E, Pardilla-Delgado E, et al. Examining sex differences in markers of cognition and neurodegeneration in autosomal dominant Alzheimer's disease: Preliminary findings from the Colombian Alzheimer's prevention initiative biomarker study. J Alzheimers Dis. 2020;77(4):1743-1753. doi:10.3233/JAD-200723
Vila-Castelar C, Tariot PN, Sink KM, et al. Sex differences in cognitive resilience in preclinical autosomal-dominant Alzheimer's disease carriers and non-carriers: Baseline findings from the API ADAD Colombia Trial. Alzheimers Dement. 2022;18(11):2272-2282. doi:10.1002/alz.12552
Ryman DC, Acosta-Baena N, Aisen PS, et al. Symptom onset in autosomal dominant Alzheimer disease: A systematic review and meta-analysis. Neurology. 2014;83(3):253-260. doi:10.1212/WNL.0000000000000596
Robinson JL, Richardson H, Xie SX, et al. The development and convergence of co-pathologies in Alzheimer's disease. Brain. 2021;144(3):953-962. doi:10.1093/brain/awaa438
Morris JC, Aisen PS, Bateman RJ, et al. Developing an international network for Alzheimer's research: The dominantly inherited Alzheimer network. Clin Investig. 2012;2(10):975-984. doi:10.4155/cli.12.93
van Dyck CH, Swanson CJ, Aisen P, et al. Lecanemab in early Alzheimer's disease. N Engl J Med. 2023;388(1):9-21. doi:10.1056/NEJMoa2212948
Bateman RJ, Xiong C, Benzinger TLS, et al. Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N Engl J Med. 2012;367(9):795-804. doi:10.1056/NEJMoa1202753
Tsubuki S, Takai Y, Saido TC, Dutch, Flemish, Italian, and Arctic mutations of APP and resistance of Aβ to physiologically relevant proteolytic degradation. The Lancet. 2003;361(9373):1957-1958. doi:10.1016/S0140-6736(03)13555-6
Morris JC. The clinical dementia rating (CDR): Current version and scoring rules. Neurology. 1993;43(11):2412-2412. doi:10.1212/WNL.43.11.2412-a
Storandt M, Balota DA, Aschenbrenner AJ, Morris JC. Clinical and psychological characteristics of the initial cohort of the dominantly inherited Alzheimer network (DIAN). Neuropsychology. 2014;28(1):19-29. doi:10.1037/neu0000030
Monserrate AE, Ryman DC, Ma S, et al. Factors associated with the onset and persistence of post-lumbar puncture headache. JAMA Neurol. 2015;72(3):325. doi:10.1001/jamaneurol.2014.3974
Fischl B, Salat DH, Busa E, et al. Whole brain segmentation. Neuron. 2002;33(3):341-355. doi:10.1016/S0896-6273(02)00569-X
McKay NS, Gordon BA, Hornbeck RC, et al. Neuroimaging within the dominantly inherited Alzheimer's network (DIAN): pET and MRI. Neuroscience. 2023. doi:10.1101/2022.03.25.485799. bioRxiv.
Dincer A, Gordon BA, Hari-Raj A, et al. Comparing cortical signatures of atrophy between late-onset and autosomal dominant Alzheimer disease. NeuroImage Clin. 2020;28:102491. doi:10.1016/j.nicl.2020.102491
Su Y, D'Angelo GM, Vlassenko AG, et al. Quantitative analysis of PiB-PET with FreeSurfer ROIs. PLoS ONE. 2013;8(11):e73377. doi:10.1371/journal.pone.0073377
Laws KR, Irvine K, Gale TM. Sex differences in cognitive impairment in Alzheimer's disease. World J Psychiatry. 2016;6(1):54. doi:10.5498/wjp.v6.i1.54
R Core Team. R: A language and environment for statistical computing. Published online 2021. Accessed 01, 2023. URL https://www.R-project.org/
McCarrey AC, An Y, Kitner-Triolo MH, Ferrucci L, Resnick SM. Sex differences in cognitive trajectories in clinically normal older adults. Psychol Aging. 2016;31(2):166-175. doi:10.1037/pag0000070
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. Alzheimers Res Ther. 2019;11(1):109. doi:10.1186/s13195-019-0565-1
Fortea J, Zaman SH, Hartley S, Rafii MS, Head E, Carmona-Iragui M. Alzheimer's disease associated with Down syndrome: A genetic form of dementia. Lancet Neurol. 2021;20(11):930-942. doi:10.1016/S1474-4422(21)00245-3. Published online.
Iulita MF, Bejanin A, Vilaplana E, et al. Association of biological sex with clinical outcomes and biomarkers of Alzheimer's disease in adults with Down syndrome. Brain Commun. 2023;5(2):fcad074. doi:10.1093/braincomms/fcad074
Moreno-Martínez FJ, Laws KR, Schulz J. The impact of dementia, age and sex on category fluency: Greater deficits in women with Alzheimer's disease. Cortex. 2008;44(9):1256-1264. doi:10.1016/j.cortex.2007.11.008
McPherson S, Back C, Buckwalter JG, Cummings JL. Gender-related cognitive deficits in Alzheimer's disease. Int Psychogeriatr. 1999;11(2):117-122. doi:10.1017/S1041610299005670
Duarte-Guterman P, Albert AY, Barha CK, Galea LAM. On behalf of the Alzheimer's disease neuroimaging initiative. Sex influences the effects of APOE genotype and Alzheimer's diagnosis on neuropathology and memory. Psychoneuroendocrinology. 2021;129:105248. doi:10.1016/j.psyneuen.2021.105248
Lin KA, Choudhury KR, Rathakrishnan BG, et al. Marked gender differences in progression of mild cognitive impairment over 8 years. Alzheimers Dement Transl Res Clin Interv. 2015;1(2):103-110. doi:10.1016/j.trci.2015.07.001
Hua X, Hibar DP, Lee S, et al. Sex and age differences in atrophic rates: an ADNI study with n = 1368 MRI scans. Neurobiol Aging. 2010;31(8):1463-1480. doi:10.1016/j.neurobiolaging.2010.04.033
Jansen WJ, Ossenkoppele R, Knol DL, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA. 2015;313(19):1924. doi:10.1001/jama.2015.4668
Villeneuve S, Vogel JW, Gonneaud J, et al. Proximity to parental symptom onset and amyloid-β burden in sporadic Alzheimer disease. JAMA Neurol. 2018;75(5):608. doi:10.1001/jamaneurol.2017.5135
Buckley RF, Mormino EC, Chhatwal J, et al. Associations between baseline amyloid, sex, and APOE on subsequent tau accumulation in cerebrospinal fluid. Neurobiol Aging. 2019;78:178-185. doi:10.1016/j.neurobiolaging.2019.02.019
Babapour Mofrad R, Tijms BM, Scheltens P, et al. Sex differences in CSF biomarkers vary by Alzheimer disease stage and APOE ε4 genotype. Neurology. 2020;95(17):e2378-e2388. doi:10.1212/WNL.0000000000010629
Yan S, Zheng C, Paranjpe MD, et al. Sex modifies APOE ε4 dose effect on brain tau deposition in cognitively impaired individuals. Brain. 2021;144(10):3201-3211. doi:10.1093/brain/awab160
Barnes LL, Lamar M, Schneider JA. Sex differences in mixed neuropathologies in community-dwelling older adults. Brain Res. 2019;1719:11-16. doi:10.1016/j.brainres.2019.05.028
Oveisgharan S, Arvanitakis Z, Yu L, Farfel J, Schneider JA, Bennett DA. Sex differences in Alzheimer's disease and common neuropathologies of aging. Acta Neuropathol (Berl). 2018;136(6):887-900. doi:10.1007/s00401-018-1920-1
Chêne G, Beiser A, Au R, et al. Gender and incidence of dementia in the Framingham Heart Study from mid-adult life. Alzheimers Dement. 2015;11(3):310-320. doi:10.1016/j.jalz.2013.10.005