Suboptimal Self-reported Sleep Efficiency and Duration Are Associated with Faster Accumulation of Brain Amyloid Beta in Cognitively Unimpaired Older Adults

Overview

Journal Alzheimers Dement (Amst)

Date 2024 Apr 23

PMID 38651160

Authors

Louise N Pivac

Belinda M Brown

Kelsey R Sewell

James D Doecke

Victor L Villemagne

Vincent Dore

Michael Weinborn

Hamid R Sohrabi

Samantha L Gardener

Romola S Bucks

Simon M Laws

Kevin Taddei

Paul Maruff

Colin L Masters

Christopher Rowe

Ralph N Martins

Stephanie R Rainey-Smith

Affiliations

Soon will be listed here.

Abstract

Introduction: This study investigated whether self-reported sleep quality is associated with brain amyloid beta (Aβ) accumulation.

Methods: Linear mixed effect model analyses were conducted for 189 cognitively unimpaired (CU) older adults (mean ± standard deviation 74.0 ± 6.2; 53.2% female), with baseline self-reported sleep data, and positron emission tomography-determined brain Aβ measured over a minimum of three time points (range 33.3-72.7 months). Analyses included random slopes and intercepts, interaction for apolipoprotein E () ε4 allele status, and time, adjusting for sex and baseline age.

Results: Sleep duration <6 hours, in ε4 carriers, and sleep efficiency <65%, in the whole sample and ε4 non-carriers, is associated with faster accumulation of brain Aβ.

Discussion: These findings suggest a role for self-reported suboptimal sleep efficiency and duration in the accumulation of Alzheimer's disease (AD) neuropathology in CU individuals. Additionally, poor sleep efficiency represents a potential route via which individuals at lower genetic risk may progress to preclinical AD.

Highlights: In cognitively unimpaired older adults self-report sleep is associated with brain amyloid beta (Aβ) accumulation.Across sleep characteristics, this relationship differs by apolipoprotein E () genotype.Sleep duration <6 hours is associated with faster brain Aβ accumulation in ε4 carriers.Sleep efficiency < 65% is associated with faster brain Aβ accumulation in ε4 non-carriers.Personalized sleep interventions should be studied for potential to slow Aβ accumulation.

Citing Articles

Suboptimal self-reported sleep efficiency and duration are associated with faster accumulation of brain amyloid beta in cognitively unimpaired older adults.

Pivac L, Brown B, Sewell K, Doecke J, Villemagne V, Dore V Alzheimers Dement (Amst). 2024; 16(2):e12579.

PMID: 38651160 PMC: 11033837. DOI: 10.1002/dad2.12579.

References

Brown B, Rainey-Smith S, Villemagne V, Weinborn M, Bucks R, Sohrabi H . The Relationship between Sleep Quality and Brain Amyloid Burden. Sleep. 2016; 39(5):1063-8. PMC: 4835305. DOI: 10.5665/sleep.5756. View

Pivac L, Brown B, Sewell K, Doecke J, Villemagne V, Dore V . Suboptimal self-reported sleep efficiency and duration are associated with faster accumulation of brain amyloid beta in cognitively unimpaired older adults. Alzheimers Dement (Amst). 2024; 16(2):e12579. PMC: 11033837. DOI: 10.1002/dad2.12579. View

Fowler C, Rainey-Smith S, Bird S, Bomke J, Bourgeat P, Brown B . Fifteen Years of the Australian Imaging, Biomarkers and Lifestyle (AIBL) Study: Progress and Observations from 2,359 Older Adults Spanning the Spectrum from Cognitive Normality to Alzheimer's Disease. J Alzheimers Dis Rep. 2021; 5(1):443-468. PMC: 8293663. DOI: 10.3233/ADR-210005. View

Sprecher K, Koscik R, Carlsson C, Zetterberg H, Blennow K, Okonkwo O . Poor sleep is associated with CSF biomarkers of amyloid pathology in cognitively normal adults. Neurology. 2017; 89(5):445-453. PMC: 5539733. DOI: 10.1212/WNL.0000000000004171. View

Sprecher K, Bendlin B, Racine A, Okonkwo O, Christian B, Koscik R . Amyloid burden is associated with self-reported sleep in nondemented late middle-aged adults. Neurobiol Aging. 2015; 36(9):2568-76. PMC: 4523445. DOI: 10.1016/j.neurobiolaging.2015.05.004. View

Hwang J, Byun M, Choe Y, Lee J, Yi D, Choi J . Moderating effect of ε4 on the relationship between sleep-wake cycle and brain β-amyloid. Neurology. 2018; 90(13):e1167-e1173. DOI: 10.1212/WNL.0000000000005193. View

Carvalho D, St Louis E, Knopman D, Boeve B, Lowe V, Roberts R . Association of Excessive Daytime Sleepiness With Longitudinal β-Amyloid Accumulation in Elderly Persons Without Dementia. JAMA Neurol. 2018; 75(6):672-680. PMC: 5885188. DOI: 10.1001/jamaneurol.2018.0049. View

Winer J, Mander B, Kumar S, Reed M, Baker S, Jagust W . Sleep Disturbance Forecasts β-Amyloid Accumulation across Subsequent Years. Curr Biol. 2020; 30(21):4291-4298.e3. PMC: 7642104. DOI: 10.1016/j.cub.2020.08.017. View

Lucey B . It's complicated: The relationship between sleep and Alzheimer's disease in humans. Neurobiol Dis. 2020; 144:105031. PMC: 7484285. DOI: 10.1016/j.nbd.2020.105031. View

10.

Hirshkowitz M, Whiton K, Albert S, Alessi C, Bruni O, DonCarlos L . National Sleep Foundation's sleep time duration recommendations: methodology and results summary. Sleep Health. 2017; 1(1):40-43. DOI: 10.1016/j.sleh.2014.12.010. View

11.

Lucey B, Hicks T, McLeland J, Toedebusch C, Boyd J, Elbert D . Effect of sleep on overnight cerebrospinal fluid amyloid β kinetics. Ann Neurol. 2017; 83(1):197-204. PMC: 5876097. DOI: 10.1002/ana.25117. View

12.

Lim A, Yu L, Kowgier M, Schneider J, Buchman A, Bennett D . Modification of the relationship of the apolipoprotein E ε4 allele to the risk of Alzheimer disease and neurofibrillary tangle density by sleep. JAMA Neurol. 2013; 70(12):1544-51. PMC: 3859706. DOI: 10.1001/jamaneurol.2013.4215. View

13.

Spira A, An Y, Wu M, Owusu J, Simonsick E, Bilgel M . Excessive daytime sleepiness and napping in cognitively normal adults: associations with subsequent amyloid deposition measured by PiB PET. Sleep. 2018; 41(10). PMC: 6187104. DOI: 10.1093/sleep/zsy152. View

14.

Buysse D, Reynolds 3rd C, Monk T, BERMAN S, Kupfer D . The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989; 28(2):193-213. DOI: 10.1016/0165-1781(89)90047-4. View

15.

Lucey B, McCullough A, Landsness E, Toedebusch C, McLeland J, Zaza A . Reduced non-rapid eye movement sleep is associated with tau pathology in early Alzheimer's disease. Sci Transl Med. 2019; 11(474). PMC: 6342564. DOI: 10.1126/scitranslmed.aau6550. View

16.

Branger P, Arenaza-Urquijo E, Tomadesso C, Mezenge F, Andre C, de Flores R . Relationships between sleep quality and brain volume, metabolism, and amyloid deposition in late adulthood. Neurobiol Aging. 2016; 41:107-114. DOI: 10.1016/j.neurobiolaging.2016.02.009. View

17.

Rowe C, Ellis K, Rimajova M, Bourgeat P, Pike K, Jones G . Amyloid imaging results from the Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging. Neurobiol Aging. 2010; 31(8):1275-83. DOI: 10.1016/j.neurobiolaging.2010.04.007. View

18.

Huynh T, Davis A, Ulrich J, Holtzman D . Apolipoprotein E and Alzheimer's disease: the influence of apolipoprotein E on amyloid-β and other amyloidogenic proteins. J Lipid Res. 2017; 58(5):824-836. PMC: 5408619. DOI: 10.1194/jlr.R075481. View

19.

Villemagne V, Burnham S, Bourgeat P, Brown B, Ellis K, Salvado O . Amyloid β deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol. 2013; 12(4):357-67. DOI: 10.1016/S1474-4422(13)70044-9. View

20.

Xu W, Tan L, Su B, Yu H, Bi Y, Yue X . Sleep characteristics and cerebrospinal fluid biomarkers of Alzheimer's disease pathology in cognitively intact older adults: The CABLE study. Alzheimers Dement. 2020; 16(8):1146-1152. DOI: 10.1002/alz.12117. View