Sleep quality, perivascular spaces and brain health markers in ageing - A longitudinal study in the Lothian Birth Cohort 1936

Aribisala, Benjamin S.; Valdés Hernández, Maria del C.; Okely, Judith A.; Cox, Simon R.; Ballerini, Lucia; Dickie, David Alexander; Wiseman, Stewart J.; Riha, Renata L.; Muñoz Maniega, Susana; Radakovic, Ratko; Taylor, Adele; Pattie, Alison; Corley, Janie; Redmond, Paul; Bastin, Mark E.; Deary, Ian; Wardlaw, Joanna M.

Abstract

Background
Sleep is thought to play a major role in brain health and general wellbeing. However, few longitudinal studies have explored the relationship between sleep habits and imaging markers of brain health, particularly markers of brain waste clearance such as perivascular spaces (PVS), of neurodegeneration such as brain atrophy, and of vascular disease, such as white matter hyperintensities (WMH). We explore these associations using data collected over 6 years from a birth cohort of older community-dwelling adults in their 70s.

Method
We analysed brain MRI data from ages 73, 76 and 79 years, and self-reported sleep duration, sleep quality and vascular risk factors from community-dwelling participants in the Lothian Birth Cohort 1936 (LBC1936) study. We calculated sleep efficiency (at age 76), quantified PVS burden (at age 73), and WMH and brain volumes (age 73 to 79), calculated the white matter damage metric, and used structural equation modelling (SEM) to explore associations and potential causative pathways between indicators related to brain waste cleaning (i.e., sleep and PVS burden), brain and WMH volume changes during the 8th decade of life.

Results
Lower sleep efficiency was associated with a reduction in normal-appearing white matter (NAWM) volume (β = 0.204, P = 0.009) from ages 73 to 79, but not concurrent volume (i.e. age 76). Increased daytime sleep correlated with less night-time sleep (r = −0.20, P < 0.001), and with increasing white matter damage metric (β = −0.122, P = 0.018) and faster WMH growth (β = 0.116, P = 0.026). Shorter night-time sleep duration was associated with steeper 6-year reduction of NAWM volumes (β = 0.160, P = 0.011). High burden of PVS at age 73 (volume, count, and visual scores), was associated with faster deterioration in white matter: reduction of NAWM volume (β = −0.16, P = 0.012) and increasing white matter damage metric (β = 0.37, P < 0.001) between ages 73 and 79. On SEM, centrum semiovale PVS burden mediated 5% of the associations between sleep parameters and brain changes.

Conclusion
Sleep impairments, and higher PVS burden, a marker of impaired waste clearance, were associated with faster loss of healthy white matter and increasing WMH in the 8th decade of life. A small percentage of the effect of sleep in white matter health was mediated by the burden of PVS consistent with the proposed role for sleep in brain waste clearance.

Citation

Aribisala, B. S., Valdés Hernández, M. D. C., Okely, J. A., Cox, S. R., Ballerini, L., Dickie, D. A., Wiseman, S. J., Riha, R. L., Muñoz Maniega, S., Radakovic, R., Taylor, A., Pattie, A., Corley, J., Redmond, P., Bastin, M. E., Deary, I., & Wardlaw, J. M. (2023). Sleep quality, perivascular spaces and brain health markers in ageing - A longitudinal study in the Lothian Birth Cohort 1936. Sleep Medicine, 106, 123-131. https://doi.org/10.1016/j.sleep.2023.03.016

• Journal Article Type: Article
• Acceptance Date: Mar 11, 2023
• Online Publication Date: Apr 16, 2023
• Publication Date: 2023-06
• Deposit Date: Mar 31, 2023
• Publicly Available Date: Apr 3, 2023
• Print ISSN: 1389-9457
• Publisher: Elsevier
• Peer Reviewed: Peer Reviewed
• Volume: 106
• Pages: 123-131
• DOI: https://doi.org/10.1016/j.sleep.2023.03.016
• Keywords: Sleep, Perivascular spaces, Virchow Robin spaces, White matter hyperintensities, Brain atrophy, Brain volume, Leukoaraiosis, Cerebrovascular disease, Ageing, Magnetic resonance imaging