Qunxing DingEditorial on the Research Topic
The 3 S's: sex, stress, and sleep as risk factors for dementias
This Research Topic delves into emerging factors beyond age that may influence the onset and severity of dementia. While age remains a primary factor, recent evidence suggests sex, stress, and sleep play significant roles. Sex differences in disease risk have sparked debate, yet studies indicate varying cognitive decline rates between genders. Stress, whether triggered by lifestyle, environment, or internal factors, impacts overall health and may contribute to dementia development via allostatic load. Irregular sleep patterns, prevalent in aging populations, pose a potential causal link to dementia-related disorders. This research aims to explore and analyze the latest findings on these impactful factors in dementia manifestation and progression. Three articles presented data related with gender and stress in this issue: a comprehensive study on the impact of prolonged social isolation (SIS) during adulthood in female leads to significant enhancements in acquisition skills, it also results in a slight impairment in memory retention, without altering anxiety and cortisol levels (Popović et al.). Moreover, males may become more prone to inflammatory states, while females are predisposed to oxidative states due to SIS (Oliva et al.). In addition, prolonged social isolation integrates cognitive-behavioral performance with multifractal dynamics of physiological signals along with the accumulation of tau and Aβ proteins in early-onset neurodegenerative conditions like Alzheimer's disease (Cavieres). These findings underscore the critical role of social interactions in the wellbeing and overall performance of social animals, shedding light on novel avenues for further exploration in the field of neuroscience and behavioral psychology.
There is no data about sleep in this issue. However, sleep is increasingly recognized as a critical factor in overall health, with emerging research shedding light on its significant role in the risk of developing dementia. The quantity, quality, sleep pattern, lifestyle factors, and other pathological conditions all contribute to the risk of dementia.
For sleeping quantity, insufficient sleep has been linked to an elevated risk of dementia. Hahn et al. (2014) found that reduced sleep time was associated with a staggering 75% increase in the risk of all-cause dementia. Similarly, Sabia et al. (2021) revealed that short sleep duration in midlife is correlated with a heightened risk of late-onset dementia. However, it's not just inadequate sleep that poses a risk. Surprisingly, prolonged sleep duration, defined as combining nighttime sleep with daytime napping totaling 9 h or more, may also be associated with an increased risk of dementia (Benito-León et al., 2009).
The quality of sleep has emerged as a critical factor in dementia risk. Brachem et al. (2020) observed that poor sleep quality and difficulties initiating sleep were associated with incident mild cognitive impairment (MCI), a precursor to dementia. Addressing sleep disturbances and deficiencies has shown promise in mitigating the risk of incident dementia and all-cause mortality among older adults, as highlighted by Robbins et al. (2021). Notably, Lysen et al. (2020) suggested that poor sleep quality, rather than disruptions in the 24-h activity rhythm, was specifically linked to an increased risk of dementia. Additionally, the presence of inflammation may serve as a significant determinant in understanding the relationship between sleep disturbances and neurodegeneration (Baril et al., 2021).
Changes in sleep patterns have been identified as potential contributors to the development of dementia, highlighting the importance of monitoring sleep behaviors for early detection and intervention. For instance, Hahn et al. (2014) found that 28.5% of individuals experiencing alterations in their sleep patterns were diagnosed with all-cause dementia, with 22.0% developing Alzheimer's disease (AD) within 6 to 9 years after baseline assessment. Furthermore, specific sleep behaviors such as spending extended periods in bed and adopting early sleep timing have been linked to heightened dementia risk. Notably, Liu et al. (2022) found that these associations with greater cognitive decline were particularly evident among older individuals aged 60–74 years and among men.
Moreover, various lifestyle factors, including sleep duration, leisure-time physical activity, and screen-based sedentary behavior, exhibit individual associations with dementia risk in non-linear patterns (Huang et al., 2022). Poor sleep is intertwined with several risk factors for dementia, including hypertension, diabetes, obesity, and cardiovascular disease, each capable of independently elevating the risk of cognitive impairment and dementia (Leritz et al., 2011; Feinkohl et al., 2018).
To bolster the connection, it's noteworthy that individuals with dementia frequently experience sleep disturbances. As people age, the duration of sleep tends to decrease, particularly in those affected by Alzheimer's disease (AD). Notably, studies have observed poor sleep quality and insufficient sleep in individuals exhibiting preclinical signs of AD (Roh et al., 2014). Inadequate sleep or sleep disorders could hinder the brain's clearance process, potentially leading to the buildup of amyloid plaques in APP/PS1 mice lacking orexin that sleep deprivation or increased wakefulness through orexinergic neuron rescue heightened A beta pathology in the brain (Roh et al., 2014; Eide et al., 2021). Moreover, adjunctive prolonged-release melatonin therapy has shown promise in enhancing cognitive function and promoting sleep maintenance in AD patients, according to Wade et al. (2014). Similar to the effects observed with A beta, acute sleep deprivation has been found to elevate tau levels in mouse brain interstitial fluid (ISF) and human cerebrospinal fluid (CSF), while chronic sleep deprivation accelerates the propagation of tau protein aggregates within neural networks (Wang and Holtzman, 2020). Additionally, chronic sleep deprivation or sleep disorders can trigger heightened levels of inflammation, a phenomenon implicated in the development and progression of various neurodegenerative diseases, including dementia, as highlighted by Irwin and Vitiello (2019). Disruption of the body's internal clock, or circadian rhythms, stemming from irregular sleep patterns or conditions like sleep apnea, may exert adverse effects on brain health, as elucidated by Foster (2020). Notably, sleep deprivation or poor sleep quality can lead to neuronal damage and impaired synaptic plasticity, crucial processes for learning and memory, and the potential mechanisms linking sleep-related brain activity to synaptic structural remodeling post-experience (Alkadhi et al., 2013; Sun et al., 2020).
In conclusion, research indicates that the quantity, quality, sleep pattern, lifestyle factors, and other pathological conditions are associated with an increased risk of dementia. Sleep disturbances are common in individuals with dementia, suggesting a bidirectional relationship between sleep and neurodegeneration. Mechanisms linking sleep disturbances to dementia risk include impaired amyloid and tau clearance, inflammation, and disruptions in circadian rhythms, all of which contribute to neuronal damage and cognitive decline. Interventions targeting sleep quality and duration show promise in mitigating dementia risk and improving cognitive function. Further research into the intricate interplay between sleep and dementia pathogenesis is crucial for developing effective preventive and therapeutic strategies.
Author contributions
QD: Writing – review & editing, Writing – original draft.
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References
Alkadhi, K., Zagaar, M., Alhaider, I., Salim, S., and Aleisa, A. (2013). Neurobiological consequences of sleep deprivation. Curr. Neuropharmacol. 11, 231–249. doi: 10.2174/1570159X11311030001
Baril, A. A., Beiser, A. S., Redline, S., McGrath, E. R., Aparicio, H. J., Gottlieb, D. J., et al. (2021). Systemic inflammation as a moderator between sleep and incident dementia. Sleep 44:zsaa164. doi: 10.1093/sleep/zsaa164
Benito-León, J., Bermejo-Pareja, F., Vega, S., and Louis, E. D. (2009). Total daily sleep duration and the risk of dementia: a prospective population-based study. Eur. J. Neurol. 16, 990–997. doi: 10.1111/j.1468-1331.2009.02618.x
Brachem, C., Winkler, A., Tebruegge, S., Weimar, C., Erbel, R., Joeckel, K. H., et al. (2020). Associations between self-reported sleep characteristics and incident mild cognitive impairment: the heinz nixdorf recall cohort study. Sci. Rep. 10:6542. doi: 10.1038/s41598-020-63511-9
Eide, P. K., Vinje, V., Pripp, A. H., Mardal, K. A., and Ringstad, G. (2021). Sleep deprivation impairs molecular clearance from the human brain. Brain 144, 863–874. doi: 10.1093/brain/awaa443
Feinkohl, I., Lachmann, G., Brockhaus, W. R., Borchers, F., Piper, S. K., Ottens, T. H., et al. (2018). Association of obesity, diabetes and hypertension with cognitive impairment in older age. Clin. Epidemiol. 10, 853–862. doi: 10.2147/CLEP.S164793
Foster, R. G. (2020). Sleep, circadian rhythms and health. Interf. Focus 10:20190098. doi: 10.1098/rsfs.2019.0098
Hahn, E. A., Wang, H. X., Andel, R., and Fratiglioni, L. (2014). A change in sleep pattern may predict Alzheimer disease. Am. J. Geriatr. Psychiat. 22, 1262–1271. doi: 10.1016/j.jagp.2013.04.015
Huang, S. Y., Li, Y. Z., Zhang, Y. R., Huang, Y. Y., Wu, B. S., Zhang, W., et al. (2022). Sleep, physical activity, sedentary behavior, and risk of incident dementia: a prospective cohort study of 431,924 UK Biobank participants. Molec. Psychiat. 27, 4343–4354. doi: 10.1038/s41380-022-01655-y
Irwin, M. R., and Vitiello, M. V. (2019). Implications of sleep disturbance and inflammation for Alzheimer's disease dementia. Lancet Neurol. 18, 296–306. doi: 10.1016/S1474-4422(18)30450-2
Leritz, E. C., McGlinchey, R. E., Kellison, I., Rudolph, J. L., and Milberg, W. P. (2011). Cardiovascular disease risk factors and cognition in the elderly. Curr. Cardiovasc. Risk Rep. 5, 407–412. doi: 10.1007/s12170-011-0189-x
Liu, R., Ren, Y., Hou, T., Liang, X., Dong, Y., Wang, Y., et al. (2022). Associations of sleep timing and time in bed with dementia and cognitive decline among Chinese older adults: a cohort study. J. Am. Geriatr. Soc. 70, 3138–3151. doi: 10.1111/jgs.18042
Lysen, T. S., Luik, A. I., Ikram, M. K., Tiemeier, H., and Ikram, M. A. (2020). Actigraphy-estimated sleep and 24-hour activity rhythms and the risk of dementia. Alzheimer's Dement. 16, 1259–1267. doi: 10.1002/alz.12122
Robbins, R., Quan, S. F., Weaver, M. D., Bormes, G., Barger, L. K., and Czeisler, C. A. (2021). Examining sleep deficiency and disturbance and their risk for incident dementia and all-cause mortality in older adults across 5 years in the United States. Aging 13:3254. doi: 10.18632/aging.202591
Roh, J. H., Jiang, H., Finn, M. B., Stewart, F. R., Mahan, T. E., Cirrito, J. R., et al. (2014). Potential role of orexin and sleep modulation in the pathogenesis of Alzheimer's disease. J. Exper. Med. 211, 2487–2496. doi: 10.1084/jem.20141788
Sabia, S., Fayosse, A., Dumurgier, J., van Hees, V. T., Paquet, C., Sommerlad, A., et al. (2021). Association of sleep duration in middle and old age with incidence of dementia. Nat. Commun. 12:2289. doi: 10.1038/s41467-021-22354-2
Sun, L., Zhou, H., Cichon, J., and Yang, G. (2020). Experience and sleep-dependent synaptic plasticity: from structure to activity. Philos. Trans. R. Soc. B 375:20190234. doi: 10.1098/rstb.2019.0234
Wade, A. G., Farmer, M., Harari, G., Fund, N., Laudon, M., Nir, T., et al. (2014). Add-on prolonged-release melatonin for cognitive function and sleep in mild to moderate Alzheimer's disease: a 6-month, randomized, placebo-controlled, multicenter trial. Clin. Interv. Aging 9, 947–961. doi: 10.2147/CIA.S65625
Keywords: gender, sleep, dementia, risk factor, neurodegeneration
Citation: Ding Q (2024) Editorial: The 3 S's: sex, stress, and sleep as risk factors for dementias. Front. Aging Neurosci. 16:1410797. doi: 10.3389/fnagi.2024.1410797
Received: 01 April 2024; Accepted: 10 April 2024;
Published: 22 April 2024.
Edited and reviewed by: Agustin Ibanez, Latin American Brain Health Institute (BrainLat), Chile
Copyright © 2024 Ding. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Qunxing Ding, qding@kent.edu