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Association between sleep disturbances and mild cognitive impairment: Clinical and research considerations

Commentary on “Late-life sleep duration associated with amnestic mild cognitive impairment” by Yuan et al.

Published online by Cambridge University Press:  31 January 2023

Joshua M. Baruth
Affiliation:
Department of Psychiatry & Psychology, Mayo Clinic, Rochester, MN, USA
Manuel Fuentes Salgado
Affiliation:
Department of Psychiatry & Psychology, Mayo Clinic, Rochester, MN, USA
Boney Joseph
Affiliation:
Department of Neurology Mayo Clinic, Rochester, MN, USA
Balwinder Singh
Affiliation:
Department of Psychiatry & Psychology, Mayo Clinic, Rochester, MN, USA
Nicolas A. Nunez*
Affiliation:
Department of Psychiatry & Psychology, Mayo Clinic, Rochester, MN, USA
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Abstract

Type
Commentary
Copyright
© International Psychogeriatric Association 2023

Over the last few decades, there has been increasing interest in understanding the potential relationship between sleep disturbances and cognitive decline. Specifically, changes in sleep duration and onset of mild cognitive impairment (MCI) has been investigated as it may provide potential opportunities for early identification of subjects and/or treatment interventions (Basta et al., Reference Basta2019; Wang et al., Reference Wang2021). The clinical presentation of MCI can be quite heterogeneous and represents a state between normal aging and dementia which obscures the diagnosis frequently. A general consensus for defining MCI includes the presence of early measurable deficits in at least one cognition domain in the absence of functional impairments without meeting criteria for dementia (APA, 2013; Ganguli et al., Reference Ganguli, Dodge, Shen and DeKosky2004).

The emergence of MCI is common in older adults, and data from the American Academy of Neurology has estimated prevalence rates up to 15% in patients older than 75 years (Petersen et al., Reference Petersen2018). Several risk factors have been highly associated with MCI such as male sex, lower educational levels, comorbid medical conditions (chronic lung disease, hypertension, and vascular risk factors), presence of neuropsychiatric symptoms, and the presence of an APOE genotype (Ganguli et al., Reference Ganguli, Dodge, Shen and DeKosky2004; Kryscio et al., Reference Kryscio, Schmitt, Salazar, Mendiondo and Markesbery2006; Petersen et al., Reference Petersen2018; Singh et al., Reference Singh2014). Similarly, a greater risk of developing dementia has been associated with increased age, hypertension, smoking habits, obesity, depression, diabetes, and social isolation (Mehta and Yeo, Reference Mehta and Yeo2017). Notably, studies have shown evidence that over a 5- to 10-year period after a diagnosis of MCI, 30% to 50% of subjects progressed to develop Alzheimer’s disease (AD) (Liss et al., Reference Liss2021).

Neuroimaging studies and several biomarkers acting as disease proxy have been identified, suggesting possible associations on serum levels of melatonin, cortisol, cholesterol, growth hormone, or thyroid-stimulating hormone with sleep disturbances and cognitive decline (Li et al., Reference Li, Vitiello and Gooneratne2018). These findings highlight the importance of further investigating potential relationships between cognitive decline, sleep changes,and changes in biomarker levels, which could improve early diagnosis and tailor early interventions. Moreover, the presence or absence of specific candidate genes such as frequency of the APOEε4 allele, APP, presenilin 1 (PSEN1), presenilin 2 (PSEN2), SORL1, and potentially others such as TLR4, CHRNB2, A2M, CTNNA3, GSTO1, GSTO2, GAPD, and ACT (Arosio et al., Reference Arosio2007) remain to be investigated as risk factors for MCI and AD which could provide a better understanding of structural and functional neuroimaging findings in correlation with clinical features.

Sleep disturbances in general affect at least one-third of patients with dementia, and specifically, insomnia is the most commonly reported symptom (Morin and Benca, Reference Morin and Benca2012); up to 50% of older adults complain of difficulty initiating or maintaining sleep (Crowley, Reference Crowley2011). Foley and colleagues emphasized a high prevalence of at least one or more comorbid medical conditions in elderly individuals with insomnia such as cardiovascular disease, chronic pain, respiratory disease, and depression (Foley et al., Reference Foley, Monjan, Brown, Simonsick, Wallace and Blazer1995). Thus, a possible bidirectional relationship has been suggested between sleep disturbances and dementia, with an increase in overall sleep disturbances in patients with dementia compared to healthy individuals (Bliwise, Reference Bliwise2004). Additionally, different studies have reported changes in sleep latency, sleep efficiency, and sleep stage duration, with increases in stage 1 and stage 2 and decreases in REM and slow wave sleep with increasing age (Ohayon et al., Reference Ohayon, Carskadon, Guilleminault and Vitiello2004; Pótári et al., Reference Pótári2017); particularly, Ohayon and colleagues have suggested a decrease in total sleep time ranging from 5 to 7 hours per night in older adults (Ohayon et al., Reference Ohayon, Carskadon, Guilleminault and Vitiello2004). In this context, a lower average of sleep efficiency, longer average sleep latency, and greater variability in total sleep time have been associated with greater risk of cognitive decline (Diem et al., Reference Diem2016). Therefore, sleep duration as a proxy may constitute an early indicator of future risk of cognitive decline which could also be a modifiable risk factor during midlife (45 to 65 years of age) capable of reducing the increasing incidence of dementia cases.

Yuan et al. in their cross-sectional findings published in International Psychogeriatrics extend prior findings related to sleep changes in older adults by investigating the relationship between sleep changes and risk of MCI. The authors examined data from the China Longitudinal Aging Study of the Shanghai Mental Health Centre collected from eight provinces (N = 2977, age range 60–96 years). Among older adults sleeping less than 7 hours, there was a decreased risk of amnestic MCI for each additional hour of sleep (Yuan et al., Reference Yuan2021) which aligns with previous studies, all having considerable public health implications (Dorffner et al., Reference Dorffner, Vitr and Anderer2015; Ohayon et al., Reference Ohayon, Carskadon, Guilleminault and Vitiello2004; Vitiello et al., Reference Vitiello, Larsen and Moe2004a).

Yuan et al. emphasized the importance of examining sleep duration and its relationship with cognitive decline (Yuan et al., Reference Yuan2021). Nevertheless, different studies have been inconsistent in determining whether increased or decreased sleep duration is associated with a higher risk of MCI or dementia. For example, a meta-analysis of five prospective studies and four cross-sectional studies (N = 62937 individuals/n = 2718 with MCI/dementia) underscored a higher risk of cognitive decline per 1 hour increase in sleep duration (Kim et al., Reference Kim, Nunes, Oliveira, Young and Lafer2016). Importantly, a longer sleep duration (>9 hours) has been associated with lower brain volumes and higher executive function impairments and could constitute a biological marker of early neurodegeneration (Westwood et al., Reference Westwood2017). In accordance with these results, a prospective study published in the International Psychogeriatrics by Zhang and colleagues examining a cohort with a 3-year follow-up duration from the Chinese Longitudinal Healthy Longevity Survey (N = 3692) has shown that long sleep duration (≥10 hours/day) may be associated with a higher risk for cognitive impairment in older individuals (OR = 1.3 95% CI 1.1–1.7) in comparison with short sleep duration (5–10 hours/day).

Conversely, a shorter sleep duration (< 6 hours per night) has been emphasized by Ma et al. and the recent published study by Yuan et al., which emphasize an association between cognitive decline and reduced sleep duration (Ma et al., Reference Ma, Liang, Zheng, Shi, Zhong and Xie2020). The Ma et al. study comprised a pooled cohort of two large observational studies, 9,254 participants from the English Longitudinal Study of Ageing and 10,811 participants from the China Health and Retirement Longitudinal Study. Specifically, there was an association between insufficient sleep (≤4 hours) or excessive (≥10 hours) sleep with cognitive decline. Similarly, Sabia and colleagues using data from the Whitehall II study (N = 7959) during a 25-year-follow-up period demonstrated a 30% increased risk of dementia associated with persistent short sleep duration in subjects aged 50–70 years of age after controlling for comorbid medical conditions and sociodemographic factors (Sabia et al., Reference Sabia2021). Importantly, a recent longitudinal study involving 1168 older adults (>50 years of age) without AD symptoms at baseline from the European Prevention of Alzheimer’s Dementia Longitudinal Cohort reported associations between AD biomarkers (total tau [t-tau], phosphorylated tau [p-tau], and amyloid-beta) in cerebrospinal fluid, cognitive performance, and sleep quality. Notably, the authors showed that sleeping less than 7 hours was linked with higher p-tau and t-tau and decreased Aβ42 after 1.5 years (Blackman et al., Reference Blackman2022).

Although the Yuan et al. study utilized subject’s self-report as a measure of sleep duration which was verified by family members, however, the possibility of recall bias cannot be ruled out (Yuan et al., Reference Yuan2021). Prior studies have shown that subjective reports of older adults regarding sleep are not fully accurate compared to objective measures (Vitiello et al., Reference Vitiello, Larsen and Moe2004b). In particular, the inclusion of self-reported data based on recollection of sleep duration would likely be even more subject to recall bias in different age groups (younger and middle-aged adults) as well as for different countries (Spitzer and Weber, Reference Spitzer and Weber2019). Additionally, including more granular measures of cognitive function like episodic memory, semantic memory, working memory, and processing speed could better characterize the relationship between sleep changes and decline in individual cognitive domains and is warranted in future study designs.

Therefore, future research considering the impact of ethnic background and diversity could increase studies generalizability as it has been addressed in a commentary published recently in the International Psychogeriatrics by Kuan and Lee (Kuan and Lee, Reference Kuan and Lee2022). Moreover, Wright and colleagues examining data from a racial and ethnically diverse population showed that there was higher incidence of MCI or dementia in Black and Caribbean Hispanics compared to Whites after controlling for sociodemographic and medical comorbidities (Wright et al., Reference Wright, DeRosa, Moon, Strobino, DeCarli, Cheung, Assuras, Levin, Stern, Sun, Rundek, Elkind and Sacco2021).

The influence of mood disorders and associations between depression, cognitive impairment, and dementia have also been studied extensively and should be mentioned in this context (Woolley et al., Reference Woolley, Khan, Murthy, Miller and Rankin2011). A systematic review and meta-analysis reported that a history of bipolar disorder was associated with a two-times-greater risk of dementia in older adults (Diniz et al., Reference Diniz2017). Additionally, depressive symptoms, particularly late-life depression, have been associated as a risk factor for developing dementia; similarly, subjective cognitive decline has been associated with the emergence of MCI and dementia increasing the risk up to 4 and 6 times compared to healthy individuals (Wang et al., Reference Wang2021). Therefore, it should also be noted that lifetime psychiatric disorders (e.g. affective disorders) can increase the risk for cognitive impairments, sleep disturbances, and neurodegenerative disorders and should be weighted in our differential diagnosis. Importantly, quantifying the role of psychiatric illnesses to cognitive decline and potentially dementia could enhance early prevention and diagnosis strategies.

Overall, the Yuan et al. study highlights an unmet need to better characterize associations between sleep duration and risk for cognitive decline. As mentioned, including more granular measures like objective sleep outcomes, biomarkers, cognitive domains, neuroimaging, medication use, and genetic risk factors has the potential to improve the design of longitudinal/observational studies. Importantly, the development of risk stratification models could contribute to earlier identification of modifiable risk factors of cognitive decline and potential for targeted interventions, in the aging population.

Conflict of interest

Dr Singh reports grant support from Mayo Clinic.

Description of authors’ roles

The authors Joshua M. Baruth, Manuel Fuentes Salgado, Boney Joseph, Balwinder Singh, and Nicolas A. Nunez equally contributed to the manuscript and revised, read, and approved the submitted version.

Acknowledgment

We would like to thank Ms. Lori Solmonson and Ms. Rene Kelly-Jambor for proofreading the manuscript and writing support.

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