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Neurol Sci

DOI 10.1007/s10072-017-2975-9

REVIEW ARTICLE

Sleep disturbance in mild cognitive impairment: a systematic


review of objective measures
Mingyue Hu 1 & Ping Zhang 1 & Chen Li 1 & Yongfei Tan 2 & Guichen Li 1 & Duo Xu 1 &
Li Chen 1,2

Received: 21 November 2016 / Accepted: 19 April 2017


# Springer-Verlag Italia 2017

Abstract Sleep disturbance frequently occurs in patients with cognitive impairment (naMCI) had more TST and less AI.
mild cognitive impairment (MCI) and appears to be involved Patients with naMCI expressed more AI than those with
in the cellular and molecular mechanisms of cognitive decline. aMCI. The results indicate that MCI patients might experience
The aim of this systematic review is to clarify whether patients more serious sleep disturbance and that different MCI sub-
with MCI demonstrate alterations in certain sleep parameters: types have different patterns of sleep disturbance.
total sleep time (TST), sleep efficiency (SE), sleep latency
(SL), rapid eye movement latency (REML), percent of rapid Keywords Mild cognitive impairment . Sleep disturbance .
eye movement (REM%), arousal index (AI), wake after sleep PSG . Actigraphy . Meta-analysis
onset (WASO), slow-wave sleep (SWS), periodic leg move-
ment in sleep (PLMS), and cyclic alternating pattern (CAP)
through polysomnography (PSG) and actigraphy. Databases Introduction
including PubMed, Web of Science, Embase, ScienceDirect,
Cochrane, CBM, CNKI, Wanfang Data, and VIP were In the World Alzheimer Report 2015, it is said that there are
searched up to January 2016 to collect literature on the corre- over 9.9 million new cases of dementia each year worldwide,
lation between sleep disturbance and MCI as assessed by ob- implying one new case every 3.2 s [1]. Mild cognitive impair-
jective measures. Meta-analysis was conducted using the ment (MCI) is viewed as a transitional stage from normal
Review Manager 5.3 software. A total of ten case-control health to dementia [2, 3], with a conversion rate of
studies involving 225 MCI patients and 235 healthy elders 60.5~100% to dementia in 5~10 years [2]. Given the limita-
(HE) were deemed eligible and included in our meta-analysis. tions of therapeutic methods for dementia, an understanding
Every type of sleep disturbance was present in our studies of the clinical features of MCI is crucial for the development
with significant differences in the MCI subtypes. Compared of preventive projects and early interventions.
with HE, overall MCI patients as a group expressed more SL Previous and recent studies all show that sleep disturbance
and less SE; MCI patients showed less TST and SE and more is one of the major causes of MCI [3, 4]. Researchers are also
SL and CAP; patients with amnestic mild cognitive impair- investigating early predictors of MCI and have identified all
ment (aMCI) had less AI; patients with non-amnestic mild kinds of markers [58], and plenty of findings have suggested
that sleep disturbance is a risk factor of MCI or that MCI
patients experienced a more serious degree of sleep distur-
Mingyue Hu and Ping Zhang contributed equally to this work.
bance than healthy elders (HE) [2, 7, 8].
* Li Chen
Sleep disturbance can be evaluated by subjective and ob-
chen_care@126.com jective measures [8]. For objective measures, medical detect-
ing and monitoring equipment has been widely used.
1
College of Nursing, Jilin University, 965 Xinjiang Road, Actigraphy is highly correlated with polysomnography
Changchun 130021, China (PSG) for detecting sleep states [8, 9]. The present review
2
Department of Pharmacology, College of Basic Medical Sciences, includes a variety of results regarding the use of PSG and
Jilin University, Changchun, China actigraphy methods to evaluate sleep disturbance [1012].
Neurol Sci

Hence, our study summarized objective measures to evaluate Bsleep disorders^[tiab] OR Bsleep disturbance^[tiab] OR
sleep disturbance and tried to explain the association between Bcircadian rhythm^[tiab] OR Bcircadian rhythms^[tiab],
sleep disturbance and MCI. Bpolysomnography^[Mesh] OR Bpolysomnographies^[tiab]
OR Bmonitoring, sleep^[tiab] OR Bsleep monitoring^[tiab] OR
Bsomnography^[tiab] OR Bsomnographies^[Mesh],
Materials and methods Bactigraphy^[Mesh] OR Bactigraph^[tiab] OR Bactigraphic
recording^[tiab] OR Bwrist actigraph^[tiab] OR Bactigraph
Inclusion criteria recording^[tiab] OR Bwrist activity^[tiab] OR Brest
activity^[tiab] OR Bactivity^[tiab] OR Bsleep-wake
The PICOS approach was used for eligibility criteria [13]: (1) activity^[tiab] OR Baccelerometry^[Mesh] OR Bsensor^[tiab].
Study participants should be diagnosed with MCI; (2) Control We also reviewed the references of the included studies to ex-
groups should contain HE with normal cognition; (3) The plore other potential candidates for inclusion. The languages
detection measures of the included articles should include were restricted to English and Chinese.
PSG and/or actigraphy; (4) The outcome should cover sleep
parameters; and (5) The continuous data and the 95% confi-
dence interval (CI) should be provided. Review selection and data extraction

Exclusion criteria In accordance with the formulated inclusion and exclusion


criteria, the titles were first reviewed for obvious exclusions.
(1) The sample did not meet all the PICOS standards; (2) The After the abstract was read, if it was unclear whether the article
study did not refer to a history of neurological conditions, should be excluded, the full text was reviewed. Two reviewers
psychiatric disorders, and/or major medical illness; the use (HMY and LC) selected articles and extracted data indepen-
of medication affecting the sleep-wake cycle (benzodiaze- dently and finally compared their lists of articles to ensure that
pines, etc.); the presence of depressive symptoms; complaints the same studies had been included or excluded. The two
of sleep-disordered breathing; movement disorders during reviewers resolved the discrepancies by discussion. If the dis-
sleep; or unusual sleep schedules (i.e., shift work); (3) The crepancies could not be solved, the final decision was made by
sample was a duplicate of another published paper without a third person (ZP).
novel information, although additional studies from the same
sample were included if they represented different outcome Quality assessment
variables; and (4) The study has missing data, and even
through a variety of methods, we were unable to contact the Two reviewers (HMY and LC) evaluated the included studies
authors. independently. The tool used for evaluating the quality of the
studies was the Newcastle-Ottawa scale (NOS) [14]. The NOS
Data source and search strategy includes the three categories of selection (four items, four
stars), comparability (one item, two stars), and exposure (three
A systematic literature search was conducted to identify studies items, three stars) for a total of nine stars. A study can be
that evaluated sleep disturbance in patients with MCI compared awarded a maximum of one star for each numbered item with-
to cognitively normal controls, and the measurement methods in the selection and exposure categories. A maximum of two
were required to contain actigraphy or PSG as an objective mea- stars can be given for comparability.
sure. The databases include PubMed, Web of Science, Embase,
ScienceDirect, Cochrane, CBM, CNKI, Wanfang Data, and VIP.
All the databases were searched up to January 2016. The key
search terms (using the PubMed query as an example) were Statistical analysis
Bmild cognitive impairment^[Mesh] OR Bcognitive impairment,
mild^[tiab] OR Bcognitive impairments, mild^[tiab] OR RevMan 5.3 was used in our meta-analysis. The standard
Bimpairment, mild cognitive^[tiab] OR Bimpairments, mild mean difference (SMD) with 95% CI was applied. To begin,
cognitive^[tiab] OR Bmild cognitive impairments^[tiab] OR the fixed-effect model was used if the result of the heteroge-
Bmental disorder^[Mesh] OR Bmental disorders^[tiab] OR neity test showed p > 0.05 and I2 < 50%. If not, the random-
Bneurocognitive disorder^[tiab] OR Bneurocognitive effect model and subgroup analysis were used to analyze the
disorders^[tiab] OR Bcognitive disorder^[tiab] OR Bcognitive sources of heterogeneity. A p value <0.05 was considered
disorders^[tiab] OR Bmci^[tiab], Bdyssomnias^[Mesh] OR significant. Sensitivity analysis was used to analyze the stabil-
Bsleep wake disorders^[Mesh] OR Bsleep wake disorder^[tiab] ity of the results, while a funnel plot was used to judge pub-
OR Bsleep deprivation^[Mesh] OR Bsleep disorder^[tiab] OR lication bias.
Neurol Sci

Fig. 1 PRISMA flowchart of


searching and selection guidelines

Publication bias Statistical analysis

The funnel plots were applied using RevMan 5.3. The SMD TST
as the x-axis and the SE (SMD) as the y-axis were used to
examine publication bias. We regarded heterogeneity as lower Eight [1012, 1618, 20] included studies showed that there
if the figure had bilateral symmetry. was no significant difference between the overall MCI and HE
groups (SMD = 0.19, 95% CI (0.75~0.47), p = 0.50)
(Fig. 2).
Results
Subgroup analysis of TST MCI subtypes: Seven [1012,
Search results 1618, 20] studies showed that the HE groups had a greater
mean than the MCI groups (SMD = 0.53, 95%CI (0.77~
The literature search method was conducted as shown in 0.28), p < 0.0001). Two [15, 20] studies showed no
Fig. 1: after the full text of the 61 potentially eligible articles
had been read, 10 studies fulfilled the eligibility criteria and Table 1 The NOS quality assessment of the ten included studies
were included [1012, 1521] (Fig. 1).
Studies Selection Comparability Exposure Total

Quality assessment of studies (NOS) Yu et al. [10] 8


Jiang et al. [11] 7
The Newcastle-Ottawa scale (NOS) was used in our study. All Hita-Yaez et al. [12] 7
the articles scored more than six stars, so all the articles were Westerberg et al. [15] 8
considered high-quality [14] (Table 1). Lou et al. [16] 8
Kim et al. [17] 8
Baseline characteristics of the included studies Maestri et al. [18] 7
Zhang et al. [19] 6
Information on all the ten articles, such as publication time, Naismith et al. [20] 9
countries, major criteria of MCI, and sample size, is listed in Hayes et al. [21] 8
Table 2.
Table 2 Main characteristics of the ten studies

Studies Year Participants country Major criteria for MCI Subtypes of Sex Age SD (years) Objective
of origin MCI measures
Cases (M / Controls (M / Cases Controls
F) F)

Yu et al. [10] 2009 Taiwan CDR/MMSE/blood test/thyroid test/GDS/CT MCI 9/4 7/5 75.1 10.7 76.4 8.3 PSG
Jiang et al. [11] 2013 Italy MRI/HIS/MoCA/Hamilton rating scale for MCI 38 / 18 33 / 15 63.0 2.5 62.0 3.6 PSG
depression/Hamilton anxiety rating scale
Hita-Yaez et al. 2013 Spain CDR/MMSE/DSM-IV/GDS/immediate and MCI 18 / 7 12 / 13 70.5 6.8 67.1 5.3 PSG
[12] delayed recall
Westerberg et al. 2010 US MMSE/trail making test parts A and B/Boston aMCI 2/8 3/7 71.1 0.0 72.5 0.0 Actigraphy
[15] naming test/word list learning and
recognition/constructions/category
fluency/CERAD/Wechsler memory scale
Lou et al. [16] 2008 China MMSE/ADL/HIS/CT/MRI MCI 6 / 11 9/9 70.0 6.0 69.0 6.0 PSG
Kim et al. [17] 2011 Korean Petersens criteria/CERAD-K/verbal MCI 9 / 21 9 / 21 68.0 4.09 67.4 3.8 PSG
fluency/Boston naming test/word list
memory/constructional praxis/word list
recall/word list recognition/constructional
recall/GDS/blood test/DSM-IV
Maestri et al. [18] 2015 Italy CDR/MMSE/MRI/blood test/immediate and MCI 6/7 4/5 68.5 7.0 69.2 12.6 PSG
delayed recall for Rey auditory verbal learning
test/attentive matrices/trail making test parts A
and B/digit span forward score
Zhang et al. [19] 2006 China MMSE/CDR/ADL/HIS/immediate and delayed MCI 21 / 28 74.0 4.8 71.6 5.3 PSG
memory test/digit symbol test
Naismith et al. [20] 2014 Australia Petersens criteria/attention, working memory, MCI 17 / 9 12 / 14 70.1 9.9 65.9 9.8 PSG Actigraphy
processing speed, verbal and visual learning and (sleep
memory, language, visuospatial, executive parameter
function/DSM-IV/MRI data from
PSG)
Hayes et al. [21] 2014 US Petersens criteria/GDS/MMSE/CDR/memory test/ aMCI naMCI 2 / 14 3 / 26 84.8 6.6 87.5 4.0 Actigraphy
language, attention, executive function test

M male, F female, MRI magnetic resonance imaging, CDR clinical dementia rating, MMSE minimum mental state examination, CERAD Consortium to Establish a Registry for Alzheimers Disease, HIS
Hachinski ischemic score, MoCA Montreal cognitive assessment, DSM diagnostic and statistical manual of mental disorders, GDS global deterioration scale, ADL activities of daily living, CT computed
tomography, MCI mild cognitive impairment, aMCI amnestic mild cognitive impairment, naMCI non-amnestic mild cognitive impairment, PSG polysomnograph.
Neurol Sci
Neurol Sci

Fig. 2 Meta-analysis of TST between the overall MCI and HE groups

significant difference between their amnestic mild cognitive SE


impairment (aMCI) and HE groups (SMD = 1.60, 95%CI
(1.25~4.44), p = 0.27). One [21] study showed that the Six [10, 11, 1517, 19] studies showed that HE had a better
non-amnestic mild cognitive impairment (naMCI) group had sleep efficiency (SE) (SMD = 0.68, 95%CI (0.92~0.45),
a greater mean total sleep time (TST) than the HE group p < 0.00001) (figures not displayed).
(SMD = 2.20, 95%CI (1.31~3.08), p < 0.00001) (Fig. 3).
Comparison between naMCI and aMCI: Only one [21] Subgroup analysis of SE MCI subtypes: Five [10, 11, 16, 17,
study provided both naMCI and aMCI data. No significant 19] studies provided MCI group data, while one [15] study
difference was observed between the naMCI and aMCI provided aMCI group data. In the MCI subgroup, greater SE
groups [SMD = 0.61, 95%CI (1.65~0.43), p = 0.25] in HE was observed (SMD = 0.73, 95%CI (0.98~0.48),
(Fig. 4). p < 0.00001). In the aMCI subgroup, no significant difference
Different measurements: Seven [1012, 1618, 20] studies was observed between the aMCI and HE groups
provided detailed PSG data, while one [15, 21] provided (SMD = 0.11, 95%CI (0.99~0.77), p = 0.81).
actigraphy data. In the PSG subgroup, longer TST was ob- Different measurements: Five [10, 11, 16, 17, 19] studies
served in the HE groups (SMD = 0.53, 95%CI (0.77~ provided detailed PSG data, while one [15] provided
0.28), p < 0.0001). In the actigraphy subgroup, no significant actigraphy data. In the PSG subgroup, greater SE was ob-
difference was observed between the overall MCI and HE served in HE (SMD = 0.73, 95%CI (0.98~0.48),
groups (SMD = 1.30, 95%CI (0.89~3.48), p = 0.25) (Fig. 5). p < 0.0001). In the actigraphy subgroup, no significant

Fig. 3 Subgroup analysis of MCI subtypes on TST


Neurol Sci

Fig. 4 Subgroup analysis of naMCI and aMCI on TST

difference was observed between the overall MCI and HE REM%


groups (SMD = 0.11, 95%CI (0.99~0.77), p = 0.81).
Six [10, 11, 1720] included studies showed that there was no
significant difference between the overall MCI and HE groups
SL (SMD = 0.70, 95%CI (1.59~0.19), p = 0.12).

Six [1012, 15, 16, 19] studies showed that overall MCI pa-
tients have a longer sleep latency (SL) (SMD = 0.78, 95%CI AI
(0.53~1.02), p < 0.00001).
Six [10, 11, 1720] included studies showed that there was no
significant difference between the overall MCI and HE groups
Subgroup analysis of SL MCI subtypes: Five [1012, 16, 19] (SMD = 0.02, 95%CI (1.46~1.51), p = 0.98).
studies provided detailed MCI data, while one [15] provided
aMCI data. In the MCI subgroup, longer SL in MCI was
observed (SMD = 0.78, 95%CI (0.53~1.04), p < 0.0001). In Subgroup analysis of AI MCI subtypes: Six [1012, 16, 18,
the aMCI subgroup, no significant difference was observed 19] studies showed that no significant difference was found
between the aMCI and HE groups (SMD = 0.78, 95%CI between the MCI groups and HE groups (SMD = 0.77,
(0.53~1.02), p = 0.17). 95%CI (0.38~1.92), p = 1.09). One [21] study showed that
the aMCI group expressed a lower arousal index (AI) than the
HE group (SMD = 8.20, 95%CI (10.42~5.98),
REML p < 0.00001) and that the naMCI group expressed a lower
AI than the HE group (SMD = 3.54, 95%CI (4.63~
Five [11, 16, 1820] included studies showed that there was 2.44), p < 0.00001).
no significant difference between the overall MCI and HE Comparison between naMCI and aMCI: Only one [21]
groups (SMD = 0.27, 95%CI (0.24~0.77), p = 0.31). study showed that the naMCI group had a greater AI than

Fig. 5 Subgroup analysis of different measurements in relation to TST


Neurol Sci

the aMCI group (SMD = 2.80, 95%CI (4.31~1.30), Table 3 Publication bias of TST
p = 0.0003). Sleep parameters Eggers test Beggs test
Different measurements: Six [1012, 16, 18, 19] studies
provided detailed PSG data, while one [21] provided TST t = 0.69 p > |t| = 0.510 z = 0.31 pr > z = 0.754
actigraphy data. In both the PSG and actigraphy subgroups,
no significant difference was observed between the MCI and
HE groups (SMD = 0.77, 95%CI (0.38~1.92), p = 1.09;
SMD = 3.54, 95%CI (4.63~2.44), p < 0.00001). final result. We also used Stata 12.0 to retest the publication
bias of TST. The p value was >0.05 (Table 3).
WASO

Four [15, 17, 18, 20] included studies showed that there was Discussion
no significant difference between the overall MCI and HE
groups (SMD = 0.32, 95%CI (0.18~0.83), p = 0.21). To the best of our knowledge, this is the first meta-analysis of
sleep disturbance in MCI as assessed by objective measures.
Subgroup analysis of WASO MCI subtypes: Three [17, 18, On the objective measures, we found that, compared with HE,
20] studies provided MCI data, while one [15] provided aMCI the overall MCI patients as a group expressed more SL and
data. In both the MCI and aMCI subgroups, no significant less SE; MCI patients showed less TST and SE and more SL
difference was observed between the MCI and HE groups and CAP; patients with aMCI had less AI; patients with
(SMD = 0.32, 95%CI (0.34~0.98), p = 0.35) or between naMCI had more TST and less AI. Patients with naMCI
t h e aM C I an d H E g r ou p s ( S M D = 0. 28 , 95 % C I expressed more AI than those with aMCI.
(0.60~1.17), p = 0.53).
Different measurements: Three [17, 18, 20] studies provid- Sleep disturbance and MCI
ed PSG data, while one [15] provided actigraphy data. In both
the PSG and actigraphy subgroups, no significant difference Several parameters of sleep architecture were identified in our
was observed between the MCI and HE groups (SMD = 0.32, study. When compared with HE, MCI patients expressed
95%CI (0.34~0.98), p = 0.35; SMD = 0.28, 95%CI more SL, a greater decline in the length of TST. The naMCI
(0.60~1.17), p = 0.53). patients expressed more TST. Sleep loss could lead to short
sleep, tiredness, fatigue, and, ultimately, cognitive decline.
The identical findings from the Whitehall II study also showed
SWS
that some changes in sleep time (decrease from 8, 7, or 6 h to
less sleep time) are associated with cognitive dysfunction [22].
Three [11, 17, 20] included studies showed that there was no
A previous study also examined the association of sleep du-
significant difference between the overall MCI and HE groups
ration with cognitive function in a cohort of 1844 community-
(SMD = 0.18, 95%CI (0.66~0.30), p = 0.45).
dwelling women; women sleeping 5 h/night scored worse
than women sleeping 7 h/night in cognitive performance
PLMS [23]. In contrast to a prior study that, after controlling for
multiple potential confounders, reported a U-shaped associa-
Three [10, 11, 17] included studies showed that there was no tion between sleep time and cognitive decline, our study was
significant difference between the overall MCI and HE groups able to confirm only the left portion of the U. The reason
(SMD = 0.72, 95%CI (0.38~1.82), p = 0.20). might be that our participants were all MCI patients and HE,
not patients with severe cognitive impairment or dementia,
CAP meaning that almost all TST values were in the range of
5~8 h, not lower than 4 h or higher than 10 h. It also confirmed
One [18] included study showed that the MCI group that MCI is a transitional stage from normal to dementia [24].
expressed less cyclic alternating pattern (CAP) than the HE Shorter sleep duration has been connected with greater -
group (SMD = 1.23, 95%CI (2.15~0.30), p = 0.009). amyloid (A) deposition, suggesting that sleep disturbance
leads to MCI and is not merely a consequence of brain lesions
Publication bias but that A deposition in the areas involved in the control of
sleep could contribute to the worsening of sleep, causing a
We used RevMan 5.3 to make the funnel plots (figures are not further increase and accumulation of A [25]. We also found
displayed). The figures appeared to have bilateral symmetry. that naMCI patients experienced more TST than HE; the rea-
We can conclude that no publication bias was evident in our son might be that naMCI patients have enough TST and
Neurol Sci

memory consolidation occurs during sleep [7]. Therefore, we Objective measurement of sleep disturbance
speculate that the memory deficits of MCI patients may be
caused by insufficient TST or increased SL. Previous studies have shown that questionnaire tools (e.g., the
SE of lower than 85% is usually used as one of the diag- consensus sleep diary, Pittsburgh sleep quality index) and self-
nostic criteria for insomnia [10]. Our study found that both the reporting are applied at the point of care and rely on patients
overall MCI and unspecified MCI patients experienced lower and caregivers ability to accurately recall things [33]. In con-
SE than HE. A related study investigated the association be- trast, early research has suggested that actigraphy may be a
tween sleep and cognition among 2932 community-dwelling useful, cost-effective method for assessing specific sleep dis-
elderly persons, finding out that lower SE was consistently turbance [27]. PSG may be used for diagnosis and for evalu-
related to MCI [26]. Another study examined 60 persons aged ation of various sleep parameters, and researchers have also
55 years or older; the correlational analysis revealed that day- recommended routine overnight PSG to measure the sleep
time performance is related to SE and that a good night of state for elderly people [34]. Both measures were sensitive
sleep is associated with better cognitive performance in good in detecting sleep [9]. In our studies, subgroup analysis of
sleepers. The reason for this phenomenon also might be A different measures showed that actigraphy is less accurate than
deposition. A 2-year longitudinal study showed that cognitive polysomnography but not does affect the results. Hence, the
impairment is associated with SE and that, compared with best practice is to include both subjective and objective mea-
those without A deposition, the A deposition with cogni- sures when examining sleep quality in elderly people [8].
tive impairment group had worse SE (80.4 vs 83.7%) [27].
Compared with HE, MCI patients also had less CAP.
The result showed a CAP rate reduction that correlated Limitation
with the cognitive decline. Consistently, a previous
study showed a decreased amplitude and robustness of Our systematic review and meta-analysis is limited in that we
the sleep-wake cycle, correlated with an increased risk searched only the English- and Chinese-language literature.
of cognitive decline [28]. The aMCI and naMCI patients Thus, some studies may have been missed, which resulted in
had a lower AI, and the effect was more severe in only ten studies being included. The small sample size includ-
naMCI than that in aMCI patients. A previous study ed is another main limitation, but we believe that with the
reported that the frequency of nocturnal AI was associ- development of modern technology, there will be more and
ated with accelerated cognitive decline [7]. These differ- more researchers using objective measures to explore the cor-
ences in sleep disruption between aMCI and naMCI relation between sleep disturbance and MCI. A third limita-
may be related to differences in the pathology underly- tion is that the different criteria of MCI may affect the included
ing these MCI subtypes [21]. MCI groups. Fourth, there are only two studies referring to the
In our study, not all the sleep parameters showed changes MCI subtypes of aMCI and naMCI; further study should em-
in MCI or the MCI subtypes. Rapid eye movement latency phasize the difference of sleep disturbance between aMCI and
(REML), percent of rapid eye movement (REM%), wake after naMCI. Finally, the existing sleep parameters were not com-
sleep onset (WASO), slow-wave sleep (SWS), and periodic prehensive; further sleep parameters need to be explored.
leg movement in sleep (PLMS) showed no changes. This is
inconsistent with some previous studies. As confirmed by Acknowledgments The authors thank the Jilin University, Dr.
prior study, rapid eye movement sleep behavior disorder Changgui Kou, Dr. Xiuying Zhang et al. for their guidance in the devel-
opment of this article.
(RBD) was a preclinical marker for a kind of neurodegenera-
tive diseases, and it may impair cognition [29]. In NREM Compliance with ethical standards
stages N1, N2, and N3, research focuses on the effects of
SWS on cognition; results suggest that SWS is related to better Conflict of interest The authors declare that they have no conflicts of
cognitive function [30]. WASO is the total amount of time interest.
awake excluding the SL, determined by the PSG or
actigraphy. One study examined 39 patients by PSG, having Funding The authors received no financial support for the article.
hypothesized that mental health would be affected by high
WASO [31]. A study reported that, after a motor learning task
performed during the day, the increase of SWS during the References
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