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Chronobiology International, 2013; 30(7): 919–929

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ISSN: 0742-0528 print / 1525-6073 online
DOI: 10.3109/07420528.2013.790041

Association of Eveningness With Problem Behavior in Children:


A Mediating Role of Impaired Sleep

Kristiaan B. van der Heijden, Leo M. J. de Sonneville, and Hanna Swaab

Department of Clinical Child and Adolescent Studies, Leiden Institute for Brain and Cognition, Leiden University,
Leiden, The Netherlands
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Eveningness, the preference of being active during the evening in contrast to the morning, has been associated with
markedly increased problem behavior in adolescents; however, the underlying mechanisms are still not understood.
This study investigates the association of eveningness with behavior and cognition in children aged 7–12 yrs, and
explores the potential mediating role of a variety of sleep factors. Parents of 333 school-aged children (mean
age ¼ 9.97 yrs; 55% girls) completed a sleep log and several questionnaires regarding eveningness, sleep habits, and
behavioral problems. Intellectual abilities, working memory, and attention were assessed using the short-form of the
Wechsler Intelligence Scale for Children (WISC) and subtasks of the Amsterdam Neuropsychological Tasks. Results
showed that eveningness predicted behavioral problems over and above the effects of demographic variables (age,
sex, and familial socioeconomic status) (p ¼ 0.003). Significant partial correlation was found for eveningness and sleep
duration during weekdays (p ¼ 0.005), and not during weekends. Furthermore, evening orientation was associated
with a reduced rested feeling on weekday mornings (p50.001), but not on weekends. The most important sleep
For personal use only.

characteristic showing association with many cognitive and behavioral measures was the subjective feeling upon
awakening—particularly during weekdays. Bootstrap mediation analyses demonstrated that sleep significantly
mediated the effects of eveningness on behavioral problems, working memory, and sustained attention. Interestingly,
mediation was only significant through the subjective feeling upon awakening on weekdays. The current findings
indicate that the subjective feeling upon awakening is a much better predictor of daytime problems than subjective
sleep quantity. Furthermore, the data suggest that negative outcomes in evening types are due to the fact that they
wake up before their circadian drive for arousal and prior to complete dissipation of sleep pressure during weekdays.
Interventions that target the misalignment of endogenous circadian rhythms and imposed rhythms are discussed.
(Author correspondence: kbheijden@fsw.leidenuniv.nl)
Keywords: Attention, behavior, chronotype, circadian rhythm, cognition, eveningness, sleep, working memory

INTRODUCTION
dissipation of sleep pressure during the respective
Human individuals show variation in the preference of wakeful and sleep periods, and to a longer circadian
being physically and mentally active during a specific period driven by the biological clock in the brain
period within the 24-h day (Adan et al., 2012). The (Phillips et al., 2010).
inclination to become more active either at dawn or at
dusk can be quantified on a morningness-eveningness
Recent research has demonstrated an intriguing link
between eveningness and behavioral problems. Several
13
20
scale. Based upon this propensity, individuals can be studies found increased rates of behavioral and emo-
classified into chronotypes (i.e., morning, evening, and tional problems, suicidality, and substance use in
neither types), although consensus criteria to classify adolescents with evening preference compared with
children are still lacking. Half of the variance in circa- intermediate and morning groups (Gau et al., 2007;
dian preference is genetically determined (Hur, 2007), Goldstein et al., 2007; Lange & Randler, 2011). Other
and the trait remains considerably stable during human studies demonstrated worse academic performance in
development despite marked shifts towards eveningness evening-type adolescents compared with morning and
during early adolescence (Carskadon et al., 1993). intermediate types (Besoluk et al., 2011; Giannotti et al.,
Physiologically, eveningness is related both to slow 2002; Randler & Frech, 2009; Taylor et al., 2011),
homeostatic processes that regulate the buildup and although performance decrements in evening types are

Submitted October 24, 2012, Returned for revision February 27, 2013, Accepted March 2, 2013
Address correspondence to Kristiaan B. van der Heijden, Department of Clinical Child and Adolescent Studies, Leiden University,
Wassenaarseweg 52, Box 9555, 2300 RB Leiden, The Netherlands. Tel.: +31715276628; E-mail: kbheijden@fsw.leidenuniv.nl

919
920 K. B. van der Heijden et al.

markedly reduced when tested at optimal times of the with eveningess, and how is sleep involved in these
day (i.e., afternoon) (Hahn et al., 2012). To date, little potential associations? Eveningness is expected to
effort has been put into a better understanding of the unfavorably affect externalizing and internalizing
nature of this relation, which is surprising because behavioral problems and performance on tasks of
insight into this important subject might help to intellectual abilities, attention, and working memory.
improve public health. Since the individual’s position Furthermore, it is hypothesized that both sleep quantity
within the morningness-eveningness spectrum has and sleep quality mediate this association.
important implications for its sleep characteristics,
sleep curtailment is a likely candidate to mediate the
METHODS
association between eveningness and behavioral prob-
lems. Studies have shown that during school days, sleep Participants
onset in evening-type children is generally almost 1 h The sample consisted of 333 children (mean age ¼ 9.97
later than in morning types, whereas differences in yrs; SD ¼ 1.50; 55.4% girls) from both urban and rural
wake-up time are absent due to fixed school schedules areas in The Netherlands. An average score of educa-
(Giannotti et al., 2002; Russo et al., 2007). During free tional level of the parents served as indicator of
days, a marked delay both in sleep onset and awake time socioeconomic status. This score was based upon the
can be seen (Russo et al., 2007), which is much more in scores of both the father and the mother on a 5-category
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line with their endogenous circadian rhythm. As a result, response scale: (a) no education, (b) primary, (c) lower
evening types show a shorter sleep duration than secondary, (d) higher secondary, and (e) tertiary. Eighty
morning types during school days. This large discrep- percent of the parents had completed at least higher
ancy in bedtimes between week- and free days leads to secondary school. Most parents were born in The
irregular sleep-wake rhythms. The fact that both sleep Netherlands (82%), Surinam (4%), or Turkey (2%).
quantity and sleep quality are compromised (Russo Three children were excluded from the sample based
et al., 2007), and that daytime sleepiness is higher in on their estimated full-scale IQ (570). All parents gave
evening types (Tonetti et al., 2012), raises the question to written informed consent. Ethical approval was given by
what extent each dimension of sleep contributes to the the institutional review board of Leiden University, and
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increase in behavioral problems. the experimental protocol conforms to international


A wealth of experimental, cross-sectional, and longi- ethical standards as outlined by Portaluppi et al. (2010).
tudinal studies has shown that sleep loss in children
leads to behavioral problems and cognitive deficits Procedures
across a wide variety of domains (Astill et al., 2012). Parents were approached with information letters via
This does not only hold for sleep quantity, but also sleep primary schools in both urban and rural areas in The
quality such as expressed in sleep efficiency, sleep Netherlands. After having provided written informed
latency (Komada et al., 2011; Taylor et al., 2008; Yang & consent, parents filled out questionnaires on back-
Spielman, 2001), and the regularity of the sleep-wake ground information, morningness-eveningness score,
rhythm (Manber et al., 1996; Takasu et al., 2012) have and behavioral problems of their children. After having
shown association with increased sleepiness, tension, received the completed questionnaires, the participants
anxiety, anger, hostility, and other internalizing and were allocated to one of three clock times (early
externalizing behavioral problems. Studies have sug- morning, late morning, and early afternoon) at which
gested that impaired sleep might have long-lasting administration of cognitive ability tests (subtests of the
effects on behavior, of which the residual effects can be Wechsler Intelligence Scale for Children [WISC]-III and
noticed even years after normalization of sleep. For Amsterdam Neuropsychological Tasks; for details on
instance, in a longitudinal study, Touchette and col- tests, see Instruments) took place, in order to avoid
leagues (2007) found that relatively short sleep duration time-of-day effects. Allocation was done using ‘‘ran-
before the age of 41 months is associated with exter- domization by minimization,’’ which is a randomization
nalizing problems such as hyperactivity and lower cog- process that balances for important factors, in this case:
nitive performance several years later in development. (1) age group (7–9 and 10–12 yrs) and (2) chronotype
Similarly, Friedman and colleagues (2009) published (morning type, evening type, neither). Thus, within both
longitudinal data revealing that individual differences in age groups there was an even distribution of each
developmental patterns of sleep problems from the age chronotype over the three test sessions. Furthermore,
of 4 yrs to 16 yrs are associated with executive control in parents were asked to fill in a sleep problem question-
late adolescence. These findings indicate that timely naire and to keep a structured pediatric sleep diary for
normalization of sleep might work as a preventive the duration of 1 wk.
measure for behavioral deficits later in development. Tests of cognitive ability were administered individu-
The current study is a first attempt to clarify the ally by trained undergraduate child psychologists (dur-
relation between eveningness and behavioral problems ation 60 min) in a separate room at the child’s school,
in children. The central questions are the following: during the week in which parents filled out the sleep
Which aspects of cognition and behavior are associated diary. Intellectual ability was estimated by means of two
Chronobiology International
Eveningness, Sleep, and Problem Behavior in Children 921

subtests (Vocabulary and Block design) of the Wechsler Sleep Diary


Intelligence Scale for Children-III (WISC-III; Kort et al., The sleep diary was filled out during 1 wk. Parents had
2005). Information processing was assessed with four to write down the time at which lights went out, the time
subtests of the Amsterdam Neuropsychological Tasks it took the child to fall asleep, and waking time in the
(ANT) (De Sonneville, 1999; De Sonneville et al., 2002). morning. From these data, sleep duration during each
Test order was counterbalanced by random allocation to night was calculated and, subsequently, mean sleep
two different series. Verbal task instructions were given, duration was determined for weekdays and weekends
emphasizing both speed and accuracy of performance. separately. Of the parents, 64.0% completed a full 7-d
Practice trials were included for each task. The test diary, 2.1% of the diaries contained weekday sleep only,
sessions took place on weekdays (Tuesday, Thursday, or and 14.1% reported some weekday and some weekend
Friday) during the months February to June 2010. sleep but not the full 7 d. Midsleep point was defined as
the midpoint between falling asleep and waking in the
Instruments morning, expressed in hh:mm, and was calculated
Morningness-Eveningness separately for weekdays and weekends. Midsleep point
Eveningness of the children was assessed with a Dutch has shown to be the most reliable (subjective) marker of
translation of the Children’s Chronotype Questionnaire the circadian phase that can be derived from sleep
(CCTQ) (Werner et al., 2009) completed by parents. The measurements (Werner et al., 2009). Eveningness indeed
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morningness-eveningness subscale consists of 10 state- significantly correlated with midsleep point during
ments about the child’s time-of-day preference for weekdays (r ¼ 0.473, p50.001) and weekends
certain activities and about waking in the morning, (r ¼ 0.363, p50.001), taking the demographic variables
based on the preceding weeks. Scores are summed, (age, sex, and familial socioeconomic status) into
yielding a continuous variable ranging from 10 to 48, account. Moreover, the phase angle (i.e., time interval)
with higher scores indicating increased eveningness. between midsleep point during weekends (free-running
Classification into chronotypes was not possible rhythm) and waking time on weekdays was calculated,
because normative data were not available for the which reflects the misalignment between sleep-wake
Dutch population. Therefore, the continuous variable rhythm during school days and internal circadian
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Total CCTQ score was used in the analyses. rhythm (short phase angle means that time of awaken-
Psychometric properties of the original CCTQ were ing occurs relatively early in reference to the individual’s
shown to be adequate (Werner et al., 2009). Cronbach’s endogenous circadian rhythm). Phase angle correlated
alpha of the Dutch version was 0.78. significantly with eveningness (r ¼ 0.284, p50.001).
To assess instability in midsleep point, the mean
Behavioral Problems standard deviation during 1 wk of sleep was derived.
The Child Behavioral Checklist (CBCL; 4–18 yrs) is a Only participants having data on three or more nights
parent-report questionnaire containing 113 items were included to calculate instability, which led to the
assessing a broad range of emotional and behavioral exclusion of one participant on this variable. Moreover,
problems in children (Achenbach, 1991; Verhulst et al., parents evaluated daily how rested the child felt upon
1996). Several scores can be derived from the question- waking up (5-point scale), a variable that was included
naire, such as internalizing and externalizing problems in the analyses as a subjective measure of sleep quality.
(broadband scales), total problems, and several sub- Sleep-wake stability and the rested feeling upon
scales clustering specific problems (narrowband scales). waking up are both considered aspects of sleep quality
In the present study, standardized T-scores (by age and (Yi et al., 2006).
sex) of the two broadband scales and the total problem The data from the sleep diary correlated highly with
scores were used, as well as the raw total score of the retrospective items on usual weekday and weekend
attention problems subscale. The Dutch translation of bedtimes in the sleep habits questionnaire CSHQ, both
the CBCL was found to have good reliability and validity for school days (r ¼ 0.834, p50.001) and for the weekend
in the Dutch population (Verhulst et al., 1996). (r ¼ 0.611, p50.001). Hence, for further analyses, the
Cronbach’s alpha in the current sample was 0.94. prospective sleep log variables were used.

Sleep Problems Intellectual Abilities


The Children’s Sleep Habits Questionnaire is a parent To estimate the intellectual abilities, a short version of
questionnaire for children aged 4 to 12 yrs, to screen for the Wechsler Intelligence Scale for Children—Third
common sleep problems (Owens et al., 2000). The total Edition (WISC-III; Kort et al., 2005) was used, including
sleep disturbance score is formed by the scores on 33 Block Design, where children put together blocks in a
items, each having a 3-point response scale (1–3). A pattern according to a displayed model, and Vocabulary,
higher score on the total scale is indicative of more sleep in which children are asked to define orally presented
problems. In a large sample of school-aged children, words. These subtests correlate within the 0.90 range
good psychometric properties were found (Owens et al., with full-scale IQ (Sattler & Saklofske, 2001). Block
2000). Cronbach’s alpha in the present sample was 0.97. Design was included in the present study as a measure
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922 K. B. van der Heijden et al.

of nonverbal intellectual ability, and Vocabulary as a error rates over part 1 to part 2 indicate worse working
measure of verbal intellectual ability. memory capacity.

Information Processing Statistical Analysis


Information processing was assessed using the Univariate and hierarchical linear regression analyses
Amsterdam Neuropsychological Tasks (De Sonneville, were performed to investigate the ability of eveningness
1999). Simple reaction time was assessed with the to predict cognitive performance and behavioral prob-
Baseline Speed task, a task that has been used also by lems, above and beyond the effect of the demographic
others as a measure of intensity (alertness) of attention variables age, sex, and socioeconomic status (SES).
(e.g., Konrad et al., 2004). On the screen, a (fixation) Mediation analyses were conducted in order to examine
cross is continuously projected. This cross unexpectedly possible mediated effects between independent and
changes into a square, the imperative stimulus, at which dependent variables. We tested the indirect effect of the
event the participant has to press a mouse button as fast independent variable (eveningness) on the dependent
as possible. A variable postresponse interval is used to variables (cognitive performance and behavioral prob-
ensure that the next stimulus will be presented between lems) through the mediators (sleep quantity and sleep
500 and 2500 ms after the response. The cognitive level quality). A significant mediation effect is present when
of this task is therefore limited to detection of the mere the mediator reduces or eliminates the effect of the
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presence of the stimulus. The task consists of a part for independent variable on the dependent variables, that
the left hand and one for the right hand, each part is, when the difference between the direct and indirect
consisting of 32 presentations. Outcome measure used effects is statistically significant. Mediation analyses
in the current study is the mean reaction time (RT) over were conducted using the ‘‘indirect’’ macro designed for
both hands. SPSS (Preacher & Hayes, 2008). In this analysis, 5000
The task Sustained Attention Dots is based on a bootstrapped samples were drawn with replacement
continuous performance paradigm and assesses sus- from the data set to estimate a sampling distribution for
tained attention. A participant is presented with three, the indirect mediation pathway (Hayes, 2009). The
bootstrapping strategy quantifies the indirect effect
four, or five dots on a screen and has to push a yes-
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and makes no assumption of multivariate normal


button when four dots are displayed, and the no-button
distribution in the sampling of indirect effects. Direct
when three or five dots are counted. The task includes
and indirect effects and 95% confidence intervals are
50 series, each with 12 presentations in a random order,
reported. The indirect effect is significant if zero is not
making the duration of the task approximately 15 to
within the confidence interval.
20 min. An incorrect response is followed by an auditory
Previous to these analyses, data were inspected to
signal; see De Sonneville et al. (2002) for further details.
check for outliers, missing data, and assumptions
Outcome measures in this study are mean series
applying to the statistical tests used, using descriptive
completion time, fluctuation in tempo (within-subject
statistics, scatterplots, histograms, and quantile-quan-
SD of mean completion times of the series), and error
tile plots (Q-Q plots). Total IQ score was not included in
rate (amount of misses and false alarms), as well as the analyses as covariate, given that IQ is a poorly
number of omissions and feedback responsiveness. This specified latent variable that is dependent on a range of
latter parameter reflects the ability of the child to adjust neuropsychological functions, and therefore as covari-
its behavior in response to feedback, and is operationa- ate in this study can lead to overcorrected or erroneous
lized as posterror slowing. After error feedback, subjects findings (Dennis et al., 2009).
are expected to react more carefully and thus slower Cases with outliers (z-score 4 on either a RT
than on other trials. Omissions are trials without a parameter and/or an error parameter) were removed
response and indicate lapses of attention. per task: Baseline Speed: n ¼ 3 (1%); Focused Attention 4
As a measure of focused attention and working Letters: n ¼ 35 (11%); and Sustained Attention Dots:
memory, the task Focused Attention 4 Letters was n ¼ 12 (4%). A probability level of p ¼ 0.05, two-sided,
included in the current study. Participants had to was maintained for statistical significance. All data
detect memorized target consonants (part 1: one con- analyses were performed using SPSS version 19 (SPSS,
sonant; part 2: three consonants) among four presented Chicago, IL, USA).
consonants on a specific diagonal. If the target conson-
ant was present on the predetermined diagonal, the
participant had to press ‘‘yes.’’ When the target con- RESULTS
sonant was not present, or present but at the wrong Descriptive and Preliminary Analyses
place, the participant had to press ‘‘no’’; see Huijbregts Sample characteristics are provided in Table 1. Bivariate
et al. (2002) for further task details. Outcome parameters correlations were calculated between demographic
included in the current study are RT and error rate for variables, sleep, behavioral problems, and cognitive
both part 1 and part 2. The working memory load variables. Age was significantly correlated with all
increases from part 1 to part 2, so increased slowing and sleep-related variables (i.e., eveningness and sleep
Chronobiology International
Eveningness, Sleep, and Problem Behavior in Children 923

diary variables), except for feeling rested upon waking Eveningness, Cognition, and Behavioral Problems
up during weekdays, and to almost all reaction time Hierarchical regression analyses were performed to
variables. Both sex and familial socioeconomic status examine the ability of morningness-eveningness to
(parental educational level; SES) correlated with several predict CBCL total score above and beyond the effects
sleep variables, behavioral problems, and cognitive of demographic variables. Age, sex, and SES were forced
variables. Sex was significantly related to eveningness in the first step and eveningness score in the second step
score. An independent-sample t test indicated that girls of the analysis. Eveningness predicted behavioral prob-
(M ¼ 27.02, SD ¼ 5.74) were more evening-oriented than lems over and above the effects of demographic
boys (M ¼ 25.06, SD ¼ 5.21; t(329) ¼ 3.20, p ¼ 0.001). variables ( ¼ 0.17, t(303) ¼ 2.95, p ¼ 0.003). This model
Furthermore, parents reported significantly more exter- (F(4, 303) ¼ 5.16, p50.001) explained 5.1% of the vari-
nalizing problems for boys (M ¼ 49.87, SD ¼ 10.01) than ance in CBCL total score, which was 2.4% more than a
for girls (M ¼ 46.82, SD ¼ 9.17; t(313) ¼ 2.82, p ¼ 0.005). model with demographic variables only. Further ana-
A higher SES score was associated with less behav- lyses revealed that the effect of eveningness on problem
ioral problems. In addition, a higher SES score was behavior concerns internalizing ( ¼ 0.14, t(308) ¼ 2.44,
associated with less sleep during weekdays. Because of p ¼ 0.015) as well as externalizing ( ¼ 0.13, t(307) ¼ 2.29,
the potential influence of age, sex, and SES on the p ¼ 0.023) and the attention problems scale ( ¼ 0.12,
findings, all further analyses were controlled for effects t(307) ¼ 2.06, p ¼ 0.040). As for the cognitive variables,
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of these variables. Consequently, all correlation values results showed that eveningness was positively asso-
reported below are partial correlations, corrected for ciated with verbal intellectual ability ( ¼ 0.087,
age, sex, and SES. t(319) ¼ 2.01, p ¼ 0.045), but not with nonverbal intel-
lectual ability, simple reaction time, sustained attention,
focused attention, or working memory.

Eveningness and Sleep


TABLE 1. Demographics, eveningness, and behavioral Average sleep duration during school days was 608 min
characteristics.
(median ¼ 607, SD ¼ 43, range ¼ 483–715 min), which
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Characteristic Total (N ¼ 333) was similar during weekends (M ¼ 608, median ¼ 606,
Sex (% girls) 55.3 SD ¼ 48, range ¼ 463–805 min). Midsleep point during
Age (years) 9.97 (1.50) weekdays (M ¼ 2:08, SD ¼ 0:28 h) was significantly dif-
ferent from midsleep point during the weekend
SESa
No education 1% (M ¼ 2:51, SD ¼ 0:47 h; t(252) ¼ 14.32, p50.001). The
Primary education 2% instability of midsleep point during 1 wk (within-subject
Lower secondary education 16% standard deviation) ranged from 0 (stable) to 91
Higher secondary education 35% (instable) min (M ¼ 29, SD ¼ 16). Midsleep point
Tertiary education 47%
during weekdays correlated highly with sleep duration
Eveningness score 26.14 (5.59); median: 26.00
CBCL total problemsb 47.27 (10.43) during weekdays (r ¼ 0.45, p50.001) (Table 2). This
CBCL internalizing problemsb 49.49 (10.61) relationship was not significant for sleep duration and
CBCL externalizing problemsb 48.21 (9.67) midsleep point during weekends (r ¼ 0.09, p ¼ 0.152).
WISC-IIINL TIQc 103.79 (14.28) Furthermore, an association was found of sleep duration
a
Familial socioeconomic status, defined by parental educational with feeling rested upon waking up during weekdays
level. (r ¼ 0.14, p ¼ 0.030). Feeling rested upon waking up was
b
Standardized T-scores. not related to sleep duration in the weekend. Instability
c
Very short form: Block Design, Vocabulary. of midsleep point was not associated with sleep

TABLE 2. Partial correlations between eveningness and sleep characteristics.


Sleep Sleep Midsleep Midsleep Feeling rested Feeling rested Sleep
duration duration point point upon awakening upon awakening stability
weekdays weekend weekdays weekend weekdays weekend MSP

Eveningness 0.18** 0.01 0.47** 0.36** 0.33** 0.13* 0.10


Sleep duration weekdays — 0.43** 0.45** 0.30** 0.14* 0.08 0.01
Sleep duration weekend — — 0.12 0.09 0.07 0.10 0.02
Midsleep point weekdays — — — 0.59** 0.33** 0.08 0.12
Midsleep point weekend — — — — 0.21** 0.04 0.74**
Feeling rested upon — — — — — 0.60** 0.08
awakening weekdays
Feeling rested upon — — — — — — 0.09
awakening weekend

*p 5 .05; **p 5 .01.

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924 K. B. van der Heijden et al.

duration. A significant correlation was found between Feeling rested upon waking up during weekdays was
eveningness and sleep duration during weekdays significantly and negatively correlated with sustained
(r ¼ 0.18, p ¼ 0.005), but not during weekends. attention reaction time (r ¼ 0.18, p ¼ 0.010) and stabil-
Furthermore, eveningness was negatively associated ity in reaction time (r ¼ 0.19, p ¼ 0.009), and with
with feeling rested upon waking up during weekdays working memory reaction time (r ¼ 0.15, p ¼ 0.041),
(r ¼ 0.33, p50.001), but not during weekends. with a more rested feeling signifying faster responses on
the tasks.
Sleep, Cognition, and Behavioral Problems Behavioral problems (CBCL total score) were signifi-
Partial correlation analyses indicated that verbal intel- cantly and negatively correlated with feeling rested
lectual ability significantly and negatively correlated upon waking up both during weekdays (r ¼ 0.24,
with sleep duration during weekdays (r ¼ 0.23, p50.001) and weekends (r ¼ 0.20, p ¼ 0.002), indicat-
p50.001), with longer sleep relating to lower intellectual ing that a more rested feeling after awakening relates
ability. Verbal intellectual ability was not significantly to less problem behavior. Similarly, internalizing
correlated with sleep duration during weekends problems were related to feeling rested upon waking
(Table 3). Nonverbal intellectual ability showed similar up both during weekdays (r ¼ 0.19, p ¼ 0.003) and
associations: a significant correlation with sleep dur- weekends (r ¼ 0.16, p ¼ 0.015). Externalizing problems
ation during weekdays (r ¼ 0.14, p ¼ 0.025), and non- were correlated with feeling rested upon waking up
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significance for weekend sleep duration. Working during weekdays (r ¼ 0.19, p ¼ 0.004) and weekends
memory errors correlated significantly and positively (r ¼ 0.18, p ¼ 0.005), and attention problems with
with sleep duration during weekdays (r ¼ 0.18, feeling rested upon waking up during weekdays
p ¼ 0.007), and during weekends (r ¼ 0.16, p ¼ 0.019). (r ¼ 0.17, p ¼ 0.010).
As for the behavioral problem scales, no significant
partial correlations were found with sleep duration Mediation
variables. Sleep as Mediator Between Eveningness
Reaction time on the Baseline Speed task was and Behavioral Problems
significantly and negatively correlated with feeling Eveningness was included as independent variable (X),
For personal use only.

rested upon awakening on weekend mornings (feeling behavioral problem scores as dependent variables (Y),
more rested indicating faster responses) (r ¼ 0.19, and sleep variables as mediating variables (Z). Age, sex,
p ¼ 0.010), and correlated near-significantly and nega- and SES were included as covariates. As previously
tively for weekday mornings (r ¼ 0.14, p ¼ 0.060). discussed (Rucker et al., 2011), an absence of total or

TABLE 3. Partial correlations between sleep, cognitive functioning, and behavioral problems.
Sleep duration Sleep duration Feeling rested Feeling rested Sleep stability
Behavioral problem weekdays weekend weekdays weekend MSP
Baseline speed
RT 0.07 0.04 0.14 0.19* 0.02
Sustained attention
RT 0.06 0.05 0.18* 0.11 0.04
Stability RT 0.01 0.09 0.19** 0.13 0.02
Error % sustained attention 0.10 0.09 0.12 0.14 0.02
Omissions 0.04 0.02 0.04 0.07 0.03
Feedback responsiveness 0.02 0.02 0.06 0.06 0.02
Focused attention
RT part 1 0.00 0.02 0.01 0.01 0.01
Error % part 1 0.06 0.02 0.10 0.02 0.07
RT part 2 0.03 0.03 0.10 0.03 0.03
Error % part 2 0.12 0.14 0.02 0.07 0.03
Working memorya
RT 0.05 0.03 0.15* 0.04 0.03
Error % 0.18** 0.16* 0.09 0.09 0.11
Intellectual ability
Verbal intellectual ability 0.23** 0.07 0.03 0.07 0.09
Nonverbal intellectual ability 0.14* 0.07 0.04 0.01 0.05
Behavioral problems
Total 0.05 0.02 0.24** 0.20** 0.05
Internalizing 0.09 0.02 0.19** 0.16* 0.02
Externalizing 0.04 0.04 0.19** 0.18** 0.06
Attention problems 0.02 0.03 0.17* 0.11 0.04
a
Focused Attention 4 Letters: part 2 minus part 1.
*p50.05; **p50.01.

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Eveningness, Sleep, and Problem Behavior in Children 925

direct effects does not exclude the possibility of an Sleep as Mediator Between Eveningness
indirect (mediated) effect, for instance, when one or and Cognitive Functioning
more direct effects oppose the indirect (mediation) Overall models of the effect of eveningness on cognitive
effects as a suppressor. Overall models showed that the performance, including all sleep variables, and correct-
effect of eveningness on the total behavioral problems ing for age, sex, and SES, showed that sleep mediated
score was mediated through all sleep variables together sustained attention RT (95% BCA bootstrap CI ¼ 0.0013,
(95% bias-corrected and -accelerated [BCA] bootstrap 0.0925), and working memory RT (95% BCA bootstrap
confidence interval [CI] ¼ 0.0169, 0.2827) (Table 4). CI ¼ 0.4178, 4.7428) (Table 5), although the total effects
Similarly, mediation through sleep was significant for were not significant. Further analyses showed that
attention problems (95% BCA bootstrap CI ¼ 0.0044, feeling rested upon waking up during weekdays acted
0.0625), but not for internalizing or externalizing behav- as a mediator (sustained attention RT: 95% BCA boot-
ioral problems. Further analyses were performed to strap CI ¼ 0.0002, 0.0195; working memory RT: 95% BCA
investigate which of the sleep variables mediated the bootstrap CI ¼ 0.0486, 3.0876).
effect of eveningness on the total behavioral problems
score and attention problems score. For both dependent
DISCUSSION
variables, there was mediation only through feeling
rested upon waking up during weekdays (total behav- The aim of this study was to investigate which aspects of
Chronobiol Int Downloaded from informahealthcare.com by Leids University on 11/04/14

ioral problems: 95% BCA bootstrap CI ¼ 0.0484, 0.2490; cognition and behavioral problems are associated with
attention problems: 95% BCA bootstrap CI ¼ 0.0057, eveningness, and if sleep quantity and sleep quality are
0.0484). involved in these potential associations. The results of
the present study confirm previous findings that
TABLE 4. Eveningness and behavioral problems: direct effects and indirect mediation through sleep variables.
Behavioral problem Sleep variables b 95% CI t p
Total behavioral problems Sleep quantity and quality# Total 0.35 2.78 0.006**
Direct 0.21 1.58 0.115
For personal use only.

Indirect 0.14 0.0169, 0.2827


Rested upon awakening weekdays Total 0.35 2.84 0.005**
Direct 0.22 1.73 0.084
Indirect 0.13 0.0484, 0.2490
#
Attention problems Sleep quantity and quality Total 0.06 2.04 0.042*
Direct 0.03 0.98 0.327
Indirect 0.02 0.0044, 0.0625
Rested upon awakening weekdays Total 0.07 2.36 0.019*
Direct 0.04 1.45 0.147
Indirect 0.02 0.0057, 0.0484

#Sleep quantity and quality: sleep duration weekdays, sleep duration weekends, feeling rested upon awakening weekdays, feeling rested
upon awakening weekends, and sleep stability.
*p50.05; **p50.01.

TABLE 5. Eveningness and cognitive performance: direct effects and indirect mediation through sleep variables.
Cognitive performance Sleep variable b 95% CI t p

Sustained attention RT Sleep quantity and quality# Total 0.05 1.22 0.225
Direct 0.01 0.12 0.906
Indirect 0.05 0.0013, 0.0925
Rested upon awakening weekdays Total 0.02 1.38 0.168
Direct 0.01 0.66 0.507
Indirect 0.01 0.0002, 0.0195
Working memory RT Sleep quantity and quality# Total 3.4 1.34 0.182
Direct 1.4 0.51 0.613
Indirect 2.0 0.4178, 4.7428
Rested upon awakening weekdays Total 3.2 1.28 0.202
Direct 1.9 0.73 0.467
Indirect 1.3 0.0486, 3.0876

RT ¼ reaction time.
#Sleep quantity and quality: sleep duration weekdays, sleep duration weekends, feeling rested upon awakening weekdays, feeling rested
upon awakening weekends, and sleep stability.
*p50.05; **p50.01.

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926 K. B. van der Heijden et al.

eveningness predicts behavioral problems in children Sleep Duration


(Gau et al., 2007; Giannotti et al., 2002; Goldstein et al., Sleep duration during weekdays correlated with verbal
2007; Lange & Randler, 2011; Paavonen et al., 2009), and nonverbal intellectual ability, in the sense that
although it needs to be emphasized that most behav- longer sleep duration was predictive of lower cognitive
ioral scores remained within the normal range and functioning. This effect was not in the expected direc-
effect sizes were rather small. tion, since we assumed that longer sleep duration would
As for the relation between eveningness and cognitive predict increased cognitive functioning (Astill et al.,
functioning, we found a significant positive association 2012). Furthermore, we expected longer sleep length to
only with verbal intellectual ability, but not for non- be associated with increased performance on higher-
verbal intellectual ability, simple reaction time, working order cognitive functions such as working memory and
memory, sustained attention, and focused attention, focused attention, but longer sleep duration was
which contradicts our initial hypotheses. How this associated with more errors on the working memory
might be explained will be discussed below. task. Multiple explanations can be proposed: (1) In the
present study, sleep duration is not experimentally
Eveningness and Sleep manipulated; hence, the variation in sleep duration
An individual’s circadian preference can influence stems from interindividual differences in naturalistic
three different, but related, aspects of sleep: quantity, sleep characteristics, which might result from a myriad
Chronobiol Int Downloaded from informahealthcare.com by Leids University on 11/04/14

quality, and circadian timing. Our study has corrobo- of factors such as inappropriate bedtimes, school start
rated this threefold association in elementary school- times, extreme eveningness, and sleep problems, but
aged children. Firstly, childhood eveningness was also from differences in sleep need, which obviously do
related to a delay in midsleep point, which is the not indicate a deficiency in sleep quantity. (2) The
most reliable (subjective) measure of circadian phase present study includes children of families with a
(or timing) derived from sleep assessment. Secondly, relatively high socioeconomic status, who are likely to
both sleep quantity (sleep duration) and quality be less sensitive to the effect of sleep curtailment on
cognitive performance, possibly because they are less
(feeling rested upon awakening) were related to
likely to be exposed to other stressors in their environ-
eveningness. Those associations were only significant
For personal use only.

ment than children from lower-socioeconomic-status


for weekdays and not for weekends, irrespective of the
families. The added stress of sleep disruptions may thus
fact that mean sleep duration on weekdays was similar
have a greater impact on children living under higher
to that in weekends. A likely explanation is that in
stress conditions (Buckhalt et al., 2009).
evening types, sleep duration on weekdays is limited by
Nevertheless, the results are in line with a recent
school start times, whereas during weekends the time
study by Geiger et al. (2010), which revealed a negative
of awakening is not restricted by school schedules,
association between sleep duration and IQ score in
which implies that weekend sleep duration depends on
children aged 7 to 11 yrs. The authors proposed that
many other heterogeneous factors (e.g., parenting
these unexpected results may be explained by the neural
factors, sleep-wake rhythm of family members,
efficiency theory (Haier et al., 1988). They expanded this
planned social activities). theory to nighttime behavior, with children having a
We did not categorize children into evening or higher daytime (cognitive) efficiency being more effi-
morning chronotypes, since reliable classification cri- cient during nighttime as well, resulting in a reduced
teria—at least for the Dutch child population—are not need for sleep and therefore a shorter sleep duration.
available. However, previous studies showed that during Another explanation proposed by Geiger et al. (2010) is
weekdays, evening-type adolescents sleep roughly half that children who sleep less benefit from the longer time
an hour less per night than morning types (Collado awake, which facilitates more time for cognitive stimu-
Mateo et al., 2012; Russo et al., 2007), which might result lation. However, if these explanations hold, one would
into a chronic sleep debt in the long term. also expect to find associations between sleep duration
The current results also demonstrate that evening- during the weekend, which corresponds more to the
ness associates with an unrested feeling upon waking up intrinsic sleep need, and intellectual ability, which was
during weekdays. Gaina et al. (2006) found similar not the case in this study.
associations in adolescents aged 12 to 15 yrs, with Another possible explanation could be that there
morning types reporting feeling better in the morning. were only few children who had a substantially short
An explanation for this might be that during weekdays, sleep duration (17 cases with less than 9 h; 2 cases with
evening types need to wake up earlier than their less than 8 h). The fact that sleep shortage was only mild
circadian system prefers, because they need to leave in this sample might have reduced the effect sizes.
for school. The presence of such a circadian misalign- Furthermore, although the data do not suggest that
ment corresponds to our finding that the phase there were excessive sleepers among the participants—
angle between midsleep point and rising time during for instance, there was only one case with a sleep
weekdays is shorter for evening types than for morning duration longer than 11 h—we cannot rule out the
types. possibility that there were individuals who suffered from
Chronobiology International
Eveningness, Sleep, and Problem Behavior in Children 927

hypersomnia. Research has shown that such individuals morning-type persons (Mongrain et al., 2006).
with an excessive need for sleep are characterized by Therefore, in spite of similarities in sleep duration,
poorer performance in processing speed and working evening types wake with more sleep pressure remaining.
memory (Calhoun et al., 2012). This explanation is in line with our finding that sleep
Interestingly, our finding that sleep duration does not duration itself did not mediate the association between
predict sustained attention is in line with recent meta- eveningness and behavior. Thus, it seems that evening
analytic results, and can be explained by findings that types show behavioral problems because they wake up
brain networks that are essential in top-down atten- before the circadian pacemaker exerts its activating
tional control—particularly the longer range connec- action on the arousal system and before homeostatic
tions along the anterior to posterior axis—start to sleep pressure has sufficiently reduced.
develop not until the final elementary school years and Are there any other factors besides sleep that might
therefore only minimally profit from sleep (Astill et al., explain the association between eveningness and
2012). Contrary to expectations, behavioral problems increased behavioral problems? Although not investi-
were not predicted by measures of sleep duration. This gated in this study, there is good reason to suggest that
contradicts recent meta-analytic findings (Astill et al., aspects of personality and temperament play a role.
2012), but the same methodological explanations can be Evening-type persons are identified as being more
proposed as described above for findings within the extrovert, impulsive, and novelty and sensation seeking
Chronobiol Int Downloaded from informahealthcare.com by Leids University on 11/04/14

cognitive domain. Another explanation might be that (Randler, 2008; Randler & Saliger, 2011; Tonetti et al.,
parents may be unaware of behavioral problems, since 2010), and those traits are strongly related to externaliz-
problem behavior is sometimes more apparent within ing behavioral problems. Furthermore, it is of note that
the context of school. This corresponds to findings by attention-deficit/hyperactivity disorder (ADHD)—
Aronen et al. (2000), who found associations between although moderately present in the current sample
sleep duration and teacher-reported behavioral prob- (1%)—is strongly related to eveningness, sleep disturb-
lems, but not between sleep duration and parent- ances, as well as cognitive/behavioral problems (Caci
reported problem behavior. et al., 2009), which might have influenced the findings.
Intriguingly, the subjective sleep quality index ‘‘feel- A third alternative explanation for the association
For personal use only.

ing more rested upon waking up’’—particularly during between eveningness and behavioral problems might be
weekdays—showed association with many cognitive that parents of evening-oriented children are biased in
and behavioral measures: faster simple reaction time their report of behavioral problems. Eveningness in
and sustained attention reaction time, more sustained children is likely to be accompanied with bedtime
attention stability, faster working memory reaction time, struggles in the evening and moodiness in the morning.
and fewer behavioral problems. This suggests that the This might bias parents in rating their child’s behavior,
subjective experience of not feeling rested upon awa- and might therefore represent an underlying mechan-
kening is a much better predictor of daytime problems ism in the relation between eveningness and behavior.
than sleep quantity. This corresponds to previous Nevertheless, associations between eveningness and
findings that subjective sleepiness is strongly associated behavioral problems have also been found in adoles-
with cognitive performance in children (Anderson et al., cents using self-report questionnaires (Gau et al., 2007).
2009; Sadeh et al., 2002).
Limitations
Mediation Several limitations of this study should be noted. First,
A central question in this study was: How is sleep sleep data were derived via sleep logs and question-
involved in the association between eveningness on the naires filled in by parents, and not through objective
one hand, and cognitive and behavioral functioning on actigraphy or polysomnography. Secondly, circadian
the other? The main finding is that evening types show markers were based on sleep-wake rhythm (midsleep
increased risk for behavioral problems, and that this can point). Dim light melatonin onset or temperature curves
be explained by the fact that they wake up feeling are more accurate markers to evaluate whether the
unrested during weekdays. For these individuals, the circadian pacemaker in evening types was delayed
small phase angle between midsleep point and waking indeed. Thirdly, the CCTQ has not been validated for
time indicates that they wake up earlier on weekdays the Dutch population, and Dutch normative data are
than preferred given their circadian rhythm. That might unavailable, although the current results showed suf-
cause them to wake up without a rested feeling, ficient internal consistency, and adequate external
resulting in decreased functioning particularly during validity with respect to sleep-wake rhythm.
morning hours, but possibly also during the rest of the
day. Furthermore, by means of electroencephalography Implications
(EEG), differences have been found between morning To summarize, this study in children corroborates
and evening types in markers of homeostatic sleep previous important findings in adolescents that even-
regulation. The decrease in sleep pressure during sleep ingness is related to increased behavioral problems.
in evening-type persons takes place more slowly than in This study builds upon those findings by testing a
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928 K. B. van der Heijden et al.

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