Accepted Manuscript Sleep habits, circadian preference, and school performance in early adolescents Paolo M. Russo, Valeria Biasi, Carlo Cipolli, Luca Mallia, Elisa Caponera PII:

S1389-9457(16)30250-7

DOI:

10.1016/j.sleep.2016.09.019

Reference:

SLEEP 3212

To appear in:

Sleep Medicine

Received Date: 18 July 2016 Revised Date:

24 September 2016

Accepted Date: 29 September 2016

Please cite this article as: Russo PM, Biasi V, Cipolli C, Mallia L, Caponera E, Sleep habits, circadian preference, and school performance in early adolescents, Sleep Medicine (2016), doi: 10.1016/ j.sleep.2016.09.019. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

Graphical abstract

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Evening-type adolescents partially recover their sleep debt on weekend days. This partial re-alignment of social and biological clocks suggests to temporarily improve their school performance by planning tests and classwork at the beginning of the following week.

ACCEPTED MANUSCRIPT Sleep habits, circadian preference, and school performance in early adolescents

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Paolo M. Russo a,*, Valeria Biasi b, Carlo Cipolli a, Luca Mallia c, Elisa Caponera d

Department of Experimental, Diagnostic and Specialty Medicine─DIMES, University of Bologna, Bologna, Italy Department of Education, “Rome Tre” University, Rome, Italy

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Department of Movement, Human and Health Sciences, University of Rome "Foro Italico", Rome, Italy

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d

National Institute for the Educational Evaluation of Instruction and Training (INVALSI), Rome, Italy

Article history: Received

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Accepted

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Received in revised form

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ARTICLE INFO

Keywords:

Sleep habits Early adolescence Chronotype Sleep debt Daytime sleepiness

ACCEPTED MANUSCRIPT School performance

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E-mail address: [email protected] (P. M. Russo)

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*Corresponding author at: Department of Experimental, Diagnostic and Specialty Medicine─ DIMES, University of Bologna, Viale Berti Pichat 5, 40127 Bologna, Italy. Tel.: +393403657002; fax: 051-243086.

ACCEPTED MANUSCRIPT 1. Introduction

Adolescence is characterized by several changes in sleep organization, such as the trend toward a later bedtime and rebound sleep during the weekend [1]. Although this developmental pattern is often associated negatively with school achievement, the relationship between sleep habits

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(including circadian preference or chronotype) and school performance has been investigated less in infancy [2] and early adolescence [3] than in late adolescence. To cast light on how insufficient quality and/or duration of sleep are related to perceived sleep problems and school performance in extreme evening-type (E-type) compared with morning-type (M-Type) early adolescents [4], we

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compared questionnaire data on type and frequency of sleep problems and school performance of two groups of eighth-grade Italian students with opposite circadian preference, as measured by the morningness/eveningness scale included in the School Sleep Habits Survey (SSHS) developed by

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Carskadon et al. [5,6].

2. Methods

A large, randomly selected sample (n = 3463) of eighth-grade Italian students (age 13.8 ± 0.5 years;

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49.6% male) who participated in an international study of achievement in mathematics and science (Trends in International Mathematics and Science Study [TIMSS]) [7] filled out the Italian version of the SSHS [8] and indicated their last report card grade points in mathematics, science, and Italian.

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The SSHS provides detailed information about sleep habits. It consists of the following three scales: (1) the Sleepiness Scale (SLS), with nine 4-point items that explore difficulty staying awake in different contexts; (2) the Sleep-Wake Problems Behaviour Scale (SWPBS), with ten 5-point items

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that assess irregular sleep habits, prolonged sleep latency, and difficulty waking up in the morning; and (3) the Morningness/Eveningness Scale (M/E), with 10 items that measure circadian preference. The students who were above the 90th percentile (n = 301) or below the 10th percentile (n = 347) were included in the extreme M-type and E-type subgroups, respectively [8]. Statistical analyses (using the χ2 test, one-way and mixed analyses of variance, and Pearson r correlation) were carried out using SPSS 21 software. Given the large number of subjects and thus the high likelihood of statistically significant effects but with negligible size, only significant findings with α < 0.001 and an effect size greater that the small effect−size criteria, according to the Cohen classification, were considered.

ACCEPTED MANUSCRIPT The local Ethics Committee approved the study protocol. Informed consent was obtained from all participants, and the study was performed in compliance with the Declaration of Helsinki.

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3. Results

Table 1 reports the proportions of sleep problems that were perceived to occur more than once per week by the total sample and by extreme E-type and M-type adolescents (upper part) and the

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frequency of struggling to and/or falling asleep in distinct everyday situations (lower part). The number of sleep problems perceived by all adolescents (2.24 ± 1.9 out of 10) was significantly related to the SLS (r = 0.39) and M/E total scores (r = −0.41). The average of M/E total score of all

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adolescents was 26.01 ± 4.95, and it is correlated to the total scores of the SWPBS (r = −0.44) and SLS (r = −0.31) scales, indicating that an evening orientation is associated with poor sleep quality and higher daytime sleepiness in this age group. Extreme E-type adolescents showed higher scores than M-type adolescents in both the SWPB (27.1 ± 6.6 vs 7.3 ± 5.2; p < 0.001; η2 = 0.40) and the SLS (16.1 ± 4.8 vs 11.7 ± 3.6; p < 0.001; η2 = 0.21) scales. No sex-related significant difference

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was found for any indicator.

E-type adolescents showed much higher proportions of all sleep problems and occurrences of daytime sleepiness in all everyday situations (particularly during studying or doing homework and

to sex.

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working at school) than did M-type adolescents. Again, there was no significant difference in regard

The sleep habits of extreme E-type and M-type adolescents are shown in Figure 1. A repeated

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mixed-model analysis of variance (using sex and night as factors) showed that E-type adolescents had significantly later bedtimes on both school nights and weekend nights; significantly shorter sleep durations (approximately 50 minutes) on school nights and longer durations (approximately 1 hour) on weekend days; and significantly later rise times on weekend days.

With respect to scholastic achievement, female students reported higher grades than male students in Italian (females, 6.99; males, 6.57), whereas there were no significant sex difference for grade in mathematics and science. On the contrary, the grades in mathematics, science, and Italian were significantly associated with SWPBS total score (−0.28, −0.29, and −0.26, respectively), SLS total

ACCEPTED MANUSCRIPT score (−0.20, −0.20, and −0.19, respectively) and, to a lesser extent, M/E total score (0.14, 0.16, and 0.13, respectively). Marked differences emerged from the comparison of school achievement between the extreme chronotypes: the grade points on the last report card were significantly lower in E-type compared with M-type adolescents in mathematics (6.0 ± 1.3 vs 6.80 ± 1.4; p < 0.001;

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η2 = 0.07), science (6.15 ± 1.3 vs 6.91 ± 1.4; p < 0.001; η2 = 0.08), and Italian (6.30 ± 1.2 vs 6.88 ±

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1.2; p < 0.001; η2 = 0.05), without sex-related significant differences.

4. Discussion

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The present proportions of early adolescents with specific sleep problems are largely similar to those reported in previous studies [1,9], making it plausible that the differences observed here between extreme E-type and M-type adolescents in regard to sleep habits and school performance are reliable. With caution due to the limitations that are intrinsic to the tools used in epidemiological studies (ie, questionnaires rather than sleep diaries or actigraphy recordings), two main inferences

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can be drawn from our findings.

First, the sleep of E-type adolescents is not only more disturbed, with a wide spectrum of problems at sleep onset and offset and with poor quality, contrary to the sleep of insomniac adolescents [10], but also varies more in duration. Moreover, the recovery during weekend days of the sleep debt

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accumulated on school days is partial. This result calls for longitudinal studies to ascertain the stability of circadian preference in early adolescence and, likewise, the reversibility of its influence

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on school performance.

Second, the lower performance (a half grade or more) of E-type adolescents is generalized to the main topics of school programs. This result is not only consistent with those of previous epidemiological studies [1,9] but also fully compatible with the indications of laboratory studies on the relationships between sleep organization and the process of memory consolidation of both declarative and procedural information [11]. This difference in school performance might be reduced by changes in the educational routine to allow E-type adolescents to achieve their learning potential. For example, under the assumption that the transitory re-alignment of social and biological clocks of E-type adolescents on weekend days may be accompanied by a temporary improvement (higher for students with a 5-day than a 6-day school schedule) in school performance

ACCEPTED MANUSCRIPT at the beginning of the following week, it may be prudent to recommend scheduling tests and

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classwork on the presumably most alert days for E-type adolescents.

ACCEPTED MANUSCRIPT References

[1] Scholle S, Beyer U, Bernhard M, et al. Normative values of polysomnographic parameters in childhood and adolescence: Quantitative sleep parameters. Sleep Med 2011;12:542–9.

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[2] Arbabi T, Vollmer C, Dörfler T, Randler C. The influence of chronotype and intelligence on academic achievement in primary school is mediated by conscientiousness, midpoint of sleep and motivation. Chronobiol Int 2015;32:349–57.

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[3] Giannotti F; Cortesi F. Sleep patterns and daytime function in adolescence: An epidemiological survey of an Italian high-school student population. In: Carskadon MA, editor. Adolescent sleep

Press; 2002, p. 132–47.

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patterns: Biological, social, and psychological influences. Cambridge, MA: Cambridge University

[4] de Bruin EJ, van Run C, Staaks J, Meijer AM. Effects of sleep manipulation on cognitive functioning of adolescents: A systematic review. Sleep Med Rev 2016, in press. doi:10.1016/j.smrv.2016.02.006.

Dev 1998;69:875–87.

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[5] Wolfson AR, Carskadon MA. Sleep schedules and daytime functioning in adolescents. Child

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[6] Wolfson AR, Carskadon MA, Acebo C, et al. Evidence for the validity of a sleep habits survey for adolescents. Sleep 2003;2:213–6.

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[7] Martin MO, Mullis IVS, editors. Methods and procedures in TIMSS and PIRLS 2011. Chestnut Hill, MA: TIMSS and PIRLS International Study Center, Boston College; 2012. [8] Russo PM, Bruni O, Lucidi F, et al. Sleep habits and circadian preference in Italian children and adolescents. J Sleep Res 2007;16:163–9. [9] Tonetti L, Natale V, Randler C. Association between circadian preference and academic achievement: A systematic review and meta-analysis. Chronobiol Int 2015;32:792–801. [10] Matricciani L, Olds T, Petkov J. In search of lost sleep: Secular trends in the sleep time of school-aged children and adolescents. Sleep Med Rev 2012;16:203–11.

ACCEPTED MANUSCRIPT [11] Wilhelm I, Prehn-Kristensen A, Born J. Sleep-dependent memory consolidation─what can be

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learnt from children? Neurosci Biobehav Rev 2012;36:1718–28.

ACCEPTED MANUSCRIPT Table 1. Frequency of sleep problems and daytime sleepiness in the total sample and subgroups of E-type and M-type adolescents.

39.7% 27.5% 19.2% 17.2% 13.0% 12.9%

18.7% 17.6% 13.4% 13.1% 11.2% 8.0% 6.1% 5.9% 2.6%

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Studying or doing homework Watching TV or listening music Traveling on bus, train, or car In a class at school Attending a performance Playing videogames During a test Doing work on a computer During a face-to face conversation

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Daytime sleepiness

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E-type, evening-type; M-type, morning type.

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72.1% 70.5% 28.5% 30.0% 29.5% 19.1%

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Sleep problems Difficulty in waking up Unsatisfied with sleep Awakening too early Difficulties in falling asleep Late to class due to oversleeping Nightmares

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Percentage of adolescents experiencing specific sleep problems more than once per week Total sample E-type adolescents M-type adolescents (N = 3463) (n = 347) (n = 301)

45.5% 20.6% 16.0% 34.6% 15.4% 10.6% 18.3% 8.1% 6.2%

11.9% 12.3% 18.5% 9.2% 4.6% 10.4%

13.4% 10.5% 5.0% 6.1% 4.3% 3.9% 8.7% 5.1% 1.1%

ACCEPTED MANUSCRIPT Figure 1. Sleep habits in extreme Evening- and Morning-type adolescents on school days (left side)

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and weekend days (right side)

M-type adolescents 22:12

E-type adolescents 01:14

M-type adolescents 23:41

(S.D. in min)

(66.1)

(47,6)

Rise Time

7:11

6:50

(S.D. in min)

(94.8)

(108.2)

Rise Time

11:22

(S.D. in min)

(26.7)

08:40

(28.1)

(S.D. in min)

(80.6)

Total sleep duration

(84.7)

469.7

517.0

Total sleep duration

610.9

554.0

(S.D. in min)

(60.2)

(51.3)

(S.D. in min)

(89.8)

(90.3)

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Bed Time

E-type adolescents 23:21

School Days

Weekend Bed Time

ACCEPTED MANUSCRIPT Highlights

School performance is lower in evening-type (E-type) eighth-grade students than in morning-type (M-type) ones.

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Sleep complaints and daytime sleepiness are more frequent in E-type students than in M-type students. The sleep debt of E-type students is partially recovered during the weekend nights.

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Scholastic performance may be improved by planning tests and classwork at the beginning of the week.

Sleep habits, circadian preference, and school performance in early adolescents.

This study aimed to cast light on the relationships between sleep habits, perceived sleep problems and school performance in Evening-type (E-type) com...
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