The difference in sleep, depression, anxiety, and Internet addiction between Korean adolescents with different circadian preference.

OBJECTIVES: Compared to adults, adolescents tend to prefer evening times developmentally. The orientation toward evening times is associated with behavioral and emotional problems. Thus, this study examined the association of circadian preference with sleep-related variables, depression, anxiety, and Internet addiction in Korean adolescents.
MATERIALS AND METHODS: Participants completed the questionnaires measuring sleep pattern, sleep problem, depression, anxiety, and Internet addiction.
RESULTS: Among 765 students (age range: 13-17 years), 211 students (N male= 134) were allocated into morning types (MT) and 258 adolescents (N male= 147) were allocated into evening types (ET) based on scores of the Morningness-Eveningness Scale. Adolescents without circadian preference (N = 296) were defined as neither type (NT). ET, compared to MT and NT, woke up later in the weekend, showed delays in bedtimes, and spent shorter time sleeping. They also reported a higher level of daytime sleepiness, insomnia, and depression than NT. However, the group difference in wake time on school days was not significant, and adolescents showed mild insomnia regardless of their circadian preference. Although smartphone using time in the weekend was significantly different between groups, group difference in Internet addiction was significant only when gender was adjusted.
CONCLUSION: Circadian preference was associated with sleep patterns and sleep problems in Korean adolescents. ET showed significantly different sleep patterns compared to MT and NT. ET not only reported a higher level of daytime sleepiness and insomnia but also more depressive symptoms compared to NT. These findings suggest that the uniqueness of adolescence and environmental factors seemed to influence the association of circadian preference with mental problem. Copyright:

INTRODUCTION

Sleep pattern is modulated by the interaction of homeostatic sleep/wake cycle with circadian component, which is a time regulator to facilitate adaptive behaviors of primates (e.g., eating and sleep/wake cycle).[1] Circadian component is shifted by internal cycle (i.e., biological time which is different from 24 h) and is reset to 24 h by external environmental zeitgebers (e.g., the change in the temperature).[2] Due to the influence of age on circadian preference, adolescence is a period when sleep cycle dramatically changes.[3]

Children, who tend to be developmentally morning types (MT),[4] start to show evening orientation at around 12–14 years.[5] Several factors (e.g., sexual maturation, decreased concentration of melatonin, and the decrease in non-Rapid Eye Movment sleep) cause delays in circadian component. Although the change into MT reoccurs at around 20 years when adolescence ends,[6] adolescents are more likely to be evening types (ET), who prefer to do intellectual and physical activities in the late afternoon or at night.[4] Moreover, despite the consistent influence of biological factors on adolescents' circadian preference, environmental factors (e.g., early time for schools[3] and increased extracurricular activities)[7] exert more influence on their sleep pattern.[8] Korean adolescents, compared to adolescents in other countries, reported heavier academic burden and showed on average 1-h delay in bedtime[9] that was associated with higher level of daytime sleepiness.[7] Thus, it was expected that circadian preference would be associated with sleep patterns in adolescents.

Circadian preference, which was biologically influenced during adolescence, was assumed to be associated with physical and mental health issues. It seemed because genes (e.g., PER1, PER2, PER3, and CLOCK) regulated not only circadian component but also the release of dopamine within reward networks of the brain.[10] While MT showed healthier lifestyle with higher level of satisfaction with their overall life than ET,[5] physical and mental illnesses (e.g., depression and seasonal affective disorder)[1112] were more frequently reported in ET.[13] Moreover, ET adolescents were also found to report depression[14] and behavioral addiction.[15] Among mental health problems that were suggested to be influenced by the imbalance in circadian component, depression, and anxiety, which were identified as major psychiatric problems influencing sleep, were chosen to be examined. As Korean adolescents who reported shorter sleeping hours[9] showed higher engagement in the Internet,[16] Internet addiction, which was negatively associated with sleep quality,[17] was also chosen to be examined in the study.

The association between clock gene, managing circadian component,[18] and the extreme level of eveningness in Korean patients with bipolar disorders became nonsignificant after the correction of age.[19] The association between circadian preference and mental health problems in adolescents was also found to be moderated by other factors (e.g., parental set bedtimes).[14] That is, findings about the association of circadian preference with mental health problems in adults seemed to be less applicable to adolescents. Moreover, the circadian preference in Korean adolescents, whose sleep patterns were more environmentally influenced, was assumed to be different from adolescents in other countries. Thus, the current study investigated whether there is a difference in sleep-related variables (i.e., sleep pattern, insomnia, and daytime sleepiness), depression, anxiety, and Internet addiction between Korean adolescents with different circadian preferences.

MATERIALS AND METHODS

Recruitment and participants

School counselors, working in cooperation with the community mental health center, were invited. Principals in schools, whose counselors expressed the interest, were contacted and informed of the study rationale. When the principals in one middle school and one high school, which were located in Seoul, showed the approval for the research, researchers visited the schools and explained the purpose of the study to adolescent students and their teachers for the recruitment. Parents were also informed of the study rationale, ethical issues (e.g., the freedom to decide the participation and confidentiality), and contact details of principal investigator by letter. The written consent for the participation was obtained by both the students and their parents, and the data of this study were collected from January to February in 2015. The Institutional Review Board for Human Subjects approved the study protocol.

Measures

The Morningness–Eveningness Scale

The Morningness–Eveningness Scale, which is a subscale of the School Sleep Habits Survey (SHS), was used to measure circadian preference and sleep pattern. SHS proved its effectiveness compared to sleep actigraphy and was validated to be used in adolescents.[20] Participants responded to 10 items about the preferred timing of activities (e.g., bedtime). The scores range from 10 to 42 and higher scores indicated MT.[20] Although upper and lower 25% were operationally classified as MT and ET, upper and lower 30% were cutoff scores for MT and ET in this study in order to include all ties corresponding to upper and lower 25% and to make the ratio of MT and ET equal.

Epworth Sleepiness Scale

As the reliability and validity of the Epworth Sleepiness Scale (ESS) in adolescents were proved,[21] it was used to assess the degree of daytime sleepiness. Adolescents rated subjective somnolence of eight situations from 1 (i.e., no weekly sleepiness) to 3 points, respectively. Total score between 11 and 15 means clinically significant sleepiness and total score >16 means morbidity. Higher total score represented more severe the daytime drowsiness.

Insomnia Severity Scale

In order to measure the degree of insomnia, the Insomnia Severity Scale (ISI), of which the reliability and validity in adolescent were proved,[22] was used. Participants rated the perceived severity of insomnia from 0 to 4 points in 7 items, and higher score indicated more severe insomnia.[23] Total score <7 indicates no insomnia, total score ranging between 8 and 14 indicates mild insomnia, total score between 15 and 21 indicates moderate insomnia, and total score >22 means severe insomnia.

The Children's Depression Inventory

The Children's Depression Inventory (CDI) (i.e., a modified version of the Beck's Depression Inventory for children aged 7–17 years)[24] was used to measure the level or the depression. It was because it was validated to be used in adolescents and found to have a high degree of internal consistency with the Cronbach's alpha of 0.88. The self-report scale consists of 27 items where people assess the mood of the last 2 weeks from 0 to 2 points, and higher scores indicated a higher level of depression. Based on previous study results, the cutoff value for depression was the scores >22.[25]

The Revised Children's Manifest Anxiety Scale

The Revised Children's Manifest Anxiety Scale (RCMAS), a self-report of 37 items developed for children and adolescents,[26] was used to measure the degree of anxiety. As it assesses the degree and pattern of anxiety, higher scores indicated more severe anxiety symptoms. Total scores >19 were regarded as a clinically significant level of anxiety.

Young's Internet Addiction Scale

The Young's Internet Addiction Scale (YIAS) was proved to be highly reliable and valid in a national study.[16] As it was validated in adolescents,[27] it was used to measure the degree of Internet addiction. As adolescents responded to 30 items from 1 to 5 points, the total score ranges from 20 to 100.[28] Higher total score indicated more severe the addiction to the Internet.[28]

Statistical analysis

In CDI, RCMAS, YIAS, sleep pattern, the time to use the Internet or smartphone, ESS, and ISI, Chi-square tests and ANOVA tests were conducted to examine the group difference in categorical and continuous variables, respectively. When significant results for ANOVA tests were attained, post hoc tests using Tukey were conducted to investigate where the significant difference lied. Chi-square tests and t-tests were additionally conducted in order to examine gender difference in mental health variables and presleep activities. Significance was set at P < 0.05 for all tests. SPSS 21.0 for Windows (SPSS Inc., Chicago, IL, USA) was used to perform statistical analyses.

RESULTS

Among students in the schools (N = 1050), 78.76% of students between 13 and 17 years (N = 827, N= 518, Nfemale= 309, mean age = 15.10 ± 1.37) volunteered to participate in this study. Although false-positive or false-negative responses were not assessed, lower response rates or responses with consistent points in the scales were excluded in coding process. As 62 students were excluded, the final sample for the analysis was 765 students (N= 466, N= 299, M= 15.07 ± 1.36). Based on the scores of the Morningness–Eveningness Scale, 211 students (N= 134, Nfemale= 77, M= 15.07 ± 1.35) were categorized as MT and 258 students (N= 147, Nfemale= 111, M= 15.12 ± 1.38) were categorized as ET. Two hundred and ninety-six students (N= 182, Nfemale= 114, M= 15.03 ± 1.37), who did not show preference toward morning and evening times, were classified as neither type (NT). Three groups were not significantly different in age (F = 0.237, P = 0.789) and gender (χ2= 2.259, P = 0.323).

The difference in sleep-related variables between morning types, neither type, and evening types

ANOVA analyses were conducted in order to examine the difference in sleep pattern and sleep problems between MT, NT, and ET. Results for sleep pattern showed that there was a significant group difference in weekend wake time, bedtime on school days, weekend bedtime, and sleep duration on school days [Table 1]. Post hoc tests showed that ET woke up later in the weekend than MT (P < 0.001) and NT (P = 0.001), that ET went to bed later on school days than MT (P < 0.001) and NT (P < 0.001), and that weekend bedtime in ET was significantly delayed compared to the bedtime in MT (P < 0.001) and NT (P < 0.001). Post hoc tests also showed that sleeping duration on school days was significantly shorter in ET than in MT (P < 0.001) and NT (P = 0.001). Results for sleep problem showed that there was a significant group difference in both daytime sleepiness level and insomnia severity [Table 1]. Post hoc tests showed that the level of daytime sleepiness was higher in ET than in NT (P = 0.013) and that ET reported more severe insomnia symptom than NT (P = 0.005).

Table 1

Comparison of five sleep-related variables between morning types, neither type, and evening types

Sleep	MT (n=211)	NT (n=296)	ET (n=258)	F
Wake time (h:min)
School days	6:52 (0:48)	6:51 (0:36)	6:55 (0:44)	0.811
Weekend	9:25 (1:42)	9:44 (1:39)	10:18 (1:58)	14.573***
Bedtime (h:min)
School days	23:46 (1:07)	23:41 (1:37)	24:18 (1:09)	16.055***
Weekend	24:09 (1:35)	24:12 (1:23)	24:58 (1:37)	22.965***
Sleep duration (h:min)
School days	7:10 (1:35)	7:04 (1:11)	6:38 (1:31)	9.346***
Weekend	9:08 (2:06)	9:24 (1:57)	9:09 (2:21)	1.274
ESS	6.35 (3.72)	6.21 (3.98)	7.20 (4.51)	4.491*
ISI	9.20 (4.03)	8.73 (3.99)	9.85 (4.41)	5.036**

*P<0.05, **P<0.01, ***P<0.001. Mean (SD). SD – Standard deviation; ESS – Epworth Sleepiness Scale; ISI – Insomnia Severity Scale; MT – Morning types; NT – Neither type; ET – Evening types

In order to examine whether adolescents' choice of presleep activities was dependent on their circadian preference, a Chi-square analysis was conducted. As shown in Table 2, types of presleep activities that adolescents reported to do were not influenced by circadian preference. Regardless of circadian preference, more than 50% of students reported to watch TV, use the Internet or smartphone, or play computer games before going to bed.

Table 2

Number of morning types, neither type, and evening types in different presleep activities

Presleep activities	Circadian preference			χ2
	MT, n (%)	NT, n (%)	ET, n (%)
Studying or reading books	44 (21.1)	76 (25.9)	50 (19.5)	7.725
Exercise	25 (12.0)	28 (9.5)	23 (9.0)
Entertaining activities	140 (67.0)	187 (63.6)	179 (69.9)
Etc.	0	3 (1.0)	4 (1.6)

Frequency (%), entertaining activities include watching TV, using Internet, computer game, or smartphone. MT – Morning types; NT – Neither type; ET – Evening types

The difference in five mental health variables between morning types, neither type, and evening types

When group difference in hours of using Internet and smartphone was examined by conducting ANOVA analyses, there was a significant group difference only in hours of using smartphones in the weekend [Table 3]. Post hoc tests showed that ET spent significantly more time using smartphone in the weekend than NT (P = 0.048). Moreover, as shown in Table 3, group difference in not Internet addiction and anxiety level but depression level was significant. Post hoc tests showed that ET reported a significantly higher level of depression than NT (P = 0.004). The group difference in depression level remained significant when age or/and gender were adjusted. It was also found that when gender was adjusted, the group difference in Internet addiction became significant.

Table 3

Group difference in five variables associated with mental health

Mental health variables	Mean (SD)			F	AP1	AP2	AP3
	MT	NT	ET
Internet (h)
School days	1.44 (1.53)	1.53 (1.66)	1.80 (2.02)	2.790
Weekend	2.75 (3.03)	2.90 (2.64)	3.34 (3.53)	2.425
Smartphone (h)
School days	3.38 (3.29)	3.64 (3.50)	3.90 (3.56)	1.298
Weekend	4.49 (4.23)	4.46 (3.66)	5.32 (4.76)	3.382*
YIAS	32.14 (13.35)	33.71 (13.87)	34.98 (13.18)	2.532	0.155	0.040	0.093
CDI	14.61 (7.63)	13.44 (7.16)	15.45 (7.13)	5.126**	0.001	0.011	0.002
RCMAS	11.38 (6.34)	10.32 (5.96)	11.07 (6.41)	1.994	0.189	0.131	0.199

*P<0.05; **P<0.01. AP1 – Adjusted P value for age; AP2 – Adjusted P value for gender; AP3 – Adjusted P value for age and gender. SD – Standard deviation; MT – Morning types; NT – Neither type; ET – Evening types; YIAS – Young's Internet Addiction Scale; CDI –Children's Depression Inventory; RCMAS – Revised Children's Manifest Anxiety Scale

Gender difference in Internet addiction, depression, anxiety, and presleep activities

In order to examine the gender difference in Internet addiction, depression, and anxiety, independent t-tests were conducted. While females showed a significantly lower level of Internet addiction than males, females reported a significantly higher level of depression and more severe anxiety symptom [Supplement Table 1]. That is, the difference in Internet addiction, depression, and anxiety between males and females was significant.

Supplement Table 1

Gender difference in Internet addiction, depression, and anxiety

Mental health variables	Mean (SD)		t
	Male	Female
YIAS	35.88 (13.84)	30.43 (12.35)	5.665***
CDI	13.27 (7.30)	16.28 (6.99)	−5.541***
RCMAS	10.07 (6.20)	12.06 (6.08)	−4.367***

***P<0.001. SD – Standard deviation; YIAS – Young's Internet Addiction Scale; CDI –Children's depression inventory; RCMAS – Revised Children's Manifest Anxiety Scale

In order to examine whether the activities that adolescents did before going to bed were dependent on gender, a Chi-square test was conducted. As shown in Supplement Table 2, more males, compared to females, reported doing entertaining activities before going to bed. More females engaged in the activity studying or reading books, which was the secondly preferred activity, compared to males.

Supplement Table 2

Numbers of males and females in different presleep activities

Presleep activities	Gender		χ2
	Male, n (%)	Female, n (%)
Studying or reading books	75 (16.4)	95 (31.5)	56.219***
Exercise	46 (10.0)	30 (10.0)
Entertaining activities	332 (72.5)	174 (57.8)
Etc.	5 (1.1)	2 (0.7)

Frequency (%), entertaining activities include watching TV, using Internet, computer game or smartphone, ***Statistically significant at P<0.001

DISCUSSION

The study investigated the association of circadian preference with mental health issues and sleep problems in Korean adolescents. Adolescents with different circadian preferences showed a significant difference in sleep pattern (i.e., weekend wake time, bedtime on school days, weekend bedtime, and sleep duration on school days), sleep problems (i.e., daytime sleepiness and insomnia severity), and depression level.

Results for sleep pattern showed that ET woke up significantly later than MT and NT in the weekend. Nonsignificant group difference in wake time on school days seemed to be explained by the time for schools, which was identified as an important environmental factor influencing the wake time on school days.[7] Environmental factors were found to play a more important role in sleep during adolescence compared to internal factors in the twin adolescent study.[8] Inconsistent with finding of the association of exercise and delayed bedtime,[29] ET did not show a significant difference in presleep activities compared to MT and NT. Despite the engagement in similar activities before going to bed, the bedtime in ET was significantly delayed than in MT and NT on school days and in the weekend. It suggested that bedtime is influenced by not only presleep activities but also various factors including genetic factors and external environmental factors. Moreover, it was found that ET spent less time sleeping than MT and NT. As sleep deprivation was associated with daytime sleepiness,[30] ET, who showed a significant delay in bedtime and reported shorter sleep duration in this study, was expected to be at higher risk of sleep problems.

Results for sleep problems showed that ET, whose wake time on school days was similar to that of MT despite delayed bedtime, showed a significantly higher level of daytime sleepiness and reported more severe symptom of insomnia than NT. It was consistent with findings that ET, whose sleeping hours were limited despite delayed biological clock, reported lower quality of sleep.[31] Although ET reported a higher level of daytime sleepiness and insomnia than MT, the difference between ET and MT was not significant. Moreover, all groups showed a mild level of insomnia. It seemed because Korean adolescents with higher academic demands showed delays in bedtime and decreases in sleeping hours.[32] When sleeping hour was limited during 3 weeks, students started to have difficulty paying attention and to show poor academic performance.[33] That is, external factors (e.g., heavy academic demands, the Internet, and phone use) resulted in chronic sleep deprivation in adolescents.[34] As insomnia was closely related to depression,[35] circadian preference was expected to be associated with mental health problems.

It was reported that affective disorders accompanied insomnia and the change in the endocrine system (e.g., cortisol, adrenocorticotropic hormone, and melatonin).[12] It was because neurotransmitters, which were closely related to melatonin production (e.g., noradrenaline, serotonin, and dopamine), not only played an important role in the reports of affective disorders but also influenced circadian component. Consistent with the finding of the association between sleep deprivation and depression in Korean adolescents,[36] this study found a significant group difference in depression level. However, while the level of depression in ET was significantly higher than in NT, the difference in depression level between MT and ET was not significant despite relatively higher level of depression in ET. Moreover, the results showed that the group difference in the severity of anxiety was not significant and that ET, who spent more time using smartphone than NT in the weekend, showed a significantly higher level of Internet addiction only when gender was adjusted. It seemed that adolescents, who were found to experience a mild level of insomnia in this study, experienced a similar level of anxiety and similarly engaged in entertaining activities before going to bed. Taken together, it was suggested that as adolescence is the period when the sleep/wake cycle changes through the influence of puberty[2] and shifts earlier after the age of 20 years,[6] it was plausible that the association of circadian preference with some mental health problems became less prominent during adolescence.

In addition, the current study showed that more female adolescents are found to be MT and more male adolescents to be ET, being consistent with findings.[37] Reproduction cycle in females altered the circadian component.[37] As intrinsic circadian period of females was shorter than that of males and 24 hr circadian component was influenced by earlier sleep phase in females.[38] When the gender difference in circadian preference was investigated by recruiting females experiencing menopause, gender difference was not found.[39] That is, internal factors influenced gender difference in circadian preference.

Limitation

The findings of this study should be interpreted with caution in that it had three limitations. The first limitation was that self-reports for sleep pattern were used as the scale in a retrospective study design. As the results of the study were based on subjective responses of recruited students, the results of findings were able to be biased. Further studies, including more objective measures for sleep patterns such as polysomnography and actinography, should be conducted. The second limitation was that the generalizability of the finding was limited. It was because two schools, participating in the study, were selected for the recruitment based on the availability during the study period. As the representativeness of selected schools may be questioned, further study with more representative sample should be conducted. The last limitation was that there were other individual or external factors which were not considered in the current study. For example, social jetlag (i.e., the difference between biological rhythms and the time for social activities)[40] was found to mediate the association between circadian preference and depression. Further studies, considering not only sleep pattern but also other factors (e.g., academic stress and peer relationships), should be conducted.

CONCLUSION

The study investigated the difference in sleep (i.e., sleep pattern, daytime sleepiness, and insomnia) and mental health (i.e., depression, anxiety, and Internet addiction) between MT, NT, and ET adolescents in South Korea. It was found that circadian preference was associated with sleep pattern, sleep problems, and the level of depression. Unlike the significant difference in sleep problems between ET and NT, reports of daytime sleepiness and insomnia in ET were not significantly different from those in MT. It seemed because adolescents without circadian preference were less likely to experience biologically and environmentally dramatic change in sleep cycles. Unlike NT, ET adolescents seemed to highly suffer from sleep deprivation due to early time for schools and MT adolescents seemed to experience sleep deprivation due to delayed bedtime resulting from environmental factors (e.g., academic burden). Additional investigation for factors, influencing the difference in mental health problems between adolescents with and without circadian preference, is necessary. Moreover, all adolescents in this study reported a mild level of insomnia. As sleep deprivation was associated with cognitive deficits, poor academic achievement, and health issues, the findings of this study are clinically important. Despite significant difference in sleep-related variables and depression level between adolescents with different circadian preference, anxiety severity was not significantly different and the level of Internet addiction was significantly different when gender was adjusted. These findings suggested that mental health issues, which were reported in adults in relation to circadian preference, became less prominent in adolescents due to complicated interaction between internal and environmental factors. Thus, further studies, considering the limitations, should be conducted in order to support the mental health of adolescents who are biologically and environmentally at higher risk of mental health problem.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.