Sleep Duration and Media Time Have a Major Impact on Insulin Resistance and Metabolic Risk Factors in Obese Children and Adolescents

Abstract

Background:

Lifestyle factors sleep duration and media time during childhood differ between countries. This study examined whether sleep duration and media time affect metabolic risk factors insulin resistance (IR), blood lipid profile, and liver enzymes, and whether there is a relationship between sleep time and media time in Turkish obese children and adolescents.

Methods:

Subjects included 108 obese children and adolescents (aged 10–15 years) whose lifestyle factors were assessed using a survey containing questions about sleep durations, television viewing, media use, and demographic factors. Metabolic risk factors were compared among groups categorized according to sleep and media duration.

Results:

Aspartate aminotransferase (AST), alanine aminotransferase (ALT), and triglyceride (TG) levels and homeostasis model assessment of insulin resistance (HOMA-IR) values were higher in subjects who spent >5 hours/day on media. Children 10–13 years old who slept <9 hours/day were more likely to have higher insulin and HOMA-IR (p < 0.05) levels and lower high-density lipoprotein cholesterol (HDL-C) levels compared with subjects who slept 9–10 hours/day and >10 hours/day. Correlation analysis revealed a negative relationship between sleep time and media time (r = −0.471, p = 0.000).

Conclusions:

Short sleep duration was associated with IR and an elevated plasma lipoprotein profile in children and adolescents. Our results suggest that insufficient sleep and excessive media exposure may contribute to metabolic risk in the context of obesity, and therefore, working to improve sleep duration and limit media time could help reduce metabolic risk in obese children and adolescents.

Introduction

From 1999 through 2007, obesity prevalence rose significantly in Turkish boys from 7.9% to 13.1% and in Turkish girls from 8.0% to 10.7%.¹ A major concern about the increased prevalence of obesity is its association with metabolic risk factors. The prevalence of metabolic risk factors—hypertriglyceridemia, high low-density lipoprotein cholesterol (LDL-C), low high-density lipoprotein cholesterol (HDL-C), hyperinsulinemia, and hypertension—increases with the rise in BMI.^2,3

To provide evidence for intervention and reduce the mortality due to obesity-related metabolic problems, it is critical to determine the relationship of childhood obesity with lifestyle factors across different populations. One of the factors effecting childhood obesity is shorter sleep duration, which has been consistently associated with higher BMI in children.^4–7 Nevertheless, the studies investigating the association between sleep duration and metabolic syndrome risk factors are inconsistent. There are reports suggesting that short sleep duration is positively associated with metabolic risk factors, whereas other papers indicate no significant association.^8–10 For example, although a study found associations only between short sleep duration and type 2 diabetes mellitus risk,¹¹ a number of other studies found a U-shape association, with both short and excessively long sleep associated with impaired glucose tolerance.^12–14 Furthermore, Iglayreger et al.¹⁵ showed that sleep duration inversely predicts cardiometabolic risk in obese adolescents.

Another factor that has been suggested to play a key role in the development of metabolic risk factors is time spent with media. For instance, Ekelund et al.¹⁶ found that viewing television increases adiposity independent of physical activity. Time spent watching television 1 hour more than usual has been reported to increase the risk of overweight and obesity 1.27 times.¹⁷ Previous studies suggested that television viewing lowers the metabolic rate in children,¹⁸ and high television viewing leads to low fitness and higher blood cholesterol levels,¹⁹ but the data are inconclusive.²⁰

To find a practical solution to the obesity-related metabolic problems, first we have to know the severity of the problem and the risk factors affecting it, including lifestyle factors. Therefore, identifying the major environmental factors that increase the severity of the metabolic status in obese children and adolescents is necessary. However, although sleep duration and media time have been reported to be closely associated with obesity, there are limited studies evaluating the relationship between metabolic syndrome risk factors and sleep duration and media time. Studies in the Turkish population are also rare. Total sleep duration in Turkish children decreases significantly with higher socioeconomic status and age.²¹ The rapid socioeconomic growth of Turkey in recent decades has led to alterations in lifestyle, decreased total sleep duration, and increased prevalence of obesity in children and adolescents. Therefore, the aim of the present study was to analyze the associations between sleep duration, media time, and biochemical markers of insulin resistance (IR) and metabolic syndrome in a cohort of obese children and adolescents.

Methods

We recruited 108 obese children and adolescents with a mean age of 13.04 ± 2.02 (range 10–15) years and a BMI z-score higher than the 90th percentile in their peer group to participate in this study. These subjects were selected from the Konya Training and Research Hospital Pediatrics Endocrine and Nutrition and Dietetic Clinic in Konya, Turkey. Data were collected between February 2014 and March 2015. All the participants gave informed consent to participate in the study. Approval from the Medical Research and Ethics Committee in accordance with the Declaration of Helsinki and written, informed parental assent were obtained before data collection.

Each child's age in years was calculated from birthday to the date of the data collection. Height and weight were used to calculate BMI (kg/m²), which was converted to BMI z-scores.²² The researchers instructed all participants on how to complete the questionnaire. For the younger children, the researchers completed the questionnaires with information elicited earlier from those children. In answering some questions, the researchers used information obtained from the parents. In addition to some demographic questions, such as those about name, sex, and the type of school (junior or senior high school), the questionnaire contained the following two categories of questions: (1) media-related questions about time spent using television, computers, and playstations and (2) questions about sleep duration from the Sleep Heart Health Questionnaire, which was validated by the Sleep Heart Health Study, a multicenter cohort study implemented by the National Heart, Lung, and Blood Institute.¹² From the Sleep Heart Health Questionnaire, questions related to the study, namely bedtime, wakeup time, and sleep duration during the weekend and during weekdays, were chosen and translated into Turkish. To test the reliability, after adapting the questionnaire, we pretested the instrument on the study population. The Cronbach's α of the adapted questionnaire was 0.85, and the questionnaire was considered reliable. The duration of sleep was determined with the following formula: (5 × time sleeping during weekdays + 2 × time sleeping during weekends) divided by 7.

Tanner staging was used to evaluate puberty development. A testicle volume of ≥4 mL in boys and breast development stage ≥2 in girls were accepted as signs indicating initiation of puberty.^23,24

Laboratory Assessments

All subjects were asked to fast from 10 pm of the evening before study and to avoid caffeine for the preceding 24-hour period. Blood samples were analyzed for concentrations of plasma glucose, serum triglyceride (TG), total cholesterol (TC), HDL-C, alanine aminotransferase (ALT), and aspartate aminotransferase (AST). Glucose was measured by the glucose oxidase technique, and plasma insulin levels were determined by a double-antibody radioimmunoassay using a recombinant human insulin standard with minimum detection level of <2 mmol/L. IR was estimated by the homeostasis model assessment of insulin resistance (HOMA-IR), calculated as fasting plasma insulin (mU/L) × fasting plasma glucose (mmol/L)/22.5. To distinguish normal from impaired insulin sensitivity, HOMA-IR >2.5 and >4.0 were the cutoff levels employed, respectively, for children and adolescents, according to the values provided by a recent national study.²⁵

Serum glucose, TC, TG, HDL-C, AST, and ALT concentrations were determined by standard enzymatic methods using the Hitachi 7060C Automatic Biochemistry Analysis System (Tokyo, Japan). LDL-C was calculated using Friedewald's equation with all concentrations in mg/dL: LDL-C = TC − HDL-C − (TG/5).²⁶

Weight was measured to the nearest 0.1 kg using an electronic scale with subjects wearing minimal clothing. Height without shoes was measured to the nearest 0.1 cm using a wall-mounted stadiometer

Statistical Analyses

Descriptive analyses were performed on the general characteristics of the study population. The Kolmogorov-Smirnov test was used to evaluate whether the distribution of continuous variables was normal. Multiple comparisons were performed by analysis of variance. The independent two-sample t-test or Mann-Whitney U-test was used to compare continuous variables between groups. Continuous variables are presented as mean ± standard deviation. Multiple logistic regression models were used to assess the association between the metabolic risk factors and sleep time and media time. The regression model was adjusted for BMI z-score and pubertal status according to Tanner stage. Odds ratios were calculated based on 95% confidence intervals. P-values <0.05 were considered statistically significant. Pearson correlation coefficients were used to assess the relationship between media time and sleep duration. Analyses were performed using commercial software SPSS 16.0 (SPSS, Chicago, IL).

Results

The mean age of the 108 obese patients (43 boys) in the study was 13.04 ± 2.02 years, and 44.4% were pubertal. Demographic features of the patients and laboratory data are shown in Table 1. The mean BMI z-score was 2.12 ± 0.63. The mean HOMA-IR value was slightly elevated at 4.48 ± 1.26, indicating the presence of IR, with 44% of pubertal subjects and 60% of prepubertal subjects having a HOMA-IR value greater than 4.0 and 2.5, respectively. The mean serum HDL-C level was 39.33 ± 8.33 mg/dL and was below 40 mg/dL in 52% of subjects. The mean TG level was 130.41 ± 60.15 mg/dL and was above 150 mg/dL in 23% of subjects. The mean TC level was 165.45 ± 37.52 mg/dL and was above 130 mg/dL in 83% of subjects. These characteristics did not significantly differ according to sex.

Table 1.

Characteristics of Children and Adolescents

Variable	Mean ± SD	Range
Age	13.04 ± 2.02	10–15
BMI (kg/m²)	30.08 ± 4.63	28–37.5
BMI z-score	2.15 ± 0.60	1.48–2.52
Glucose	87.42 ± 8.96	64–107
Insulin	20.54 ± 12.86	7.52–47.64
HOMA-IR	4.48 ± 1.26	1.15–9.41
TC (mg/dl)	165.45 ± 37.52	123–224
HDL-C (mg/dl)	39.33 ± 8.33	22–57.2
LDL-C (mg/dl)	101.42 ± 31.67	48.5–155.0
TG (mg/dl)	130.41 ± 60.15	97–276

HDL-C, high-density lipoprotein cholesterol; HOMA-IR, homeostasis model assessment of insulin resistance; LDL-C, low-density lipoprotein cholesterol; SD, standard deviation; TC, total cholesterol; TG, triglycerides.

The mean media time, including time spent on television, other media, computers, and playstations, in obese children was 3.06 ± 1.90 hours/day. Children who spent >5 hours/day using media had significantly (p < 0.05) higher AST and ALT levels as well as higher HOMA-IR, glucose, and TG levels.

İn the 10–13 year-old age group, HOMA-IR and fasting insulin were more or less as stated (highest in those sleeping <9 hours), but TC levels were lowest in children sleeping 9–10 hours, higher in those sleeping >11 hours, and highest in those sleeping <9 hours, while HDL-C was highest in those sleeping 9–10 hours and essentially equivalent in those sleeping <9 or >11 hours. On the other hand, in the 14–15 year-old group, HOMA-IR values were highest in those sleeping <8 hours, while HDL-C was lower in those sleeping 8–9 hours than those sleeping >10 hours.

We proceeded to investigate whether differences in sleep time and media time among these obese children were associated with metabolic risk factors (TG, TC, HDL-C, LDL-C, and HOMA-IR) independent of BMI z-score. We performed multiple regression analysis with each outcome as the dependent variable, and BMI z-score, pubertal status, sleep time, and media time as independent variables. Media time independent of BMI z-score explained 8% of the variance in HOMA-IR (r² = 0.11, p = 0.03) and 11% of variance in TG (r² = 0.151, p = 0.01). Also independent of BMI z-score, sleep time explained 13% of the variance in TC (r² = 0.198, p = 0.001) and 9% of the variance in HOMA-IR (r² = 0.12, p = 0.024) but none of the variance in the other dependent variables. Correlation analysis showed a significant negative relationship between sleep time and media time (r = −0.471, p = 0.000).

Discussion

Regarding obesity-related problems in children, IR is an important risk factor for metabolic issues including type 2 diabetes and dyslipidemia.²⁷ Furthermore, in this study, as an indicator of IR, the homeostatic indicator HOMA-IR was analyzed.²⁸ We noted a U-shape association between sleep duration and metabolic risk factors, with increased HOMA-IR and AST and decreased HDL-C at both higher and lower sleep durations. This study found middle sleep groups (9–10 hours for those 10–13 years old, 8–9 hours for those 14–15 years old) having the best levels of HOMA-IR, HDL-C, and AST. Our findings concur with recent studies suggesting that sleep duration might be associated with risk of IR in adolescents.^29,30 Iglayreger et al.¹⁵ reported that metabolic syndrome score was inversely correlated with total sleep time and sleep session length but not physical activity in adolescents. However, in another study, lower TG levels were predicted by shorter sleep duration according to self-report and actigraphy, and shorter parent-reported sleep duration was associated with higher HDL-C.³¹ Another unexpected report showed that the risk of metabolic syndrome increased with long sleep duration.³² Some studies showed only association between short sleep and IR,^15,31 while others found U-shape association.^29,30 So, the relation between sleep duration and metabolic syndrome risk factors seems controversial and seems to differ according to the characteristics of the study subjects.

A number of epidemiological studies in children have reported that short sleep generally defined as ≤10 hours/day for school children⁷ and ≤9 hours/day for adolescents predispose to obesity and IR.^7,15 Javaheri et al. have reported U-shape association, with HOMA-IR lowest in those sleeping 7.75 hours/day for adolescents also highest in short (5.0 hours/day) and long (10.5 hours/day) sleepers. Another study found a clear association between inadequate (<6 hours/day) sleep duration and IR in obese children.³³ But we should stress that it is difficult to quantify an optimum sleep duration because of the different intervals that each author used to classify sleep duration. This study suggests 9–10 hours/day sleep time for 10–13 year-old children and 8–9 hours/day for 14–15 year-old children are metabolically adverse in the Turkish population. Our findings were not aligned with National Sleep Foundation (NSF)³⁴ recommendations of sleep duration 9–11 hours for school children and 8–10 hours for teenagers. So it is important to determine an adverse high limit for sleep time in addition to a low limit for different age groups.

Table 2.

Comparison of Metabolic Risk Factors and Media Time^a Adolescent

Hours/day	≤2	3–4	≥5	P
N	48	37	23
HOMA-IR	4.48 ± 2.3	4.03 ± 1.10	5.35 ± 1.90	0.038
Glucose	87.19 ± 8.5	82.80 ± 4.16	90.10 ± 10.24	0.031
Insulin	20.31 ± 11.9	17.94 ± 12.60	26.26 ± 14.30	0.112
TC (mg/dL)	166.51 ± 34.7	166.05 ± 44.40	157.41 ± 4.50	0.621
HDL-C (mg/dL)	39.75 ± 8.5	38.8 ± 7.9	40.6 ± 7.2	0.753
LDL-C (mg/dL)	102.56 ± 31.7	102.21 ± 37.10	94.67 ± 24.30	0.371
TG (mg/dL)	123.90 ± 31.3	132.75 ± 22.90	146.4 ± 17.8	0.041
AST (U/L)	23.12 ± 9.2	27.3 ± 12.5	30.8 ± 13.6	0.036
ALT (U/L)	20.62 ± 10.70	26.63 ± 16.30	40.0 ± 32.0	0.001

108 obese children and adolescents.

The association between long sleep duration and adverse metabolic outcomes may be explained by the following factors: psychiatric diseases like depression and underlying disease processes such as sleep apnea. For example, depressive symptoms were strongly associated with long sleep,³⁵ and depression is associated with increased risk of type 2 diabetes.³⁶ This may partially explain the association between long sleep duration and adverse metabolic outcomes. Furthermore, long sleepers reported difficulty falling asleep and awakening unrefreshed compared to normal sleepers.³⁷ Thus, long sleep duration may be related to poor sleep quality, and poor sleep quality was found to be associated with IR.³⁸

It is suggested that short sleep duration increases body weight and changes glucose metabolism.³⁹ In experimental studies, inadequate sleep duration significantly affects the main components of energy homeostasis, including glucose tolerance, food craving, and hormones critical to appetite regulation.⁴⁰ For instance, Taheri et al.⁴¹ and Spiegel et al.⁴² reported that sleep restriction is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Also, insufficient sleep is a proinflammatory condition; experimental sleep restriction increases levels of inflammatory cytokines and inflammation is a part of IR.⁴³

We noted a significant relationship between media time and plasma glucose and TG levels. Time spent watching television 1 hour more than usual has been reported to increase the risk of overweight and obesity 1.27 times.¹⁹ Other researchers have found television viewing to be associated with obesity and some metabolic risk factors^44,45 and suggested that television viewing may be an indicator of sedentary behavior. There are several mechanisms to explain the relationship between television viewing and obesity, including reduced time available for physical activity,⁴⁶ reduced resting metabolic rate,⁴⁷ and increased energy intake.^48,49 In agreement with previous research, the present study indicates that increased media time is associated with decreased sleep duration.

The prevalence of nonalcoholic fatty liver disease (NAFLD) is unclear and depends on the detection method. Between 10% and 25% of obese children have elevated transaminase levels, primarily ALT; as the degree of obesity increases, so does the prevalence of elevated ALT levels.⁵⁰ In this study, liver enzymes were affected by media time and sleep time. ALT and AST levels were significantly lower in obese children who sleep 8–9 hours/day compared with the other groups. A better understanding of the mechanisms responsible for the pathogenesis and pathophysiology of NAFLD will potentially identify novel biomarkers for metabolic risk.

Our study is subject to several limitations. First, sleep duration was measured using questionnaires rather than objective actigraphy. However, in previous studies, self-reported sleep duration assessments were well correlated with values obtained through actigraphic monitoring.⁵¹ Television viewing was also self-reported, and it is difficult to assess the validity of these self-reports. Another limitation is the lack of an assessment of the potential impact of sleep-disordered breathing/obstructive sleep apnea on the parameters measured.

Table 3.

Comparison of Metabolic Risk Factors and Sleeping Time of 108 Obese Children and Adolescents

Aged 10–13
Hours/day	<9	9–10	≥11	P
N	34	19	15
HOMA-IR	4.72 ± 2.80	3.14 ± 1.30	3.42 ± 2.50	0.019
Glucose	90.21 ± 8.20	88.54 ± 7.60	89.24 ± 7.90	0.170
Insulin	24.52 ± 8.50	19.38 ± 12.00	17.48 ± 8.90	0.031
TC (mg/dL)	184.2 ± 21.0	148.24 ± 31.20	161.54 ± 26.50	0.001
HDL-C (mg/dL)	36.41 ± 4.60	42.72 ± 5.80	35.46 ± 5.90	0.001
LDL-C (mg/dL)	112.0 ± 20.0	93.7 ± 36.2	98.92 ± 22.00	0.092
TG (mg/dL)	164.6 ± 79.1	140.33 ± 70.80	120.86 ± 51.80	0.166
AST (U/L)	34.8 ± 16.4	29.0 ± 6.7	31.55 ± 9.40	0.541
ALT (U/L)	44.6 ± 28.8	38.85 ± 7.60	39.11 ± 12.80	0.321

Aged 14–15
Hours/day	<8	8–9	≥10	P
N	11	17	10
HOMA-IR	6.60 ± 3.07	3.47 ± 1.20	4.48 ± 2.20	0.021
Glucose	89.24 ± 9.10	85.31 ± 6.90	90.11 ± 12.30	0.101
Insulin	25.21 ± 11.80	21.82 ± 12.70	22.35 ± 8.50	0.055
TC (mg/dL)	163.45 ± 24.70	144.0 ± 65.7	134.21 ± 65.30	0.143
HDL-C (mg/dL)	35.0 ± 2.2	43.75 ± 8.30	30.66 ± 7.40	0.001
LDL-C (mg/dL)	99.51 ± 49.80	108.25 ± 60.70	76.02 ± 51.30	0.173
TG (mg/dL)	135.0 ± 29.6	111.0 ± 13.3	134.33 ± 72.70	0.413
AST (U/L)	23.5 ± 1.6	17.50 ± 2.2b	31.66 ± 8.60	0.000
ALT (U/L)	19.52 ± 8.20	17.25 ± 3.50	35.0 ± 26.6	0.050

Despite these limitations, we investigated the relationships between sleep associated with duration, media time, and metabolic risk factors associated with obesity in children and adolescents. Our findings demonstrate an association between inadequate sleep duration and IR in obese children and adolescents independent of BMI and physical activity. The results of this study indicate that both short and long sleep durations are associated with a low HDL-C level among our subjects. IR and TG levels were associated with media time. We demonstrated a negative correlation between media time and sleep time in obese children and adolescents. Additional research is needed to evaluate the relationship between the etiology of short sleep and long sleep (e.g., insomnia and psychiatric comorbidities) and metabolic risk factors.

Footnotes

Author Disclosure Statement

The authors declare no conflict of interest or competing financial interests.

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