Abstract
Objective/Background
Rates of overweight/obesity and insufficient/delayed sleep are high among adolescents and are also unique risk factors for mood/behavior difficulties. This study aimed to evaluate relationships between sleep/circadian health and mood/behavior in a cohort of adolescents with overweight/obesity.
Participants
Twenty-two adolescents (16.4±1.1 years) with overweight/obesity attending high school completed in the study.
Methods
Participants completed one week of home sleep monitoring (actigraphy), questionnaires assessing chronotype (diurnal preference; Morningness/Eveningness Scale for Children) and mood/behavior (Strengths & Difficulties Questionnaire), and had in-laboratory salivary melatonin sampling on a Thursday or Friday during the academic year.
Results
Linear regressions revealed later weekday bedtime and shorter weekday time in bed and sleep duration were associated with worse mood/behavior scores. Shorter duration of melatonin secretion and greater “eveningness” were also associated with worse mood/behavior scores.
Conclusions
Short and late sleep, shorter melatonin secretion, and eveningness chronotype are associated with worse mood/behavior symptoms in a cohort of adolescents with overweight/obesity. Clinicians should assess for both sleep and mood/behavior symptoms and further research is needed to evaluate the impact of improved sleep on mood/behavior in adolescents with overweight/obesity.
Keywords: chronotype, adolescents, obesity, mood, behavior
Typical duration of nighttime sleep declines in adolescence compared to childhood and teens are more likely to endorse a late chronotype (eveningness preference). The combination of a delay in circadian rhythms, coupled with environmental and psychosocial factors such as early school start times results in high rates of insufficient sleep in adolescence (Crowley, Wolfson, Tarokh, & Carskadon, 2018). Over 70% of high school students nationwide in the U.S. report getting insufficient sleep compared to the recommended 8–10 hours for this age group (Paruthi et al., 2016; Wheaton, Jones, Cooper, & Croft, 2018).
Additionally, overweight/obesity is prevalent in adolescents, occurring in over 1/3 of U.S. teens (Skinner, Ravanbakht, Skelton, Perrin, & Armstrong, 2018). Obesity-related comorbidities, such as type 2 diabetes (T2D), are also increasing in this age-group (Suglia et al., 2018). A bidirectional relationship between sleep and overweight/obesity has been reported, with insufficient and delayed sleep a risk factor for overweight/obesity in children and adolescents (Miller, Kruisbrink, Wallace, Ji, & Cappuccio, 2018). Conversely, teens with overweight/obesity have greater risk of sleep-disordered breathing and have been found to have later sleep onset time and shorter sleep duration compared to controls without overweight/obesity (Beebe et al., 2007).
Both poor sleep and weight status have been independently associated with mood and behavior problems. Adolescents with overweight/obesity are at increased risk for psychosocial difficulties, including poor self-concept and reduced quality of life (QOL) (Loth, Mond, Wall, & Neumark-Sztainer, 2011; Swallen, Reither, Haas, & Meier, 2005). Twelve to 14-year-olds from the nationally representative National Longitudinal Study of Adolescent Health reported a significant negative impact of obesity on depressive symptoms, self-esteem, and school/social functioning (Swallen et al., 2005). Participants in a multidisciplinary community-based weight management program in New Zealand reported mood/behavior difficulties at six times the rate compared to reported norms (Anderson et al., 2017). Finally, larger reductions in BMI following participation in a weight treatment program were associated with greater improvements in QOL, mood, and body satisfaction for one sample of youth (Fonvig et al., 2017).
Youth with mood disorders are less likely to meet recommendations for sleep duration (Suglia et al., 2018). Anxiety and depressive symptoms have been associated with sleep disturbance, insufficient school night sleep, and greater variability between weekday and weekend sleep duration (Wolfson & Carskadon, 1998). Greater sleep duration was also associated with higher positive affect the next day as assessed by ecological momentary assessment for youth ages 8–16 years diagnosed with anxiety or depression (Cousins et al., 2011).
Experimental studies demonstrate a causal relationship between insufficient sleep and mood symptoms in healthy adolescents. One night of 6.5 hours sleep opportunity, or time in bed (TIB), at home followed by one night of 2 hours TIB in-lab reduced adolescent-report ratings of positive affect and increased susceptibility to negative mood following worry and catastrophizing tasks (Dagys et al., 2012). Adolescents randomized to a single night of sleep restriction of 4 hours TIB reported greater reactivity to negative images and an association between sleep duration and anxiety and negative affect compared to teens randomized to one night of “idealized sleep” (9.5 hours/night) (Reddy, Palmer, Jackson, Farris, & Alfano, 2017). In a study more closely simulating typical levels of sleep restriction experienced by adolescents during the school year, researchers found that adolescents self-reported significantly more mood/behavior symptoms following one week of restricted sleep (6.5 hours TIB) compared to a week of longer sleep duration (10 hours TIB) (Baum et al., 2014). In healthy adolescents, later dim light melatonin onset (DLMO) was associated with greater negative affect in the evening (Dolsen & Harvey, 2018) and youth endorsing an eveningness preference reported the lowest mood levels during the school day compared to other chronotypes, independent of sleep time (Diaz-Morales, Escribano, & Jankowski, 2015).
There are several proposed mechanisms for the relationship between sleep, circadian disruption, and mood. One hypothesis is that insufficient sleep impacts emotion generation (increased negative emotions and reduced positive emotions) and regulation, impacting the ability to identify problematic emotions, and to choose and utilize appropriate emotion regulation strategies (Palmer & Alfano, 2017). In addition, circadian rhythms regulate not only sleep, but also systems related to mood disorders, including activity and hormone secretion (McClung, 2013). It has been posited that circadian disruptions within monoamine signaling, the HPA axis, and the suprachiasmatic nucleus may result in circadian desynchronization and subsequent mood problems (McClung, 2013; Vadnie & McClung, 2017). Moreover, pharmacotherapies such as selective serotonin reuptake inhibitors may synchronize endogenous rhythms thus improving symptoms in those with mood disorders (Vadnie & McClung, 2017). Mood disorders are a common comorbidity in patients with cardiometabolic disorders, and the circadian disruption of metabolic peptides in the liver, stomach, and adipose tissue may be associated with mood difficulties particularly in individuals with overweight/obesity (Lanfumey, Mongeau, & Hamon, 2013; McClung, 2013).
To date, no research has specifically examined the relationship between sleep and circadian health and mood/behavior in adolescents with overweight/obesity. Adolescence is a critical physiological and psychological period, characterized by physiological changes, as well as behavioral changes in diet, physical activity, sedentary behavior, and emotional health (Alberga, Sigal, Goldfield, Prud’homme, & Kenny, 2012). Many of these factors are worsened or accentuated when overweight/obesity is present. These factors, combined with the habitual short and delayed sleep of adolescence may place youth with overweight/obesity at particular risk for mood and behavior difficulties.
Mood and anxiety disorders are recognized as increasing the risk for cardiometabolic morbidity and mortality by the American Heart Association (Goldstein et al., 2015; Suglia et al., 2018). In addition, greater depressive symptoms are associated with increased attrition and lower weight loss success from weight management interventions (Fabricatore et al., 2009). Thus, mood is a salient target for health intervention and prevention efforts in adolescents with overweight/obesity, and identifying factors that may be associated with mood is of particular urgency for youth with overweight/obesity. The goal of the current study was to examine the relationship between sleep duration, sleep and circadian rhythm (melatonin), and chronotype with mood and behavior symptoms in a sample of adolescents with overweight/obesity. We hypothesized that those with shorter sleep duration, later sleep timing, later and shorter melatonin timing, and an eveningness chronotype would have greater endorsement of mood and behavior symptoms.
Methods
Participants and Procedures
The reported cohort was taken from a study examining insulin sensitivity in adolescents with overweight/obesity ((Simon et al., 2019); NCT02585830). Participants were recruited from adolescent medicine and weight-management specialty clinics at Children’s Hospital Colorado between March 2016 and May 2017. High school students ages 14–19 years with BMI ≥90th percentile for age and sex and with habitual sedentary behavior (<3 hours of physical activity per week) were eligible for participation. Exclusion criteria included diabetes (HbA1c ≥6.5%), sleep disorder diagnosis per chart review (e.g., obstructive sleep apnea, circadian rhythm sleep disorder), and medications impacting sleep (e.g., stimulants or regular use of melatonin or other sleep aids). A research assistant approached potentially eligible patients during their clinic appointments to describe the study. If interested, a brief screening was conducted to determine eligibility, and if eligible, they were scheduled for an outpatient study visit. A total of 75 patients were approached. Primary reasons for declining participation included not wanting to drive the distance to the hospital, being too busy, or agreeing to participate but not arriving for the study appointment. All procedures were approved by the University of Colorado Scientific Advisory Review Board and the Colorado Multiple Institutional Review Board and all youth and their parents provided informed assent and/or consent prior to participation. Participants completed questionnaires at an outpatient study visit. They wore a wrist actigraphy monitor for seven days at home prior to an inpatient overnight hospital stay where salivary melatonin was collected. Overnight study visits took place on Thursdays or Fridays and all study participation took place during the academic year, avoiding school holidays and daylights saving changes.
Measures
Objective sleep monitoring.
Participants wore a Spectrum Plus actigraphy monitor (Phillips Respironics, Bend, OR), a watch-like device that estimates sleep duration, timing, and quality, on their non-dominant wrist for 7 days at home. Concurrent with watch-wear, participants completed a sleep log documenting bedtimes and waketimes to facilitate accurate scoring of sleep/wake episodes (Ancoli-Israel et al., 2015). Total sleep time (TST), time in bed (TIB), sleep onset latency (SOL), minutes of wake after sleep onset (WASO), and sleep efficiency (SE) were calculated for weekdays (Sunday-Thursday nights) and weekend days (Friday and Saturday nights) using Actiware Sleep v6 software and standard scoring rules and a medium sensitivity (Phillips Respironics, Pittsburgh, PA) (Ancoli-Israel et al., 2015).
Melatonin.
Saliva was collected every 60 minutes from 5pm to 12pm the following day, with additional samples every 30 minutes around actigraphy-estimated habitual bed and wake times, in dim light conditions (<5 lux; EasyView Light Meter, Extech Instruments, Boston, MA). Participants were asked to sit or lay in bed and to refrain from eating or drinking for at least 15 minutes prior to sampling. Samples were analyzed with radioimmunoassay (Buhlmann Laboratories AG, Schonenbuch, Switzerland) at the Sleep and Chronobiology Laboratory at the University of Colorado Boulder. Using linear interpolation between samples, a threshold of 3pg/mL was used to determine melatonin onset (DLMOn) and offset (DLMOff) (Crowley, 2013). Duration of melatonin secretion was calculated as the minutes between DLMOn and DLMOff. Phase angles of entrainment, a quantification of the temporal alignment between actual sleep behaviors and internal circadian clock, were computed as the interval between each circadian marker (DLMOn and DLMOff) and actigraphic estimates of sleep (bedtime and wake time) (Crowley, 2013).
Chronotype.
The Morningness/Eveningness Scale for Children (MESC) (Carskadon, Vieira, & Acebo, 1993) was completed by participants to determine chronotype (diurnal preference). The MESC consists of 10 multiple-choice items and asks youth to select their preferred timing of activities (e.g., bedtime, exams). Scores range from 10–42 with lower scores indicating least morning preference and higher scores indicating most morning preference.
Mood and behavior symptoms.
The Strengths & Difficulties Questionnaire (SDQ) (Goodman, 1997; Goodman, Meltzer, & Bailey, 1998), an adolescent self-report tool assessing symptoms of mood and behavior problems over the past 6-months, was completed by participants. The SDQ includes 25 items and derives subscale scores for Conduct Problems, Hyperactivity/Inattention, Emotional Symptoms, Peer Problems, and Pro-Social Behavior, as well as a Total Difficulties Score. Scores range from 0–40, with scores 0–15 considered in the normal range, 16–19 borderline, and 20–40 abnormal (Goodman et al., 1998). The SDQ demonstrates adequate internal consistency (Cronbach’s alpha = 0.82) and has been shown to discriminate between clinical and community samples (Goodman et al., 1998).
Sleep Disorders Symptoms.
The Sleep Disturbance Scale for Children (SDSC) (Bruni et al., 1996) is a 27-item questionnaire designed to assess symptoms of common sleep disorders over the past 6 months, and the Sleep Breathing Disorders subscale was used for the current study. Scores > 70 indicate clinically significant symptoms. The SDSC has demonstrated adequate internal consistency in both clinical and non-clinical populations (Cronbach’s alpha = 0.71–0.79) (Bruni et al., 1996).
Analyses
Descriptive statistics are reported using mean and standard deviation. Sex, BMI, and the Sleep Breathing Disorders subscale of the SDSC were examined as possible covariates and controlled for if significant in subsequent analyses. Pearson correlations were examined between BMI percentile and the Sleep Breathing Disorders subscale with sleep/circadian and mood variables. Independent-samples t-tests examined sex differences between sleep/circadian and mood variables. Linear regression analyses were conducted to examine the association between sleep/circadian variables with mood/behavior symptoms. SPSS Statistics 24 software was utilized for analyses.
Results
Participant Characteristics
Twenty-six participants met inclusion and exclusion criteria and were enrolled in the study. Two participants were lost to follow up and did not complete any study measures after signing consent. An additional two participants were excluded due to missing actigraphy and/or questionnaire data. Demographic characteristics and sleep and mood questionnaire scores are presented in Table 1. Participants were predominantly Hispanic, consistent with the demographic make-up of our clinics. Mood questionnaires revealed self-reported mood and behavior ratings on average in the normal range across the sample. Specifically, average SDQ Total score was 10.5 (SD = 4.0), which is similar to a community sample (Goodman et al., 1998). Only 3 participants had scores in the borderline range; no participants scored in the abnormal range. Actigraphy and melatonin data are presented in Table 2. The majority of adolescents obtained <8h sleep on weekends (62.3% of participants) and weeknights (84.0% of participants). Participants on average obtained over 1.5 h more sleep on weekends compared to weekdays, primarily attributable to later waketime on weekends. No sex differences were found for any sleep/circadian or mood variables, with the exception of MESC scores. Specifically, males had significantly higher MESC scores than females (males = 28.9, females = 25.4, p = .009), indicating a greater morningness preference for males. BMI percentile was not significantly associated with any sleep/circadian or mood variables. Participants with higher Sleep Breathing Disorders subscale scores had significantly shorter weekday TST (r = −0.44, p = .048), later weekend wake time (r = 0.46, p = .035), and later DLMOn (r = 0.44, p = .045).
Table 1.
Participant Characteristics and Questionnaire Results (mean, SD)
| N = 22 | |
|---|---|
| Demographic Characteristics | |
| Age (years) | 16.4 (1.1) |
| Female Sex N (%) | 14 (63.6) |
| BMI Percentile | 97.0 (2.4) |
| HbA1c % | 5.6 (0.2) |
| Race N (%) | |
| African American | 7 (33.3) |
| Caucasian | 8 (38.1) |
| Multiracial | 6 (28.6) |
| Ethnicity N (%) | |
| Hispanic or Latino | 15 (71.4) |
| Chronotype | |
| MESC | 26.5 (3.1) |
| Mood and Behavior | |
| SDQ | |
| Emotional Symptoms | 2.7 (1.7) |
| Conduct Problems | 2.0 (1.1) |
| Hyperactivity/Inattention | 3.1 (1.7) |
| Peer Problems | 2.6 (1.8) |
| Prosocial Behavior | 7.1 (1.9) |
| Total Difficulties | 10.5 (4.0) |
| Sleep Disorders Symptoms | |
| SDSC | |
| Sleep Breathing Disorders | 53.8 (9.6) |
MESC – Morningness/Eveningness Scale for Children, minimum score = 10 (minimal morning preference) and maximum score = 42 (maximal morning preference); SDQ – Strengths & Difficulties Questionnaire, normal range for Total Difficulties score = 0-15; SDSC – Sleep Disturbance Screening for Children, Sleep Breathing Disorders subscale score >70 indicates clinically significant symptoms
Table 2.
Actigraphy and Melatonin Variables (mean, SD)
| Actigraphy | Weekday | Weekend |
|---|---|---|
| Total Sleep Time (min) | 374.9 (51.6) | 470.7 (73.0) |
| Time in Bed (min) | 449.2 (62.4) | 564.6 (75.1) |
| Onset Latency (min) | 15.5 (10.6) | 15.7 (12.3) |
| Sleep Efficiency (%) | 84.1 (4.6) | 83.6 (7.0) |
| WASO (min) | 48.4 (21.6) | 68.3 (36.7) |
| Bedtime M (range) | 23:06 (21:41, 01:34) | 23:48 (21:04, 02:01) |
| Waketime M (range) | 06:34 (05:01, 08:06) | 09:09 (07:16, 11:50) |
| Melatonin | Weekday | |
| DLMOn (time) | 21:00 (1.5 h) | |
| DLMOff (time) | 08:24 (1.0 h) | |
| PA DLMOn & Bedtime (h) | 1.9 (1.1) | |
| PA DLMOn & Waketime (h) | 9.6 (1.2) | |
| PA Bedtime & DLMOff (h) | −1.9 (1.1) | |
| PA Waketime & DLMOff (h) | −9.6 (1.2) | |
| Duration of melatonin (h) | 11.0 (1.1) | |
WASO - wake after sleep onset; DLMOn – dim light melatonin onset; DLMOff – dim light melatonin offset; PA – phase angle.
Sleep/Circadian Rhythm and Strengths & Difficulties Questionnaire
Actigraphy
Results of regression analyses revealed that SDQ Total Difficulties scores were significantly associated with actigraphy-estimated bedtime, TIB, and TST on weekdays, indicating higher mood and behavior scores with later bedtimes, shorter time in bed, and shorter sleep duration (bedtime: ß = 0.52, p = 0.01; TIB: ß = −0.51, p = 0.02; TST: ß = −0.56, p = 0.008; Figure 1). The Sleep Breathing Disorders subscale score was included as a covariate for the analysis with TST and this analysis remained significant (ß = −0.56, p = 0.019). Analyses between weekend sleep variables were non-significant with mood and behavior scores (p > 0.05).
Figure 1.
Regression analyses between weekday bedtimes, weekday total sleep time, duration of melatonin secretion, and the Morningness Eveningness Scale for Children (MESC) with the Strengths & Difficulties Questionnaire (SDQ) Total Difficulties score. Later weekday bedtime (a), shorter weekday sleep duration (b), shorter duration of melatonin secretion (c), and greater eveningness preference (d) were significantly associated with higher SDQ Total Difficulties scores, indicating more mood/behavior symptoms.
Melatonin
Shorter duration of melatonin secretion was significantly associated with more mood and behavior symptoms (ß = −0.49, p = 0.02; Figure 1). Melatonin onset, offset, and phase angles of entrainment were not significantly associated with mood and behavior symptoms (p > 0.05).
Chronotype
A lower score on the MESC, indicating a greater eveningness preference, was associated with more mood and behavior symptoms from the SDQ Total Difficulties scale (ß = −0.44, p = 0.04; Figure 1). This relationship remained significant after controlling for sex (ß = −0.71, p = 0.007).
Discussion
In this sample of adolescents with overweight/obesity, objectively-measured short sleep duration, later bedtime, shorter duration of melatonin secretion, and eveningness chronotype were associated with greater endorsement of mood and behavior symptoms. These findings confirm our hypotheses and add to the literature demonstrating a significant relationship between sleep and circadian health and mood/behavior in adolescents with overweight/obesity, as has been previously seen in healthy weight adolescents.
Our findings are similar to the extant literature in healthy adolescents, including both cross-sectional studies finding that short sleep duration, eveningness preference, and later dim light melatonin onset were associated with greater negative affect or mood problems (Cousins et al., 2011; Diaz-Morales et al., 2015; Dolsen & Harvey, 2018), and experimental studies reporting that short sleep duration resulted in greater negative mood or mood/behavior symptoms compared to longer sleep duration (Baum et al., 2014; Dagys et al., 2012; Reddy et al., 2017). Of note, with the exception of 2 studies with weight-related exclusionary criteria (Baum et al., 2014; Cousins et al., 2011), these studies either broadly describe participants as “healthy” or do not mention health status but do not report the weight status of participants, making it difficult to make weight-based comparisons between our findings and the extant literature. Thus, future study using a healthy weight control group to examine differences in the relationships between sleep, circadian rhythms, and mood is needed. Nonetheless, preliminary evidence suggests that adolescents with overweight/obesity have similar relationships between sleep, circadian rhythms, and mood as healthy adolescents, but are an important group for further study and intervention given their increased risk for both sleep and mood difficulties.
Our cohort of adolescents with overweight/obesity obtained nearly 2 hours less sleep on weekdays than the recommended minimum 8 hours of sleep per night for this age-group (Paruthi et al., 2016). Short sleep duration on weekdays was associated with more overall mood/behavior problems over the past six months. Of note, adolescent respondents to a survey completed following a 30-minute delay in their high school start time reported a significant improvement in mood and behavior, suggesting that even modest increases in sleep duration may result in improved outcomes (Owens, Belon, & Moss, 2010).
Due to a combination of biological, environmental, and psychosocial influences, adolescents tend to have a later circadian rhythm than other age groups, resulting in a drive to stay up late and sleep in late (Crowley et al., 2018). In our cohort, later weekday bedtimes, shorter duration of melatonin secretion, and an eveningness chronotype were associated with increased mood and behavior symptoms. Similarly, reduced melatonin secretion has been measured in young adults with affective disorders (Naismith et al., 2012). Spanish adolescents with eveningness preference reported worse mood compared to those with a morning chronotype (Diaz-Morales et al., 2015). In contrast to a sample of older adolescents and adults with a diagnosis of a circadian rhythm sleep disorder, delayed sleep-wake phase disorder, where melatonin timing was associated with greater symptoms of depression (Murray et al., 2017), we did not find a significant relationship with melatonin onset or offset in our sample. However, to our knowledge, this study is the first evaluation using objective assessment of circadian rhythm and examining relation to mood/behavior in adolescents with overweight/obesity.
Generalizability of our study is limited by small sample size which limited our ability to examine specific SDQ subscales and power to detect sex differences. Additional limitations include average mood/behavior scores in the normal range, and a lack of a healthy weight control group for comparison. Additionally, mood/behavior was queried over the past 6 months, while our sleep assessment occurred over the past week. Strengths of the study include multiple objective measures of sleep and circadian rhythm, including actigraphy monitoring for multiple nights in the home environment and full-night salivary melatonin sampling in dim light conditions.
Adolescents with overweight/obesity are at risk for both sleep problems and mood/behavior difficulties, and our study demonstrates a link between sleep and circadian health and mood/behavior symptoms. Thus, both sleep and mood/behavior symptoms should be assessed by clinicians working with adolescents with overweight/obesity. Further research is needed with a larger sample to investigate mechanisms behind these relationships and considering other behavioral constructs, and to evaluate the impact of sleep and circadian health interventions on mood/behavior symptoms in this at-risk population.
Acknowledgments:
We would like to thank the participants and their families for taking part in our research and our CTRC nursing staff for their assistance in performing these studies. These data were previously reported at a poster presentation at the 2018 Society of Pediatric Psychology Annual Conference, Orlando, FL.
Funding: This work was supported by the Children’s Hospital Colorado & Colorado School of Mines (awarded to Simon & Diniz-Behn), and the National Institutes of Health National Center for Clinical and Translational Science Awards UL1 TR002535.
Footnotes
Conflicts of Interest: CDB has research funding support from Jazz Pharmaceuticals. KPW has research funding support from Philips Inc., CurAegis Technologies (formerly known as Torvec Inc.) and Somalogics, consulting fees from or served as a paid member of scientific advisory boards for the Sleep Disorders Research Advisory Board - National Heart, Lung and Blood Institute, CurAegis Technologies, Circadian Therapeutics, LTD. and has received speaker/educational consultant honorarium fees from the American Academy of Sleep Medicine, American College of Chest Physicians, American College of Sports Medicine, American Diabetes Association, Associated Professional Sleep Societies, and the Obesity Medicine Association. No conflicts of interest are reported for any other authors.
Data Sharing: Data available on request from the authors
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