Impact of Sleep Duration and Weekend Oversleep on Body Weight and Blood Pressure in Adolescents

Stuart F. Quan, M.D.*^†

Daniel Combs, M.D.^{‡ ¶}

Sairam Parthasarathy, M.D.^{†§ ¶}

*Division of Sleep and Circadian Disorders, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA USA

^†Asthma and Airways Research Center, University of Arizona College of Medicine, Tucson, AZ USA

^‡Department of Pediatrics, University of Arizona College of Medicine, Tucson, AZ USA

^§Department of Medicine, University of Arizona College of Medicine, Tucson, AZ USA

^¶ Center for Sleep and Circadian Sciences, University of Arizona Health Sciences Center, Tucson, AZ USA

Abstract

Introduction: Weekend oversleep or catchup sleep is a frequent occurrence in children, but there are relatively little data concerning its impact on weight and blood pressure. The aim of this study was to assess the association between sleep duration and oversleep, and weight and blood pressure in adolescents. 

Methods: Sleep duration, weight and blood pressure of 327 children (51.4% boys, mean age 13.3 + 1.7 years) who had polysomnograms performed during both exam cycles of the Tucson Children’s Assessment of Sleep Apnea study (TuCASA) were analyzed. Sleep duration on school nights and non-school nights was used to compute a weighted average of child and parent reported overall sleep duration respectively. Oversleep was defined as the difference between self and parent reported weekend sleep and weekday sleep separately. Simple correlations between overall sleep duration, sleep on school and non-school nights and oversleep, and blood pressure, standardized body mass index (BMI), snoring, respiratory disturbance index (RDI) and age were calculated. Significant bivariate associations then were used to develop multivariate partial correlation models.

Results: Unadjusted negative correlations with BMI were noted for parent reported total sleep duration at the 1^st exam cycle, parent and child reported total sleep and school night sleep duration, and parent reported non-school night sleep duration at the 2^nd exam cycle. Additionally, for BMI, positive correlations were observed for log RDI at both exam cycles and snoring at the 2^nd exam cycle. For blood pressure, there were positive associations with age, parent reported oversleep, caffeine consumption and snoring. Additionally, for blood pressure, negative relationships were observed with parent reported total sleep duration at the 1^st exam cycle, and parent and child reported total sleep and school night sleep durations at the 2^nd exam cycle. Partial correlations found that BMI was negatively correlated with parent reported total sleep duration at the 1^st exam cycle and parent reported total sleep duration at the 2^nd exam cycle, and positively correlated with snoring and log RDI at both exam cycles. Systolic blood pressure was only associated with age and snoring. Diastolic blood pressure was positively correlated with age and caffeine consumption, and negatively correlated with parent reported total and school night sleep duration. Oversleep and child reported sleep duration were not represented in any of these models.

Conclusion: Lower amounts of sleep especially on school nights is associated with higher body weight and blood pressure. Oversleep was not associated with either body weight or blood pressure.

Introduction

Insufficient sleep in children is associated an increased likelihood of negative behavioral and physical health consequences (1). In particular, short sleep duration has been linked to weight gain and greater risk of obesity, (2-5) and hypertension (6-9). Sleep disordered breathing (SDB) in children also has been implicated as a factor in elevations in blood pressure (10-13). Therefore, it is unclear whether sleep duration and SDB are independent risk factors for this condition.

Weekend oversleep occurs when sleep on weekends exceeds sleep occurring on weekdays. Recently, it was observed in children that greater amounts oversleep were associated with a reduced likelihood of being overweight (4). It was suggested that oversleep represented a compensatory behavior in children for insufficient sleep during weeknights and that it was protective against the deleterious impact of inadequate sleep. Similarly, in adults, oversleep has been associated with a decreased risk of hypertension (14). However, there have been no previous studies of the relationship between oversleep and blood pressure in children.

The Tucson Children’s Assessment of Sleep Apnea Study (TuCASA) was a longitudinal cohort study to assess the impact of SDB on a variety of physiologic and behavioral endpoints (15). The goal of this analysis was to examine whether sleep duration, SDB and oversleep were associated with weight and blood pressure in adolescent children in a general population cohort as represented by TuCASA.

Methods

Subjects and Study Design: Details of the TuCASA study design have been published previously (15, 16). Briefly, 6-11 year-old Hispanic and Caucasian children from the Tucson Unified School District (TUSD) were recruited to undergo unattended home polysomnography. In addition, demographic and anthropometric information was obtained and a neurocognitive assessment performed. From 1999-2004, 503 children aged 6-11 years completed home polysomnograms (Exam Cycle 1).  Approximately five years later (Exam Cycle 2, mean 4.7 years), 348 children participated in the second phase of the study; 319 children had home visits where acceptable in-home polysomnography was completed a second time.  On both occasions, all of the families completed sleep screening, sleep habits, and morning questionnaires.  At the time of the second phase of the study, a comprehensive dietary and physical activity assessment was performed as well (17). The TuCASA study was approved by the University of Arizona Institutional Review Board (IRB) as well as the TUSD Research Committee.

Data collection: The methods for obtaining data have been previously described (11, 15, 16). In brief, for both exam cycles, a two person team arrived at the home approximately one hour before the child’s normal bedtime.  Prior to performing any study procedures, parents gave informed consent and the child gave assent to the study using language appropriate forms approved by the IRB.  Each child’s height, weight, neck circumference, and blood pressure were measured. One parent was asked to complete a comprehensive Sleep Habits Questionnaire (SHQ) that inquired about their child’s sleep history, sleep characteristics and additional questions regarding parental health including smoking status. For the 2^nd exam cycle, the child was asked to complete a SHQ, and a dietary and physical activity questionnaire as well.

Parent and Child Reported Sleep Durations: The SHQ for both parent and child inquired about hours of sleep on school nights and non-school nights. Overall parent and child sleep durations were estimated by computing a weighted average ([school night sleep x 5] + [non-school night sleep x 2] / 7).

Blood Pressure (BP): After a few minutes of rest while seated, the child’s BP was measured in triplicate from the right arm using a portable mercury sphygmomanometer and standardized techniques. The appropriate BP cuff was selected according to the measured arm size (upper arm circumferences of 6-15 cm, infant cuff, 16-22 cm, child cuff, and 23-30 cm, regular-sized adult cuff). The initial cuff inflation pressure was determined by adding 30 mm Hg to the palpated systolic BP. Cuff deflation was at 2 mm/second. At least 30 seconds elapsed between each of the 3 successive measurements. The mean of the final 2 of 3 BP measurements was used for the analyses in this report. Blood pressure percentiles based on height, age and gender were calculated using data from the Centers for Disease Control (CDC) (18).

Obesity:  Height was obtained using a folding ruler on a level surface after removal of shoes, and the head in the Frankfort plane.  Weight was measured on a platform scale.  A standardized BMI z score was calculated using an equation from the CDC which adjusted for age, sex and ethnicity (http://www.cdc.gov/nccdphp/dnpao/growthcharts/resources/sas.htm). 

Polysomnography:  A single, unattended overnight polysomnogram was obtained using the Compumedics PS-2 system (Abbotsford, Victoria, Australia).  The following signals were acquired as part of the TuCASA montage: C3/A2, C4/A1 electroencephalogram (EEG), right and left electrooculogram, a bipolar submental electromyogram, thoracic and abdominal displacement (inductive plethysmography), airflow (nasal/oral thermistor), nasal pressure cannula, finger pulse oximetry, ECG (single bipolar lead), snoring microphone, body position (Hg gauge sensor), and ambient light (sensor attached to the vest to record on/off).

Scoring of the polysomnograms was performed by a single registered polysomnographic technologist using Rechtschaffen and Kales criteria (19). Apneas were scored if the amplitude (peak to trough) of the airflow signal using the thermistor decreased below at least 25% of the amplitude of baseline breathing (identified during a period of regular breathing with stable oxygen levels), if this change lasted for more than 6 seconds or 2 breath cycles.  Hypopneas were designated if the amplitude of any respiratory signal decreased below (approximately) 70% of the amplitude of baseline and if the thermistor signal did not meet the criterion for apnea.  Central events were marked if no displacement was noted on both the chest and abdominal inductance channels.  However, central events that occurred after movement were not included.  Otherwise, events were scored as obstructive.  After full scoring, analysis software was used to link each event to data from the oxygen saturation and EEG channels.  The Respiratory Disturbance Index (RDI) was defined as the number of respiratory events (apneas and hypopneas) per hour of the total sleep time.  For this analysis, a 3% oxygen desaturation was required for an event to be counted in the total RDI.

Data: AnalysisDescriptive data are presented as mean + standard deviation (SD) or as percentages. The distributions of RDI and mg caffeine consumption were skewed with some children having values of zero. Therefore, RDI at both exam cycles and caffeine consumption were log transformed. To adjust for zero values, a small number (0.01) was added to each value before the log transformation. Analyses of RDI and caffeine consumption were subsequently performed using log transformed values.

To determine the relationships between the physiologic attributes of weight and blood pressure at the 2^nd exam cycle, and variables representing sleep duration, sleep disordered breathing, and caffeine consumption and age, Pearson correlation coefficients were computed. Incorporating only those variables that demonstrated significant bivariate correlations, multivariate models were constructed by calculating partial correlations. Analyses were performed using IBM SPSS Statistics, V24.

Results

There were 327 children (51.4% boys, mean age 13.3+ 1.7 years) who had PSGs performed during both TuCASA exam cycles. In comparison to children who only participated in the 1^st exam cycle, there were no differences with respect to age, standardized BMI, RDI, sleep duration on school nights and non-school nights and 1^st exam cycle systolic blood pressure (data not shown). However, 1^st exam cycle diastolic blood pressure was slightly higher in those who participated in both exam cycles (60.5 + 9.5 vs. 58.4 + 10.3 mmHg, p<0.05).

Analyses of the relationships of household smoking with BMI and blood pressure showed no differences between children living in households with smokers and those with non-smokers. Similarly, there were no associations with physical activity (data not displayed).

Shown in Table 1 are mean values for sleep, anthropometric and blood pressure variables.

Table 1: Mean Values for Sleep, Anthropometric and Blood Pressure Data.*

Of note is that parent reported sleep duration declined from the 1^st (9.6+0.8 hours) to the 2^nd exam cycle (8.9+0.9 hours). Parent reported sleep durations (overall, school night, non-school night and oversleep) were greater than corresponding child reported values.

Unadjusted correlations between standardized BMI and blood pressure, and sleep duration metrics, log RDI, age, caffeine consumption and snoring are provided in Table 2.

Table 2. Unadjusted Correlations with BMI and Blood Pressure.

For standardized BMI, significant negative associations with standardized BMI were present for parent reported total sleep duration at the 1^st exam cycle, parent and child reported total sleep and school night sleep duration, and parent reported non-school night sleep duration at the 2^nd exam cycle. Additionally, for standardized BMI, positive correlations were observed for log RDI at both exam cycles and snoring at the 2^nd exam cycle. For blood pressure, there were positive associations with age, caffeine consumption, oversleep and snoring. Additionally, for blood pressure, negative relationships were observed with parent reported total sleep duration at the 1^st exam cycle, and parent and child reported total sleep and school night sleep durations at the 2^nd exam cycle.

Partial correlations representing multivariate models including only those variables with significant univariate correlations are shown in Table 3.

Table 3. Partial Correlations with BMI and Blood Pressure.

Standardized BMI was negatively correlated with parent reported total sleep duration at the 1^st exam cycle, parent reported total sleep duration at the 2^nd exam cycle, and positively correlated with snoring and log RDI at both exam cycles. Parent reported school night sleep duration exhibited multicollinearity with other sleep duration metrics. Systolic blood pressure was only associated with age and snoring. Diastolic blood pressure was positively correlated with age and weakly positively correlated with caffeine consumption. It also was weakly negatively correlated with parent reported total and school night sleep duration. Analyses using blood pressure expressed as gender, age and height-adjusted percentiles yielded similar findings (data not shown). Oversleep was not represented in any of these models.

Discussion

The major findings from this analysis were that sleep duration was inversely associated with BMI and to a lesser extent with blood pressure. However, there was no association between oversleep and BMI or blood pressure. Thus, overall sleep duration, but not oversleep, is an important behavioral factor affecting body weight and blood pressure in children.

We observed that parent reported sleep duration overall was inversely correlated with BMI. Our findings are consistent with previous studies that have also found that less sleep in children is associated with greater body weight (2, 3, 5). However, our observation that there was collinearity with parent reported school night sleep duration emphasizes the importance of obtaining adequate sleep during the week. Several mechanisms have been proposed to explain why reduced sleep results in greater body weight. These include alterations in the hormonal processes that regulate carbohydrate metabolism and increase the desire to consume caloric dense foods, and greater available time to eat (20). In a previous analysis of food intake in the TuCASA study, we did not find a relationship between dietary composition and body weight (17). Thus, it is unclear what underlying mechanism explains our finding.

Not surprisingly, age was the primary determinant of blood pressure in our analysis. This is consistent with the normal maturation in children’s blood pressure. However, there was a weak negative correlation between parent reported total and school night sleep durations and diastolic blood pressure. These findings are consistent with previous observations linking reduced sleep duration to higher blood pressure and hypertension in children (7-9). Proposed mechanisms for this relationship include heightened sympathetic nervous system activity and greater exposure to higher daytime blood pressures (6).

A weak association was also noted between diastolic blood pressure and caffeine consumption. In one study in adolescents, a dose response in diastolic but not systolic blood pressure was observed after acute administration of caffeine (21). However, this specificity has not always been found (22). Whether caffeine consumption is a significant risk factor in development of childhood hypertension is unclear. Although a recent large analysis of the NHANES cohort found that the prevalence of elevated blood pressure in children has declined in recent years, a corresponding reduction in caffeine consumption was not statistically significant (23).

In contrast to the inverse associations between parent reported sleep duration and BMI and blood pressure, no relationships were observed between these endpoints and oversleep. Thus, our findings differ from those of Kim et al who found that oversleep exerted a protective effect on weight in children (4). The explanation for this discordance is unclear, but racial and ethnic differences may have been a factor. Our cohort was comprised of Hispanic and Caucasian children and there were systematic differences in bedtime and sleep duration between Hispanics and Caucasian children. Specifically, parent-reported sleep duration during weekdays was shorter in Hispanic than in Caucasian children which appeared to be attributable to a later bedtime in the Hispanic children (24). The children in the afore-mentioned Kim et al study were Korean and the protective effect of oversleep on weight may be attributable to racial, socio-cultural, or dietary differences.

We found that sleep disordered breathing as represented by the RDI and snoring also impacted BMI and blood pressure. This is consistent with our previous findings (11), and others related to SDB and blood pressure in children (10, 12, 13).

In contrast to the associations between parent reported sleep duration and BMI and blood pressure, multivariate analyses failed to confirm any associations between child reported sleep duration and these outcomes. In addition, parent reported sleep times were greater than those reported by their children. Children as young as 8 years can provide meaningful health information when developmentally appropriate instruments are utilized (25). With respect to sleep, the report of the child may be quite different from a parent’s perception (26). Furthermore, both could differ from objective assessment. In the current study, univariate analyses indicated that both child and parent report of sleep duration were associated with BMI and blood pressure. However, only parent report was significant on multivariate analyses. It is possible that greater variability in the child reports was in part responsible for the failure to detect any significant associations. Regardless, it appears that parent reported sleep time represents a better signal than child report for any associations with body weight or blood pressure.

Major limitations to this analysis include a relatively small number of children in comparison to other cohorts and reliance on parent and children reporting of sleep durations. Although polysomnography was performed as part of TuCASA, there was no consistency as to whether they were performed on school or non-school nights. Furthermore, because only a single night of study was recorded, calculation of oversleep would not have been possible. Despite these limitations, TuCASA has several strengths including standardized data collection from a general population cohort and objective documentation of the presence of sleep disordered breathing.     

In conclusion, reductions in sleep duration are associated with higher body weight and blood pressure. Reductions in school night sleep are particularly important. However, oversleep does not appear to have an impact on either body weight or blood pressure. 

Acknowledgments

This work was supported by grant HL 62373 from the National Heart Lung and Blood Institute.

References

1. Paruthi S, Brooks LJ, D'Ambrosio C, et al. Consensus Statement of the American Academy of Sleep Medicine on the Recommended Amount of Sleep for Healthy Children: Methodology and Discussion. J Clin Sleep Med. 2016;12(11):1549-61. [CrossRef] [PubMed]
2. Li L, Zhang S, Huang Y, Chen K. Sleep duration and obesity in children: A systematic review and meta-analysis of prospective cohort studies. J Paediatr Child Health. 2017;53(4):378-85. [CrossRef] [PubMed]
3. Ruan H, Xun P, Cai W, He K, Tang Q. Habitual Sleep Duration and Risk of Childhood Obesity: Systematic Review and Dose-response Meta-analysis of Prospective Cohort Studies. Sci Rep. 2015;516160. [CrossRef][PubMed]
4. Kim CW, Choi MK, Im HJ, et al. Weekend catch-up sleep is associated with decreased risk of being overweight among fifth-grade students with short sleep duration. J Sleep Res. 2012;21(5):546-51. [CrossRef] [PubMed]
5. Fatima Y, Doi SA, Mamun AA. Longitudinal impact of sleep on overweight and obesity in children and adolescents: a systematic review and bias-adjusted meta-analysis. Obes Rev. 2015;16(2):137-49. [CrossRef] [PubMed]
6. Dean E, Bloom A, Cirillo M, et al. Association between habitual sleep duration and blood pressure and clinical implications: a systematic review. Blood Press. 2012;21(1):45-57. [CrossRef] [PubMed]
7. Guo X, Zheng L, Li Y, et al. Association between sleep duration and hypertension among Chinese children and adolescents. Clin Cardiol. 2011;34(12):774-81. [CrossRef] [PubMed]
8. Javaheri S, Storfer-Isser A, Rosen CL, Redline S. Sleep quality and elevated blood pressure in adolescents. Circulation. 2008;118(10):1034-40. [CrossRef] [PubMed]
9. Kuciene R, Dulskiene V. Associations of short sleep duration with prehypertension and hypertension among Lithuanian children and adolescents: a cross-sectional study. BMC Public Health. 2014;14255-2458-14-255. [CrossRef] [PubMed]
10. Bixler EO, Vgontzas AN, Lin HM, et al. Blood pressure associated with sleep-disordered breathing in a population sample of children. Hypertension. 2008;52(5):841-6. [CrossRef] [PubMed]
11. Enright PL, Goodwin JL, Sherrill DL, Quan JR, Quan SF, Tucson Children's Assessment of Sleep Apnea study. Blood pressure elevation associated with sleep-related breathing disorder in a community sample of white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea study. Arch Pediatr Adolesc Med. 2003;157(9):901-4. [CrossRef] [PubMed]
12. Kwok KL, Ng DK, Chan CH. Cardiovascular changes in children with snoring and obstructive sleep apnoea. Ann Acad Med Singapore. 2008;37(8):715-21. [PubMed]
13. Nisbet LC, Yiallourou SR, Walter LM, Horne RS. Blood pressure regulation, autonomic control and sleep disordered breathing in children. Sleep Med Rev. 2014;18(2):179-89. [CrossRef] [PubMed]
14. Hwangbo Y, Kim WJ, Chu MK, Yun CH, Yang KI. Association between weekend catch-up sleep duration and hypertension in Korean adults. Sleep Med. 2013;14(6):549-54. [CrossRef] [PubMed]
15. Goodwin JL, Enright PL, Kaemingk KL, et al. Feasibility of using unattended polysomnography in children for research--report of the Tucson Children's Assessment of Sleep Apnea study (TuCASA). Sleep. 2001;24(8):937-44. [PubMed]
16. Goodwin JL, Kaemingk KL, Mulvaney SA, Morgan WJ, Quan SF. Clinical screening of school children for polysomnography to detect sleep-disordered breathing--the Tucson Children's Assessment of Sleep Apnea study (TuCASA). J Clin Sleep Med. 2005;1(3):247-54. [PubMed]
17. Drescher AA, Goodwin JL, Silva GE, Quan SF. Caffeine and screen time in adolescence: associations with short sleep and obesity. J Clin Sleep Med. 2011;7(4):337-42. [CrossRef] [PubMed]
18. National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis,  evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics. 2004;114(2 Suppl 4th Report):555-76. [PubMed]
19. Rechtschaffen A, Kales A. A Manual of Standardized Terminology,
    Techniques and Scoring System for Sleep Stages of Human Subject. Washington, D.C.: US Government Printing Office, National Institute of Health Publication, 1968.
20. Ash T, Taveras EM. Associations of short sleep duration with childhood obesity and weight gain: summary of a presentation to the National Academy of Science's Roundtable on Obesity Solutions. Sleep Health. 2017;3(5):389-92. [CrossRef] [PubMed]
21. Temple JL, Dewey AM, Briatico LN. Effects of acute caffeine administration on adolescents. Exp Clin Psychopharmacol. 2010;18(6):510-20. [CrossRef] [PubMed]
22. Temple JL, Ziegler AM, Graczyk A, Bendlin A, Sion T, Vattana K. Cardiovascular responses to caffeine by gender and pubertal stage. Pediatrics. 2014;134(1):e112-9. [CrossRef] [PubMed]
23. Xi B, Zhang T, Zhang M, et al. Trends in Elevated Blood Pressure Among US Children and Adolescents: 1999-2012. Am J Hypertens. 2016;29(2):217-25. [CrossRef] [PubMed]
24. Combs D, Goodwin JL, Quan SF, Morgan WJ, Parthasarathy S. Longitudinal differences in sleep duration in Hispanic and Caucasian children. Sleep Med. 2016;1861-6. [CrossRef] [PubMed]
25. Riley AW. Evidence that school-age children can self-report on their health. Ambul Pediatr. 2004;4(4 Suppl):371-376. [CrossRef] [PubMed]
26. Owens JA, Spirito A, McGuinn M, Nobile C. Sleep habits and sleep disturbance in elementary school-aged children. J Dev Behav Pediatr. 2000;21(1):27-36. [PubMed]

Cite as: Quan SF, Combs D, Parthasarathy S. Impact of sleep duration and weekend oversleep on body weight and blood pressure in adolescents. Southwest J Pulm Crit Care. 2018;16(1):31-41. doi: https://doi.org/10.13175/swjpcc150-17 PDF 

Incidence and Remission of Parasomnias among Adolescent Children in the Tucson Children’s Assessment of Sleep Apnea (TuCASA) Study

Oscar Furet, RN M.P.H.

Arizona Arthritis Center, University of Arizona, Tucson, AZ

oscarf@arthritis.arizona.edu

James L. Goodwin, Ph.D.

Arizona Respiratory Center, University of Arizona, Tucson, AZ

jgoodwin@email.arizona.edu

Stuart F. Quan, M.D.

Arizona Respiratory Center, University of Arizona, Tucson, AZ. Division of Sleep Medicine, Brigham and Womens Hospital and Harvard Medical School, Boston, MA

Correspondent:             Stuart F. Quan, M.D.

                                    Division of Sleep Medicine

                                    Harvard Medical School

                                    401 Park Dr., 2^nd Floor East

                                    Boston, MA 02215

                                    Email: squan@arc.arizona.edu

                                    Voice: 617-998-8842

                                    Fax:    617-998-8823

Reference as: Furet O, Goodwin JL, Quan SF. Incidence and remission of parasomnias among adolescent children in the Tucson Children’s Assessment of Sleep Apnea (TuCASA) Study. Southwest J Pulm Crit Care 2011;2:93-101. (Click here for PDF version)

Abstract

Background: Longitudinal assessments of parasomnias in the adolescent population are scarce. This analysis aims to identify the incidence and remission of parasomnias in the adolescent age group.

Methods: The TuCASA study is a prospective cohort study that initially enrolled children between the ages of 6 and 11 years (Time 1) and subsequently re-studied them approximately 5 years later (Time 2). At both time points parents were asked to complete a comprehensive sleep habits questionnaire designed to assess the severity of sleep-related symptoms that included questions about enuresis (EN), sleep terrors (TR), sleep walking (SW) and sleep talking (ST).

Results: There were 350 children participating at Time 1 who were studied as adolescents at time 2. The mean interval between measurements was (4.6 years). The incidence of EN, TR, ST, and SW in these 10-18 year old children was 0.3%, 0.6%, 6.0% and 1.1% respectively. Remission rates were 70.8%, 100%, 64.8% and 50.0% respectively.

Conclusions:  The incidence rates of EN, TR, and SW were relatively low moving from childhood to adolescence while remission rates were high across all parasomnias.

Introduction

Parasomnias are unpleasant or undesirable behavioral or experiential phenomena which occur predominantly or exclusively during sleep.¹ When occurring during childhood, they can result in substantial parental sleep disruption, anxiety and concern. In addition, there may be adverse consequences on the child's behavior and self-esteem.^2-4 There are 4 parasomnias that are commonly observed during childhood. Sleepwalking (SW) and sleep terrors (NT) are parasomnias associated with arousal that usually occur during slow wave sleep.⁵  Sleepwalking is semi-purposeful ambulatory behavior without awareness. Night terrors (also called sleep terrors) are recurrent episodes of abrupt awakening from deep non-REM sleep, usually with a scream and signs of intense fear and autonomic arousal.⁵ Sleep talking (somniloquy) (ST) consists of vocalizations, frequently nonsensical, during both REM and non-REM sleep.⁶  Enuresis (EN) is characterized by recurrent involuntary micturition that occurs during sleep.⁷ In contrast to SW, and NT, enuresis may occur during non-rapid eye movement (NREM) or rapid eye movement (REM) sleep.⁸

Epidemiological surveys investigating parasomnias in the general population are uncommon, perhaps because these parasomnias are usually considered harmless childhood occurrences. However, the prevalence of parasomnias in the general population of children has been estimated at approximately 3%–17% for SW,^{5, 9, 10} 1%–7% for NT,^{5, 9} 2%–18% for EN^9-12 and 5%–27% for ST. ^9-12 These estimates vary greatly because rarely are the same definitions for the frequency of events used. Although it is generally accepted that childhood parasomnias remit with age, virtually all studies have been cross-sectional. ^{4, 10, 11, 13-15} To our knowledge, there have been no studies investigating the remission and incidence of parasomnias in a community-based adolescent population. Therefore, it is the purpose of this analysis to describe the incidence and remission of parasomnias in such a cohort using data from the Tucson Children’s Assessment of Sleep Apnea (TuCASA) study.

Methods

TuCASA was designed to investigate the incidence, prevalence and correlates of objectively measured sleep-related breathing disorders (SRBD) in a prospective cohort study of preadolescent Hispanic and Caucasian children ages 6 to 12 years. Detailed recruitment methods have been described previously.¹⁶ Briefly, Hispanic and Caucasian children ages 6 to 12 years were recruited through the Tucson Unified School District (TUSD), a very large district with a substantial elementary school population. Parents were asked to complete a short screening questionnaire and to provide their contact information if they were willing to allow study personnel to contact them to determine if their child was eligible for the study. A total of 7,055 screening questionnaires were sent home with children in a “notes home” folder. Of these, 2,327 (33%) were returned. Recruitment information was supplied on 52% of the returned questionnaires. From these questionnaires, children were selected for potential participation based on pre-established inclusion and exclusion criteria, and after parents gave informed consent and the child gave assent using language-appropriate IRB approved forms. The TuCASA protocol was approved by both the University of Arizona Human Subjects Committee and the TUSD Research Committee.

Initially from 1999-2003, 503 children were enrolled (Time 1) and subsequently 350 were re-studied approximately 5 years later (Time 2). In addition to undergoing home polysomnography at both time points, parents were asked to complete a comprehensive sleep habits questionnaire (SHQ) that recorded the characteristics of their child’s sleep history including questions about EN, NT, SW and ST.

Specific questions were the following: "Does this child sleepwalk?", and "Does this child talk in his or her sleep? (Talk without being fully awake?)". For these 2 questions, possible responses were "Never", "less than three times per month", "three to five times per month", or "more than five times per month". The occurrence of these parasomnias was defined as follows: SW was present if it was reported more than three times per month, and ST was present if it was reported more than five times per month. Additionally, the parent was asked "How often does this child awaken at night afraid or appearing tearful?” If the parent answered that the child had more than five fearful awakenings per month then the child was classified as having NT. EN was present if it was reported as occurring more than five times per month. These definitions were chosen to be consistent with our previous analyses of parasomnias in this cohort and were thought to be clinically meaningful when these children were preadolecents.⁹

The SHQ was also used to define the occurrence of habitual snoring (SN), excessive daytime sleepiness (EDS), witnessed apnea (WITAP), difficulty initiating and maintaining sleep (INSOM), and learning problems (LP).  These sleep problems were considered present if they were reported 'frequently' or more (5 or more times per week). Although the specific range and order of questions used on the TuCASA SHQ and screening questionnaires have not been previously validated, key questions in the questionnaire have face validity and were taken from those used by Carroll and colleagues.¹⁷

As described in previous analyses from the TuCASA cohort,^9,16 we computed a respiratory disturbance index (RDI) as the total number of apneas and hypopneas/total sleep time (TST). Hypopneas were required to have an associated oxygen desaturation of 3%. Sleep disordered breathing (SDB) was considered present if the RDI was > 1 event/hour TST.

Statistical analysis of the data was performed using Stata 10 (StataCorp LP, College Station, TX)  and IBM SPSS Statistics 18 (New York, NY). As appropriate, comparisons of means and proportions were performed using two-sample t-tests for continuous data, and chi-squared tests and the exact binomial test for categorical data.  Data are expressed as means + SD and percentages.

Results 

There were a total of 503 children participating at Time 1 and 350 adolescents at time 2. Characteristics for the study group are shown in Table 1.

Table 1: Description of the TuCASA Cohort at Time 1 and Time 2

	Time 1	Time 2	p
Number in Cohort	503	350	-
Age (Mean + SD)	8.8 ± 1.6	13.3 ±1.7	-
Age (Min-Max)	[6,12.6]	[9.9,17.5]	-
Gender (% Male)	50	51	0.7643
Ethnicity (% Caucasian)	58	63	0.1283
Standardized BMI (Mean + SD)	.30 ± 1.2	.50 ± 1.1	0.0249
Obesity (%)	13	24	0.017

The mean age at first assessment was 8.8 years (min/max: 6-12.6 years) while mean age at second assessment was 13.3 years (min-max: 9.9-17.5 years). The mean time between assessments was 4.6 years (range: 2.9-7.3 years). There were 51% males and 49% females at the Time 2, approximately the same ratio as Time1. The gender ratio remained approximately the same at both measurements. Notably, standardized BMI increased and the % of the cohort classified as obese increased over the time interval. However, standardized BMI was not significantly higher in those children with parasomnias (data not shown).

As shown in Table 2, at Time 1 there were no differences in the prevalence rates of all 4 parasomnias using the entire cohort in comparison to a cohort restricted only to those children who had assessments made at both time points (Restricted Cohort). In addition, the prevalence of parasomnias at Time 2 remained similar to the prevalence at Time 1 with the exception of EN which declined markedly from 7% to 2%. Also shown in Table 2 are the prevalence, remission and incidence rates of the 4 parasomnias at Time 2. The incidence of EN, TR, and SW in our 10-17 year old children were approximately 1% for all 3 contrasting with ST with an incidence rate of approximately 6%. Furthermore, remission rates were high for all the parasomnias. All 9 adolescents had remission from NT. 17 of 24 subjects, approximately 71%, had remission from EN. 24 of 37 participants had remission from ST, approximately 65%. 1 out of 2 subjects (50%) with SW had remission. Incidence and remission of all parasomnias were not related to SN, WITAP, INSOM, or LP although limited incidence and remission numbers precluded extensive meaningful analyses. At Time 1, the prevalence of SDB was  27.8% (89/320). At Time 2, 14.4% (46/320)  Children with SDB on both occasions were 25/320 or 7.8%. There were 15 boys and 10 girls with persistent SDB with no ethnic differences. Because of the relatively small numbers of children with parasomnias and SDB at Time 2, we were unable to determine whether persistent SDB was a risk for prevalent or incident parasomnias .

In Table 3 is shown the number and percent of parasomnias that occurred in association with other parasomnias at Time 2. Except for an association between sleep walking and sleep talking, parasomnias occurred independent of each other.  

Discussion 

The TuCASA study has documented the prevalence, incidence and remission of parasomnias in a population-based sample of 10-17 year old subjects. We found that incidence rates for parasomnias were very low for EN NT and SW and remission rates were high for all parasomnias. Furthermore, incidence and remission rates did not appear to be related to symptoms of sleep disturbances or learning problems, and except for sleep walking and sleep talking, they generally were not co-prevalent.

In this study, except for ST, prevalence rates for parasomnias in our cohort of adolescents were relatively low. Available data documenting the prevalence rates of various parasomnias in this age group are relatively sparse with previous reports largely restricted to preadolescents. ^{4, 9-12, 15} However, with respect to SW, 3 previous studies in adolescents have observed prevalence rates ranging from 3 to 15% which are higher than the 1.4% noted in our study.^18-20 Inconsistent prevalence rates have been noted for NT with one study reporting rates <4%,²⁰  but another reporting 10.2%.¹⁹ In contrast, the prevalence of enuresis ^{7, 18, 20} and the prevalence of ST ^{6,13, 20} in adolescents have been reported to be consistently low and high respectively. Our data are concordant with these previous reports. However, the relevance of these comparisons is unclear since no standard method of assessing the frequency of parasomnias exists. Our requirement that these events occurred more than three to five times per month are more stringent than those employed in most studies. Thus, it not surprising that our prevalence rates for SW and NT in adolescence are discordant with previous observations.

There is general consensus that childhood parasomnias remit as children develop from childhood to adolescence and that few adolescents develop them.^{5, 21} However, this impression is based primarily on empiric observations because there are few longitudinal studies.^{20, 22, 23} The largest longitudinal study prospectively interrogated parents of children at age 10 through age 13 years, but retrospectively questioned parents to determine if a parasomnia was present between ages 3 and 9 years.²⁰ In this study, prevalence rates were noted to decline markedly by age 13 years to 3.3%, 1.2% and 2.0% for SW, NT and EN, respectively. In contrast, there was only a slight nonsignificant decrease in ST with 29.2% of children still having this condition at age 13 years. Our data are generally consistent with the results of this previous study although our prevalence of ST is somewhat lower. However, we extend these foregoing findings by documenting incidence and remission rates. Except for ST, very few adolescents developed new parasomnias. Nonetheless, although remission rates were high, some participants in this study had persistent symptoms which likely continue through into adulthood.^{24, 25}

We previously examined the prevalence of parasomnias in the TuCASA cohort when the children were preadolescents.⁹ We found an associations between parasomnias, and SDB, symptoms of other sleep disturbances and learning problems. Unfortunately, because of the small numbers of children with parasomnias in this follow-up cohort, we were unable to determine whether these latter findings are still present.

In this study, standardized BMI increased as did the % of the cohort classified as obese. While these observations most likely are a reflection of the ongoing obesity epidemic in the United States, those with parasomnias did not have significantly higher standardized BMI.

Some evidence indicates that individuals with one parasomnia have a greater likelihood of having another one.^{20, 25} Consistent with these previous studies, we found a modest association between ST and SW, both of which are disorders of arousal. Otherwise, we found little evidence to support the contention that parasomnias are more likely to be co-prevalent.

Although our study is the first to prospectively document the incidence and remission of parasomnias in a large general population of children, it is not without some limitations. First, it is possible that parents underestimated the actual number of parasomnias that occurred. Depending on the bedtime of the child and the severity of the event, it is probable that parents are not awake during every occurrence. Second, recruitment may have incurred a selection bias so that parents who agreed to have their children participate might be more likely to have symptomatic children than those who did not. We think this unlikely because the focus of the study was SDB and it is unlikely that parents agreed to have their children participate based on the presence of parasomnias. Lastly, there were 153 subjects that participated at Time 1 but that did not participate at Time 2. There was no difference related to gender between those that participated at Time 2 and those that did not although slightly more Hispanic adolescents were lost to follow-up than Caucasians. In addition, the prevalence rates of parasomnias in the entire cohort and the restricted were the same. Thus, we do not believe that the restricted cohort of children who had data at both time points was markedly different than the larger group of children recruited at Time 1.

In conclusion, although parasomnias are relatively common in childhood, our study demonstrates that most remit, and that the development of parasomnias in older children is uncommon. Our findings provide objective data supporting the generally accepted perception that most parasomnias in children will resolve over time.

Acknowledgements         

This study was supported by Grant HL 62373 from the National Heart Lung and Blood Institute. All authors contributed to the writing and analyses contained in the study and had full access to the data. Dr. Quan is the Principal Investigator of the TuCASA study. Drs. Quan and Goodwin supervised the recruitment of participants and the operations of TuCASA.

References

1 . Matwiyoff G, Lee-Chiong T. Parasomnias: an overview. Indian J Med Res 2010; 131:333-337.

2 . Heussler HS. 9 Common causes of sleep disruption and daytime sleepiness: childhood sleep disorders II. Med J Aust 2005; 182(9):484-489.

3 . Chokroverty S. Overview of sleep & sleep disorders. Indian J Med Res 2010; 131:126-140.

4 . Agargun MY, Cilli AS, Sener S, et al. The prevalence of parasomnias in preadolescent school-aged children: a Turkish sample. Sleep 2004; 27(4):701-705.

5 . Avidan AY, Kaplish N. The parasomnias: epidemiology, clinical features, and diagnostic approach. Clin Chest Med 2010; 31(2):353-370.

6 . Arkin AM. Sleep-talking: a review. J Nerv Ment Dis 1966; 143(2):101-122.

7 . Hansakunachai T, Ruangdaraganon N, Udomsubpayakul U, Sombuntham T, Kotchabhakdi N. Epidemiology of enuresis among school-age children in Thailand. J Dev Behav Pediatr 2005; 26(5):356-360.

8 . Mikkelsen EJ, Rapoport JL, Nee L, Gruenau C, Mendelson W, Gillin JC. Childhood enuresis. I. Sleep patterns and psychopathology. Arch Gen Psychiatry 1980; 37(10):1139-1144.

9 . Goodwin JL, Kaemingk KL, Fregosi RF, et al. Parasomnias and sleep disordered breathing in Caucasian and Hispanic children - the Tucson children's assessment of sleep apnea study. BMC Med 2004; 2:14.

10 . Arruda MA, Guidetti V, Galli F, Albuquerque RC, Bigal ME. Childhood periodic syndromes: a population-based study. Pediatr Neurol 2010; 43(6):420-424.

11 . Liu X, Ma Y, Wang Y, et al. Brief report: An epidemiologic survey of the prevalence of sleep disorders among children 2 to 12 years old in Beijing, China. Pediatrics 2005; 115(1 Suppl):266-268.

12 . Simola P, Niskakangas M, Liukkonen K, et al. Sleep problems and daytime tiredness in Finnish preschool-aged children-a community survey. Child Care Health Dev 2010; 36(6):805-811.

13 . Garcia-Jimenez MA, Salcedo-Aguilar F, Rodriguez-Almonacid FM, et al. The prevalence of sleep disorders among adolescents in Cuenca, Spain. Rev Neurol 2004; 39(1):18-24.

14 . Ipsiroglu OS, Fatemi A, Werner I, Tiefenthaler M, Urschitz MS, Schwarz B. Prevalence of sleep disorders in school children between 11 and 15 years of age. Wien Klin Wochenschr 2001; 113(7-8):235-244.

15 . Petit D, Touchette E, Tremblay RE, Boivin M, Montplaisir J. Dyssomnias and parasomnias in early childhood. Pediatrics 2007; 119(5):e1016-25.

16 . Goodwin JL, Enright PL, Kaemingk KL, et al. Feasibility of using unattended polysomnography in children for research--report of the Tucson Children's Assessment of Sleep Apnea study (TuCASA). Sleep 2001; 24(8):937-944.

17 . Carroll JL, McColley SA, Marcus CL, Curtis S, Loughlin GM. Inability of clinical history to distinguish primary snoring from obstructive sleep apnea syndrome in children. Chest 1995; 108(3):610-618.

18 . Klackenberg G. Incidence of parasomnias in children in a general population. In: Sleep and its Disorders in Children. Guilleminault C, ed. New York: Raven Press, 1987; 99-113

19 . Ipsiroglu OS, Fatemi A, Werner I, Paditz E, Schwarz B. Self-reported organic and nonorganic sleep problems in schoolchildren aged 11 to 15 years in Vienna. J Adolesc Health 2002; 31(5):436-442.

20 . Laberge L, Tremblay RE, Vitaro F, Montplaisir J. Development of parasomnias from childhood to early adolescence. Pediatrics 2000; 106(1 Pt 1):67-74.

21 . Guilleminault G. Disorders of arousal in children: Somnambulism and night terros. In: Guilleminault C, ed. New York: Raven Press, 1987; 243-252

22 . DiMario FJ,Jr, Emery ES,3rd. The natural history of night terrors. Clin Pediatr (Phila) 1987; 26(10):505-511.

23 . Klackenberg G. Somnambulism in childhood--prevalence, course and behavioral correlations. A prospective longitudinal study (6-16 years). Acta Paediatr Scand 1982; 71(3):495-499.

24 . Oluwole OS. Lifetime prevalence and incidence of parasomnias in a population of young adult Nigerians. J Neurol 2010; 257(7):1141-1147.

25 . Bjorvatn B, Gronli J, Pallesen S. Prevalence of different parasomnias in the general population. Sleep Med 2010; 11(10):1031-1034.