pii: jc- 00374-15http://dx.doi.org/10.5664/jcsm.5802
S CI E NT IF IC IN VES TIGATIONS
Sleep/Wake Patterns and Parental Perceptions of Sleep in Children Born Preterm Sarah N. Biggs, PhD1; Lisa J. Meltzer, PhD2; Ignacio E. Tapia, MD, MS3; Joel Traylor, RPsgT3; Gillian M. Nixon, MD1,4; Rosemary S.C. Horne, PhD1; Lex W. Doyle, MD5; Elizabeth Asztalos, MD6; Jodi A. Mindell, PhD3,7; Carole L. Marcus, MBBCh3; Caffeine for Apnea of Prematurity-Sleep Study Group The Ritchie Centre, Hudson Institute of Medical Research and Department of Paediatrics, Monash University, Melbourne, Australia; 2Department of Pediatrics, National Jewish Health, Denver, CO; 3Department of Pediatrics, Sleep Center, Children’s Hospital of Philadelphia; University of Pennsylvania School of Medicine, Philadelphia, PA; 4Melbourne Children’s Sleep Centre, Monash Children’s, Monash Medical Centre. Melbourne, Australia; 5Department of Obstetrics and Gynaecology, The Royal Women’s Hospital, University of Melbourne, and Clinical Sciences, Murdoch Children’s Research Institute, Melbourne, Australia; 6Department of Pediatrics, University of Toronto, Toronto, Canada; 7Department of Psychology, Saint Joseph’s University, Philadelphia, PA 1
Study Objectives: To compare sleep/wake patterns in children born preterm in Australia vs Canada and determine cultural differences in the relationship between parental perception of sleep and actual sleep behaviors. Methods: Australian and Canadian children born preterm were recruited from the Caffeine for Apnea of Prematurity trial (n = 188, 5–12 y) and underwent 14 days actigraphy monitoring. Parents completed the National Sleep Foundation 2004 Sleep in America questionnaire. Cross-cultural differences in sleep characteristics assessed by actigraphy and parent-reported questionnaire were examined. Correlational analyses determined the associations between parental perceptions of child sleep need and sleep behavior. Results: Actigraphy showed preterm children obtained, on average, 8 h sleep/night, one hour less than population recommendations for their age. There was no difference in total sleep time (TST) between Australian and Canadian cohorts; however, bed and wake times were earlier in Australian children. Bedtimes and TST varied by 60 minutes from night to night in both cohorts. Parent-reported child TST on the National Sleep Foundation questionnaire was 90 minutes longer than recorded by actigraphy. Both bedtime and TST on weekdays and weekends were related to parental perception of child sleep need in the Australian cohort. Only TST on weekdays was related to parental perception of child sleep need in the Canadian cohort. Conclusions: This study suggests that short sleep duration and irregular sleep schedules are common in children born preterm. Cultural differences in the association between parental perception of child sleep need and actual sleep behaviors provide important targets for future sleep health education. Keywords: preterm, sleep duration, actigraphy, sleep patterns, cross-cultural Citation: Biggs SN, Meltzer LJ, Tapia IE, Traylor J, Nixon GM, Horne RS, Doyle LW, Asztalos E, Mindell JA, Marcus CL. Sleep/wake patterns and parental perceptions of sleep in children born preterm. J Clin Sleep Med 2016;12(5):711–717.
I N T RO D U C T I O N
BRIEF SUMMARY
Current Knowledge/Study Rationale: Sleep disorders, short sleep duration and irregularity of sleep/wake schedules have detrimental effects on daytime functioning. Children born preterm are at increased risk of some sleep disorders, however whether they are also at risk of maladaptive sleep behaviors remains unknown. Study Impact: Short sleep duration is common in children born preterm with up to 38% of this cross-cultural cohort sleeping less than recommended. Timing of bed and wake times were culturally specific; however, short sleep duration and irregular sleep schedules were not.
Sleep during childhood is at a lifetime maximum and is vital for healthy development. Short sleep duration, and more recently, irregular night-to-night scheduling of bedtimes, have been associated with impaired cognitive performance, behavioral problems, and poor quality of life.1–5 Maintaining healthy sleep practices may be particularly important for children born preterm, as preterm birth is also associated with the deleterious outcomes listed above.6 In addition, children born preterm are at increased risk of sleep disorders such as obstructive sleep apnea (OSA) and periodic limb movements of sleep (PLMS).7 If preterm children are found to have short sleep duration or irregular scheduling of bed and wake times, this may have an additive effect on daytime dysfunction. There is evidence that the sleep patterns of children are largely driven by parental perceptions surrounding how much sleep children need.8 The current recommendations for optimal sleep duration in childhood are presumed to be universal9; however, sleep practices vary substantially across cultures.10–12 There are limited studies examining cultural differences
across predominantly Caucasian countries and the few studies that do, have relied solely on parental report measures. A comparison of 10 European countries showed differences in both the timing and duration of sleep in children.13 Australian adolescents were recently reported to obtain 47 minutes more sleep than their American counterparts, with the difference attributable to a significantly earlier wake time for the American teens.14 A more recent internet based study showed that Australian preschool children woke approximately 40 711
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minutes earlier and were reported to have 17 minutes longer sleep duration than Canadian preschool children. In that study, average bedtime was also almost 30 minutes earlier in Australian preschool children compared with Canadian preschool children.11 It is currently unknown whether differences in parental perceptions of child sleep need across predominantly Caucasian countries are influencing these differences in sleep/ wake timing. Knowledge of the cross-cultural differences in the association between parental perception of child sleep need and actual sleep behaviors could provide a key target area for culturally relevant sleep education. This study aimed to provide novel data on sleep/wake patterns, through the use of both actigraphy and parental questionnaires, in children aged 5–12 years who were born preterm. We also aimed to provide objective information regarding cultural differences in sleep/wake patterns, and the relationship between parental perception of sleep and actual sleep behaviors, across two predominantly Caucasian countries: Australia and Canada. Based on the pattern observed in preschool children,11 we hypothesized that Australian preterm children would go to bed earlier and have longer sleep duration than Canadian preterm children. We also hypothesized that parental perception of sleep need would be related to actual sleep practices.
OR). Actigraphy is a validated wristwatch-like device that distinguishes sleep from wakefulness based on accelerometer measured movement.18,19 Caregivers simultaneously completed a daily sleep diary which was used to identify bedtime and wake time, as well as to identify when the device was removed. Data were analyzed and interpreted centrally by a single technologist and a single pediatric sleep medicine specialist, respectively. Subjects with < 5 nights of recordings were excluded (n = 10). A number of key sleep/wake variables were calculated for analyses (Philips Actiware 6.0.2, Bend, OR): sleep onset latency (SOL: time taken to fall asleep after reported lights out), wake after sleep onset (WASO: number of minutes recorded as wake between sleep onset and sleep offset), total sleep time (TST: difference between sleep onset and offset less WASO), and sleep efficiency (TST/time in bed, reported as a percent). As the number of nights available for analysis varied across individuals (ranging between 5–14; mean ± SD = 11 ± 2), weighted means were calculated for each participant and used for overall group means.20 Variability of nightly scheduling of bedtime and wake time, and of sleep duration was calculated according to methods described by Sanchez-Ortuno et al.21 For each participant, differences between each consecutive measurement (e.g., bedtime night 2 minus bedtime night 1) were calculated and squared, capturing both variability and temporal dependency across time.22 These values were used to determine differences in mean variability between groups. The square roots of the weighted means are reported.
METHODS The protocol for the current study has been previously published.7 In brief, a subset of children enrolled in follow-up studies for the Caffeine for Apnea of Prematurity (CAP) trial15,16 underwent 2-week actigraphy monitoring prior to a single night of comprehensive, ambulatory polysomnography. Polysomnography results are published elsewhere7,17 and will not be reported here. Caregivers completed questionnaires relating to general sleep at the end of the 2-week actigraphy study. Data were collected from children born at 4 clinical sites: McMaster University Medical Centre, Hamilton, Canada; Sunnybrook Health Sciences Centre, Toronto, Canada; Royal Women’s Hospital, Melbourne, Australia; and Mercy Hospital for Women, Melbourne, Australia. Ethical approval for this study was provided by the research ethics board at each institution. Informed consent was obtained from parents/guardians.
Questionnaires
The caregiver completed an abbreviated form of the National Sleep Foundation 2004 Sleep in America (NSF) questionnaire,23 a comprehensive review of children’s sleep habits. Items used for the current analysis were usual wake time, usual bedtime, minutes to fall asleep, hours and minutes of actual night-time sleep, and perception of how much sleep the child needs. Wake time and bedtimes were reported as a forced choice category of 15 different ranges of time over a 24-h period. Parents also reported on their own nocturnal sleep duration (hours and minutes) and perception of how much sleep they needed. Subjects with incomplete data were excluded (n = 3).
Statistical Analyses
Participants
Data were tested for normality and equal variance prior to analyses. Actigraphy assessed SOL, WASO, and variability measures were corrected using logarithmic transformations.24 Analyses were conducted on transformed means; however, untransformed data are reported for ease of interpretation. Group differences in sex, race, and season when data were collected were tested using χ2 analyses. Differences in age, birth weight, gestational age, and amount of daylight when data were collected were tested with an independent samples t-test. Amount of daylight during data collection was calculated as the difference between sunrise and sunset on the first day of actigraphy monitoring. Cohort characteristics found significantly different were correlated with all sleep outcomes to determine confounders.
Children, aged 5–12 years (n = 201) were studied from August 2009 to July 2013. For both countries, data were collected equally across seasons. Eligibility criteria for the initial CAP trial included preterm birth with birth weights of 500–1,250 g, absence of major congenital anomalies or syndromes, and considered to be candidates for methylxanthine therapy for apnea of prematurity during the first 10 days of life.15,16 Thirteen children were excluded from final analyses due to incomplete actigraphy (n = 10) or questionnaire data (n = 3).
Actigraphy
Sleep/wake patterns over a 2-week period were assessed with actigraphy (Actiwatch 2, Philips Respironics, Bend, Journal of Clinical Sleep Medicine, Vol. 12, No. 5, 2016
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Table 1—Cohort characteristics. Age at assessment (y) Sex, n (% male) Maternal Race, n (%) White Black Asian Other Maternal Education, n (%) ≤ 11 Years schooling High School Graduate Some College/University University Graduate Unknown Birth weight (g) Gestational Age (weeks) Season of Study, n (%) Spring Summer Fall Winter Amount of daylight (hh:mm)
Australia (n = 87) 9.6 (1.9) 50 (58)
Canada (n = 101) 9.0 (2.0) 57 (56)
78 (90) 0 (0) 0 (0) 9 (10)
72 (71) 6 (6) 12 (12) 11 (11)
14 (16) 19 (22) 19 (22) 32 (37) 3 (3) 998 (171) 27.5 (1.6)
16 (16) 27 (27) 24 (24) 33 (32) 1 (1) 942 (165) 27.0 (1.7)
17 (20) 20 (23) 16 (18) 34 (39) 11:50 (1:55)
15 (15) 26 (26) 32 (32) 28 (28) 11:55 (2:19)
p value 0.03 0.80 < 0.001
0.70
0.02 0.05 0.12
0.80
Data are expressed as mean (± standard deviation) or n (%).
Univariable analyses of variance were conducted to determine group differences in sleep characteristics, controlling for age and race. Actigraphy reported bedtime, wake time, and TST on weekdays were categorized for comparison with the NSF questionnaire. Categories were collapsed into 6 discrete time periods for bedtime and wake time and 5 discrete time periods for TST. Differences between Australia and Canada in the proportion of children within each time period were analyzed using Z-distributions. Correlational analyses were conducted between parental perception of sleep need, actigraphy recorded bedtime, wake time and TST to determine the associations between parental perceptions of sleep need and sleep behavior. Fisher’s r-Z transformations were conducted to determine the difference in the magnitude of the correlations.
Age and race were therefore included as covariates in the univariable analyses. There were no differences in the seasonal timing of data collection or in the average amount of daylight over the data collection period between the two countries.
Sleep Characteristics and Cross-Cultural Comparisons
Table 2 shows the mean nocturnal sleep outcomes for actigraphy and the NSF questionnaire in the Australian, Canadian and total cohort. The actigraphy data showed that, overall, the complete cohort of preterm children obtained, on average, 491 min sleep per night over the 2-week period of monitoring, with weeknights only slightly longer than weekend nights (mean difference 11 min; t183 = 2.9, p = 0.004). Bedtimes were later (t183 = −16.5, p < 0.001), but wake times were earlier (t183 = 12.5, p < 0.001) on weekends than weekdays. Cross-country comparison of actigraphy recorded sleep/ wake patterns showed that Australian children went to bed earlier on week nights (Sunday-Thursday) and weekends (Friday/ Saturday) than Canadian children (Table 2). Australian children also woke earlier, significantly so on weekends (Saturday/ Sunday), resulting in no difference in TST. Night to night variability of bedtimes, wake times, SOL, and TST were equivalent between groups. Parents reported their children’s TST to be an average of 90 min longer than recorded by actigraphy on weekdays (t178 = −18.6, p < 0.001), with Australian parents reporting significantly longer TST than Canadian parents. Australian parents also felt their children needed an average of ~ 20 min more
R ES U LT S
Participants
The characteristics of the Australian and Canadian cohorts are shown in Table 1. 188 subjects were included in the analysis (Australia n = 87; Canada n = 101). The Australian cohort was minimally older and consisted of proportionately more White participants than the Canadian cohort. They were also, on average, heavier at birth than the Canadian cohort, although gestational age was not different. Correlational analysis with sleep outcome variables showed significant associations with age and race, but not with gestational age or weight at birth. 713
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Table 2—Univariable analyses of differences between Australia and Canada in sleep characteristics, controlling for age and race, as measured by actigraphy and parent-report questionnaire. Actigraphy – Weekdays Bedtime Sun-Thurs (hr:min,min) Wake time Mon-Fri (hr:min,min) SOL Sun-Thurs (min) WASO Sun-Thurs (min) TST Sun-Thurs (min) Sleep Efficiency Sun-Thurs (%) Actigraphy – Weekends Bedtime Fri-Sat (hr:min,min) Wake time Sat-Sun (hr:min,min) SOL Fri-Sat (min) WASO Fri-Sat (min) TST Fri-Sat (min) Sleep Efficiency Fri-Sat (%) Actigraphy – Variability Bedtime SSD (min) Wake time SSD (min) SOL SSD (min) TST SSD (min) Questionnaire Reported Child TST (min) Perception child sleep need (min) Reported Parent TST (min) Perception of parent sleep need (min)
Australia
Canada
Mean Difference
F1,178
p value
20:54 (132) 08:31 (150) 28 (50) 77 (68) 491 (111) 79 (14)
21:13 (138) 08:41 (156) 27 (50) 73 (70) 493 (101) 81 (15)
0:19 0:10 1 5 2 2
10.0 1.9 0.7 1.9 0.1 1.2
0.002 0.17 0.42 0.17 0.82 0.27
21:35 (102) 07:42 (88) 26 (35) 76 (46) 480 (76) 79 (10)
22:02 (90) 08:05 (90) 20 (24) 70 (39) 485 (74) 81 (9)
0:27 0:23 6 6 5 3
13.6 8.5 1.9 1.6 0.1 1.3
0.001 0.004 0.17 0.20 0.74 0.25
57 (109) 42 (89) 29 (60) 64 (145)
54 (104) 44 (78) 33 (78) 63 (107)
598 (52) 606 (58) 438 (78) 486 (66)
565 (72) 585 (66) 406 (72) 480 (57)
3 2 4 1
0.4 0.4 0.01 1.8
0.52 0.52 0.98 0.18
33 21 32 6
14.6 7.2 4.9 0.04
0.001 0.008 0.03 0.83
Actigraphy data are weighted by the number of nights recorded. Data are presented as mean (± standard deviation). SOL, sleep onset latency, WASO, wake after sleep onset, TST, total sleep time, SSD, square successive differences.
and parent-reported bedtimes than wake times, with parents reporting their children waking much earlier than actigraphy designated them as awake. Figure 1C shows that, based on actigraphy, 38% of the Australian and 35% of the Canadian cohort slept less than an average of 8 h/night. No child slept more than 10 h by actigraphy. The highest proportion of the total cohort slept between 8 and 9 h/night on average (47% Australia, 60% Canada). Based on parental report, the majority of the cohort were sleeping longer than 9 h (93% Australia, 83% Canada), demonstrating the overestimation of TST in parental report.
sleep than Canadian parents. In total, the difference between the parent’s perception of how much sleep a child needed and what they reported as TST was also significantly different (t177 = 3.8, p < 0.001), in that both Canadian and Australian parents felt their child needed more sleep than they were getting (mean difference = 12 min). According to the self-reported data, both Australian and Canadian parents had similar perceptions of how much sleep they needed. Parents from both countries also reported getting less sleep than they thought they needed, however the difference between perception of parent sleep need and self-reported sleep was less in the Australian parents, who reported average of 30 min longer TST than the Canadian parents. Figure 1 shows the comparison between actigraphy and parent-report of the child’s bedtimes, wake times, and TST on weekdays (Sunday-Thursday) in the Australian (black bars) and Canadian cohorts (white bars). Only weekdays are shown as the NSF asks parents to report their child’s usual bed and wake times on a “typical” night or day. It was assumed that this would likely be a weekday and thus provide the most accurate comparison. There was a clear shift to earlier bedtimes in the Australian compared to the Canadian cohort, which was not observed in the wake times on weekdays. There was also a greater agreement between actigraphy recorded bedtimes Journal of Clinical Sleep Medicine, Vol. 12, No. 5, 2016
Correlations between Parental Perception of Child Sleep Need and Sleep/Wake Patterns
Significant correlations were found between parental perception of sleep need and actigraphy reported bedtime and TST in the Australian cohort, but not the Canadian group (Table 3). The more sleep that parents felt their child needed, the earlier the child went to bed on both weekdays and weekends and the longer the child slept. In the Canadian cohort, perception of sleep needs was only significantly correlated with TST on weekdays. Fisher r-to-Z transformations revealed significant differences in the magnitude of these correlations for bedtime and TST on weekends, but not weekdays. 714
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Table 3—Correlations between parental perception of child sleep need and actigraphy recorded sleep outcomes
Bedtime Weeknights Bedtime Weekends Waketime Weekdays Waketime Weekends TST Weeknights TST Weekends
Perception of Child Sleep Need Australia, r-value Canada, r-value −0.38*** −0.20 −0.34** −0.09 0.06 0.03 0.01 −0.07 −0.31** 0.34** 0.34** 0.10
Fisher’s r-Z transformation −1.3 1.8* 0.2 0.5 −0.2 1.7*
*p < 0.05, **p < 0.01, ***p < 0.001. TST, total sleep time.
Figure 1—Comparison of Australian and Canadian cohorts.
D I SCUS S I O N This study provides, for the first time, actigraphy assessed as well as parental reported sleep/wake patterns in an Australian and Canadian cohort of children born preterm. The results demonstrated that school-aged children born preterm obtained, on average, 8 hours sleep per night and a night-to-night variability in bedtimes and total sleep time of approximately an hour across the week (Table 2). There were no differences in the amount of sleep obtained between Australian and Canadian preterm children, with both cohorts sleeping less on weekend nights than weeknights. This reduction of sleep on weekends is consistent with previous studies conducted in Australia in this age group.25,26 There was a difference in the timing of sleep, with Australian children going to bed earlier than Canadian children. Group comparisons also showed that Australian children woke earlier on weekends than Canadian children. Bedtime and TST on both weekdays and weekends was related to parental perception of sleep need in the Australian cohort. Only TST on weekdays was related to parental perception of sleep need in the Canadian cohort. The National Sleep Foundation recently published new recommendations for optimal sleep durations across the lifespan following a review of 312 studies from around the world.27 The recommended sleep duration for 5-year olds is 10–13 hours, and for 6- to 13-year olds 9–11 hours, with no less than 8 and 7 hours, respectively. Although less than 2% of the current cohort obtained less than 7 hours’ sleep, 38% of the Australian cohort and 35% of the Canadian had an actigraphy recorded sleep duration of less than 8 hours (Figure 1C), suggesting that children born preterm may be vulnerable to sleep-related daytime dysfunction as a result of short sleep duration. However, it must be noted that these recommendations are predominantly based on studies examining time in bed, rather than actual sleep time. A longitudinal birth cohort study showed no difference in parent-reported sleep duration, bedtime resistance or sleep-onset difficulties between children born preterm and a cohort of term children from birth to 10 years.28 Indeed, overall mean sleep duration in the current cohort as reported by parents was within the recommended range (9.7 ± 1.1 h) and similar to what was reported in American children aged 6–10 years by the 2004 Sleep in America poll (n = 637; TST = 9.4 ± 1.1 h).23 Further research comparing sleep-related dysfunction between preterm and term children using more
A
B
C
Comparison of proportion of the Australian (black bars) and Canadian (white bars) cohorts between actigraphy recorded and parent-reported bedtimes (A), wake times (B), and total sleep times (C). Raw data have been collapsed into categories. *p < 0.05, **p < 0.01, ***p < 0.001.
objective assessments of sleep is required before definitive conclusions can be made. 715
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Importantly however, previous actigraphy based studies have shown a sleep duration of less than 9 hours to be associated with emotional lability, hyperactive behavior,2 and poor school performance in this age group.29 In addition to a substantial proportion of the cohort sleeping less than 8 hours, up to 42% showed a night-to-night variability in bedtimes and TSTs of more than 60 minutes across the 14-day actigraphy monitoring period. This is concerning because recent research suggests that the variability of sleep/wake patterns has a greater impact on daytime functioning than the amount of sleep obtained.4,5,26 It has been shown that school-aged children with a greater than 60-minute difference in bedtimes across the week are four times more likely to exhibit hyperactive behaviors than children who sleep less than is recommended for their age.4 These results have important implications for clinical management of preterm children as well as for future sleep health education. The cross-cultural comparisons in the current study are similar to a recent internet study by Mindell and colleagues11 that reported bedtimes, wake time, nocturnal sleep duration, and daytime sleep in preschool children in 13 countries. Although the Mindell study focused on differences between the predominantly Caucasian and predominantly Asian countries, the results showed a similar difference in the timing of sleep between the Australian and Canadian cohorts to the current study. As school start times are consistent across the countries with the first class beginning between 08:20 and 09:00,30,31 one explanation for the difference in timing could be related to the geographical location and the amount of daylight exposure. Melbourne gets approximately 30 minutes more light during the day than Toronto in winter and approximately an hour less during summer,32,33 although it must be noted that examination of the timing of each study revealed there were no differences in the average length of daylight between the two countries during the study period (Table 1). Another explanation is the difference in parental perceptions of sleep need. This study found that parental perception of how much sleep a child needs was significantly different across the countries, with Australian parents believing their children required more sleep than Canadian parents. These results also showed that perception of sleep need was associated with bedtime as well as TST in the Australian cohort, with the magnitude of the correlations significantly different between countries on weekends. It is unclear why the relationship was found for Australian and not Canadian participants, as sleep education messages regarding optimal sleep in children are consistent across the two countries.34,35 Future research is needed to examine possible factors that may have contributed to these differences, including number of activities children participate in, and/or societal beliefs about the importance of sleep relative to other health behaviors (e.g., diet, exercise). To date, cross-cultural comparisons of sleep in children have been based solely on parental report of usual sleep patterns, which is prone to memory bias and overestimation. Indeed, the comparison between parent-reported TST showed that Australian parents reported significantly longer sleep duration in their children than Canadian parents, but they were also more prone to overestimate sleep duration (Figure 1C). A strength of this Journal of Clinical Sleep Medicine, Vol. 12, No. 5, 2016
study is the use of actigraphy to provide a more objective estimate of sleep/wake patterns. Despite the known limitations of actigraphy,36 the current results are more likely to accurately reflect true sleep patterns. This study is limited in that assessments of cognition and behavior were not included and thus cannot describe any association between short sleep duration, night-to-night variability, and daytime outcomes in these preterm children. In addition, although comparisons were made with data from term born children in the Sleep in America poll, the current study did not contain term controls. These would be important considerations for future research. Another limitation was the global nature of the NSF questions regarding bedtime, wake time and TST. A questionnaire with more specific questions, separating week nights from weekends, would benefit future research. Despite these limitations, this study provides novel data on sleep/wake patterns in a large preterm cohort, and suggests that short sleep duration and irregular sleep schedules are common in children born preterm. In addition, the cross-cultural differences in parental perception of sleep need and the relationship to objective sleep/wake patterns adds substantially to our current state of knowledge. The results from this study provide objective information on which to inform the future clinical management of children born preterm, as well as sleep health educational messages targeting both the perception of sleep need and sleep/wake patterns across two predominantly Caucasian countries. A B B R E V I AT I O N S CAP, Caffeine for Apnea of Prematurity Trial NSF, National Sleep Foundation Sleep in America questionnaire OSA, obstructive sleep apnea PLMS, periodic limb movements of sleep SOL, sleep onset latency SSD, square successive differences TST, total sleep time WASO, wake after sleep onset R E FE R E N CES 1. Gruber R, Laviolette R, Deluca P, Monson E, Cornish K, Carrier J. Short sleep duration is associated with poor performance on IQ measures in healthy school-age children. Sleep Med 2010;11:289–94. 2. Nixon GM, Thompson JM, Han DY, et al. Short sleep duration in middle childhood: risk factors and consequences. Sleep 2008;31:71–8. 3. Paavonen EJ, Raikkonen K, Lahti J, et al. Short sleep duration and behavioral symptoms of attention-deficit/hyperactivity disorder in healthy 7- to 8-year-old children. Pediatrics 2009;123:e857–64. 4. Biggs SN, Lushington K, van den Heuvel CJ, Martin AJ, Kennedy JD. Inconsistent sleep schedules and daytime behavioral difficulties in schoolaged children. Sleep Med 2011;12:780–6. 5. Kelly Y, Kelly J, Sacker A. Changes in bedtime schedules and behavioral difficulties in 7 year old children. Pediatrics 2013;132:e1184–93. 6. Moreira RS, Magalhaes LC, Alves CR. Effect of preterm birth on motor development, behavior, and school performance of school-age children: a systematic review. J Pediatr (Rio J) 2014;90:119–34.
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27. Hirshkowitz M, Whiton K, Albert SM, et al. National Sleep Foundation’s sleep time duration recommendations: methodology and results summary. Sleep Health 2015;1:40–3. 28. Iglowstein I, Latal Hajnal B, Molinari L, Largo RH, Jenni OG. Sleep behaviour in preterm children from birth to age 10 years: a longitudinal study. Acta Paediatr 2006;95:1691–3. 29. Keller PS, El-Sheikh M, Buckhalt JA. Children’s attachment to parents and their academic functioning: sleep disruptions as moderators of effects. J Dev Behav Pediatr 2008;29:441–9. 30. Toronto District School Board. Elementary Schools. Accessed November 9, 2015. Available from: http://www.tdsb.on.ca. 31. Victoria State Government. Living in Victoria. Accessed November 9, 2015. Available from: www.liveinvictoria.vic.gov.au. 32. National Research Council Canada. Sunrise/sunset calculator. Accessed February 26, 2015. Available from: http://www.nrc-cnrc.gc.ca/eng/services/ sunrise/. 33. City of Melbourne. Melbourne in numbers. Accessed February 26, 2015. Available from: http://www.melbourne.vic.gov.au/AboutMelbourne/Statistics/ Pages/MelbourneSnapshot.aspx. 34. Canadian Sleep Society. Sleep in Children. Accessed February 26, 2015. Available from: http://css-scs.ca/menu/education-and-information/brochures. 35. Sleep Health Foundation. Sleep need across the lifespan. Accessed February 25, 2015. Available from: http://www.sleephealthfoundation.org.au/fact-sheetsa-z.html. 36. Meltzer LJ, Montgomery-Downs HE, Insana SP, Walsh CM. Use of actigraphy for assessment in pediatric sleep research. Sleep Med Rev 2012;16:463–75.
SUBM I SSI O N & CO R R ESPO NDENCE I NFO R M ATI O N Submitted for publication August, 2015 Submitted in final revised form January, 2016 Accepted for publication January, 2016 Address correspondence to: Dr. Sarah Biggs, The Ritchie Centre, Level 5 Monash Medical Centre, 246 Clayton Road, Clayton, Victoria 3168, Australia; Tel: +61 3 95944759; Fax: +61 3 95946811; Email: [email protected]
D I SCLO S U R E S TAT E M E N T This research was funded by NIH R01 HL098045 and Canadian Institutes of Health Research grant MCT 13288. The Ritchie Centre is supported by the Victorian Government’s Operational Infrastructure Support Program. Phillips Respironics. Inc. provided the actigraphy devices. Dr. Marcus has investigator-initiated research support from Philips Respironics and Ventus. Dr. Mindell has served as a consultant and speaker for Johnson & Johnson. The other authors have indicated no financial conflicts of interest. Author contributions: Dr. Biggs participated in data collection, conducted data analysis for the current manuscript, drafted the initial manuscript, and approved the final manuscript as submitted. Drs. Meltzer, Doyle, Mindell, and Marcus were responsible for the study design, participated in data analysis, commented on drafts of the manuscript and approved the final manuscript as submitted. Drs. Tapia, Traylor, Asztalos, Nixon and Horne were involved in data collection and analysis, commented on drafts of the manuscript, and approved the final version.
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S CI E NT IF IC IN VES TIGATIONS
Sleep/Wake Patterns and Parental Perceptions of Sleep in Children Born Preterm Sarah N. Biggs, PhD1; Lisa J. Meltzer, PhD2; Ignacio E. Tapia, MD, MS3; Joel Traylor, RPsgT3; Gillian M. Nixon, MD1,4; Rosemary S.C. Horne, PhD1; Lex W. Doyle, MD5; Elizabeth Asztalos, MD6; Jodi A. Mindell, PhD3,7; Carole L. Marcus, MBBCh3; Caffeine for Apnea of Prematurity-Sleep Study Group The Ritchie Centre, Hudson Institute of Medical Research and Department of Paediatrics, Monash University, Melbourne, Australia; 2Department of Pediatrics, National Jewish Health, Denver, CO; 3Department of Pediatrics, Sleep Center, Children’s Hospital of Philadelphia; University of Pennsylvania School of Medicine, Philadelphia, PA; 4Melbourne Children’s Sleep Centre, Monash Children’s, Monash Medical Centre. Melbourne, Australia; 5Department of Obstetrics and Gynaecology, The Royal Women’s Hospital, University of Melbourne, and Clinical Sciences, Murdoch Children’s Research Institute, Melbourne, Australia; 6Department of Pediatrics, University of Toronto, Toronto, Canada; 7Department of Psychology, Saint Joseph’s University, Philadelphia, PA 1
Study Objectives: To compare sleep/wake patterns in children born preterm in Australia vs Canada and determine cultural differences in the relationship between parental perception of sleep and actual sleep behaviors. Methods: Australian and Canadian children born preterm were recruited from the Caffeine for Apnea of Prematurity trial (n = 188, 5–12 y) and underwent 14 days actigraphy monitoring. Parents completed the National Sleep Foundation 2004 Sleep in America questionnaire. Cross-cultural differences in sleep characteristics assessed by actigraphy and parent-reported questionnaire were examined. Correlational analyses determined the associations between parental perceptions of child sleep need and sleep behavior. Results: Actigraphy showed preterm children obtained, on average, 8 h sleep/night, one hour less than population recommendations for their age. There was no difference in total sleep time (TST) between Australian and Canadian cohorts; however, bed and wake times were earlier in Australian children. Bedtimes and TST varied by 60 minutes from night to night in both cohorts. Parent-reported child TST on the National Sleep Foundation questionnaire was 90 minutes longer than recorded by actigraphy. Both bedtime and TST on weekdays and weekends were related to parental perception of child sleep need in the Australian cohort. Only TST on weekdays was related to parental perception of child sleep need in the Canadian cohort. Conclusions: This study suggests that short sleep duration and irregular sleep schedules are common in children born preterm. Cultural differences in the association between parental perception of child sleep need and actual sleep behaviors provide important targets for future sleep health education. Keywords: preterm, sleep duration, actigraphy, sleep patterns, cross-cultural Citation: Biggs SN, Meltzer LJ, Tapia IE, Traylor J, Nixon GM, Horne RS, Doyle LW, Asztalos E, Mindell JA, Marcus CL. Sleep/wake patterns and parental perceptions of sleep in children born preterm. J Clin Sleep Med 2016;12(5):711–717.
I N T RO D U C T I O N
BRIEF SUMMARY
Current Knowledge/Study Rationale: Sleep disorders, short sleep duration and irregularity of sleep/wake schedules have detrimental effects on daytime functioning. Children born preterm are at increased risk of some sleep disorders, however whether they are also at risk of maladaptive sleep behaviors remains unknown. Study Impact: Short sleep duration is common in children born preterm with up to 38% of this cross-cultural cohort sleeping less than recommended. Timing of bed and wake times were culturally specific; however, short sleep duration and irregular sleep schedules were not.
Sleep during childhood is at a lifetime maximum and is vital for healthy development. Short sleep duration, and more recently, irregular night-to-night scheduling of bedtimes, have been associated with impaired cognitive performance, behavioral problems, and poor quality of life.1–5 Maintaining healthy sleep practices may be particularly important for children born preterm, as preterm birth is also associated with the deleterious outcomes listed above.6 In addition, children born preterm are at increased risk of sleep disorders such as obstructive sleep apnea (OSA) and periodic limb movements of sleep (PLMS).7 If preterm children are found to have short sleep duration or irregular scheduling of bed and wake times, this may have an additive effect on daytime dysfunction. There is evidence that the sleep patterns of children are largely driven by parental perceptions surrounding how much sleep children need.8 The current recommendations for optimal sleep duration in childhood are presumed to be universal9; however, sleep practices vary substantially across cultures.10–12 There are limited studies examining cultural differences
across predominantly Caucasian countries and the few studies that do, have relied solely on parental report measures. A comparison of 10 European countries showed differences in both the timing and duration of sleep in children.13 Australian adolescents were recently reported to obtain 47 minutes more sleep than their American counterparts, with the difference attributable to a significantly earlier wake time for the American teens.14 A more recent internet based study showed that Australian preschool children woke approximately 40 711
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minutes earlier and were reported to have 17 minutes longer sleep duration than Canadian preschool children. In that study, average bedtime was also almost 30 minutes earlier in Australian preschool children compared with Canadian preschool children.11 It is currently unknown whether differences in parental perceptions of child sleep need across predominantly Caucasian countries are influencing these differences in sleep/ wake timing. Knowledge of the cross-cultural differences in the association between parental perception of child sleep need and actual sleep behaviors could provide a key target area for culturally relevant sleep education. This study aimed to provide novel data on sleep/wake patterns, through the use of both actigraphy and parental questionnaires, in children aged 5–12 years who were born preterm. We also aimed to provide objective information regarding cultural differences in sleep/wake patterns, and the relationship between parental perception of sleep and actual sleep behaviors, across two predominantly Caucasian countries: Australia and Canada. Based on the pattern observed in preschool children,11 we hypothesized that Australian preterm children would go to bed earlier and have longer sleep duration than Canadian preterm children. We also hypothesized that parental perception of sleep need would be related to actual sleep practices.
OR). Actigraphy is a validated wristwatch-like device that distinguishes sleep from wakefulness based on accelerometer measured movement.18,19 Caregivers simultaneously completed a daily sleep diary which was used to identify bedtime and wake time, as well as to identify when the device was removed. Data were analyzed and interpreted centrally by a single technologist and a single pediatric sleep medicine specialist, respectively. Subjects with < 5 nights of recordings were excluded (n = 10). A number of key sleep/wake variables were calculated for analyses (Philips Actiware 6.0.2, Bend, OR): sleep onset latency (SOL: time taken to fall asleep after reported lights out), wake after sleep onset (WASO: number of minutes recorded as wake between sleep onset and sleep offset), total sleep time (TST: difference between sleep onset and offset less WASO), and sleep efficiency (TST/time in bed, reported as a percent). As the number of nights available for analysis varied across individuals (ranging between 5–14; mean ± SD = 11 ± 2), weighted means were calculated for each participant and used for overall group means.20 Variability of nightly scheduling of bedtime and wake time, and of sleep duration was calculated according to methods described by Sanchez-Ortuno et al.21 For each participant, differences between each consecutive measurement (e.g., bedtime night 2 minus bedtime night 1) were calculated and squared, capturing both variability and temporal dependency across time.22 These values were used to determine differences in mean variability between groups. The square roots of the weighted means are reported.
METHODS The protocol for the current study has been previously published.7 In brief, a subset of children enrolled in follow-up studies for the Caffeine for Apnea of Prematurity (CAP) trial15,16 underwent 2-week actigraphy monitoring prior to a single night of comprehensive, ambulatory polysomnography. Polysomnography results are published elsewhere7,17 and will not be reported here. Caregivers completed questionnaires relating to general sleep at the end of the 2-week actigraphy study. Data were collected from children born at 4 clinical sites: McMaster University Medical Centre, Hamilton, Canada; Sunnybrook Health Sciences Centre, Toronto, Canada; Royal Women’s Hospital, Melbourne, Australia; and Mercy Hospital for Women, Melbourne, Australia. Ethical approval for this study was provided by the research ethics board at each institution. Informed consent was obtained from parents/guardians.
Questionnaires
The caregiver completed an abbreviated form of the National Sleep Foundation 2004 Sleep in America (NSF) questionnaire,23 a comprehensive review of children’s sleep habits. Items used for the current analysis were usual wake time, usual bedtime, minutes to fall asleep, hours and minutes of actual night-time sleep, and perception of how much sleep the child needs. Wake time and bedtimes were reported as a forced choice category of 15 different ranges of time over a 24-h period. Parents also reported on their own nocturnal sleep duration (hours and minutes) and perception of how much sleep they needed. Subjects with incomplete data were excluded (n = 3).
Statistical Analyses
Participants
Data were tested for normality and equal variance prior to analyses. Actigraphy assessed SOL, WASO, and variability measures were corrected using logarithmic transformations.24 Analyses were conducted on transformed means; however, untransformed data are reported for ease of interpretation. Group differences in sex, race, and season when data were collected were tested using χ2 analyses. Differences in age, birth weight, gestational age, and amount of daylight when data were collected were tested with an independent samples t-test. Amount of daylight during data collection was calculated as the difference between sunrise and sunset on the first day of actigraphy monitoring. Cohort characteristics found significantly different were correlated with all sleep outcomes to determine confounders.
Children, aged 5–12 years (n = 201) were studied from August 2009 to July 2013. For both countries, data were collected equally across seasons. Eligibility criteria for the initial CAP trial included preterm birth with birth weights of 500–1,250 g, absence of major congenital anomalies or syndromes, and considered to be candidates for methylxanthine therapy for apnea of prematurity during the first 10 days of life.15,16 Thirteen children were excluded from final analyses due to incomplete actigraphy (n = 10) or questionnaire data (n = 3).
Actigraphy
Sleep/wake patterns over a 2-week period were assessed with actigraphy (Actiwatch 2, Philips Respironics, Bend, Journal of Clinical Sleep Medicine, Vol. 12, No. 5, 2016
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Table 1—Cohort characteristics. Age at assessment (y) Sex, n (% male) Maternal Race, n (%) White Black Asian Other Maternal Education, n (%) ≤ 11 Years schooling High School Graduate Some College/University University Graduate Unknown Birth weight (g) Gestational Age (weeks) Season of Study, n (%) Spring Summer Fall Winter Amount of daylight (hh:mm)
Australia (n = 87) 9.6 (1.9) 50 (58)
Canada (n = 101) 9.0 (2.0) 57 (56)
78 (90) 0 (0) 0 (0) 9 (10)
72 (71) 6 (6) 12 (12) 11 (11)
14 (16) 19 (22) 19 (22) 32 (37) 3 (3) 998 (171) 27.5 (1.6)
16 (16) 27 (27) 24 (24) 33 (32) 1 (1) 942 (165) 27.0 (1.7)
17 (20) 20 (23) 16 (18) 34 (39) 11:50 (1:55)
15 (15) 26 (26) 32 (32) 28 (28) 11:55 (2:19)
p value 0.03 0.80 < 0.001
0.70
0.02 0.05 0.12
0.80
Data are expressed as mean (± standard deviation) or n (%).
Univariable analyses of variance were conducted to determine group differences in sleep characteristics, controlling for age and race. Actigraphy reported bedtime, wake time, and TST on weekdays were categorized for comparison with the NSF questionnaire. Categories were collapsed into 6 discrete time periods for bedtime and wake time and 5 discrete time periods for TST. Differences between Australia and Canada in the proportion of children within each time period were analyzed using Z-distributions. Correlational analyses were conducted between parental perception of sleep need, actigraphy recorded bedtime, wake time and TST to determine the associations between parental perceptions of sleep need and sleep behavior. Fisher’s r-Z transformations were conducted to determine the difference in the magnitude of the correlations.
Age and race were therefore included as covariates in the univariable analyses. There were no differences in the seasonal timing of data collection or in the average amount of daylight over the data collection period between the two countries.
Sleep Characteristics and Cross-Cultural Comparisons
Table 2 shows the mean nocturnal sleep outcomes for actigraphy and the NSF questionnaire in the Australian, Canadian and total cohort. The actigraphy data showed that, overall, the complete cohort of preterm children obtained, on average, 491 min sleep per night over the 2-week period of monitoring, with weeknights only slightly longer than weekend nights (mean difference 11 min; t183 = 2.9, p = 0.004). Bedtimes were later (t183 = −16.5, p < 0.001), but wake times were earlier (t183 = 12.5, p < 0.001) on weekends than weekdays. Cross-country comparison of actigraphy recorded sleep/ wake patterns showed that Australian children went to bed earlier on week nights (Sunday-Thursday) and weekends (Friday/ Saturday) than Canadian children (Table 2). Australian children also woke earlier, significantly so on weekends (Saturday/ Sunday), resulting in no difference in TST. Night to night variability of bedtimes, wake times, SOL, and TST were equivalent between groups. Parents reported their children’s TST to be an average of 90 min longer than recorded by actigraphy on weekdays (t178 = −18.6, p < 0.001), with Australian parents reporting significantly longer TST than Canadian parents. Australian parents also felt their children needed an average of ~ 20 min more
R ES U LT S
Participants
The characteristics of the Australian and Canadian cohorts are shown in Table 1. 188 subjects were included in the analysis (Australia n = 87; Canada n = 101). The Australian cohort was minimally older and consisted of proportionately more White participants than the Canadian cohort. They were also, on average, heavier at birth than the Canadian cohort, although gestational age was not different. Correlational analysis with sleep outcome variables showed significant associations with age and race, but not with gestational age or weight at birth. 713
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Table 2—Univariable analyses of differences between Australia and Canada in sleep characteristics, controlling for age and race, as measured by actigraphy and parent-report questionnaire. Actigraphy – Weekdays Bedtime Sun-Thurs (hr:min,min) Wake time Mon-Fri (hr:min,min) SOL Sun-Thurs (min) WASO Sun-Thurs (min) TST Sun-Thurs (min) Sleep Efficiency Sun-Thurs (%) Actigraphy – Weekends Bedtime Fri-Sat (hr:min,min) Wake time Sat-Sun (hr:min,min) SOL Fri-Sat (min) WASO Fri-Sat (min) TST Fri-Sat (min) Sleep Efficiency Fri-Sat (%) Actigraphy – Variability Bedtime SSD (min) Wake time SSD (min) SOL SSD (min) TST SSD (min) Questionnaire Reported Child TST (min) Perception child sleep need (min) Reported Parent TST (min) Perception of parent sleep need (min)
Australia
Canada
Mean Difference
F1,178
p value
20:54 (132) 08:31 (150) 28 (50) 77 (68) 491 (111) 79 (14)
21:13 (138) 08:41 (156) 27 (50) 73 (70) 493 (101) 81 (15)
0:19 0:10 1 5 2 2
10.0 1.9 0.7 1.9 0.1 1.2
0.002 0.17 0.42 0.17 0.82 0.27
21:35 (102) 07:42 (88) 26 (35) 76 (46) 480 (76) 79 (10)
22:02 (90) 08:05 (90) 20 (24) 70 (39) 485 (74) 81 (9)
0:27 0:23 6 6 5 3
13.6 8.5 1.9 1.6 0.1 1.3
0.001 0.004 0.17 0.20 0.74 0.25
57 (109) 42 (89) 29 (60) 64 (145)
54 (104) 44 (78) 33 (78) 63 (107)
598 (52) 606 (58) 438 (78) 486 (66)
565 (72) 585 (66) 406 (72) 480 (57)
3 2 4 1
0.4 0.4 0.01 1.8
0.52 0.52 0.98 0.18
33 21 32 6
14.6 7.2 4.9 0.04
0.001 0.008 0.03 0.83
Actigraphy data are weighted by the number of nights recorded. Data are presented as mean (± standard deviation). SOL, sleep onset latency, WASO, wake after sleep onset, TST, total sleep time, SSD, square successive differences.
and parent-reported bedtimes than wake times, with parents reporting their children waking much earlier than actigraphy designated them as awake. Figure 1C shows that, based on actigraphy, 38% of the Australian and 35% of the Canadian cohort slept less than an average of 8 h/night. No child slept more than 10 h by actigraphy. The highest proportion of the total cohort slept between 8 and 9 h/night on average (47% Australia, 60% Canada). Based on parental report, the majority of the cohort were sleeping longer than 9 h (93% Australia, 83% Canada), demonstrating the overestimation of TST in parental report.
sleep than Canadian parents. In total, the difference between the parent’s perception of how much sleep a child needed and what they reported as TST was also significantly different (t177 = 3.8, p < 0.001), in that both Canadian and Australian parents felt their child needed more sleep than they were getting (mean difference = 12 min). According to the self-reported data, both Australian and Canadian parents had similar perceptions of how much sleep they needed. Parents from both countries also reported getting less sleep than they thought they needed, however the difference between perception of parent sleep need and self-reported sleep was less in the Australian parents, who reported average of 30 min longer TST than the Canadian parents. Figure 1 shows the comparison between actigraphy and parent-report of the child’s bedtimes, wake times, and TST on weekdays (Sunday-Thursday) in the Australian (black bars) and Canadian cohorts (white bars). Only weekdays are shown as the NSF asks parents to report their child’s usual bed and wake times on a “typical” night or day. It was assumed that this would likely be a weekday and thus provide the most accurate comparison. There was a clear shift to earlier bedtimes in the Australian compared to the Canadian cohort, which was not observed in the wake times on weekdays. There was also a greater agreement between actigraphy recorded bedtimes Journal of Clinical Sleep Medicine, Vol. 12, No. 5, 2016
Correlations between Parental Perception of Child Sleep Need and Sleep/Wake Patterns
Significant correlations were found between parental perception of sleep need and actigraphy reported bedtime and TST in the Australian cohort, but not the Canadian group (Table 3). The more sleep that parents felt their child needed, the earlier the child went to bed on both weekdays and weekends and the longer the child slept. In the Canadian cohort, perception of sleep needs was only significantly correlated with TST on weekdays. Fisher r-to-Z transformations revealed significant differences in the magnitude of these correlations for bedtime and TST on weekends, but not weekdays. 714
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Table 3—Correlations between parental perception of child sleep need and actigraphy recorded sleep outcomes
Bedtime Weeknights Bedtime Weekends Waketime Weekdays Waketime Weekends TST Weeknights TST Weekends
Perception of Child Sleep Need Australia, r-value Canada, r-value −0.38*** −0.20 −0.34** −0.09 0.06 0.03 0.01 −0.07 −0.31** 0.34** 0.34** 0.10
Fisher’s r-Z transformation −1.3 1.8* 0.2 0.5 −0.2 1.7*
*p < 0.05, **p < 0.01, ***p < 0.001. TST, total sleep time.
Figure 1—Comparison of Australian and Canadian cohorts.
D I SCUS S I O N This study provides, for the first time, actigraphy assessed as well as parental reported sleep/wake patterns in an Australian and Canadian cohort of children born preterm. The results demonstrated that school-aged children born preterm obtained, on average, 8 hours sleep per night and a night-to-night variability in bedtimes and total sleep time of approximately an hour across the week (Table 2). There were no differences in the amount of sleep obtained between Australian and Canadian preterm children, with both cohorts sleeping less on weekend nights than weeknights. This reduction of sleep on weekends is consistent with previous studies conducted in Australia in this age group.25,26 There was a difference in the timing of sleep, with Australian children going to bed earlier than Canadian children. Group comparisons also showed that Australian children woke earlier on weekends than Canadian children. Bedtime and TST on both weekdays and weekends was related to parental perception of sleep need in the Australian cohort. Only TST on weekdays was related to parental perception of sleep need in the Canadian cohort. The National Sleep Foundation recently published new recommendations for optimal sleep durations across the lifespan following a review of 312 studies from around the world.27 The recommended sleep duration for 5-year olds is 10–13 hours, and for 6- to 13-year olds 9–11 hours, with no less than 8 and 7 hours, respectively. Although less than 2% of the current cohort obtained less than 7 hours’ sleep, 38% of the Australian cohort and 35% of the Canadian had an actigraphy recorded sleep duration of less than 8 hours (Figure 1C), suggesting that children born preterm may be vulnerable to sleep-related daytime dysfunction as a result of short sleep duration. However, it must be noted that these recommendations are predominantly based on studies examining time in bed, rather than actual sleep time. A longitudinal birth cohort study showed no difference in parent-reported sleep duration, bedtime resistance or sleep-onset difficulties between children born preterm and a cohort of term children from birth to 10 years.28 Indeed, overall mean sleep duration in the current cohort as reported by parents was within the recommended range (9.7 ± 1.1 h) and similar to what was reported in American children aged 6–10 years by the 2004 Sleep in America poll (n = 637; TST = 9.4 ± 1.1 h).23 Further research comparing sleep-related dysfunction between preterm and term children using more
A
B
C
Comparison of proportion of the Australian (black bars) and Canadian (white bars) cohorts between actigraphy recorded and parent-reported bedtimes (A), wake times (B), and total sleep times (C). Raw data have been collapsed into categories. *p < 0.05, **p < 0.01, ***p < 0.001.
objective assessments of sleep is required before definitive conclusions can be made. 715
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Importantly however, previous actigraphy based studies have shown a sleep duration of less than 9 hours to be associated with emotional lability, hyperactive behavior,2 and poor school performance in this age group.29 In addition to a substantial proportion of the cohort sleeping less than 8 hours, up to 42% showed a night-to-night variability in bedtimes and TSTs of more than 60 minutes across the 14-day actigraphy monitoring period. This is concerning because recent research suggests that the variability of sleep/wake patterns has a greater impact on daytime functioning than the amount of sleep obtained.4,5,26 It has been shown that school-aged children with a greater than 60-minute difference in bedtimes across the week are four times more likely to exhibit hyperactive behaviors than children who sleep less than is recommended for their age.4 These results have important implications for clinical management of preterm children as well as for future sleep health education. The cross-cultural comparisons in the current study are similar to a recent internet study by Mindell and colleagues11 that reported bedtimes, wake time, nocturnal sleep duration, and daytime sleep in preschool children in 13 countries. Although the Mindell study focused on differences between the predominantly Caucasian and predominantly Asian countries, the results showed a similar difference in the timing of sleep between the Australian and Canadian cohorts to the current study. As school start times are consistent across the countries with the first class beginning between 08:20 and 09:00,30,31 one explanation for the difference in timing could be related to the geographical location and the amount of daylight exposure. Melbourne gets approximately 30 minutes more light during the day than Toronto in winter and approximately an hour less during summer,32,33 although it must be noted that examination of the timing of each study revealed there were no differences in the average length of daylight between the two countries during the study period (Table 1). Another explanation is the difference in parental perceptions of sleep need. This study found that parental perception of how much sleep a child needs was significantly different across the countries, with Australian parents believing their children required more sleep than Canadian parents. These results also showed that perception of sleep need was associated with bedtime as well as TST in the Australian cohort, with the magnitude of the correlations significantly different between countries on weekends. It is unclear why the relationship was found for Australian and not Canadian participants, as sleep education messages regarding optimal sleep in children are consistent across the two countries.34,35 Future research is needed to examine possible factors that may have contributed to these differences, including number of activities children participate in, and/or societal beliefs about the importance of sleep relative to other health behaviors (e.g., diet, exercise). To date, cross-cultural comparisons of sleep in children have been based solely on parental report of usual sleep patterns, which is prone to memory bias and overestimation. Indeed, the comparison between parent-reported TST showed that Australian parents reported significantly longer sleep duration in their children than Canadian parents, but they were also more prone to overestimate sleep duration (Figure 1C). A strength of this Journal of Clinical Sleep Medicine, Vol. 12, No. 5, 2016
study is the use of actigraphy to provide a more objective estimate of sleep/wake patterns. Despite the known limitations of actigraphy,36 the current results are more likely to accurately reflect true sleep patterns. This study is limited in that assessments of cognition and behavior were not included and thus cannot describe any association between short sleep duration, night-to-night variability, and daytime outcomes in these preterm children. In addition, although comparisons were made with data from term born children in the Sleep in America poll, the current study did not contain term controls. These would be important considerations for future research. Another limitation was the global nature of the NSF questions regarding bedtime, wake time and TST. A questionnaire with more specific questions, separating week nights from weekends, would benefit future research. Despite these limitations, this study provides novel data on sleep/wake patterns in a large preterm cohort, and suggests that short sleep duration and irregular sleep schedules are common in children born preterm. In addition, the cross-cultural differences in parental perception of sleep need and the relationship to objective sleep/wake patterns adds substantially to our current state of knowledge. The results from this study provide objective information on which to inform the future clinical management of children born preterm, as well as sleep health educational messages targeting both the perception of sleep need and sleep/wake patterns across two predominantly Caucasian countries. A B B R E V I AT I O N S CAP, Caffeine for Apnea of Prematurity Trial NSF, National Sleep Foundation Sleep in America questionnaire OSA, obstructive sleep apnea PLMS, periodic limb movements of sleep SOL, sleep onset latency SSD, square successive differences TST, total sleep time WASO, wake after sleep onset R E FE R E N CES 1. Gruber R, Laviolette R, Deluca P, Monson E, Cornish K, Carrier J. Short sleep duration is associated with poor performance on IQ measures in healthy school-age children. Sleep Med 2010;11:289–94. 2. Nixon GM, Thompson JM, Han DY, et al. Short sleep duration in middle childhood: risk factors and consequences. Sleep 2008;31:71–8. 3. Paavonen EJ, Raikkonen K, Lahti J, et al. Short sleep duration and behavioral symptoms of attention-deficit/hyperactivity disorder in healthy 7- to 8-year-old children. Pediatrics 2009;123:e857–64. 4. Biggs SN, Lushington K, van den Heuvel CJ, Martin AJ, Kennedy JD. Inconsistent sleep schedules and daytime behavioral difficulties in schoolaged children. Sleep Med 2011;12:780–6. 5. Kelly Y, Kelly J, Sacker A. Changes in bedtime schedules and behavioral difficulties in 7 year old children. Pediatrics 2013;132:e1184–93. 6. Moreira RS, Magalhaes LC, Alves CR. Effect of preterm birth on motor development, behavior, and school performance of school-age children: a systematic review. J Pediatr (Rio J) 2014;90:119–34.
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SN Biggs, LJ Meltzer, IE Tapia et al. Sleep/Wake Patterns in Preterm Children 7. Marcus CL, Meltzer LJ, Roberts RS, et al. Long-term effects of caffeine therapy for apnea of prematurity on sleep at school-age. Am J Respir Crit Care Med 2014;190:791–9 8. Biggs SN, Pizzorno VA, van den Heuvel CJ, Kennedy JD, Martin AJ, Lushington K. Differences in parental attitudes towards sleep and associations with sleep-wake patterns in Caucasian and Southeast Asian school-aged children in Australia. Behav Sleep Med 2010;8:207–18. 9. Hirshkowitz M, Whiton K, Albert SM, et al. National Sleep Foundation’s sleep time duration recommendations: methodology and results summary. Sleep Health 2015;In press. 10. Liu X, Liu L, Owens JA, Kaplan DL. Sleep patterns and sleep problems among schoolchildren in the United States and China. Pediatrics 2005;115:241–9. 11. Mindell JA, Sadeh A, Kwon R, Goh DY. Cross-cultural differences in the sleep of preschool children. Sleep Med 2013;14:1283–9. 12. Owens JA. Introduction: culture and sleep in children. Pediatrics 2005;115:201–3. 13. Tynjala J, Kannas L, Valimaa R. How young Europeans sleep. Health Educ Res 1993;8:69–80. 14. Short MA, Gradisar M, Lack LC, et al. A cross-cultural comparison of sleep duration between US And Australian adolescents: the effect of school start time, parent-set bedtimes, and extracurricular load. Health Educ Behav 2013;40:323–30. 15. Schmidt B, Roberts RS, Davis P, et al. Caffeine therapy for apnea of prematurity. N Engl J Med 2006;354:2112–21. 16. Schmidt B, Roberts RS, Davis P, et al. Long-term effects of caffeine therapy for apnea of prematurity. N Engl J Med 2007;357:1893–902. 17. Marcus CL, Traylor J, Biggs SN, et al. Feasibility of comprehensive, unattended ambulatory polysomnography in school-aged children. J Clin Sleep Med 2014;10:913–8. 18. Hyde M, O’Driscoll DM, Binette S, et al. Validation of actigraphy for determining sleep and wake in children with sleep disordered breathing. J Sleep Res 2007;16:213–6. 19. Meltzer LJ, Walsh CM, Traylor J, Westin AM. Direct comparison of two new actigraphs and polysomnography in children and adolescents. Sleep 2012;35:159–66. 20. Bland JM, Kerry SM. Statistics notes. Weighted comparison of means. BMJ 1998;316:129. 21. Sanchez-Ortuno MM, Carney CE, Edinger JD, Wyatt JK, Harris A. Moving beyond average values: assessing the night-to-night instability of sleep and arousal in DSM-IV-TR insomnia subtypes. Sleep 2011;34:531–9. 22. Jahng S, Wood PK, Trull TJ. Analysis of affective instability in ecological momentary assessment: indices using successive difference and group comparison via multilevel modeling. Psychol Methods 2008;13:354–75. 23. Mindell JA, Meltzer LJ, Carskadon MA, Chervin RD. Developmental aspects of sleep hygiene: findings from the 2004 National Sleep Foundation Sleep in America Poll. Sleep Med 2009;10:771–9. 24. Tabachnick BG, Fidell LS. Using multivariate statistics. 4th ed. Boston, MA: Allyn and Bacon, 2001. 25. Biggs SN, Lushington K, James Martin A, van den Heuvel C, Declan Kennedy J. Gender, socioeconomic, and ethnic differences in sleep patterns in schoolaged children. Sleep Med 2013;14:1304–9. 26. Cho M, Quach J, Anderson P, Mensah F, Wake M, Roberts G. Poor sleep and lower working memory in grade 1 children: cross-sectional, population-based study. Acad Pediatr 2015;15:111–6.
27. Hirshkowitz M, Whiton K, Albert SM, et al. National Sleep Foundation’s sleep time duration recommendations: methodology and results summary. Sleep Health 2015;1:40–3. 28. Iglowstein I, Latal Hajnal B, Molinari L, Largo RH, Jenni OG. Sleep behaviour in preterm children from birth to age 10 years: a longitudinal study. Acta Paediatr 2006;95:1691–3. 29. Keller PS, El-Sheikh M, Buckhalt JA. Children’s attachment to parents and their academic functioning: sleep disruptions as moderators of effects. J Dev Behav Pediatr 2008;29:441–9. 30. Toronto District School Board. Elementary Schools. Accessed November 9, 2015. Available from: http://www.tdsb.on.ca. 31. Victoria State Government. Living in Victoria. Accessed November 9, 2015. Available from: www.liveinvictoria.vic.gov.au. 32. National Research Council Canada. Sunrise/sunset calculator. Accessed February 26, 2015. Available from: http://www.nrc-cnrc.gc.ca/eng/services/ sunrise/. 33. City of Melbourne. Melbourne in numbers. Accessed February 26, 2015. Available from: http://www.melbourne.vic.gov.au/AboutMelbourne/Statistics/ Pages/MelbourneSnapshot.aspx. 34. Canadian Sleep Society. Sleep in Children. Accessed February 26, 2015. Available from: http://css-scs.ca/menu/education-and-information/brochures. 35. Sleep Health Foundation. Sleep need across the lifespan. Accessed February 25, 2015. Available from: http://www.sleephealthfoundation.org.au/fact-sheetsa-z.html. 36. Meltzer LJ, Montgomery-Downs HE, Insana SP, Walsh CM. Use of actigraphy for assessment in pediatric sleep research. Sleep Med Rev 2012;16:463–75.
SUBM I SSI O N & CO R R ESPO NDENCE I NFO R M ATI O N Submitted for publication August, 2015 Submitted in final revised form January, 2016 Accepted for publication January, 2016 Address correspondence to: Dr. Sarah Biggs, The Ritchie Centre, Level 5 Monash Medical Centre, 246 Clayton Road, Clayton, Victoria 3168, Australia; Tel: +61 3 95944759; Fax: +61 3 95946811; Email: [email protected]
D I SCLO S U R E S TAT E M E N T This research was funded by NIH R01 HL098045 and Canadian Institutes of Health Research grant MCT 13288. The Ritchie Centre is supported by the Victorian Government’s Operational Infrastructure Support Program. Phillips Respironics. Inc. provided the actigraphy devices. Dr. Marcus has investigator-initiated research support from Philips Respironics and Ventus. Dr. Mindell has served as a consultant and speaker for Johnson & Johnson. The other authors have indicated no financial conflicts of interest. Author contributions: Dr. Biggs participated in data collection, conducted data analysis for the current manuscript, drafted the initial manuscript, and approved the final manuscript as submitted. Drs. Meltzer, Doyle, Mindell, and Marcus were responsible for the study design, participated in data analysis, commented on drafts of the manuscript and approved the final manuscript as submitted. Drs. Tapia, Traylor, Asztalos, Nixon and Horne were involved in data collection and analysis, commented on drafts of the manuscript, and approved the final version.
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