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The roles of sleep and eating patterns in adiposity gain among
preschool-aged children
Amy R Goetz,1,2 Ishita Jindal,1,3 Jennette P Moreno,1 Maurice R Puyau,1 Anne L Adolph,1 Salma Musaad,1 Nancy F Butte,1
and Fida Bacha1,3
1 Department of Pediatrics, USDA and Agricultural Research Service Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX, USA;
2 Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, USA; and 3 Division of Pediatric Endocrinology and Diabetes,

Texas Children’s Hospital, Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA

ABSTRACT Introduction
Background: Short sleep durations are related to risks for obesity Short sleep duration has been linked to higher BMI z-scores
in preschool children. However, the underlying mechanism or
(BMIz values) and elevated risks for obesity in young children
mechanisms are not clear.
(1–3). Furthermore, sleep duration has received the bulk of
Objectives: We evaluated the relationships between sleep charac-
attention in assessments of risks for obesity, despite being only
teristics and body composition, energetics, and weight-regulating
1 component of sleep. Other dimensions of sleep, such as day-to-
behaviors in preschool-aged children, as well as the longitudinal
day regularity and timing, may impact the energy balance–related
associations between children’s sleep and eating patterns and body
behaviors of young children [e.g., dietary patterns, physical
composition at a 1-year follow-up.
activity (PA)]. Indeed, sleep patterns are maturing as children
Methods: Data were drawn from a longitudinal study of 118 children
aged 3–5 years. Sleep (duration, midpoint, regularity) and physical
transition from multiple sleep periods per day to 1 consolidated
activity (PA) were measured by accelerometry over 6 consecutive sleep period at night. Moreover, the process of phasing out
days; total energy expenditure (TEE) was measured using the daytime naps (4) may contribute to greater variability in sleep
doubly labeled water method; body composition (fat mass, fat-free schedules, as napping results in delayed sleep onset (5); thus,
mass, and percent body fat) was measured by DXA; and dietary there may be greater opportunity for day-to-day shifts in young
intake (energy intake, timing) was measured using two 24-hour children’s sleep. Later sleep timing and greater variability in
recalls. Multivariable regression was used to estimate interindividual sleep patterns may contribute to shorter sleep duration, especially
associations of sleep parameters with body composition, PA, among young children, who often fail to compensate for later
TEE, and dietary outcomes and to examine the relationships bedtimes with later wake times (6–8).
between sleep and dietary behaviors and body composition 1 year It is possible that later sleep timing and greater day-to-day
later. variability in sleep timing may result in the mistiming of sleep
Results: Cross-sectionally, later sleep midpoint is associated with with the endogenous circadian clock, affecting the timing of other
having a greater fat mass (0.33; 95% CI: 0.05, 0.60) and a higher energy balance–related behaviors, including dietary patterns and
percent body fat (0.92; 95% CI: 0.15, 1.70). Later sleep midpoint PA. The misalignment of these behaviors with endogenous
was associated with delayed morning mealtimes (0.51; 95% CI: rhythms may result in metabolic changes and weight gain in
0.28, 0.74) and evening mealtimes (0.41; 95% CI: 0.29, 0.53),
higher nighttime energy intakes (45.6; 95% CI: 19.7, 71.4), and
This work was made possible with grant funding from the USDA and
lower morning energy intakes (−44.8; 95% CI: −72.0, −17.6).
Agricultural Research Service CRIS Awards 6250-5100-054 (to NFB) and
Longitudinally, shorter sleep duration (−0.02; 95% CI: −0.03, 0.00)
3092-5-001-057 (to FB).
and later meal timing (0.83; 95% CI: 0.24, 1.42) were associated with The content is solely the responsibility of the authors and does not
higher percent body fat measurements 1 year later. necessarily represent the official views of the NIH or the USDA and
Conclusions: Shorter sleep duration and later meal timing are Agricultural Research Service.
associated with adiposity gains in preschoolers. Am J Clin Nutr Address correspondence to Fida Bacha (e-mail: fbacha@bcm.edu).
2022;116:1334–1342. Abbreviations: BMIz, BMI z-score; MVPA, moderate to vigorous physical
activity; PA, physical activity; TEE, total energy expenditure.
Keywords: sleep, obesity, physical activity, dietary behaviors, Received February 23, 2022. Accepted for publication July 12, 2022.
First published online July 14, 2022; doi: https://doi.org/10.1093/ajcn/
energy expenditure
nqac197.

1334 Am J Clin Nutr 2022;116:1334–1342. Printed in USA. © The Author(s) 2022. Published by Oxford University Press on behalf of the American
Society for Nutrition. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
Sleep and energetics among preschoolers 1335
children (9). Recent reviews have found that shorter duration is
associated with poorer diets (10) but inconsistently related to PA
in young children (11–13). Among adults, later sleep timing has
been shown to contribute to a higher energy intake, adiposity,

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and having a greater fat mass (14–17). Because children’s eating
patterns (i.e., timing, energy intakes) are in part controlled by
parental influences (e.g., food availability, timing of meals), it is
unknown whether similar associations between later sleep timing
and meal patterns are present among preschool-aged children.
We previously found that shorter sleep duration is associated
with changes in fat mass over a 1-year period in preschool-
aged children. The current study expands upon this previous
observation (18) by considering novel pathways through which
different dimensions of sleep may influence energetics, as well
as the contributions of the timing of children’s sleep and dietary
patterns to changes in adiposity over time. We specifically aimed
to examine the following: 1) the relationships between different
components of sleep (duration, timing, and day-to day regularity)
and children’s body composition; total energy expenditure (TEE),
measured by the doubly labeled water method; PA, measured by
accelerometry; and energy intake and meal timing, measured by
dietary recall; and 2) the longitudinal associations of different
sleep components and dietary patterns with children’s adiposity at FIGURE 1 Flowchart of participant enrollment in the study.
a 1-year follow-up. Our primary hypothesis was that shorter sleep
duration, later sleep timing, and more irregular sleep schedules
would be associated cross-sectionally with having a greater fat family was asked to have the child wear an accelerometer for the
mass and higher percent body fat measurements. Furthermore, week following the visit. The second 24-hour dietary recall was
our secondary hypothesis was that poorer sleep characteristics completed during the week. At the end of the week following the
would be associated with less PA, TEE, higher energy intake, and visit, the urine samples were collected and the accelerometer data
later meal timing. An additional secondary hypothesis was that were downloaded. Children were studied throughout the year.
shorter sleep duration, later sleep timing, and more irregular sleep Thirty-six were studied in the summer, 33 in the winter, 18 in
schedules would relate to greater 1-year increases in fat mass and the spring, and 28 in the fall. One year later, anthropometric and
percent body fat. body composition measures were repeated.

Methods Demographics questionnaire


Study population Data on each child’s age, sex, race and ethnicity, and time spent
in childcare settings were obtained based on the parents’ report.
Healthy children aged 3 to 5 years who were without a major
The mother’s age, height and weight (used to derive maternal
medical illness and living in the greater Houston area were
BMI; kg/m2 ), family income, and number of people living in
recruited into this study. Flyers were posted at local clinics
the home were also reported. The income-to-needs ratio was
and preschool centers, and interested families contacted the
calculated, with values ≤1.0 considered to indicate the household
study team to obtain information on the study opportunity.
was at or below the poverty level (19).
Children who were diagnosed with a chronic disease or had
been prescribed medications that may affect growth or limit
activity were excluded (Figure 1) (18). Preterm children were Anthropometrics and body composition
excluded due to differences in postnatal growth trajectories.
The Institutional Review Board at Baylor College of Medicine Child weight and height were measured using standardized
approved the study protocol, and parents provided written procedures (18). Age- and sex-specific BMIz values and BMI
informed consent to participate in this study. percentiles were calculated using US growth references (20).
Having a healthy weight was defined as having a BMI <85th
percentile and having overweight or obesity was defined as
Procedures having a BMI ≥85th percentile for age and sex (20). The
Parent-child dyads completed baseline and 1-year follow-up fat-free and fat masses were measured using DXA (Delphi-A;
visits in the Children’s Nutrition Research Center Metabolic Hologic).
Research Unit. At baseline, parents completed a demographics
questionnaire and the first of two 24-hour dietary recalls for Sleep and PA
the child. Child anthropometric data were collected and a body Sleep and PA data were collected using the ActiGraph GT3X+
composition assessment was completed. Detailed procedures for accelerometer (ActiGraph LLC) and an Actiheart monitor
collecting urine samples each day over 1 week were described, in (CamNtech Ltd.). The accelerometer was worn on the child’s
order to assess TEE via the doubly labeled water method, and the right hip and the Actiheart was worn on the chest and secured
1336 Goetz et al.

with electrodes. Families were asked to have the child wear both Energy expenditure by doubly labeled water
monitors for 7 days and remove them for bathing and swimming. TEE was measured over a 7-day period using the doubly
During the week of accelerometry data collection, the parents labeled water method and was expressed as kilocalories per day,
completed a sleep log to note the times the child went to bed as described previously (18, 26).

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and woke in the morning, as well as the periods of the day the
device was removed for water-based activities. Upon return, data
from both monitors were downloaded in 1-minute epochs and Statistical analysis plan
analyzed for missing wear time. A day was defined as the time Descriptive statistics, including means (SDs) and frequencies
from sleep onset of 1 day to sleep onset on the next day. A (%), were calculated to describe children’s sleep, energetics, PA,
valid day required ≥1000 minutes of wear time—consistent with and dietary behaviors. Linear relationships between dependent
the criteria described by others (21, 22)—and having complete variables and the residuals, normality, and homogeneity of
data was defined as having ≥4 valid days, including 1 weekend variance were examined. There was no collinearity between
day. The last day of wear was excluded from analyses due to the 3 sleep predictor variables included in the model. Bivariate
incomplete data. Approximately 89% of the sample had 6 days correlations were used to explore the relationships between
of complete data. The average wear time was 1410 ± 35 min/d sleep duration, sleep midpoints, and sleep regularity. Multiple
(range: 1293–1527 min/d). regression was conducted to examine the cross-sectional rela-
Sleep onset, offset, and nap times were identified by the parent- tionships at baseline between all 3 sleep variables and body
completed sleep log, visual inspection of 24-hour daily plots, composition (i.e., fat mass and percent body fat). To better
and the epoch-by-epoch data. Sleep onset was defined as having understand how children’s sleep patterns influence energetics,
≥5 minutes of inactivity (vector magnitude counts at 0) and a we used multiple regression to model the associations between
gradual decline in heart rate, and sleep offset was defined as sleep duration, midpoint, and regularity together with TEE and
an abrupt increase in vector magnitude activity and heart rate. minutes in sedentary, light, and MVPA as separate outcomes.
During visual inspection of the daily plots, we identified and We additionally examined the mean total energy intake, energy
removed periods of nonwear time. Wake after sleep onset was intakes in the morning and night, and the timing of the first and
determined using the Sadeh algorithm (23, 24), which was also last eating events of the day as outcomes in separate models.
used to confirm observations of sleep onset and offset.. The Finally, multiple regression was used to test the longitudinal
sleep duration was defined as the period between sleep onset associations between children’s sleep parameters and dietary
and sleep offset minus wake times after sleep onset. The sleep patterns and body composition (fat mass and percent body fat)
midpoint was defined as the halfway point between sleep onset 1 year later while controlling for baseline fat mass and percent
and sleep offset for the nighttime sleep period. Mean values of body fat in separate models.
sleep duration and midpoints were used in this study. The sleep Age, sex, race and ethnicity, income-to-needs ratio, childcare
regularity index—the probability of being asleep or awake at any attendance, and BMIz data were included as covariates in the
2 times that were 24 hours apart on any 2 consecutive days— above models. Fat-free mass and fat mass were included as
was computed using Python code developed by Avery-Lunsford covariates in place of BMIz in the model that tested TEE as
et al. (25). Values on the sleep regularity index range from 0– the outcome. The accelerometer wear time was controlled for
100, with higher scores indicating more consistent sleep-wake in the analyses of sedentary, light PA, and MVPA times. The
timing. models were tested in Mplus Version 8.1 (Muthen & Muthen)
Minutes spent sedentary, doing light PA, and doing moderate and constructed using full-information maximum likelihood
to vigorous PA (MVPA) were defined according to published estimation.
vector magnitude cut points (26). Similar to the sleep duration Using multiple regression and power conditional on the model
and midpoint values, mean values of the time spent sedentary, R2 , a sample size of 65 was considered to be the minimum
doing light PA, and doing MVPA were calculated. sample size necessary to achieve 80% power to detect an R2 of
0.08 attributed to the 3 independent variables (sleep duration,
midpoints, and regularity) using an F-test with a significance
level (alpha) of 0.05. The models were adjusted for additional
Energy intake and meal timing by dietary recall covariates that increased the explained proportions of variance in
Two 24-hour recalls using the multiple-pass method were the dependent variables.
conducted and analyzed using the Nutrition Data Systems for
Research software (Nutrition Coordinating Center, University
of Minnesota). Parents were queried on their child’s food and
Results
beverage intake. Recalls were analyzed to obtain the average A total of 118 children were included in this study, with a
daily energy consumption and the times of the first and last eating mean ± SD age of 4.6 ± 0.9 years (Table 1). Half were male and
events. Although over-reporting of energy intake has been noted 29% were non-Hispanic white, 29% were non-Hispanic black,
in studies of young children (27), 24-hour dietary recall was 35% were Hispanic, and 7% were of another race and ethnicity.
a more accurate method to estimate energy intake in children The majority were considered to have healthy weight. The mean
compared with the doubly labeled water method (28). Average sleep onset, offset, and midpoint times were at the following times
energy intakes in the morning (06:00 to <10:00) and at night of day: 22:16 (±1:32 hours), 07:42 (±1:20 hours), and 03:01
(19:00 to <06:00) were calculated using defined criteria (29). (±1:18 hours), respectively (Table 2). Nearly 79% of children
Sleep and energetics among preschoolers 1337
TABLE 1 Baseline characteristics for children and families for the total sample and by child age1

3 years (n = 38) 4 years (n = 41) 5 years (n = 39) Total (N = 118)


Age, years 3.6 ± 0.3 4.5 ± 0.3 5.6 ± 0.3 4.6 ± 0.9

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Sex, % male 53% 49% 49% 50%
Race and ethnicity
Non-Hispanic White 18% 37% 31% 29%
Non-Hispanic Black 35% 22% 31% 29%
Hispanic 37% 39% 28% 35%
Other or mixed race 11% 2% 10% 7%
Out of home childcare, % 53% 67% 78% 65%
Daycare, h/wk 18.1 ± 19.5 21.0 ± 18.0 27.2 ± 16.7 22.1 ± 18.3
BMI z-score 0.2 ± 1.0 0.2 ± 1.1 0.2 ± 1.0 0.2 ± 1.0
Weight status, % with 16% 20% 18% 18%
overweight or obesity
Fat-free mass, kg 11.2 ± 1.6 13.4 ± 2.1 15.1 ± 2.6 13.3 ± 2.7
Fat mass, kg 4.8 ± 1.8 5.1 ± 2.2 5.5 ± 2.0 5.1 ± 2.0
Mother’s age, y 34.4 ± 8.2 34.1 ± 6.4 35.7 ± 7.2 34.7 ± 7.3
Maternal BMI, kg/m2 29.9 ± 7.0 27.9 ± 5.5 29.1 ± 7.3 29.9 ± 6.6
Income-to-needs ratio, % 16% 18% 26% 20%
poverty
1 Values are presented as means ± SDs or percentages.

took at least 1 nap and napped, on average, 39 ± 28 minutes. The relationship of children’s sleep patterns with body
One-half of the sample met the National Sleep Foundation (30) composition
recommendations for 10 to 13 hours of sleep based on the time in Age was associated with having a greater fat mass ( B = 0.47;
bed (duration from sleep onset to offset) plus nap duration. Later 95% CI: 0.11, 0.82) but lower percent body fat (−1.3; 95%
sleep midpoints were associated with poorer sleep regularity CI: −2.38, −0.23). At baseline, being female was associated
(r = −0.30; P < 0.05). There was a significant relationship with having a greater fat mass (0.84; 95% CI: 0.28, 1.40) and
between season and sleep onset, such that children studied in a higher percent body fat (5.40; 95% CI: 3.67, 7.13). Relative
the summer had later sleep onset compared to children studied in to white children, black children had a lower fat mass (−1.34;
the fall [F(3,114) = 3.85; P < 0.05], with a significant pairwise 95% CI: −2.23, −0.46) and a lower percent body fat (−5.83;
difference between youth studied during the summer (M = 22:79; 95% CI: 8.25, −3.39), while the fat mass and percent body
SD: 1.91) relative to those who provided sleep data in the fall fat measurements of white and Hispanic children did not differ.
(M = 21:71; SD: 0.99). Later sleep midpoints were associated with having a greater

TABLE 2 Mean sleep parameters, physical activity, energy expenditure, and dietary intake behaviors for the total sample and by child age1

3 years 4 years 5 years Total


n = 38 n = 41 n = 39 N = 118
Sleep
Sleep onset, h:min 22:28 ± 1:29 22:00 ± 1:30 22:24 ± 1:35 22:16 ± 1:32
Sleep midpoint, h:min 3:10 ± 1:18 2:50 ± 1:26 3:06 ± 1:28 3:01 ± 1:18
Sleep offset, h:min 7:49 ± 1:17 7:31 ± 1:23 7:49 ± 1:23 7:42 ± 1:20
Time in bed, min 557.8 ± 54.3 573.3 ± 44.8 566.6 ± 46.5 565.8 ± 48.7
Wake after sleep onset, min 56.5 ± 21.3 57.2 ± 22.4 46.7 ± 19.9 53.5 ± 21.6
Total sleep duration, min 551.2 ± 40.6 543.5 ± 43.4 535.2 ± 41.1 543.4 ± 41.8
Sleep regularity index 65.9 ± 8.5 70.3 ± 7.4 73.7 ± 8.5 69.9 ± 8.7
Physical activity and energy expenditure
Sedentary, min/d 361.7 ± 75.0 369.9 ± 80.4 394.3 ± 56.0 375.2 ± 72.0
Light physical activity, min/d 385.6 ± 64.9 381.8 ± 53.4 381.1 ± 47.9 382.8 ± 55.5
Moderate to vigorous physical 52.8 ± 22.6 54.4 ± 30.0 53.4 ± 22.2 53.5 ± 24.9
activity, min/d
Total energy expenditure, kcal/d 1079 ± 143 1239 ± 176 1277 ± 176 1197 ± 186
Dietary intake
Total energy intake, kcal/d 1360 ± 326 1374 ± 277 1489 ± 316 1405 ± 308
Morning energy intake, kcal/d 294 ± 117 293 ± 116 307 ± 127 299 ± 119
Nighttime energy intake, kcal/d 352 ± 177 387 ± 202 409 ± 233 379 ± 207
Time of first eating event, h:min 8:49 ± 1:58 8:23 ± 1:38 8:31 ± 1:30 8:34 ± 1:38
Time of last eating event, h:min 19:19 ± 1:00 19:04 ± 1:08 19:11 ± 1:04 19:11 ± 1:04
1 Values are presented as means ± SDs.
1338 Goetz et al.

TABLE 3 Parameter estimates for the associations between sleep duration, midpoint, and regularity with body composition at baseline (N = 118)1

Predictors Fat mass, kg Percent body fat


Effect estimate (95% CI)
− 0.03 (−0.06, −0.01)

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Sleep duration, min/d 0.00 (−0.01, 0.01)
Sleep midpoint, hours/d 0.33 (0.05, 0.60)2 0.92 (0.15, 1.70)2
Sleep regularity,3 units 0.00 (−0.04, 0.04) 0.10 (−0.04, 0.24)
1 All regression models were adjusted for age, sex, race and ethnicity, childcare attendance, and income-to-needs ratio, as well as sleep duration,

midpoint, and regularity.


2 P < 0.05
3 The index scores range from 0 to 100, with higher scores reflecting more consistent sleep and wake timing.

fat mass (0.33; 95% CI: 0.05, 0.60) and a higher percent body (45.58; 95% CI: 19.72, 71.43), a lower morning energy intake
fat (0.92; 95% CI: 0.15, 1.70); (Table 3). Sleep duration and (−44.78; 95% CI: −71.97, −17.58), and delayed timing for both
sleep regularity were not associated with measures of body the first (0.51; 95% CI: 0.28, 0.74) and last (0.41; 95% CI: 0.29,
composition. 0.53) eating events in the day. Furthermore, a 1-hour delay in
the sleep midpoint was associated with an estimated consumption
increase of 46 calories at night and with consumption of 45 fewer
The association between children’s sleep patterns and other calories in the morning. Additionally, for every 1-hour delay in
energy balance–related behaviors the sleep midpoint, eating events were delayed by 25–31 minutes.
Shorter sleep duration (−0.71; 95% CI: −1.20, −0.21) Sensitivity analyses were conducted to examine each sleep
and later sleep midpoints (25.00; 95% CI: 9.20, 40.79) were predictor variable with each outcome, excluding mutual adjust-
associated with greater TEE (Table 4). Shorter sleep duration ment for the other sleep variables. Results were unchanged when
(−0.45; 95% CI: −0.69, −0.22) and greater sleep regularity sleep variables were examined in isolation of each other (data not
(2.80; 95% CI: 1.65, 3.95) were associated with more time spent shown). In addition, the sleep onset was substituted for the sleep
doing light PA. For every 1-hour decrease in sleep duration, midpoint in all analyses. The estimates between sleep onset and
an estimated 27 additional minutes was spent doing light PA, outcome variables were comparable to the estimates between the
and a 1-unit increase in sleep regularity was associated with sleep midpoint and these variables. The only variable in which
approximately 2–3 additional minutes of light PA. Later sleep the magnitude of effect decreased was between sleep onset and
midpoints were related to having a higher nighttime energy intake fat mass (0.29; 95% CI: 0.02, 0.56).

TABLE 4 Parameter estimates for the average interindividual associations between sleep duration, midpoint, and regularity with energy expenditure,
physical activity, and dietary intake (N = 118)1

Sleep midpoint,
Outcomes Sleep duration, min/d hours/d Sleep regularity units2
Effect estimate (95% CI)
Total energy expenditure,3 − 0.71 (−1.20, −0.21)4 25.00 (9.20, 40.79)4 2.45 (−0.11, 5.01)
kcal/d
Sedentary time,5 min/d − 0.31 (−0.61, 0.00) − 5.24 (−14.51, 4.02) − 0.52 (−1.99, 0.95)
Light physical activity,5 min/d − 0.45 (−0.69, −0.22)6 4.09 (−2.40, 10.57) 2.80 (1.65, 3.95)4
Moderate to vigorous physical − 0.09 (−0.21, 0.04) 0.30 (−3.69, 4.29) 0.11 (−0.41, 0.33)
activity,5 min/d
Total energy intake, kcal/d − 1.19 (−2.50, 0.11) − 7.70 (−50.19, 34.80) 2.90 (−4.93, 10.74)
Morning energy intake, kcal/d − 0.29 (−0.87, 0.28) − 44.78 (−71.97, −17.58)6 0.24 (−3.14, 3.62)
Nighttime energy intake, − 0.23 (−1.23, 0.78) 45.58 (19.72, 71.43)6 2.33 (−2.41, 7.07)
kcal/d
Time of first eating event, 0.00 (−0.01, 0.01) 0.51 (0.28, 0.74)4 0.02 (−0.01, 0.06)
hours/d
Time of last eating event, − 0.01 (−0.01, 0.00) 0.41 (0.29, 0.53)4 0.00 (−0.02, 0.03)
hours/d
1 Allregression models were adjusted for age, sex, race and ethnicity, childcare attendance, income-to-needs ratio, and BMI z-score, as well as sleep
duration, midpoint, and regularity.
2 The index ranges from 0–100 with higher scores reflecting more consistent sleep and wake timing.
3 Adjusted for fat and fat-free masses but not BMI z-score.
4 P < 0.01.
5 Adjusted for accelerometer wear time.
6 P < 0.05.
Sleep and energetics among preschoolers 1339
TABLE 5 Parameter estimates for the longitudinal associations between sleep, dietary patterns, and body composition (N = 116)1

Predictors Fat mass, kg Percent body fat


Effect estimate (95% CI)

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Baseline fat mass, kg 1.21 (1.12, 1.30)2 —
Baseline percent body fat — 0.97 (0.89, 1.04)2
Sleep duration, min/d − 0.04 (−0.09, 0.00) − 0.02 (−0.03, 0.00)3
Sleep midpoint, hours/d − 0.04 (−0.19, 0.10) − 0.23 (−0.69, 0.23)
Sleep regularity,4 units 0.01 (−0.01, 0.02) 0.03 (−0.03, 0.08)
Total Energy Intake, kcal/d 0.00 (−0.01, 0.00) 0.01 (−0.01, 0.03)
Morning Energy Intake, kcal/d 0.00 (−0.02, 0.02) − 0.03 (−0.09, 0.03)
Nighttime Energy Intake, kcal/d 0.00 (−0.01, 0.01) − 0.01 (−0.04, 0.02)
Time of First Eating Event, hours/d − 0.01 (−0.14, 0.11) − 0.12 (−0.50, 0.27)
Time of Last Eating Event, hours/d 0.17 (0.02, 0.33) 0.83 (0.24, 1.42)∗
1 Allregression models were adjusted for age, sex, race and ethnicity, childcare attendance, and income-to-needs ratio.
2P < 0.01.
3 P < 0.05.
4 The index scores range from 0 to 100, with higher scores reflecting more consistent sleep and wake timing.

The longitudinal relationship of children’s sleep and dietary sleep midpoints were not associated with higher overall energy
patterns to body composition intakes. Though we cannot discern the directionality of these
When examining the longitudinal associations between chil- relationships, these cross-sectional findings underscore the inter-
dren’s sleep and dietary patterns and body composition, only the relatedness of sleep midpoints and the timing of eating behaviors
fat mass at baseline was associated with the fat mass 1 year later (31–34).
(1.21; 95% CI: 1.12, 1.30; Table 5). In a similar model with Later bedtimes have been correlated with breakfast skipping
percent body fat as the dependent variable, shorter sleep duration (35, 36), delayed meals (37), and higher evening energy
(−0.02; 95% CI: −0.03, 0.00) and later timing of the last meal consumption (37) in children. Several studies have reported
of the day (0.83; 95% CI: 0.24, 1.42) at baseline independently that having a higher energy intake later in the day—as a
contributed to percent body fat measurements 1 year later. proportion of total energy intake—is related to having a higher
body fat percentage (38) and to prospective increases in BMIz
values (39). The additional time awake in the evening due to
Discussion later bedtimes likely provides more opportunities to eat, as
The current study examined pathways through which the was observed when children’s energy intakes were compared
duration, timing, and regularity of preschoolers sleep patterns between conditions of sleep restriction and sleep extension
may be related to the risks for childhood obesity. Cross- (40).
sectionally, later sleep timing was associated with adiposity Though the exact mechanisms through which sleep and meal
(fat mass and percent body fat); longitudinally, both shorter timing in the absence of increased total energy intake are
sleep duration and later meal timing were associated with related to adiposity gains is beyond the scope of the current
greater adiposity 1 year later. These results are consistent study, we speculate that chronodisruption (i.e., the misalignment
with those previously observed by our research group (24). between the behavioral rhythms of sleep and meal patterns with
Sleep midpoints and regularity did not account for unique endogenous circadian rhythms) may explain these associations
variance in change in children’s adiposity, although we found (9, 14, 41–43). Eating later in the biological day may lead
an association between meal timing and percent body fat 1 year to changes in metabolism, resulting in exposure to higher
later. evening blood glucose levels, with effects persisting through
The current study sought to expand upon our understanding the next morning (44, 45). This may affect substrate utilization.
of the relationship between sleep and adiposity by examining Furthermore, diet-induced thermogenesis has been shown to
multiple dimensions of sleep behavior. We first explored the be lower after later eating events (14, 46–49), suggesting that
connections between sleep duration, sleep timing, and sleep eating later may contribute to greater weight gain; however,
regularity [as assessed by the sleep regularity index (35)]. Later these relationships have only been delineated in adults. Overall,
sleep midpoints were related to lower sleep regularity. In addition, the mechanisms through which shorter sleep and later meal
we observed that later sleep midpoints were linked with greater timing affect adiposity among preschoolers is in need of further
nighttime and lower morning energy intakes, as well as delayed research.
timing of both the first and last eating occasions of the day. Interestingly, shorter sleep duration was associated with
Furthermore, the relationships between sleep midpoints and eat- greater TEE and more time spent doing light PA. While this may
ing behaviors demonstrated the largest effect sizes in the current be due to time reallocation (i.e., the additional time awake may
study. Other relationships, such as the association between sleep account for the higher energy expenditure), it is also possible that
regularity and doing light PA, while statistically significant, may sleep restriction elevates energy expenditure through increased
not be clinically meaningful. Interestingly, meal patterns were PA (50–52). In our recent work with youth, shorter sleep duration
not associated with sleep duration or sleep regularity, and later was similarly associated with higher activity energy expenditure
1340 Goetz et al.

by doubly labeled water (24). However, sleep duration was compared to those studied during the fall. However, only one-
positively related to basal metabolic rates (BMRs; i.e., the third of children were studied in the summer, so it is unlikely
major component of energy expenditure) evaluated by room that seasonality is the only driver of the late sleep onset times
calorimetry, such that shorter sleep duration was associated with observed here. Although half of our sample met sleep duration

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having lower BMRs. Though the BMR was not assessed here, recommendations based on accelerometry, the mean total sleep
its relationship with sleep offers 1 possibility for the association duration does appear comparable to other actigraphy estimates
between shorter sleep duration and greater weight gain. Future obtained for preschoolers (63, 65). Finally, while gold-standard
studies should examine the impact of sleep duration on BMR, assessments of dietary intake were utilized, these relied on parent
and its impact on body composition. reports, which are prone to error (28, 67). This may have limited
In comparison, we found that sleep regularity was associated our ability to fully understand the impacts of eating patterns on
with more time spent doing light PA. The sleep regularity index adiposity gains.
is a novel measure used to characterize the consistency of sleep- In summary, among healthy preschoolers, later sleep timing
wake schedules (25, 53–57). Greater intraindividual variability was associated with increased adiposity cross-sectionally. Addi-
in children’s sleep duration—a similar but distinct construct tionally, going to bed later portended having a higher nighttime
to sleep regularity—was related to greater energy, fat, and energy intake, lower morning energy intake, and delayed timing
carbohydrate intakes (58) and consumption of sugar-sweetened of both the first and last eating occasions of the day. Moreover,
beverages (59). In the current study, more consistent sleep greater sleep regularity is linked to more time spent doing light
patterns were associated with greater engagement in light PA, PA. Longitudinally, shorter sleep duration and later meal timing
which parallels the positive associations between sleep regularity were associated with having a higher percent body fat 1 year later.
and PA in older adults (25) and school-aged children (60). Overall, our findings suggest that earlier bedtimes may promote
Furthermore, in older adults, sleep irregularity correlated with earlier meal timings, which may be protective of adiposity gain.
10-year risks of obesity, cardiometabolic disease, and dysg- Taken together, these results suggest promoting specific sleep
lycemia (25). patterns (e.g., adequate duration, earlier bedtimes to ensure the
The strengths of this study include its robust measurements optimal timing of food intake) is of critical importance for obesity
and the recruitment of families from diverse backgrounds. In prevention efforts and is worthy of further research.
addition, we embraced a multidimensional approach to sleep The authors’ responsibilities were as follows—ARG: analyzed the data
health by studying 3 sleep characteristics in tandem. To this end, and wrote the first draft of the manuscript; IJ: contributed to the data
we calculated the novel sleep regularity index, a measure of day- analyses and writing of the first draft of the manuscript; NFB, MRP, and
to-day consistency of sleep-wake timing. Although this metric ALA: conducted the research; JPM: contributed to the data interpretation,
has not been validated with preschoolers, it allowed us to account conceptual development of the research question, and writing of the
for daytime napping and address the variability in sleep schedules manuscript; MRP and SM: contributed to the data analyses; FB: designed
inherent within this developmental period. A limitation of this the research, oversaw the analysis plan and data interpretation, contributed to
writing and editing of the manuscript, and had primary responsibility for the
work is that our analyses were conducted from the standpoint that
final content; and all authors; read and approved the final manuscript.
poor sleep promotes obesogenic behaviors, which ultimately lead Author disclosures: JPM receives support from the Eunice Kennedy
to greater weight gain. The reverse pattern of weight influencing Shriver National Institute of Child Health & Human Development of the NIH
sleep and relevant behaviors is equally important to consider. (R00 HD091396). FB and NB report funding from the USDA/ Agricultural
Second, our data are limited to a select sample of preschoolers, Research Services (FB and NB). FB received funding from AstraZeneca and
and research is needed to understand the generalizability of these Takeda through her institution for research not related to this work. All other
findings. Third, it is possible that the use of a 1-minute epoch authors report no conflicts of interest.
influenced the allocation of times spent in different levels of
PA intensity. The use of a longer epoch may have incorrectly Data Availability
classified youth as participating in light PA while actually Data described in the manuscript, code book, and analytic code
engaged in short bouts of MVPA. That said, a 1-minute epoch will be made available upon request pending application and
has been validated in preschoolers when comparing actigraphy approval.
to videosomnography (61). Fourth, residual confounding may
account for some of the observed relationships. While we References
controlled for several important covariates, there are many factors 1. Patel SR, Hu FB. Short sleep duration and weight gain: a systematic
(e.g., bedroom environment, food availability) that may be review. Obesity (Silver Spring) 2008;16(3):643–53.
2. Fatima Y, Doi S, Mamun A. Longitudinal impact of sleep on overweight
implicated in the relationships between sleep, PA, and eating and obesity in children and adolescents: a systematic review and bias-
behaviors that warrant rigorous statistical controls. In addition, adjusted meta-analysis. Obes Rev 2015;16(2):137–49.
we conducted a large number of statistical tests, which may have 3. Miller MA, Kruisbrink M, Wallace J, Ji C, Cappuccio FP. Sleep
inflated our type 1 error rate. Fifth, the average sleep onset time duration and incidence of obesity in infants, children, and adolescents:
a systematic review and meta-analysis of prospective studies. Sleep
of our sample was later, and SDs were larger, than those of 2018;41(4):zsy018.
estimates obtained by parent reports (62) or accelerometry (63– 4. Galland BC, Taylor BJ, Elder DE, Herbison P. Normal sleep patterns in
65) in other preschool samples, though our mean was consistent infants and children: a systematic review of observational studies. Sleep
with at least 1 study that used accelerometry (66). We did find Med Rev 2012;16(3):213–22.
5. Thorpe K, Staton S, Sawyer E, Pattinson C, Haden C, Smith S. Napping,
a significant relationship between season and sleep onset, such development and health from 0 to 5 years: a systematic review. Arch Dis
that children studied during summer had later sleep onset times Child 2015;100(7):615–22.
Sleep and energetics among preschoolers 1341
6. Nixon GM, Thompson JM, Han DY, Becroft DM, Clark PM, Robinson method of doubly labeled water. J Am Diet Assoc 2010;110(10):1501–
E, et al. Short sleep duration in middle childhood: risk factors and 10.
consequences. Sleep 2008;31(1):71–8. 29. McDonald L, Wardle J, Llewellyn CH, Johnson L, van Jaarsveld
7. Moreno JP, Razjouyan J, Lester H, Dadabhoy H, Amirmazaheri CH, Syrad H, et al. Sleep and nighttime energy consumption in
M, Reesor-Oyer L, et al. Later sleep timing predicts accelerated early childhood: a population-based cohort study. Pediatr Obes

Downloaded from https://academic.oup.com/ajcn/article/116/5/1334/6643558 by Mahidol University, Faculty of Medicine, Ramathibodi Hospital user on 15 January 2023
summer weight gain among elementary school children: a prospective 2015;10(6):454–60.
observational study. Int J Behav Nutr Phys Act 2021;18(1):94. 30. Hirshkowitz M, Whiton K, Albert SM, Alessi C, Bruni O,
8. Wickersham L. Time-of-day preference for preschool-aged children. DonCarlos L, et al. National Sleep Foundation’s sleep time duration
Chrestomathy 2006;5:259–68. recommendations: methodology and results summary. Sleep Health
9. Moreno JP, Crowley SJ, Alfano CA, Hannay KM, Thompson D, 2015;1(1):40–3.
Baranowski T. Potential circadian and circannual rhythm contributions 31. Golley RK, Maher C, Matricciani L, Olds T. Sleep duration or bedtime?
to the obesity epidemic in elementary school age children. Int J Behav Exploring the association between sleep timing behaviour, diet and BMI
Nutr Phys Act 2019;16(1):25. in children and adolescents. Int J Obes 2013;37(4):546–51.
10. Ward AL, Reynolds AN, Kuroko S, Fangupo LJ, Galland BC, Taylor 32. Arora T, Taheri S. Associations among late chronotype, body mass
RW. Bidirectional associations between sleep and dietary intake in 0– index and dietary behaviors in young adolescents. Int J Obes
5 year old children: a systematic review with evidence mapping. Sleep 2015;39(1):39–44.
Med Rev 2020;49:101231. 33. Jansen EC, Peterson KE, Lumeng JC, Kaciroti N, LeBourgeois MK,
11. Kreitsch KN, Chardon ML, Beebe DW, Janicke DM. Sleep and weight- Chen K, et al. Associations between sleep and dietary patterns
related factors in youth: a systematic review of recent studies. Sleep among low-income children attending preschool. J Acad Nutr Diet
Med Rev 2019;(46):87–96. 2019;119(7):1176–87.
12. Janssen X, Martin A, Hughes AR, Hill CM, Kotronoulas G, Hesketh 34. Honkala S, Behbehani JM, Honkala E. Daily consumption of sugary
KR. Associations of screen time, sedentary time and physical activity drinks and foods as a behavioural risk for health of adolescents in
with sleep in under 5s: a systematic review and meta-analysis. Sleep Kuwait. Oral Health Prev Dent 2012;10(2):113–22.
Med Rev 2020;49:101226. 35. Yaginuma S, Sakuraba K, Kadoya H, Koibuchi E, Matsukawa T,
13. Antczak D, Lonsdale C, Lee J, Hilland T, Duncan MJ, del Pozo Ito H, et al. Early bedtime associated with the salutary breakfast
Cruz B, et al. Physical activity and sleep are inconsistently related in intake in Japanese nursery school children. Int Med J 2015;22(1):
healthy children: a systematic review and meta-analysis. Sleep Med Rev 30–2.
2020;(51):101278. 36. Thivel D, Isacco L, Aucouturier J, Pereira B, Lazaar N, Ratel S,
14. McHill AW, Phillips AJ, Czeisler CA, Keating L, Yee K, Barger LK, et al. Bedtime and sleep timing but not sleep duration are associated
et al. Later circadian timing of food intake is associated with increased with eating habits in primary school children. J Dev Behav Pediatr
body fat. Am J Clin Nutr 2017;106(5):1213–9. 2015;36(3):158–65.
15. McHill AW, Wright KP Jr. Role of sleep and circadian disruption on 37. Spaeth AM, Hawley NL, Raynor HA, Jelalian E, Greer A, Crouter SE,
energy expenditure and in metabolic predisposition to human obesity et al. Sleep, energy balance, and meal timing in school-aged children.
and metabolic disease. Obes Rev 2017;18(Suppl 1):15–24. Sleep Med 2019;60:139–44.
16. Thomas EA, Zaman A, Cornier MA, Catenacci VA, Tussey EJ, Grau 38. Maffeis C, Provera S, Filippi L, Sidoti G, Schena S, Pinelli L, et al.
L, et al. Later meal and sleep timing predicts higher percent body fat. Distribution of food intake as a risk factor for childhood obesity. Int J
Nutrients 2020;13(1):73. Obes 2000;24(1):75–80.
17. St-Onge MP, Pizinger T, Kovtun K, RoyChoudhury A. Sleep and meal 39. Thompson O, Ballew C, Resnicow K, Gillespie C, Must A, Bandini L,
timing influence food intake and its hormonal regulation in healthy et al. Dietary pattern as a predictor of change in BMI z-score among
adults with overweight/obesity. Eur J Clin Nutr 2019;72(S1):76–82. girls. Int J Obes 2006;30(1):176–82.
18. Butte NF, Puyau MR, Wilson TA, Liu Y, Wong WW, Adolph AL, 40. Hart CN, Carskadon MA, Considine RV, Fava JL, Lawton J, Raynor
Zakeri IF. Role of physical activity and sleep duration in growth and HA, et al. Changes in children’s sleep duration on food intake, weight,
body composition of preschool-aged children. Obesity (Silver Spring) and leptin. Pediatrics 2013;132(6):e1473–80.
2016;24(6):1328–35. 41. Bray MS, Young ME. Circadian rhythms in the development of obesity:
19. El-Sheikh M, Bagley EJ, Keiley M, Elmore-Staton L, Chen E, Buckhalt potential role for the circadian clock within the adipocyte. Obes Rev
JA. Economic adversity and children’s sleep problems: multiple 2007;8(2):169–81.
indicators and moderation of effects. Health Psychol 2013;32(8):849. 42. Bray MS, Young ME. Chronobiological effects on obesity. Curr Obes
20. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Rep 2012;1(1):9–15.
Wei R, et al. CDC growth charts: United States. Adv Data 2000;314:1– 43. Coomans CP, Lucassen EA, Kooijman S, Fifel K, Deboer T, Rensen PC,
27. et al. Plasticity of circadian clocks and consequences for metabolism.
21. Graef DM, Janicke DM, McCrae CS. Sleep patterns of a primarily Diabetes, Obesity & Metabolism 2015;17(Suppl 1):65–75.
obese sample of treatment-seeking children. J Clin Sleep Med 44. Leung GKW, Huggins CE, Bonham MP. Effect of meal timing
2014;10(10):1111–7. on postprandial glucose responses to a low glycemic index meal:
22. Krietsch KN, Armstrong B, McCrae CS, Janicke DM. Temporal a crossover trial in healthy volunteers. Clin Nutr 2019;38(1):
associations between sleep and physical activity among 465–71.
overweight/obese youth. J Pediatr Psychol 2016;41(6):680–91. 45. Tsuchida Y, Hata S, Sone Y. Effects of a late supper on digestion and the
23. Sadeh A, Sharkey M, Carskadon MA. Activity-based sleep-wake absorption of dietary carbohydrates in the following morning. J Physiol
identification: an empirical test of methodological issues. Sleep Anthropol 2013;32(1):9.
1994;17(3):201–7. 46. Bo S, Fadda M, Castiglione A, Ciccone G, De Francesco A, Fedele D,
24. Jindal I, Puyau M, Adolph A, Butte N, Musaad S, Bacha F. The et al. Is the timing of caloric intake associated with variation in diet-
relationship of sleep duration and quality to energy expenditure and induced thermogenesis and in the metabolic pattern? A randomized
physical activity in children. Pediatr Obes 2021;16(6):e12751. cross-over study. Int J Obes 2015;39(12):1689–95.
25. Lunsford-Avery JR, Engelhard MM, Navar AM, Kollins SH. Validation 47. McHill AW, Melanson EL, Higgins J, Connick E, Moehlman TM,
of the sleep regularity index in older adults and associations with Stothard ER, et al. Impact of circadian misalignment on energy
cardiometabolic risk. Sci Rep 2018;8(1):14158. metabolism during simulated nightshift work. Proc Natl Acad Sci
26. Butte NF, Wong WW, Lee JS, Adolph AL, Puyau MR, Zakeri IF. 2014;111(48):17302–7.
Prediction of energy expenditure and physical activity in preschoolers. 48. Morris CJ, Garcia JI, Myers S, Yang JN, Trienekens N, Scheer FA.
Med Sci Sports Exerc 2014;46(6):1216. The human circadian system has a dominating role in causing the
27. Fisher JO, Butte NF, Mendoza PM, Wilson TA, Hodges EA, Reidy KC, morning/evening difference in diet-induced thermogenesis. Obesity
et al. Overestimation of infant and toddler energy intake by 24-h recall 2015;23(10):2053–8.
compared with weighed food records. J Clin Nutr 2008;88(2):407–15. 49. Romon M, Edme JL, Boulenguez C, Lescroart JL, Frimat P.
28. Burrows TL, Martin RJ, Collins CE. A systematic review of the validity Circadian variation of diet-induced thermogenesis. Am J Clin Nutr
of dietary assessment methods in children when compared with the 1993;57(4):476–80.
1342 Goetz et al.

50. Klingenberg L, Chaput J-P, Holmbäck U, Jennum P, Astrup A, Sjödin is associated with caloric intake in adolescents. Sleep Med
A. Sleep restriction is not associated with a positive energy balance in 2015;16(7):856–61.
adolescent boys. Am J Clin Nutr 2012;96(2):240–8. 59. Kjeldsen JS, Hjorth MF, Andersen R, Michaelsen KF, Tetens I, Astrup
51. Patterson RE, Emond JA, Natarajan L, Wesseling-Perry K, Kolonel LN, A, et al. Short sleep duration and large variability in sleep duration are
Jardack P, et al. Short sleep duration is associated with higher energy independently associated with dietary risk factors for obesity in Danish

Downloaded from https://academic.oup.com/ajcn/article/116/5/1334/6643558 by Mahidol University, Faculty of Medicine, Ramathibodi Hospital user on 15 January 2023
intake and expenditure among African-American and non-Hispanic school children. Int J Obes 2014;38(1):32–9.
white adults. J Nutr 2014;144(4):461–6. 60. Stone MR, Stevens D, Faulkner GE. Maintaining recommended sleep
52. McNeil J, Doucet É, Brunet J-F, Hintze LJ, Chaumont I, Langlois throughout the week is associated with increased physical activity in
É, et al. The effects of sleep restriction and altered sleep timing children. Prev Med 2013;56(2):112–7.
on energy intake and energy expenditure. Physiol Behav 2016;164: 61. Sitnick SL, Goodlin-Jones BL, Anders TF. The use of actigraphy to
157–63. study sleep disorders in preschoolers: some concerns about detection of
53. Li A, Chen S, Quan SF, Silva GE, Ackerman C, Powers LS, et al. Sleep nighttime awakenings. Sleep 2008;31(3):395.
patterns and sleep deprivation recorded by actigraphy in 4th-grade and 62. Mindell JA, Sadeh A, Kwon R, Goh DY. Cross-cultural differences
5th-grade students. Sleep Med 2020;67:191–9. in the sleep of preschool children. Sleep Med 2013;14(12):
54. Phillips AJ, Clerx WM, O’Brien CS, Sano A, Barger LK, Picard RW, 1283–9.
et al. Irregular sleep/wake patterns are associated with poorer academic 63. Kahn M, Schnabel O, Gradisar M, Rozen GS, Slone M, Atzaba-Poria N,
performance and delayed circadian and sleep/wake timing. Sci Rep et al. Sleep, screen time and behaviour problems in preschool children:
2017;7(1):3216. an actigraphy study. Eur Child Adolesc Psychiatry 2020;(30):1793–
55. Carskadon MA, Chappell KR, Barker DH, Hart AC, Dwyer K, Gredvig- 802.
Ardito C, et al. A pilot prospective study of sleep patterns and DNA 64. Goodlin-Jones BL, Tang K, Liu J, Anders TF. Sleep patterns in
methylation-characterized epigenetic aging in young adults. BMC Res preschool-age children with autism, developmental delay, and typical
Notes 2019;12(1):583. development. J Am Acad Child Adolesc Psychiatry 2008;47(8):930–8.
56. Murray JM, Phillips AJ, Magee M, Sletten TL, Gordon C, Lovato 65. Iwasaki M, Iwata S, Iemura A, Yamashita N, Tomino Y, Anme T,
N, et al. Sleep regularity is associated with sleep-wake and circadian et al. Utility of subjective sleep assessment tools for healthy preschool
timing, and mediates daytime function in Delayed Sleep-Wake Phase children: a comparative study between sleep logs, questionnaires, and
Disorder. Sleep Med 2019;58:93–101. actigraphy. J Epidemiol 2010;20(2):143–9.
57. Brooks AT, Raju S, Barb JJ, Kazmi N, Chakravorty S, Krumlauf 66. Lam JC, Mahone EM, Mason TB, Scharf SM. Defining the roles of
M, et al. Sleep regularity index in patients with alcohol dependence: actigraphy and parent logs for assessing sleep variables in preschool
daytime napping and mood disorders as correlates of interest. Int J children. Behav Sleep Med 2011;9(3):184–93.
Environ Res Public Health 2020;17(1):331. 67. Wallace A, Kirkpatrick SI, Darlington G, Haines J. Accuracy of
58. He F, Bixler EO, Berg A, Kawasawa YI, Vgontzas AN, Fernandez- parental reporting of preschoolers’ dietary intake using an online self-
Mendoza J, et al. Habitual sleep variability, not sleep duration, administered 24-h recall. Nutrients 2018;10(8):987.

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