Long sleep duration and childhood overweight/obesity and body fat.
ABSTRACT To assess the association between short sleep duration and overweight/obesity and body fat (BF) and to identify correlates of short sleep duration in a sample of Portuguese children. A cross-sectional study of children 7-9 years (n = 4511) was performed between October 2002 and June 2003. Weight, height, and skinfolds were measured, and parents filled out a questionnaire about family characteristics as well as sleep duration. The prevalence of overweight/obesity and BF (%) both decreased by long sleep duration. After adjusted for confounders, the odds ratio (OR) for overweight/obesity and sleep duration were as follows: reference >11 h/d; 10-11 h/d, OR: 1.3; confidence interval (CI):1.26, 1.33; 9-10 h/d, OR: 1.16; CI: 1.13, 1.19; and <9 h, OR: 3.22; CI: 3.11, 3.32. Children whose parents had a low educational level slept less time during each night than children whose parents had a higher educational level; children who spent more time watching television slept less time than those who watched less television, and those children engaged in physical activity slept more time each night than sedentary children. Our results showed an inverse relationship between long sleep duration and overweight/obesity prevalence as well as with body fat, and these findings are important because sleep duration is a potentially modifiable risk factor that could be important to consider in the prevention and treatment of childhood obesity.
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ABSTRACT: Evidence has shown correlations between obesity and sleep in children. The purpose of this review was to identify sleep interventions that could be utilized in primary care settings to prevent obesity in children. Results Three themes emerged: bedtime routines and environment; parental presence and graduated extinction; and health education. Effective strategies to improve sleep in children include consistent bedtime routine and self-soothing. Conclusion Health care professionals can provide innovative and prevention-based sleep education for parents early in a child’s development. Education, related to sleep, and appropriate sleep strategies may help prevent obesity and its long-term consequences.Journal of Pediatric Nursing 09/2014; · 0.92 Impact Factor
- The Journal of Behavioral Health. 01/2014; 3(3):156-160.
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ABSTRACT: There are widespread differences in overweight/obesity prevalence in children, and understanding the reasons for this is very important. The present study aims: (I) to conduct a meta-analysis on overweight/obesity prevalence in Portuguese children; (II) to identify differences in biological and behavioural characteristics between normal-weight and overweight/obese children; and (III) to investigate the importance of individual- and school-level correlates of variation in children's BMI using multilevel modelling. A search was done for all published papers including Portuguese children during the last decade; further, 686 Portuguese children (9-11 years old) were sampled and their BMI, family income, maturity offset, nutritional habits, physical activity, sedentariness, sleep time, and school environment information were collected. Results showed a stabilization of overweight/obesity during the last decade, 30.6% (95%CI: 0.287-0.34) for boys, 28.4% (95%CI: 0.23-0.35) for girls, and 30.3% (95%CI: 0.27-0.34) for boys and girls together. Differences between weight groups were only found in individual-level biological traits. The multilevel analysis did not identify significant contributions of school-level variables to children's BMI variation. In conclusion, no increase was found in the prevalence of overweight/obesity among Portuguese children since 2000. Normal-weight and overweight/obese children only differ in individual-level characteristics, and school context variables were not related to variation in BMI.International Journal of Environmental Research and Public Health 11/2014; 11(11):11398-417. · 1.99 Impact Factor
Original Research Article
Long Sleep Duration and Childhood Overweight/Obesity and Body Fat
CRISTINA PADEZ,1*ISABEL MOURAO,2PEDRO MOREIRA,3AND VITOR ROSADO4
1Department of Anthropology, Research Centre for Anthropology and Health, University of Coimbra, Coimbra, Portugal
2Department of Sports, University of Tras-os-Montes e Alto Douro, Portugal
3Faculty of Nutrition, University of Porto, Porto, Portugal
4Instituto Investigacao Cientifica Tropical, Lisboa, Portugal
identify correlates of short sleep duration in a sample of Portuguese children. A cross-sectional study of children 7–9 years
(n 5 4511) was performed between October 2002 and June 2003. Weight, height, and skinfolds were measured, and
parents filled out a questionnaire about family characteristics as well as sleep duration. The prevalence of overweight/obe-
sity and BF (%) both decreased by long sleep duration. After adjusted for confounders, the odds ratio (OR) for overweight/
obesity and sleep duration were as follows: reference >11 h/d; 10–11 h/d, OR: 1.3; confidence interval (CI):1.26, 1.33; 9–10
h/d, OR: 1.16; CI: 1.13, 1.19; and <9 h, OR: 3.22; CI: 3.11, 3.32. Children whose parents’ had a low educational level slept
less time during each night than children whose parents’ had a higher educational level; children who spent more time
watching television slept less time than those who watched less television, and those children engaged in physical activity
slept more time each night than sedentary children. Our results showed an inverse relationship between long sleep dura-
tion and overweight/obesity prevalence as well as with body fat, and these findings are important because sleep duration
is a potentially modifiable risk factor that could be important to consider in the prevention and treatment of childhood
obesity. Am. J. Hum. Biol. 21:371–376, 2009.
' 2009 Wiley-Liss, Inc.
To assess the association between short sleep duration and overweight/obesity and body fat (BF) and to
The prevalence of childhood obesity is rising rapidly
and has already raised concern in Europe, North and
South America, and more recently in other parts of the
world such as in developing countries (Wang and Lob-
stein, 2006; WHO, 2000).
Obesity in childhood is associated with adverse out-
comes such as hypertension, dyslipidaemia, chronic
inflammation, hyperinsulinaemia, orthopedic problems
(Ebbeling et al., 2002), as well as substantial psychosocial
consequences (Hill and Silver, 1995; Strauss, 2000).
Obesity is a multifactorial problem and its development
is due to multiple interactions between genes and environ-
ment (Maffeis, 2000). Risk factors for childhood obesity
include genetic factors (Hebebrand et al., 2000), the level of
parental obesity, socioeconomic status, birth weight, pat-
terns of physical activity and diet (Agras et al., 2004).
Many studies have focused on lifestyle factors in the devel-
opment of childhood obesity to clarify the causes of this cur-
rent epidemic for a better public health approaches. Among
these factors, recently, some studies showed that sleep du-
ration seems to be important in the regulation of body
weight and metabolism. Some works have focused on the
association between short sleeping hours and childhood
obesity (Biggs and Dollman, 2007; Chaput et al., 2006;
Eisenmann et al., 2006; Locard et al., 1992; Lumeng et al.,
2007; Nixon et al., 2008; Sekine et al., 2002; von Kries
et al., 2002) and with abdominal adiposity in children
(Chaput and Trembley, 2007). Recently, in a sample of Chi-
nese adolescents, Yu et al. (2007) showed that the observed
association between sleep duration and body mass index
(BMI) is largely due to adiposity. Two meta-analysis (Cap-
puccio et al., 2008; Chen et al., 2008) and a systematic
review paper (Patel and Hu, 2008) showed a consistent
increased risk of obesity among short sleepers in children.
Up to now, few studies related child behavior such
as television viewing and physical activity with sleep
duration, as well as, parental education with child sleep
duration. Many adverse effects of television viewing on
children and adolescents have been studied, including
obesity (Robinson, 1999), aggressive behavior (Comstock
and Strasburger, 1990; Johnson et al., 2002; Ozmert et al.,
2002; Singer et al., 1998), decreased physical activity
(DuRant et al., 1994), attention problems (Christakis
et al., 2004), and sleep disorders (Johnson et al., 2004;
Owens et al., 1999; Thompson and Christakis 2005; Tyn-
jala et al., 1993). Only three studies related television
viewing with sleep duration (Adam et al., 2007; Owens
et al., 1999; van den Bulck, 2004).
The aim of this study was to examine whether an associ-
ation between short sleep duration, overweight/obesity
and body fat (BF) (%) exists in a sample of Portuguese
children. Our study provides new clues by introducing
new elements such as: the association of some family and
lifestyle factors such as TV viewing, physical activity,
parent’s educational level, and sleep duration. Based on
the reported association between sleep duration and obe-
sity and some indications of the effect of lifestyle factors
on sleep duration, we hypothesized that these lifestyle fac-
tors such as TV viewing, physical activity, and parental
education would be associated with sleep duration.
This work was done using the data from the first
national survey in Portugal to evaluate the prevalence of
Contract grant sponsor: Fundac ¸a ˜o Cio ˜ncia e Tecnologia; Contract grant
*Correspondence to: Cristina Padez, Department of Anthropology, Uni-
versity of Coimbra, Rua Arco da Traic ¸a ˜o, 3030-056 Coimbra, Portugal.
Received 2 April 2008; Revision received 4 November 2008; Accepted 10
Published online 2 February 2009 in Wiley InterScience (www.interscience.
AMERICAN JOURNAL OF HUMAN BIOLOGY 21:371–376 (2009)
C2009 Wiley-Liss, Inc.
childhood overweight and obesity and the influence of
sociodemographic factors on it.
The study was carried out from October 2002 to June
2003 and a sample of 7- to 9-year-old children was
Subjects were selected from the population of children
attending public schools. Schools were randomly selected
in the districts, and from each of them the participating
children were selected using stratified randomization for
age, with the aid of a table of random numbers. All chil-
dren of 7- to 9-year-old were targeted for enrollment.
From a total of 6,865 initially selected, 4,847 parents gave
consent and filled out a questionnaire with family charac-
teristics, which gives a response rate of 70.6%. School in-
formation about parents showed that the nonresponders
did not differ in their demographic characteristics.
Finally, a total of 4,511 subjects were included in our anal-
ysis, comprising 2,274 girls and 2,237 boys. Some children
were not included in our analysis (n 5 336), because they
were from Asian countries (n 5 16), African countries (n
5 114), other European countries (n 5 4), South America
(n 5 10), three had Down syndrome, one had diabetes,
and one had nanism. Children from other ethnic groups
were not included doing the small sample size of each one.
We asked parents about preexisting health conditions,
and we excluded those related to growth and obesity prob-
lems. Finally, 187 were less than 6 years or more than 10
Detailed information about sampling characteristics
was given in Padez et al. (2004).
The study protocol was approved by Direcc ¸a ˜o Regional
de Educac ¸a ˜o, the ethical committee of the Portuguese
Ministry of Education. Informed consent was previously
obtained from children’s parents.
In each school, two trained technicians performed an-
thropometric measurements using a standardized proce-
dure. Anthropometric measurements were performed
with the children lightly dressed and without shoes.
Height was measured using a stadiometer, with the head
positioned according to the Frankfort plane, weight was
measured using an electronic scale with a precision of 100
g Triceps, and subscapular skinfolds were measured using
Lange Skinfold Calipers.
BMI was calculated as weight/height2(kg/m2). Over-
weight and obesity were then estimated according to the
IOTF age- and gender-specific child BMI cutoff points
(Cole et al., 2000).
The BF (%) was calculated using triceps and subscapu-
lar skinfold in the Slaughter equation (Slaughter et al.,
Parents filled out a questionnaire about family charac-
teristics that may have a potential influence in childhood
obesity. In this work, we included the following variables:
(1) mother and father obesity: metric self-reporting,
height in cm, and weigh in kg (BMI ? 30 kg/m2in either
parent); (2) parental education: highest level attained by
each parent; (3) watching TV: they were asked for by
hours per day; (4) sports activities apart from school: cate-
gorized into three levels from none to more than 2 h.
The questions on sleep were as follows: When does your
child usually go to bed during the week (from Monday to
Friday)? Options (a) before 8 pm, (b) between 8 and 9 pm,
(c) between 9 and 10 pm, (d) between 10 and 11 pm, and
(e) later than 11 pm; when does your child usually get up
in the morning during the week (from Monday to Friday)?
with the options (a) before 6 am, (b) between 6 and 7 am,
(c) between 7 and 8 am, and (d) after 8 am. If the bedtime
or time for getting up had been given as the interval, for
example, ‘‘between 8 and 9 am,’’ the time was set as the
lower figure plus 30 min. If the time had been given as
before or after an hour, the time was set as this specific
hour (e.g., before 6 am was set as 6 am). The sleeping time
was calculated by the difference between bedtime and
time for getting up. We did the same questions about Sat-
urday and Sunday. Total sleep duration (h/day) was then
estimated by week days (S), Saturday (St), and Sunday
(Su). Then, we calculated the total sleep duration with the
equation T 5 (5S 1 St 1 Su)/7. Finally, total sleep dura-
tion (h/day) was categorized as follows: <9; 9–10 h, 10–11
h, and ?11 h.
Mean, standard deviation, and frequency (%) were cal-
culated for the statistical analysis. Chi-squared test (v2)
was performed for comparison of frequencies between
groups at the 0.05 level of significance. A first analysis to
see the interaction for sex by sleep duration on obesity
was done for both genders combined. We did not find any
statistically significant gender interaction, and data for
both sexes were combined. For the entire sample, a v2test
was performed to compare family and child characteristics
with overweight and obesity and with sleep duration.
Multivariate logistic regression analysis was performed to
evaluate the strength of the association between family
and child characteristics and overweight/obesity and sleep
duration and childhood overweight/obesity. The odds ratio
(OR) and its 95% confidence interval (CI) were calculated
for each categorical variable (presence 5 1, absence 5 0).
Multivariate logistic regression analysis was done in two
steps: first, crude OR was calculated and second, OR was
adjusted for father education, mother education, father
obesity, mother obesity, physical activity, and TV watch-
ing. Statistical analysis was performed by SPSS (version
Table 1 presents the percentage of the sample with over-
weight/obesity across different levels of sociodemographic
variables. The educational level of both parents was sig-
nificantly associated with boys’ and girls’ overweight/obe-
sity. Parents with a university degree had less percentage
of overweight/obese children. Children who watched tele-
vision more time (?3 h/d) presented the highest percent-
age of overweight/obesity. Physical activity did not showed
any statistical association on the prevalence of over-
weight/obesity in both sexes. On the other hand, sleep du-
ration showed a statistically significant association with
overweight/obesity percentages in boys (P < 0.01) and
C. PADEZ ET AL.
American Journal of Human Biology
almost reached a significant association in girls (P <
Multivariate logistic regression in Table 2 showed that
paternal education was a protective factor for overweight/
obesity for those children whose father had a university
degree (OR: 0.71). The same association was found for
maternal education. There was a significant association
between childhood overweight/obesity and paternal and
maternal obesity with an higher association with mater-
nal obesity than paternal obesity. The OR for children
whose mother had a BMI 30.0 was 6.85 and for the father
was 2.56. The number of hours of TV viewing by the chil-
dren was significantly associated with overweight/obesity
with children that spent more than 3 h/d having and OR
of 1.45. A small but still significant association was found
with child overweight/obesity and physical activity.
Table 3 shows the BF (%) in relation to sleep duration.
Those children who slept more than 11 h showed less BF
(20.9%) than those who slept less than 9 h (23.4%), (P <
0.001). Multivariate logistic regression (Table 3) shows a
significant association between sleep duration and over-
weight/obesity after adjustment for potential risk factors
(mother education, father education, mother obesity, fa-
ther obesity, TV watching, and physical activity). We con-
sidered children that slept more than 11 h as a reference.
Boys and girls who slept less than 9 h per day presented
TABLE 2. Association between family and child characteristics and
Paternal obesity (Kg/m2)
Maternal obesity (Kg/m2)
Physical activity (h/d)
TABLE 3. Body fat (%) in relation to sleep duration and association
between sleep duration and overweight/obesity
Sleep (h)N (total)Fat (%)
P < 0.001
P < 0.001
F 5 6.5, P < 0.001
aAdjusted for father education, mother education, father obesity, mother obesity,
physical activity, and TV watching.
TABLE 1. Prevalence of obesity and overweight in boys and girls by sociodemographic factors and sleep duration
Boys Girls Total
v25 7.64, P 5 0.022
v25 14.56, P 5 0.001
v25 18.92, P 5 0.000
v25 6.09, P 5 0.048
v25 12.252, P 5 0.002
v25 15.42, P 5 0.000
v25 12.78, P 5 0.002
v25 7.72, P 5 0.021
v25 17.57, P 5 0.000
Physical activity (h/d)
v250.162, nsv25 0.106, nsv25 0.175, ns
Sleep duration (h)
v25 23.83, P 5 0.000
v257.75, P 5 0.051
v25 27.56, P 5 0.000
SLEEP DURATION AND OVERWEIGHT/OBESITY
American Journal of Human Biology
an higher OR of overweight/obesity than those sleeping
11 h or more per day, OR 5 3.22 (95% CI 5 3.11, 3.32).
Family lifestyle characteristics and children sleep duration
In Table 4, we analyzed the relationship between sleep-
ing time and some family characteristics such as parental
education and some behavioral factors such as TV watch-
ing and children’s physical activity. Boys and girls whose
parents had a lower education (Primary school—4 years)
slept less than those children whose parents had an
higher educational level. For instance, those who slept
less than 9 h per night, 3.7% belong to families where the
father had a primary school compared with just 0.7%
whose father had a university degree. Those children who
watched more TV slept less time: in the group that slept
less than 9 h, 1.2% spent 0–2 h watching TV compared
with 4.3% of those that spent more than 3 h watching tele-
vision. Physical activity showed a significant association
with sleep duration: in the group that slept less than 9 h,
2.9% did not spend any time in physical activity compared
with 1.5% of those that spent more than 2 h in physical
activity (P < 0.001).
The results of our study confirm prior findings and
extends our knowledge regarding on the association
between sleep duration and overweight/obesity but also
add new clues in our knowledge, between parental educa-
tional level, physical activity, and sleep duration. Another
major strength of our study was the large representative
sample studied representing children.
We found significant associations between sleep dura-
tion and overweight/obesity as well as an inverse response
between sleep duration and BF (%). After adjusted for
potential confounders, we found that children with
shorter sleep duration (<9 h/d) had an higher risk for
overweight/obesity (OR 5 3.22) than children having lon-
ger sleep duration (>11 h/d). These results are in agree-
ment with previous studies (Chaput et al., 2006; Eisen-
mann et al., 2006; Hui et al., 2003; Locard et al., 1992;
Nixon et al., 2008; Sekine et al., 2002; von Kries et al.,
2002). However, we should stress that it is very difficult to
compare our results with the above studies doing the dif-
ferent intervals that each author used to classify sleep du-
ration and, also, different potential confounders adjusted
in logistic regression analysis. Previous studies found val-
ues that go from OR 5 1.4 (Locard et al., 1992), OR 5 2.87
(Sekine et al., 2002), OR 5 3.45 (Chaput et al., 2006) and
OR 5 2.42 (males) and OR 5 1.41 (females), (Eisenmann
et al., 2006) and OR 5 3.32 (Nixon et al., 2008). However,
only Sekine et al. (2002), Chaput et al. (2006), and Nixon
et al. (2008) adjusted for several confounders like we did.
This suggests a clear protective effect of sleep duration in
the risk of childhood obesity but is difficult to quantify a
dose relationship. Two recent meta-analysis made by Cap-
puccio et al. (2008) and Chen et al. (2008) found that in
children the pooled OR for short duration of sleep and obe-
sity was 1.89 and 1.58, respectively, showing that, despite
different measures of sleep duration and adjusted risk fac-
tors, the association between these variables is statisti-
cally significant. Doing the high increase in the preva-
lence of obesity worldwide, some factors such as physical
activity and nutrition have been major research focus on
obesity prevention. All the above studies strength the im-
portance of considering sleep behavior in future public
health measures to prevent childhood obesity. However,
we need further research using the same sleep intervals
and adjusted well-known risk factors to make com-
parisons between populations and to find a clear dose
The explanation of the relationship between short sleep
duration, obesity, and metabolic risk factors appears to be
complex and is still under discussion. Locard et al. (1992)
hypothesized that an increased secretion of growth hor-
mone (GH) might be instrumental. GH is mainly secreted
during non-REM sleep periods in the beginning of the
night with some release during the following hours during
the rest of the night. A higher net excretion of GH may
therefore result from a large duration of sleep. A higher
activity of the somatotropic axis might increase GH-medi-
ated lypolysis, and thus reduce the risk of overweight and
obesity. Based on both clinical and experimental studies,
insufficient sleep has been shown to associate with multi-
ple metabolic and hormonal changes including reducing
in glucose tolerance, increase in cortisol levels, and sym-
pathovagal response (Spiegel et al., 1999, 2003). Besides,
sleep deprivation is associated with several neuroendo-
crine and metabolic function such as reduced leptin and
increased ghrelin levels, both of which can increase appe-
tite and, hence, possibly, weight gain (Chaput et al., 2007;
Knutson et al., 2007; Mullington et al., 2003; Spiegel
et al., 2003, 2004; Taheri, 2006; van Cauter et al., 2007).
Another important result of our study was the associa-
tion between parental education level, physical activity,
TV viewing, and sleep duration. Doing the consistent
association between sleep duration and obesity, it is im-
portant to understand which family and lifestyle factors
underlie the number of hours that children sleep because
children are very depend on their parents and their
behavior. Parent’s educational level is one of those factors
that are important if we consider an intervention study.
TABLE 4. Family and child characteristics in relation to sleeping
hours during week
Sleeping time (h/day)
v25 58.2, P < 0.001
v25 64.88, P < 0.001
v25 49.439, P < 0.001
Physical activity (h/d)
v25 25.442, P < 0.001
C. PADEZ ET AL.
American Journal of Human Biology
We found that parent’s educational level was significantly
associated with the number of hours that children sleep.
Children where both parents had a low educational level
sleep less time per night. This trend was also found by
Bahammam et al. (2006) in a sample of Saudi elementary
school children aged 6–13 years, where the authors shown
that children whose mothers had high-school education or
higher had longer night time sleep duration compared
with children whose mothers had lower educational level.
Few other studies related sleep duration with environ-
mental factors (Ota et al., 2007) and home environment
(Spilsbury et al., 2005). However, both suggested a great
influence of family factors on sleep habits.
Avery important behavior also related to sleep duration
is the amount of time that children spent watching televi-
sion. We found that those children that spent more time
watching television spent less time sleeping like Baham-
man et al. (2006) found. In their sample, watching TV or
playing computer games after 20.00 h was also related to
less sleep duration. Other studies found many adverse
effects of television viewing on children such as sleep dis-
orders (Johnson et al., 2004; Owens et al., 1999; Tynjala
et al., 1993; van den Bulch, 2004) and poor sleep habits
(Gupta et al., 1994). Cross-sectional studies found that tele-
vision/videotape viewing was associated with late bedtimes
and sleep disturbances among school-aged children and
adolescents (Owens et al., 1999; Tynjala et al., 1993). In
young children with less than 3 years of age, Thompson
and Christakis (2005) found that the number of hours of
television viewing per day among infants and toddlers was
associated with an increased risk of having an irregular
naptime schedule (OR 5 1.09) and an irregular bedtime
schedule (OR 5 1.13). This means that besides the well
known effect of television viewing on obesity, we should
consider their effect on sleeping time. This is important to
consider in intervention studies to reduce childhood obesity
and in messages for families with young children.
Another important factor is physical activity. Contrary
to the study of Yu et al. (2007) who found no statistically
significant association between physical activity and sleep
duration in Chinese adolescents, in our sample of chil-
dren, we found that those not engaged in physical activity
slept less time then those who had some physical activity
(P < 0.001). However, despite the research that has been
done on sleep and exercise in adults (Driver and Taylor,
2000), there is insufficient knowledge about the effects of
physical activity on sleep patterns in children. Recently,
Dworak et al. (2008) studied the effects of exercise on
school-aged children and provide supplementary evidence
for the hypothesis of homoeostatic sleep regulation. To
clarify the association of physical activity and sleep dura-
tion, further research is needed in children. One hypothe-
sis, that needs further confirmation, is that children with
low energy expenditure during the day are less tired than
children who spent more energy daily, and need to sleep
less. This means that physical activity is important not
only in weight regulation but also because children who
go to bed early in the night, will spend less time watching
television and, perhaps, having less food.
A major strength of our study is our sample that is a
large general population and data on social status and
family characteristics directly from the parents, as well
as, information on sleep duration during week days as
well as during the weekend days. On the other hand, reli-
ance on parent’s report of sleep duration has limitations.
They report times for going to bed rather than times for
going to sleep, reported sleeping hours may be longer than
accurate sleeping hours assessed by electroencephalo-
gram. A limitation of our study was the fact that we did
not asked the exact time that children wake up or went to
bed but we gave options to choose. We should also empha-
size that our data are cross-sectional and we are able to
see an association between sleep duration and obesity and
not a cause-effect relationship.
In conclusion, consistent with previous studies, our
findings support the hypothesis that sleeping time is asso-
ciated with overweight/obesity levels and also with BF
(%). However, because sleep duration is a potentially mod-
ifiable risk factor, our results might provide important
public health advices in the prevention of childhood obe-
sity. Regarding the relationship that we found with some
family characteristics (parental education) and children’s
behavior (TV watching and physical activity), this is also
a very important association suggesting that any inter-
vention program must be done within a family context.
The authors thank the two anonymous reviewers for all
their suggestionsand comments
improved the manuscript.
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