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Eur J Nutr

DOI 10.1007/s00394-017-1446-7

ORIGINAL CONTRIBUTION

An obesity‑preventive lifestyle score is negatively associated


with pediatric asthma
Constantina Papoutsakis1,2   · Eleni Papadakou2 · Maria Chondronikola3,4 ·
Georgios Antonogeorgos4 · Vasiliki Matziou2 · Maria Drakouli2 ·
Evanthia Konstantaki2 · Kostas N. Priftis5,6 

Received: 7 April 2016 / Accepted: 4 April 2017


© Springer-Verlag Berlin Heidelberg 2017

Abstract  target lifestyle behaviors that were either favorable or


Purpose  Lifestyle (diet and physical activity) may increase unfavorable in preventing obesity (i.e., screen time was
asthma risk, but evidence in this area is lacking. The aims an unfavorable lifestyle behavior). The score was devel-
of the present study were to calculate an obesity-preventive oped using the recommendations of the Expert Committee
lifestyle score comprising of eating and physical activity of American Academy of Pediatrics. Score values ranged
behaviors and investigate the overall effect of lifestyle on from 0–18 points; the higher the score, the more protective
asthma in children. against high body weight.
Methods A cross-sectional case–control study was car- Results  The OPLS was negatively associated with obesity
ried out in 514 children (217 asthma cases and 297 indices (BMI, waist circumference, and hip circumference),
healthy controls). Data were collected on medical his- (p < 0.05). Control children had a higher score when com-
tory, anthropometry, dietary intake, and physical activity. pared to asthma cases (9.3 ± 2.7 vs. 8.6 ± 2.9, p = 0.007).
We constructed an overweight/obesity-preventive score A high OPLS was protective against physician-diagnosed
(OPLS) using study-specific quartile rankings for nine asthma (OR 0.92; 95% CI 0.86–0.98, p = 0.014), adjusted
for several confounders. The OPLS was no longer protec-
tive after adjustment for BMI.
Electronic supplementary material  The online version of this Conclusion Higher adherence to an obesity-preventive
article (doi:10.1007/s00394-017-1446-7) contains supplementary lifestyle score—consistent with several behaviors for the
material, which is available to authorized users. prevention of childhood overweight/obesity—is nega-
tively associated with obesity indices and lowers the odds
* Constantina Papoutsakis
cpapoutsakis@eatright.org for asthma in children. Lifestyle behaviors that contribute
to a higher body weight may contribute to the obesity–
1
Academy of Nutrition and Dietetics, 120 South Riverside asthma link. These findings are hypothesis-generating and
Plaza, Suite 2000, Chicago, IL 60606‑6995, USA
warrant further investigation in prospective intervention
2
Department of Nursing, National and Kapodistrian studies.
University of Athens, Athens, Greece
3
Department of Internal Medicine‑Nutritional Science, Keywords  Asthma · Obesity · Lifestyle · Children
Washington University School of Medicine, St. Louis, MO,
USA
4
Abbreviations
Department of Nutrition and Dietetics, Harokopio University,
BMI Body mass index
Athens, Greece
5
FEV1 Forced expiratory volume in 1 s
Pediatric Allergy and Pulmonology Units, Third Department
FVC Forced expiratory vital capacity
of Pediatrics, School of Medicine, University General
Hospital ‘Attikon’, National and Kapodistrian University METs Metabolic equivalents
of Athens, Athens, Greece OPLS Obesity-preventive lifestyle score
6
Department of Allergy‑Pneumonology, Penteli Children’s PEF Peak expiratory flow
Hospital, Penteli, Greece

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Eur J Nutr

Introduction Greece. Permission to conduct the study was obtained


from the Institutional Review Board of Harokopio Uni-
Pediatric asthma and overweight/obesity has increased versity and has, therefore, been performed in accordance
in recent years. These two major public health problems with the ethical standards laid down in the 1964 Decla-
may be causally linked, but associated mechanisms are ration of Helsinki and its later amendments. Parents and
unclear. Epidemiologic evidence has established a sig- caregivers were informed about the purpose and meth-
nificant yet weak association between asthma and obesity ods of the study and signed an informed consent form.
[1]. Prospective studies demonstrate obesity/overweight In addition, participating children provided verbal assent.
likely precedes asthma, although other studies support Each asthma patient received budesonide via a dry pow-
the opposite or that overweight/obesity and asthma may der inhaler 200 mcg twice daily or fluticasone propionate
develop in tandem during growth periods and maturation via inhalation aerosol at dosages of 100 mcg twice daily
[1]. Irrespective of which of the two conditions appears for at least 1 year and an average of 4.02 ± 2.63 years.
first, two meta-analyses (a meta-analysis of seven stud- Exclusion criteria were any disease known to affect
ies of more than 300,000 adults and children [2], and a growth (cystic fibrosis, Klinefelter syndrome, Turner syn-
pediatric meta-analysis of six prospective studies [3]) drome, endocrine systemic, and skeletal disease). In addi-
have both supported that BMI is associated with inci- tion, any child with clinically evident respiratory tract
dent asthma. Overweight and obese individuals are at infection in the previous 2 weeks or presence of wheezing
increased risk of asthma in comparison to normal weight or current respiratory infection on physical examination
counterparts. A westernized lifestyle (decreased energy was excluded. Children with FEV1 <80% predicted were
expenditure and increased energy consumption coupled also excluded. Spirometry was performed using a portable
with intakes of nutrient poor food choices) may be in part spirometer (MicroLab, Micro Medical Ltd., Rochester,
responsible, especially in inner city populations [4] and UK). Three acceptable measurements were conducted and
developing countries undergoing rapid nutrition transi- the highest FEV1, FVC, and PEF were recorded as abso-
tion [5]. Investigations have shown associations between lute and % predicted values.
diet and asthma [6] or physical activity and asthma sepa- Asthma diagnosis was established by a pediatric pul-
rately [7]. There is abundant evidence, showing the asso- monologist–allergist (KP) according to the Global Initia-
ciation between dietary quantity and quality and physi- tive for Asthma Report, Global Strategy for Asthma Man-
cal activity and overweight/obesity [8]. The combined agement and Prevention (www.ginasthma.org). Trained
impact of an obesity-preventive lifestyle (diet and exer- interviewers recorded information on questionnaires and
cise together) on asthma has not been studied. Here, we obtained anthropometric measurements, as described
explore the complex relationship between asthma, obe- below. The recruitment rate was 86.8%. According to the a
sity, diet, and exercise in children using a predefined priori power analysis that was conducted, the current study
score [9]. Specifically, the aims of the present study are has power greater than 80% to detect associations between
to calculate an obesity-preventive lifestyle score compris- two variables with an odds ratio of 2.2 at a significance
ing of eating and physical activity behaviors to assess level α = 0.05 between case and control groups.
adherence to pediatric obesity prevention guidelines [8]
and evaluate the association of this obesity-preventive Anthropometrics
lifestyle score on asthma in children.
Body weight was measured to the nearest 0.1 kg with
a scale (Seca Corp., Hanover, MD) with subjects in light
clothing and barefoot. In addition, standing height was
Methods measured with a stadiometer (Holtain Ltd., Crymych,
Dyfed, UK) to the nearest 0.1 cm. Waist circumference (to
Study subjects the nearest 0.1 cm) was measured in a standing position
using a soft measuring tape, midway between the lower rib
The study sample consisted of 514 children (217 cases margin and the iliac crest, at the end of a gentle expiration.
of physician-diagnosed asthma, and 297 gender-matched During a single interview, measurements were repeated
healthy controls), aged 5–11 years. Recruitment took three times and averaged for analyses. Physical measure-
place between November 2007 and September 2010 at the ments of body weight and height were used to calculate
Department of Allergy-Pneumonology, Penteli Children’s BMI [BMI = weight (kg) divided by height (m squared)].
Hospital, Penteli, Greece and two municipal multi-clinic BMI was used for subjects’ classification as normal weight,
centers in Galatsi and Pefki, in the greater area of Athens, overweight, or obese by sex and age [10]. Maturity status

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by Tanner stage was assessed with the previously validated (METs) for the reported duration and type of each physical
method of self-evaluation using standardized drawings in activity.
the presence of a pediatrician [11].
Obesity‑preventive lifestyle score
Family and health history, and demographic
information For the purpose of this study, an overweight/obesity-pre-
ventive lifestyle score (OPLS) was developed. This is a
The approved Greek translation of the ISAAC question- modified version of the obesity-preventive score described
naire [12, 13] was used to obtain data on family history elsewhere [9]. The score was constructed, so that a high
of atopic disease (asthma and allergic rhinitis), housing achieved score represents high adherence to an obesity-pre-
details, tobacco exposure, and early and perinatal-life con- ventive lifestyle, a medium score represents medium adher-
ditions. A supplementary questionnaire was used to record ence, and a low score represents low adherence to an obe-
demographic information regarding age, socioeconomic sity-preventive lifestyle. The score comprised of nine target
status of the family (i.e., parental education, number of lifestyle behaviors. Each target behavior and the resulting
cars in the family, and number of family members), and score (sum of nine target behaviors) was categorized into
information on the child’s past medical history, current and tertiles to reflect the three categories: high, medium, and
past drug regimens, supplement use, history and duration low adherence. The nine target lifestyle behaviors that were
of breastfeeding, early feeding practices, birth weight, and used to construct the OPLS are based on the recommen-
self-reported parental and siblings’ height and weight. dations of the Expert Committee of American Academy
of Pediatrics for the prevention of pediatric obesity [8]:
consumption of fruit (servings/day), consumption of veg-
Dietary assessment etables (servings/day), consumption of sugar sweetened
beverages (servings/day), consumption of breakfast (times/
A validated 63-item semi-quantitative Food Frequency week), eating food from restaurants/fast food (times/week),
Questionnaire (FFQ) was used to evaluate participants’ screen time (h/week), moderate/intense physical activ-
usual dietary intake for the last 12 months [14]. The par- ity (kcal kg−1 day−1), school sport physical activity (min/
ent/caregiver and child were instructed to report on the week), and active commuting (kcal kg−1 day−1). To reflect
frequency of consumption (weekly or daily) of food items. a child’s routine physical activity, the obesity-preventive
The FFQ examined the frequency of consumption of fruits, score included the types of physical activity that were
vegetables, dairy and cheese, grains, nuts and seeds, snacks most likely to be scheduled or be part of a daily routine
(salty and sweet), traditional Greek foods, soda drinks, and (active commuting, school sport activities, and participa-
other beverages. Standardized portions were indicated by tion in moderate/intense activities). Each target behavior
typical serving sizes and household measures (e.g., ten cher- had either a negative impact or positive impact on the score
ries, one slice of bread, two cups of beans, etc.). In addition, calculation. Target behaviors described in the recommen-
frequency of eating breakfast, number of meals and snacks dations [8] as preventing obesity or favorable behaviors
per day, eating out, fast food consumption, cooking meth- (consumption of fruits, consumption of vegetables, break-
ods, snacking habits during school time, type of milk con- fast, moderate/intense activities, school sport activities, and
sumed, type of fat/oil used for cooking, and salad dressing active commuting) contributed positive points to the score
use were recorded. The recorded dietary information from and vice versa (consumption of sugar sweetened beverages,
the FFQ was further decoded to daily food group consump- eating at restaurants/fast food, and screen time). Each target
tion (in portions) to estimate daily energy intake (kcal/d). behavior was categorized into tertiles and assigned ascend-
ing values (0, 1, 2) for favorable behaviors and descend-
Physical activity ing values (2, 1, 0) for unfavorable behaviors. The itemized
scoring scheme appears in Supplementary Table 1. For each
Information on the frequency and duration of leisure time subject, all points from all behaviors were summed and the
and physical activity was evaluated using a previously vali- overweight/obesity-preventive score was calculated. Score
dated questionnaire [15]. Questions inquired about the fre- values ranged from 0–18 points with higher scores repre-
quency of sedentary and non-sports related activities during senting healthier lifestyles.
free time, usual ways of transport, and frequency of par-
ticipation in structured physical activity in school or in free Statistical analysis
time, as well as intensity and type of exercise. The daily
energy expenditure of participants was assessed by esti- Continuous variables are presented as mean ± stand-
mating a physical activity score in metabolic equivalents ard deviation, and categorical variables are presented as

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Table 1  Summary Asthma cases (n = 217) Control subjects (n = 297) p value


characteristics of asthma case
and control subjects Male gender 133 (61%) 164 (55%) 0.169
Age, y 7.7 ± 1.9 7.6 ± 1.8 0.490
BMI, kg/m2 18.56 ± 3.52 17.79 ± 2.90 0.007
Height, m 1.27 ± 0.15 1.27 ± 0.13 0.962
Waist circumference, cm 62.68 ± 9.13 60.79 ± 7.29 0.010
Overweight/obese 100 (46.1%) 108 (36.3%) 0.026
Lung function,  % predicted
 FEV1 98.4 ± 6.3 97.7 ± 5.1 0.634
 FVC 94.4 ± 5.7 93.8 ± 5.5 0.875
 PEF 92.0 ± 5.8 88.9 ± 5.7 0.289
Mother’s education, y 13.6 ± 3 13.9 ± 2.6 0.220
Father’s education, y 13.4 ± 3.3 13.8 ± 3.2 0.171
House, ­m2 110.6 ± 41.8 117.3 ± 46.7 0.09
Number of children 1.9 ± 0.7 2.0 ± 0.7 0.251
Smoking inside the house, yes/no 68 (31%) 107 (36%) 0.269
Breastfeeding, yes/no 165 (76%) 261 (88%) 0.001
Tanner pubic hair, ≥1/0 145 (67%) 166 (56%) 0.012
Energy intake, kcal/d 2091 ± 614 2142 ± 601 0.353
Physical activity, METs 10.9 ± 4.2 11.8 ± 4.0 0.004
Mother’s atopy, yes/no 89 (41%) 77 (26%) 0.000
Father’s atopy, yes/no 65 (30%) 62 (21%) 0.013

Data are presented as mean ± SD or no (%) unless otherwise indicated. Missing values in some variables
BMI body mass index, METs metabolic equivalents, SD standard deviation, FEV1 forced expiratory vol-
ume in 1 s, FVC forced expiratory vital capacity, PEF peak expiratory flow

absolute and relative frequencies. Histograms and normal- for VIF, for each independent variable of the model. Linear
ity plots were used to evaluate the assumption of normal- regression models were used to study the effect of obesity
ity of the distribution of the continuous variables. Inde- indices (BMI, waist circumference, and hip circumference)
pendent sample Student’s t tests assessed the differences on the score adjusting for potential confounders (sex, age,
in continuous variables between asthma cases and healthy and puberty status). All statistical tests were two-sided, and
controls. Chi-square tests were used to assess the differ- p < 0.05 was required to reject the null hypothesis. Statisti-
ences between categorical variables. Pearson’s correla- cal analysis was performed using SPSS 21.0 for Windows
tion coefficients were determined to identify significant (SPSS, Chicago, IL).
correlations between continuous variables of interest. A
one-way ANOVA was used to test for differences in the
OPLS among the three BMI categories (normal weight, Results
overweight, obese). Logistic regression models were con-
ducted to estimate the association between asthma and the Approximately 28.8% (n  = 148) of children were over-
obesity-preventive score adjusting for potential confound- weight and 11.3% were obese. Children with asthma
ers (sex, age, maternal and paternal atopy, energy intake, had a higher BMI and waist circumference than healthy
Tanner stage, breastfeeding, and BMI). These variables subjects (18.56 ± 3.52 vs. 17.79 ± 2.9, p  = 0.007 and
were selected, because they have been reported in the lit- 62.7  ± 9.1 cm vs 60.8 ± 7.3 cm, p  = 0.01, respectively)
erature as important confounders or because they were (Table 1). The prevalence of overweight/obesity was almost
significantly different between cases and controls. Data 10% higher in the asthma group when compared to controls
are presented as odds ratios (ORs) and 95% confidence (46.1% vs. 36.3%, p = 0.026). Energy intake did not differ
intervals (CI). The Hosmer–Lemeshow statistic was calcu- between the two groups (2091 ± 614 vs. 2142 ± 601 kcal,
lated to evaluate the model’s goodness-of-fit. For all logis- p  = 0.353); however, asthma cases had a lower physical
tic regression models, multicollinearity was checked using activity score compared to healthy children (10.9 ± 4.2 vs.
Tolerance and the Variance Inflation Factor (VIF), with 11.8 ± 4.0, p = 0.004). Breastfeeding during infancy (yes
cut-off values of 0.1 or less for tolerance, and 10 or more vs no) was lower in asthma cases than in healthy controls

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(76% vs. 88%, p = 0.001). History of maternal and pater- and overweight counterparts [9.33 ± 2.79, 95% CI (8.89–
nal atopy was reported in higher frequencies in the asthma 9.79)], p  = 0.009. The difference between the normal
group than the control group (41% vs. 26%, p = 0.000 and weight and the overweight group was not significant at
30% vs. 21%, p  = 0.013, respectively). All measures of p < 0.05.
lung function (FEV1, FVC, and PEF) were similar between The OPLS was negatively associated with obesity
asthma cases and healthy controls (Table 1). indices: BMI (b  =  −0.09, p  = 0.041), waist circumfer-
The average measure of each of the nine diet and physi- ence (b  =  −0.019, p  = 0.001), and hip circumference
cal activity behaviors used to construct the OPLS and the (b = −0.044, p = 0.009) after adjustment for gender, age,
resulting score were calculated for the entire sample and and Tanner stage.
by study group. When examined individually, target behav- The OPLS was negatively associated with physician-
iors showed no difference between the two groups except diagnosed asthma (OR 0.927, 95% CI 0.864–0.995)
for moderate/intense activities and school sport activities (Table 3). For every one point increase of the OPLS, sub-
both of which were lower in children with asthma com- jects were almost 7% less likely to have asthma even after
pared to controls (10.8 ± 4.27 vs. 11.88 ± 4 kcal kg−1 d−1, adjustment for several confounders (gender, age, maternal
p  = 0.004 and 56.82 ± 30 vs. 62.58 ± 27.51 min/week, and paternal atopy, history of breastfeeding, and puberty
p = 0.026). status). Further adjustment for BMI rendered the associa-
Asthma cases also displayed a significantly lower tion nonsignificant.
OPLS when compared to controls (8.6 ± 2.9 vs. 9.3 ± 2.7,
p  = 0.008). In addition, logistic regression models were
conducted to estimate the association between asthma and Discussion
each target behavior of the OPLS, and the resulting OPLS
adjusting for potential confounders (sex, age, maternal and To the best of our knowledge, this is the first study to
paternal atopy, energy intake, Tanner stage, breastfeeding, investigate the relation between pediatric asthma and life-
and BMI). This was done to describe the individual effects style (dietary and physical activity behaviors combined).
vs the combined effects of the lifestyle factors investi- We found that a 1-unit increase in the Obesity-Preventive
gated (Table 2). With the exception of two physical activity Lifestyle Score (OPLS), (meaning a lifestyle closer to rec-
parameters, each lifestyle factor alone was not significant ommended guidelines for the prevention of pediatric over-
in reducing the odds for asthma, but the combined lifestyle weight/obesity) [8] was associated with a 7% decrease in
factors (OPLS) were significant (Table 2). the odds of physician-diagnosed asthma after adjustment
A one-way ANOVA was used to test for differences in for several confounders.
the OPLS among the three BMI categories (normal weight, Various hypotheses have been proposed to explain the
overweight, obese). Scores differed across the three cat- link between overweight/obesity and asthma including a
egories (F  = 4.542, p  = 0.011). Additional Bonferroni common genetic background, comorbidities, mechani-
post hoc comparisons showed that the obese children had a cal changes associated with high body weight, changes in
lower score [8.0 ± 2.8, 95% CI (7.23–8.77)] than their nor- airway hyperresponsiveness, abnormal lipid and glucose
mal weight [9.06 ± 2.8, 95% CI (8.74–9.39)], p = 0.032, metabolism, low-grade systemic inflammation, shared

Table 2  Logistic regression for Target behavior Model 1 OR (95% CI) Model 2 OR (95% CI)
the evaluation of the association
between each target behavior of Fruits (servings/day) 0.996 (0.849–1.170) 0.955 (0.843–1.175)
the obesity-preventive lifestyle
Vegetables (servings/day) 0.894 (0.744–1.075) 0.955 (0.744–1.090)
score and physician-diagnosed
asthma Sugar sweetened beverages (servings/day) 0.920 (0.725–1.169) 1.005 (0.784–1.289)
Breakfast (times/week) 1.083 (0.983–1.194) 1.083 (0.978–1.199)
Restaurants/fast food (times/week) 1.024 (0.889–1.180) 0.970 (0.834–1.127)
Screen time (h/week) 1.006 (0.955–1.060) 1.002 (0.949–1.057)
Moderate/intense activities (kcal kg−1 day−1) 0.920 (0.877–0.965)ª 0.922 (0.878–0.969)ª
School sport activities (min/week) 0.992 (0.986–0.998)ª 0.992 (0.986–0.999)ª
Active commuting (kcal kg−1 day−1) 0.991 (0.978–1.003) 0.995 (0.982–1.008)

Model 1 adjusted for gender, age


Model 2 adjusted for gender, age, maternal atopy, paternal atopy, breastfeeding, and Tanner stage
OR odds ratio, CI confidence interval
ª p < 0.05

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Table 3  Multivariate logistic Model ­1a OR (95% CI) Model ­2b OR (95% CI)
regression for the evaluation
of the association between the Gender 1.279 (0.87–1.864) 1.3 (0.884–1.914)
obesity-preventive lifestyle
Age 1.012 (0.914–1.120) 0.947 (0.842–1.065)
score and physician-diagnosed
asthma Obesity-preventive lifestyle score 0.910 (0.851–0.973)c 0.927 (0.865–0.994)c
Maternal atopy, yes/no 1.613 (1.077–2.416)c
Paternal atopy, yes/no 1.625 (1.057–2.499)c
Breastfeeding, yes/no 0.440 (0.269–0.722)c
Tanner stage pubic hair, ≥1/0 1.650 (1.058–2.573)c

OR odds ratio, CI confidence interval


a
  Model 1 adjusted for gender, age
b
  Model 2 adjusted for gender, age, maternal atopy, paternal atopy, breastfeeding, and Tanner stage
c
  p < 0.05

psychosocial factors, and undesirable lifestyle changes in measures are different, effect sizes were relatively small.
diet or physical activity [16–19]. The school activity difference is about 10% or 6 min per
There is an increasing interest in the role of lifestyle week which does not appear clinically significant. These
in the development of asthma, since lifestyle is subject to results support that not any one individual lifestyle measure
manipulation. The majority of studies have evaluated the may be influential on its own and that there are complex
role of specific nutrients, food groups, or physical activity interactions between them. When we assessed lifestyle as a
on asthma measures in children separately [20, 21]. Some composite score which combined diet and physical activity,
studies have shown a positive association between a west- we showed that adherence to an obesity-preventive lifestyle
ernized diet (low consumption of fruits and vegetables, may have a protective effect in reducing the odds of asthma
high fast food, and soft drink consumption) or a sedentary in children (Table 3). The difference in the OPLS between
behavior (long duration of screen time and reduced physi- the two groups is about 0.7 (8.6 ± 2.9 asthma cases, vs.
cal activity) and asthma or asthma symptoms, but others 9.3 ± 2.7 healthy controls, p = 0.008).
have not [7, 22]. The variability of results on the asso- It is intriguing that such a small difference contributes
ciation between diet and asthma or physical activity and to a detectable influence on the odds of asthma in children.
asthma may be influenced by the definitions and categori- The small difference is consistent with evidence support-
zations of these entities. Epidemiologic studies differ in the ing a weak yet significant association between obesity and
measures of dietary/physical activity exposures and in the asthma [1].
use of asthma definitions. A ‘healthy diet’ has been defined in several different
The relationships between diet, exercise, sedentarism, ways in the form of dietary recommendations across coun-
and asthma are complex and studying these behaviors in tries. A frequently used approach to quantify adherence to
isolation may fail to reveal a possible synergy. A holistic a healthy diet is to construct a composite score that catego-
approach that assesses various lifestyle aspects together rizes individuals according to the intakes of foods or nutri-
has not been investigated. In this study, a general lack of ents that have been associated with diseases or risk factors
association was noted between individual target behaviors [24–26]. The widely recognized concept of a dietary score
(Table  2) and asthma. The only individual measures that was extended to that of a lifestyle score. The OPLS was
were different between cases and control children were two negatively associated with indexes of overweight/obesity
physical activity-related measures (moderate/intense activi- (BMI, waist circumference, and hip circumference) after
ties and school sport activities). We also found that school adjustment for gender, age, and puberty status.
sports activities were significantly higher by about 6 min/ Multiple regression analysis showed that the OPLS
week in normal weight than overweight/obese children decreases the odds of asthma. However, this finding was
(data not shown). These findings may be attributed to the no longer significant after adjustment for BMI. This sup-
fact that it might be easier to accurately report organized/ ports that associations between asthma development and
scheduled physical activity than other aspects of lifestyle lifestyle behaviors are mediated by BMI, and that possibly
[23]. An initial observation might be that it is not surprising a normal weight BMI in and of itself is protective against
children with asthma are less active; yet, it should be noted asthma. Thus, the conclusion that overweight/obese chil-
that in this study, asthma in cases is well controlled given dren are more likely to have asthma than those of normal
their similar respiratory measures (FEV1, FCV, and PEF) weight remains. A question that is still open is the exact
to control children. Although these two physical activity mechanism of the association between obesity and asthma

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as well as the management of this association. Our results Such an approach is limited by the content of existing
are hypothesis-generating and lend support that a high guidelines that define optimal lifestyle patterns. In any
body weight due to lifestyle behaviors influences the odds investigation, utilizing a composite score, it should be
of asthma in children. Thus, adopting an obesity-preven- clear what the score intends to accomplish. Is it to measure
tive lifestyle as a means to a healthier body weight status absolute diet and lifestyle contribution or to evaluate over-
may have a role as a complementary non-pharmacologi- all adherence to guidelines? The aim of the present study
cal intervention [1]. The OPLS encompasses key behav- is the latter. The American Academy of Pediatrics (AAP)
iors to focus on during weight-management/weight loss has underlined the need for research aimed at developing
counseling. These behaviors include increasing fruit and methods to comprehensively assess all behaviors that could
vegetable intake, limiting sugar sweetened beverage con- prevent chronic disease risk [8]. Most existing indexes are
sumption, limiting screen time, eating breakfast, limiting able to predict health outcome to an extent, but the associa-
eating out, and increasing physical activity. In our study, tions are generally moderate for all scores, creating doubts
obese children had a lower (worse) score [8.0 ± 2.8, 95% about their usefulness. Nevertheless, scores can be useful
CI (7.23–8.77)] than their normal weight [9.06 ± 2.8, 95% to measure the extent to which individuals adhere to guide-
CI (8.74–9.39)], p  = 0.032 and overweight counterparts lines, and these scores like the one we have applied need
[9.33 ± 2.79, 95% CI (8.89–9.79)], p = 0.009. In addition, to be used and interpreted with caution. Further research is
we found that overweight children had a higher (better) needed to evaluate this index prospectively and in diverse
score than the normal weight children, yet the difference populations, and improvements to this index may be
between the score of overweight and normal weight chil- needed.
dren was not significant. It is important to highlight that the Observed associations between the OPLS and BMI,
cohort we studied was 28.8% overweight and 11.3% obese. waist circumference, and hip circumference are biologi-
The increased prevalence of overweight/obesity in the pre- cally plausible thus serving, to an extent, as evidence of
sent study is in line with levels reported in other young construct validity. The odds reduction of asthma attrib-
Greek populations [27, 28]. The alarmingly high preva- uted to the OPLS was modest. Although this is consist-
lence of overweight/obese children underscores the need ent with most studies of associations between dietary fac-
for effective interventions. tors or physical activity factors, and asthma, our results
BMI is a widely used measure of weight status in epide- should be interpreted with consideration of their clinical
miologic and clinical studies; yet, in children, a higher BMI importance. The presented evidence does not provide any
may not always represent higher fat mass but increased lean information about the impact of improved lifestyle in the
mass instead. This is important, because a higher lean mass short term, a point that is important to consider in design-
is associated with better respiratory function [1]. Still, in ing intervention studies and/or prevention programs. The
children, when BMI was compared to other body composi- sample of Greek children we studied is fairly homogene-
tion measures like percent body fat measurement, and sum ous in ethnic and socioeconomic background. The relation-
of skinfold thicknesses, it provided similar results about the ship between asthma and lifestyle may be underestimated,
relationship between overweight/obesity and asthma [29, because children from different ethnicities or impoverished
30]. backgrounds were not represented in this sample. Finally,
Some caveats are warranted when interpreting the pre- limitations of this study are those inherent to case–control
sented data. Our observations are based on a modest size studies, and hence, the possibility of residual confounding
sample. A basic assumption is that the dietary and physi- cannot be ruled out. The results of this study cannot be used
cal activity factors most relevant for influencing asthma to prove causality due to the lack of temporal sequence of
diagnosis were included in the OPLS and that these fac- events and reverse causality cannot be excluded.
tors were adequately measured based on the previous vali- Our case–control study had several strengths. Cases
dation studies [14, 15]. Self-report measures of physical included children with physician-diagnosed asthma accord-
activity and dietary intake are subject to recall bias, and the ing to previously established criteria, minimizing diagnostic
respondents’ willingness/ability to report accurately. misclassification. Weight, height, and waist circumference
In the present paper, we have applied a predefined index were objectively measured. We measured lung function
based on diet and lifestyle that has previously been pub- (FEV1, FVC, and PEF) at rest which may not be the best
lished as a composite measure [9]. Several such indexes marker, yet lung function at rest is frequently used in typi-
have been proposed and validated by relating a composite cal clinical settings such as ours. The three lung function
index score to a health outcome in children [9, 31, 32]. This measures (FEV1, FVC, and PEF) were similar between
approach is an ‘a priori’ procedure, because the index is cases and healthy controls. This may be attributed to well-
developed based on current scientific knowledge (i.e., rec- controlled asthma in cases. Because cases were treated
ommended evidence-based guidelines). with low-dose inhaled steroids, the pharmacotherapy is not

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Eur J Nutr

likely to account for the differences in overweight/obese 3. Egan KB, Ettinger AS, Bracken MB (2013) Childhood body
indices. Finally, the possible role of Tanner stage, and other mass index and subsequent physician-diagnosed asthma: a sys-
tematic review and meta-analysis of prospective cohort stud-
known confounders (age, sex, breastfeeding history, and ies. BMC Pediatr 13:121
maternal and paternal atopy) was accounted for by includ- 4. Platts-Mills TA, Erwin E, Heymann P, Woodfolk J (2005)
ing them in the multiple logistic regression models. Is the hygiene hypothesis still a viable explanation for the
increased prevalence of asthma? Allergy 60(Suppl 79):25–31
5. Asher MI, Montefort S, Bjorksten B, Lai CK, Strachan DP,
Weiland SK, Williams H (2006) Worldwide time trends in
the prevalence of symptoms of asthma, allergic rhinocon-
Conclusion junctivitis, and eczema in childhood: ISAAC Phases One and
Three repeat multicountry cross-sectional surveys. Lancet
Adhering to an obesity-preventive lifestyle may decrease 368(9537):733–743
6. Boeing H, Bechthold A, Bub A, Ellinger S, Haller D, Kroke A,
the odds of asthma in children, yet this relationship is
Leschik-Bonnet E, Muller MJ, Oberritter H, Schulze M, Ste-
dependent upon BMI. These findings are hypothesis-gen- hle P, Watzl B (2012) Critical review: vegetables and fruit in
erating and warrant further investigation in the form of pro- the prevention of chronic diseases. Eur J Nutr 51(6):637–663.
spective/intervention studies. doi:10.1007/s00394-012-0380-y
7. Eijkemans M, Mommers M, Draaisma JM, Thijs C, Prins MH
(2012) Physical activity and asthma: a systematic review and
Acknowledgements The authors thank all faculty, students of Ath-
meta-analysis. PLoS ONE 7(12):e50775
ens University, Harokopio University, and all clinical staff of Penteli
8. Barlow SE (2007) Expert committee recommendations regarding
Children’s Hospital and the municipal multi-clinic centers in Galatsi
the prevention, assessment, and treatment of child and adolescent
and Pefki for their invaluable assistance. The authors also thank the
overweight and obesity: summary report. Pediatrics 120(Suppl
participants of these studies and their families.
4):S164–S192
9. Ntalla I, Yannakoulia M, Dedoussis GV (2016) An Overweight
Author contribution  Dr. CP conceptualized and designed the study, Preventive Score associates with obesity and glycemic traits.
drafted the initial manuscript, and approved the final manuscript as Metabolism 65(1):81–88. doi:10.1016/j.metabol.2015.09.021
submitted. Dr. EP carried out the initial analyses, co-drafted parts 10. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establish-
of the initial manuscript, reviewed and revised the manuscript, and ing a standard definition for child overweight and obesity world-
approved the final manuscript as submitted. Ms. MC conducted wide: international survey. BMJ 320(7244):1240–1243
data collection and analyses, critically reviewed the manuscript, and 11. Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment
approved the final manuscript as submitted. Dr. GA conducted data of sexual maturation. Pediatrics 66(6):918–920
analyses, critically reviewed the manuscript, and approved the final 12. Papadopoulou A, Hatziagorou E, Matziou VN, Grigoropoulou
manuscript as submitted. Dr. VM coordinated and supervised data DD, Panagiotakos DB, Tsanakas JN, Gratziou C, Priftis KN
collection, critically reviewed the manuscript, and approved the final (2011) Comparison in asthma and allergy prevalence in the two
manuscript as submitted. Ms. MD conducted data collection, criti- major cities in Greece: the ISAAC phase II survey. Allergol
cally reviewed the manuscript, and approved the final manuscript Immunopathol (Madr) 39(6):347–355
as submitted. Ms. EK conducted data collection, critically reviewed 13. Jenkins MA, Clarke JR, Carlin JB, Robertson CF, Hopper JL,
the manuscript, and approved the final manuscript as submitted. Dr. Dalton MF, Holst DP, Choi K, Giles GG (1996) Validation of
KNP contributed to the design of the study, analyses, and drafting the questionnaire and bronchial hyperresponsiveness against respira-
article. tory physician assessment in the diagnosis of asthma. Int J Epi-
demiol 25(3):609–616
Compliance with ethical standards  14. Antonogeorgos G, Grigoropoulou D, Papadimitriou A, Priftis
KN (2011) Validation of food frequency questionnaire designed
Conflict of interest  On behalf of all authors, the corresponding author for children 10–12 years: the PANACEA-FFQ. In: 52nd annual
states that there is no conflict of interest. meeting of the European Society for Paediatric Research, New-
castle, UK
15. Avgerinos A, Argiropoulou EC, Almond I, Michalopoulou M
Funding Dr. Papoutsakis was supported by a post-doctoral grant, (2000) A new instrument for evaluating energy expenditure: con-
Greek State Scholarship Foundation. Dr. Chondronikola was sup- vergent validity and reliability of the physical activity and life-
ported by a scholarship grant, Onassis Foundation. style questionnaire (PALQ). Sport Perform Health 4:281–300
16. Farah CS, Salome CM (2012) Asthma and obesity: a known asso-
ciation but unknown mechanism. Respirology 17(3):412–421
17. Black MH, Anderson A, Bell RA, Dabelea D, Pihoker C, Say-
dah S, Seid M, Standiford DA, Waitzfelder B, Marcovina SM,
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