Diet and Respiratory Health in Children from 11 Latin American Countries: Evidence from ISAAC Phase III

Abstract

Background and aim:
The burden of childhood asthma and its risk factors is an important but neglected public health challenge in Latin America. We investigated the association between allergic symptoms and dietary intake in children from this region.

Methods:
As part of the International Study of Asthma and Allergies in Childhood (ISAAC) Phase III, questionnaire collected dietary intake was investigated in relation to risk of parental/child reported current wheeze (primary outcome) and rhino-conjunctivitis and eczema. Per-country adjusted logistic regressions were performed, and combined effect sizes were calculated with meta-analyses.

Results:
143,967 children from 11 countries had complete data. In children aged 6-7 years, current wheeze was negatively associated with higher fruit intake (adjusted odds ratio [aOR] 0.65; 95% CI 0.74, 0.97). Current rhino-conjunctivitis and eczema were statistically negatively associated with fruit intake (aOR 0.72; 95% CI 0.64, 0.82; and OR 0.64, 95% CI 0.56, 0.74, respectively). Vegetable intake was negatively associated with risk of symptoms in younger children, but these associations were attenuated in the 13-14 years old group. Fastfood/burger intake was positively associated with all three outcomes in the older children.

Conclusion:
A higher intake of fruits and vegetables was associated with a lower prevalence of allergic symptoms in Latin American children. Conversely, intake of fastfood was positively associated with a higher prevalence of wheeze in adolescents. Improved dietary habits in children might help reduce the epidemic of allergic symptoms in Latin America. Food interventions in asthmatic children are needed to evaluate the possible public health impact of a better diet on respiratory health.

Full text

ASTHMA
Diet and Respiratory Health in Children from 11 Latin American
Countries: Evidence from ISAAC Phase III
Alfonso Mario Cepeda
1
•Sumaiyya Thawer
2
•Robert J. Boyle
3
•Sara Villalba
1
•
Rodolfo Jaller
1
•Elmy Tapias
1
•Ana Marı
´a Segura
1
•Rodrigo Villegas
4
•
Vanessa Garcia-Larsen
5
•and the ISAAC Phase III Latin America Group
Received: 25 February 2017 / Accepted: 5 August 2017 / Published online: 28 August 2017
ÓThe Author(s) 2017. This article is an open access publication
Abstract
Background and Aim The burden of childhood asthma and
its risk factors is an important but neglected public health
challenge in Latin America. We investigated the associa-
tion between allergic symptoms and dietary intake in
children from this region.
Methods As part of the International Study of Asthma and
Allergies in Childhood (ISAAC) Phase III, questionnaire
collected dietary intake was investigated in relation to risk
of parental/child reported current wheeze (primary out-
come) and rhino-conjunctivitis and eczema. Per-country
adjusted logistic regressions were performed, and com-
bined effect sizes were calculated with meta-analyses.
Results 143,967 children from 11 countries had complete
data. In children aged 6–7 years, current wheeze was
negatively associated with higher fruit intake (adjusted
odds ratio [aOR] 0.65; 95% CI 0.74, 0.97). Current rhino-
conjunctivitis and eczema were statistically negatively
associated with fruit intake (aOR 0.72; 95% CI 0.64, 0.82;
and OR 0.64, 95% CI 0.56, 0.74, respectively).
Vegetable intake was negatively associated with risk of
symptoms in younger children, but these associations were
attenuated in the 13–14 years old group. Fastfood/burger
intake was positively associated with all three outcomes in
the older children.
Conclusion A higher intake of fruits and vegetables was
associated with a lower prevalence of allergic symptoms in
Latin American children. Conversely, intake of fastfood
Collaborators of the ISAAC Phase III Latin America Groups are listed
in ‘‘Acknowledgement’’.
Electronic supplementary material The online version of this
article (doi:10.1007/s00408-017-0044-z) contains supplementary
material, which is available to authorized users.
&Vanessa Garcia-Larsen
vgla@jhu.edu
Alfonso Mario Cepeda
alerlab@yahoo.es
Sumaiyya Thawer
s.thawer14@imperial.ac.uk
Robert J. Boyle
r.boyle@nhs.net
Sara Villalba
saravivar@yahoo.es
Rodolfo Jaller
rodolfojaller@hotmail.com
Elmy Tapias
elmtapias@yahoo.es
Ana Marı
´a Segura
asegurar25@yahoo.es
Rodrigo Villegas
villegas.ro@gmail.com
1
Fundacio
´n Hospital Universitario Metropolitano de
Barranquilla, Barranquilla, Colombia
2
Population Health and Occupational Disease Group, NHLI
Imperial College London, London, UK
3
Department of Paediatrics, Faculty of Medicine, Imperial
College London, London, UK
4
School of Public Health, University of Chile, Santiago, Chile
5
Department of International Health, Johns Hopkins
Bloomberg School of Public Health, 615 N Wolfe, Suite
E2546, Baltimore, MD 21205, USA
123
Lung (2017) 195:683–692
DOI 10.1007/s00408-017-0044-z
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

was positively associated with a higher prevalence of
wheeze in adolescents. Improved dietary habits in children
might help reduce the epidemic of allergic symptoms in
Latin America. Food interventions in asthmatic children
are needed to evaluate the possible public health impact of
a better diet on respiratory health.
Keywords Diet ISAAC Phase III Wheeze Asthma 
Latin America Children Fruits Vegetables
Introduction
Asthma continues to represent a major public health burden
worldwide. The Global Burden of Disease (GBD) reported
that symptoms of asthma in low- and middle- income
countries can be as high as the rates found in more
developed countries [1]. In line with the large variations in
economic and social development observed in Latin
America, the prevalence of asthma is also diverse, with
rates of current wheeze ranging between 4 and 30% in
adolescents, and between 8 and 37% in younger children
[1–3]. These rates are comparable to that of developed
countries or those with higher economic wealth. Children
with symptomatic asthma lose time off school and are less
productive, with direct and indirect costs to themselves and
society [4]. In children aged 5–14 years, asthma alone is in
the top ten global ranking of disability-adjusted life years
in children [5].
Despite the high rates of asthma in Latin America,
studies examining the association between environmental
risk factors (including diet) and allergic diseases have so
far been scant [6]. Cross-sectional studies in Bolivia and
Ecuador have shown a negative association between fruit
intake and asthma symptoms, and evidence from two
small case–control studies in Brazil showed conflicting
results [7,8]. In a sample of Colombian children, higher
intake of fruits and vegetables was negatively associated
with several allergic symptoms [9]. In young adults from
Chile, dietary intake of flavonoids was associated with
improved ventilatory function [10], but neither fruits,
vegetables, or antioxidant nutrients were associated with
subjective or objective measures of asthma [11]. The
social inequalities and socio-demographic variations
within and between countries of this region make inter-
pretation of findings more difficult. The International
Study on Asthma and Allergies in Children (ISAAC) has
contributed to address the knowledge gap on dietary
factors that could be related to asthma and allergic dis-
eases [12].We aimed at investigating the association
between dietary intake of foods with antioxidant, anti-
inflammatory, and anti-allergic properties, with
respiratory and allergic symptoms in children from across
Latin America.
Methods
Sample
As part of ISAAC Phase III [13], eleven Latin American
countries were included in this study (Argentina, Brazil,
Bolivia, Chile, Colombia, Ecuador, Mexico, Panama, Peru,
Venezuela, and Urugay) [14]. Participant countries col-
lected information on dietary exposures and asthma-related
symptoms following the ISAAC protocols.
Outcome Assessment
The primary outcome for this analysis was current wheeze,
which was defined as children (or they parents) answering
yes to the question ‘Have you (Has your child) had
wheezing or whistling in the chest in the past 12 months?’.
Current rhino-conjunctivitis and current eczema were also
analysed as secondary outcomes. The questions for current
symptoms of rhino-conjunctivitis were ‘In the past
12 months, have you (has your child) had a problem with
sneezing or a runny or blocked nose when you (he/she) did
not have a cold or flu?’ and ‘In the past 12 months, has this
nose problem been accompanied by itchy watery eyes?’.
The questions for current symptoms of eczema were ‘Have
you (Has your child) had this itchy rash at any time in the
past 12 months?’ and ‘Has this itchy rash at any time
affected any of the following places: the folds of the
elbows, behind the knees, in front of the ankles, under the
buttocks, or around the neck, ears or eyes?’. These ques-
tions were preceded by the question ‘Have you (Has your
child) ever had an itchy rash coming and going for at least
6 months?’.
Dietary Exposures
The questions on diet included in the Environmental
Questionnaire (EQ) enquired about foods which had earlier
been suggested to influence the risk of allergic diseases.
Respondents were asked: ‘In the past 12 months, how
often, on average, did you (did your child) eat or drink the
following: fruit; vegetables (green and root); and fast food/
burgers?’. Centres were encouraged to include local names
to define foods if necessary. Frequency of food intake was
categorised as follows: rarely or never (reference); once or
twice per week; and C3 times per week (comparison). We
investigated the association between allergic symptoms
and these food groups for their possible antioxidant, anti-
or pro-inflammatory effect on these diseases.
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Statistical Analyses
Data from centres of a same country were merged and
results are presented per country. Distribution of general
characteristics, potential confounders, and prevalence of
outcomes are presented as percentages per country and for
the total population. The three outcomes of interest were
treated as binary variables (yes/no for having the disease).
The association between each outcome and dietary expo-
sures in each country was examined with multivariable
logistic regressions, adjusting for potential confounders
(physical activity (frequency of exercise per week), number
of hours watching television (1, 2, or 3 per day), maternal
education (primary, secondary, higher education), body
mass index (BMI), and current maternal smoking (yes/no)).
The adjusted odds ratios from the country-level analyses
were meta-analysed to give an overall effect estimate. The
I
2
statistic was used to assess heterogeneity between
countries.
Ethical Approval
Each participant centre obtained their own funding and
ethical approval prior to taking part in the study.
Results
Sample Characteristics and Prevalence of Allergic
Symptoms
General characteristics of children aged 6–7 years are
summarised in Table 1. A total of 53,635 children from
seven countries had complete data on respiratory symp-
toms and dietary exposures. Over a third of the population
(36.8%) reported watched television for at least 3 h a day,
whilst only 24% of these children practised exercise three
times per week. An overall 14% of mothers reported being
current smokers, with the highest prevalence of smoking
observed in Chile (35.7%) and the lowest (8.3%) in Brazil.
The overall prevalence of current wheeze was 12.4% (95%
confidence interval 12.1, 12.6).
The 13- to 14-year-old group was composed of
90,332 children from eleven countries (Table 2). Over
half of them (57.1%) reported watching television for at
least 3 h a day. Regular exercise (3 times per week) was
practised by 27% of these children. Maternal current
smoking showed large variations across countries, with
a prevalence of 4% in Panama and 37% in Uruguay. In
the majority of the countries, mothers completed sec-
ondary education. The overall prevalence of current
wheeze was (13.3% (95% CI 13.1, 13.5) in the group of
adolescents.
Table 1 General characteristics of children participating in ISAAC Phase III in Latin America (age group 6–7 years)
Variable Country Total
Brazil
(n=1070)
Chile
(n=6129)
Colombia
(n=12,679)
Mexico
(n=26,302)
Panama
(n=2943)
Venezuela
(n=3000)
Uruguay
(n=1512)
N=53,635
Males (%) 49.4 48.8 46.9 49.7 48.5 47.1 47.8 48.7
Body mass index (BMI) (kg/(height)
2
(Median, IQR difference)
16.5 (3.9) 17.4 (3.8) 16.5 (4.3) 16.5 (3.8) 16.5 (4.2) 17.2 (4.2) 16.3 (3.3) 16.6 (4.0)
C3 daily hours watching TV (n, %) 246 (23.0) 2273 (37.1) 5219 (41.2) 9365 (35.6) 680 (23.1) 1686 (56.2) 379 (25.1) 19,758 (36.8)
Physical activity 3 times per week (n, %) 94 (8.8) 1829 (29.8) 3328 (26.2) 5770 (21.9) 1112 (37.8) 516 (17.2) 381 (25.2) 13,030 (24.3)
Current maternal smoking (n, %) 89 (8.3) 2190 (35.7) 988 (7.8) 2811 (10.7) 111 (3.8) 724 (24.1) 355 (23.5) 7268 (13.6)
Maternal secondary education (n, %) 341 (31.9) 2552 (41.6) 6312 (49.8) 13,246 (50.4) 978 (33.2) 1396 (46.5) 720 (47.6) 25,545 (47.6)
Respiratory outcomes (n,%)
Current wheeze 183 (17.1) 987 (16.1) 1792 (14.1) 2063 (7.8) 659 (22.4) 599 (20.0) 341 (22.6) 6624 (12.4)
(95% CI 12.1, 12.6)
Current rhino-conjunctivitis 178 (16.6) 760 (12.4) 1950 (15.4) 2998 (11.4) 335 (11.4) 611 (20.4) 102 (6.7) 6934 (12.9)
(95% CI 12.6, 13.2)
Current eczema 62 (5.8) 823 (13.4) 1847 (14.6) 1523 (5.8) 411 (14.0) 371 (12.4) 119 (7.9) 5156 (9.5)
(95% CI 9.3, 9.8)
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Table 2 General characteristics of children participating in ISAAC Phase III in Latin America (age group 13–14 years)
Variable Country Total
Argentina Bolivia Brazil Chile Colombia Ecuador Mexico Panama Peru Venezuela Uruguay N =90,332
(n =6466) (n =3263) (n =9618) (n =10,689) (n =13,344) (n =3082) (n =29,747) (n =3184) (n =3022) (n =3000) (n =4917)
Males (%) 51.4 47 48.1 47.9 46.8 49.2 49.2 49.4 64.1 51.9 48.4 49.2
Body mass index
(BMI) (kg/
(height)
2
(Median, IQR
difference)
19 (3.4) 20 (4.3) 19 (3.9) 20.4 (3.8) 18.6 (3.8) 20.3 (4.2) 20.6 (4.3) 18.6 (2.6) 19.7 (3.5) 20.5 (4.5) 19.8 (3.6) 19.8 (4.1)
C3 daily hours
watching TV
(n, %)
3523 (54.5) 1712 (52.5) 5476 (56.9) 6809 (63.7) 9285 (69.6) 2094 (67.9) 15,339 (51.6) 739 (23.2) 1767 (58.5) 2109 (70.3) 2719 (55.3) 51,572 (57.1)
Physical activity
3 times per
week (n, %)
1139 (17.6) 1002 (30.7) 2390 (24.8) 3581 (33.5) 3435 (25.7) 692 (22.5) 8282 (27.8) 1194 (37.5) 239 (7.9) 686 (22.9) 1700 (34.6) 24,340 (26.9)
Current maternal
smoking
(n, %)
2153 (33.3) 763 (23.4) 1761 (18.3) 3092 (28.9) 2084 (15.6) 424 (13.8) 5465 (18.4) 117 (3.7) 632 (20.9) 845 (28.2) 1815 (36.9) 19,151 (21.2)
Maternal
secondary
education
(n, %)
2617 (40.5) 1258 (38.6) 2501 (26.0) 4952 (46.3) 6675 (50.0) 1550 (50.3) 11,153 (37.5) 1029 (32.3) 1023 (33.9) 1306 (43.5) 2592 (52.7) 36,656 (40.6)
Respiratory outcomes (n,%)
Current wheeze 844 (13.1) 422 (12.9) 1974 (20.5) 1608 (15.0) 1584 (11.9) 479 (15.5) 2533 (8.5) 720 (22.6) 592 (19.6) 463 (15.4) 807 (16.4) 12,026 (13.3)
(95% CI 13.1, 13.5)
Rhino-
conjunctivitis
1209 (18.7) 713 (21.9) 1458 (15.2) 2153 (20.1) 3470 (26.0) 737 (23.9) 4460 (15.0) 364 (11.4) 560 (18.5) 746 (24.9) 512 (10.4) 16,382 (18.1)
(95% CI 17.9, 18.4)
Eczema 454 (7.0) 664 (20.4) 413 (4.3) 1679 (15.7) 2119 (15.9) 409 (13.3) 1429 (4.8) 445 (14.0) 306 (10.1) 215 (7.2) 259 (5.3) 8392 (9.3)
(95% CI 9.1, 9.5)
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Only 62% of children aged 6–7 years and 61% of those
aged 13–14 years reported eating fruits 3 or more times per
week (Table S1, supplementary file) and less than half of
the children in both age groups had an intake of vegeta-
bles 3 or more times per week.
Association Between Respiratory Symptoms
and Dietary Intake
Fruits
Figure 1shows the adjusted per-country associations
between fruit intake and current wheeze. In children aged
6–7 years, there was a negative association between having
current wheeze and eating fruits three or more times per
week compared to less frequent consumption (adjusted
overall OR 0.85; 95% CI 0.74; 0.97). The meta-analysis
showed moderate heterogeneity (I
2
=46.4%). In children
aged 13–14 years, there was also a negative association
between current wheeze and intake of fruits, although this
was slightly attenuated (OR 0.89; 95% CI 0.82, 0.97).
There was very little evidence of heterogeneity across
countries (I
2
=7.0%).
Vegetables
A higher intake of vegetables was negatively associated
with current wheeze in children aged 6–7 years (Fig. 2;
I
2
=0%), whilst in older children there was no association,
and there was moderate heterogeneity in the estimates
across countries (Fig. 2;I
2
=67%).
Fastfood
Current wheeze was positively associated with eating
fastfood/burgers three or more times per week (Fig. 3). The
positive associations were found in both age groups, with
the effect size being slightly greater in younger children.
Heterogeneity was small in both meta-analyses.
We also investigated the association between these food
groups with secondary outcomes eczema and rhino-con-
junctivitis (supplementary file). In the younger children, a
more frequent intake of fruits was associated with a lower
prevalence of eczema (OR 0.64; 95% CI 0.56, 0.74; Fig-
ure S1; and OR 0.72; 95% CI 0.64, 0.82, Figure S4), whilst
the associations in the older children were less consistent
(Figures S1 and S4). A more frequent intake of fastfood
was positively associated with a higher prevalence of
eczema and rhino-conjunctivitis in older children (Fig-
ures S3 and S6; ORs 1.32; 95% CI 1.22, 1.43, and OR 1.32;
95% CI 1.24, 1.40, respectively).
Discussion
In this large multi-centre epidemiological study including
11 Latin American countries, we found that the overall
prevalence of allergic symptoms in children aged
6–7 years fluctuated between 9.9% (current eczema) and
12.5% (current wheeze). We found a consistent trend
across countries of a statistically significantly negative
association between fruit, and vegetable, and allergic
symptoms in the younger children. Such associations were
attenuated in older children. We also found that frequent
intake of fast foods or burgers was positively associated
with a greater prevalence of allergic symptoms in adoles-
cents and with wheeze in the younger children.
The meta-analyses on fruit intake and wheeze, eczema,
and rhino-conjunctivitis showed very small heterogeneity
in the group of 6- to 7-year-old children. The large sample
size of the study, and the use of a standardised protocol to
ascertain the prevalence of allergic symptoms and of fre-
quency of food intake, might have contributed to the small
heterogeneity. The fact that the effect sizes were fairly
consistent across countries suggests that these associations
might be biologically plausible. The heterogeneity and
effect sizes were less consistent in the meta-analyses that
examined dietary intake of vegetable and fastfood in ado-
lescents, which might partly be explained by the increasing
differentiation in the diet of older children.
Our findings also showed that three quarters of all the
children studied had a sedentary lifestyle, reflected in the
low frequency of physical exercise practised per week.
Similarly, despite the strong public health promotion of
daily intake of fruits and vegetables in children, we found
that only 60% of the children eat these foods at least three
times per week.
Diet is one of the key factors that can influence the
susceptibility to allergic diseases [15] and can explain, at
least in part, the current rates of asthma prevalence in Latin
American countries. Latin America groups the Spanish and
Portuguese-speaking countries south of the United States.
In addition to the language, the population in this region
has several common characteristics. The Latin American
nations are largely composed of ‘Mestizos’ (those having
Indigenous and Spanish/other European/African ascent)
and indigenous people. The staple diet in most of these
countries includes fresh cereals and vegetables (potatoes,
maize, rice), although as with most growing economies, the
effects of ‘Westernisation’ are increasingly departing the
traditional diets towards consumption of fast food and
other energy-dense and low-cost foods.
The ISAAC study provided for the first time standard-
ised estimates of childhood asthma prevalence worldwide.
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ISAAC Phase Three produced internationally comparable
estimates of direction and magnitude of change in symp-
toms of asthma, rhino-conjunctivitis, and atopic eczema
[5]. The study also showed that in developing countries
asthma and allergic disease were increasing.
We found that 75% of children had a fruit and veg-
etable intake below the five portions a day recommended
by the WHO [16]. Worldwide variations in frequency of
consumption of fruits and vegetables were reported for the
first time in 2009 for adults from 52 countries, showing that
lower income countries also have difficulties adhering to
these recommendations [17]. The study showed figures for
four countries from Latin America (Brazil, Ecuador,
Paraguay, and Uruguay), all of which reported having at
least 50% of adults eating less than 5 portions of fruits or
vegetables per day. Our study is the first to demonstrate
6-7 years old
13-14 years old
Fig. 1 Meta-analyses of
adjusted associations between
current wheeze and fruit intake
in children participating in
ISAAC Phase III Latin America
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that the vast majority of Latin American children are not
meeting these recommendations.
Despite the fact that asthma is an important public
health burden in countries from this region [1], there have
been few studies investigating the role that diet and other
lifestyle-related risk factors might play in the risk of
allergic diseases in Latin America. A negative association
between fruit intake and childhood asthma has been sug-
gested in low- and high-affluent countries [18]. A recent
overview of high-quality systematic reviews on diet and
asthma concluded that there is evidence to suggest that
children who have a higher intake of fruits, or have diets
which are rich in these foods, are less likely to suffer from
asthma or allergic symptoms [19].
There is biological plausibility for the possible effect of
fruits and vegetables on allergic symptoms. Oxidative
stress plays a role in the inflammatory process that leads to
the clinical expression of asthma and other allergic con-
ditions such as eczema and rhino-conjunctivitis. Fruits and
vegetables are rich in a number of antioxidant vitamins and
6-7 years old
13-14 years old
Fig. 2 Meta-analyses of
adjusted associations between
current wheeze and
vegetable intake in children
participating in ISAAC Phase
III Latin America
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minerals, as well as flavonoids whose antioxidant and anti-
inflammatory properties have been suggested to reduce and
modulate airway and allergic diseases. Experimental
studies have demonstrated that flavonoids can inhibit the
release of histamine and of several inflammatory cytokines
including IL-4 and IL-13 [20], which are closely involved
in the chain of events leading to the clinical manifestation
of symptoms. Several well-designed randomised controlled
trials (RCTs) have been carried out to test the demonstra-
bility of such effects, but have so far shown little or no
effect of the use of nutritional supplements on allergic
outcomes [21].
A new concept of ‘indigenous microbiota’ which sug-
gests that food consumed directly from the soil where it is
harvested (rather than industrially produced) might also
protect against the risk of asthma and allergies. It is known
6-7 years old
13-14 years old
Fig. 3 Meta-analyses of
adjusted associations between
current wheeze and fastfood
intake in children participating
in ISAAC Phase III Latin
America
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that fruits and vegetables are densely covered with
microbiota (ectophytes), but the idea that these fresh
products harbour a microbial world within (endophytes)
has been only recently shown [22]. A low gut microbiota
might be linked to poorer respiratory [23] and allergic [24]
outcomes in children, and a rich microbiota is facilitated by
freshly produced plant-based foods. Developed countries in
Europe are now often able to market fruits and vegeta-
bles regardless of their seasonality, due to the high pro-
cessing and artificial maturation these foods undergo. In
Latin America, food markets are still common and widely
accessed by the general population, often preferred to
supermarkets (grocery shops) for their lower cost. Our
findings could lend support to educational and intervention
strategies to make fruits and vegetables more accessible to
the population, like those investigated in other populations
[25].
The introduction of a more ‘Westernised’ lifestyle has
been increasingly suggested to play a role in the current
burden of asthma in countries that are shifting towards a
higher consumption of more energy-dense diet, which are
characterised for their lower cost and high content of sat-
urated fats. Our findings show that fast food intake in Latin
America is very common in children, particularly in ado-
lescents, of whom nearly a 20% reported eating these foods
three or more times per week. The risk of current wheeze
was positively associated with intake of fastfood in
younger and older children, but this risk was higher in the
adolescents. As consequence of the Westernisation of diet
and of lifestyle in Latin America, the rates of cardio-
metabolic diseases is increasing and the rates of obesity are
a major public health challenge in the region [26]. The low
cost of these foods and the high calorie content make fast
food an appealing option for many families, in particular to
those in a more vulnerable socio-economic position. The
easy access that children have to processed and sugary food
is also a major issue in many primary schools across the
continent.
A major challenge to improve childhood global health in
Latin America is to provide evidence from studies that can
translate in public health interventions and in affordable
and sustainable health care to the population [27]. Latin
America is a region with large economic and social vari-
ations, and where public health resources are usually lim-
ited. Our results suggest that dietary intake of fruits might
reduce the risk of allergic diseases in children, and that
Westernisation of diet might contribute to the increase in
the prevalence of allergic symptoms as children grow
older. Timing appears to be an important factor, as the
protective effect observed from higher intake of fruits and
vegetables in younger children attenuates or disappears in
older children. These results provide a foundation to inform
public health policy.
Acknowledgements We are grateful to the mothers and children who
took part in the study. The ISAAC Phase III study in Latin America
was made possible through independent funding secured by each
participant centre. We are grateful to the Coordinating Centre in New
Zealand for the helpful support with the access to the data. We are
indebted to Professor Majid Ezzati for his careful comments on the
interpretation of the results.
Collaborators for the Latin American ISAAC Phase 3 Study
Group ARGENTINA: Carlos E Baena-Cagnani, Gustavo E Zabert,
Carlos D Crisci, Maximiliano Go
´mez, Hugo Neffen; BOLIVIA:
Rosario Pinto-Vargas; BRAZIL: Dirceu Sole
´, Jackeline Machado-
Motta, Ricardo A Gurgel , Paulo A Camargos, Wellington G Borges,
Almerinda Silva, Nelson A Rosa
´rio, Leda Solano Costa Leda de
Freitas Souza, Cla
´udia Dutra-Bernhardt, Francisco Jose
´Passos-
Soares, Mercia Lamenha, Maria do Socorro Cardoso, Anto
ˆnio Ledo
Aves da Cunha, Arnaldo Porto-Neto, Gilberto Bueno Fischer, Victor
E Cassol, Cassia Gonzales , Karyn C Melo, Cristina A Jacob, Fabio
Kuschnir, Emanuel Sarinho Murilo de Britto, Neusa Wandalsen,
Antonio Carlos Pastorino; BOLIVIA: Rosario Pinto, Esther Serrate,
Roberto Paz, Pitias Sua
´rez, Oscar Go
´mez, Janet Aguirre; CHILE:
Viviana Aguirre-Camposano, Luis Vera-Benavides, Amanda Contr-
eras, Lidia Amarales, Pedro Aguilar, Mario A Calvo, Javier Mallol
(Regional Coordinator); COLOMBIA: Alfonso M. Cepeda, Gustavo
Aristiza
´bal, Gustavo A Ordon
˜ez; COSTA RICA: Manuel Soto-
Quiroz. CUBA: Patricia Varona-Pere
´z, ECUADOR: Ce
´sar Bustos,
Sergio Barba, Rocı
´o de Jano
´n, Mireya Rodas, Alfredo Sierra, Jose
´
Ulloa,. EL SALVADOR: Margarita Figueroa-Colorado; HON-
DURAS: Agustin Bueso-Engelhardt; MEXICO: Manuel Baeza-Ba-
cab, Blanca E Del Rı
´o-Navarro, Mercedes Barraga
´n-Meijueiro, Nelly
Ramı
´rez-Chanona, Roberto Garcı
´a-Almaraz, Isabelle Romieu,
Valente Merida-Palacio, Sandra Nora Gonza
´lez-Dı
´az, Francisco J.
Linares-Zapie
´n, Sergio Romero-Tapia; NICARAGUA: Jose
´FSa
´n-
chez; PANAMA: Gherson Cukier; PARAGUAY: Jaime A. Guggiari-
Chasse; PERU: Pascual Chiarella; URUGUAY: Dolores Holgado,
Marı
´a Cristina Lapides; VENEZUELA: Oscar Aldrey.
Compliance with Ethical Standards
Conflict of interest The authors declare that they have no conflict of
interest.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://crea
tivecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
References
1. Forno E, Gogna M, Cepeda A, Yanez A, Sole D, Cooper P et al
(2015) Asthma in Latin America. Thorax 70:898–905
2. Asher MI, Montefort S, Bjorksten B, Lai CK, Strachan DP,
Weiland SK et al (2006) Worldwide time trends in the prevalence
of symptoms of asthma, allergic rhinoconjunctivitis, and eczema
in childhood: ISAAC Phases One and Three repeat multicountry
cross-sectional surveys. Lancet 368:733–743
3. Mallol J, Sole D, Baeza-Bacab M, Aguirre-Camposano V, Soto-
Quiros M, Baena-Cagnani C et al (2010) Regional variation in
asthma symptom prevalence in Latin American children.
J Asthma 47:644–650
Lung (2017) 195:683–692 691
123
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

4. Pearce N, Asher I, Billo N, Bissell K, Ellwood P, El Sony A et al
(2013) Asthma in the global NCD agenda: a neglected epidemic.
Lancet 1:96–98
5. Asher I, Pearce N (2014) Global burden of asthma among chil-
dren. Int J Tuberc Lung Dis 18:1269–1278
6. Cooper PJ, Rodrigues LC, Cruz AA, Barreto ML (2009) Asthma
in Latin America: a public heath challenge and research oppor-
tunity. Allergy 64:5–17
7. Silveira DH, Zhang L, Prietsch SO, Vecchi AA, Susin LR (2015)
Association between dietary habits and asthma severity in chil-
dren. Indian Pediatr 52:25–30
8. Mendes AP, Zhang L, Prietsch SO, Franco OS, Gonzales KP,
Fabris AG et al (2011) Factors associated with asthma severity in
children: a case-control study. J Asthma 48:235–240
9. Cepeda AM, Del Giacco SR, Villalba S, Tapias E, Jaller R,
Segura AM et al (2015) A traditional diet is associated with a
reduced risk of eczema and wheeze in Colombian children.
Nutrients 7:5098–5110
10. Garcia-Larsen V, Amigo H, Bustos P, Bakolis I, Rona RJ (2015)
Ventilatory function in young adults and dietary antioxidant
intake. Nutrients 7:2879–2896
11. Garcia-Larsen V, Chinn S, Arts IC, Amigo H, Rona RJ (2007)
Atopy, wheeze and bronchial responsiveness in young Chilean
adults. Do dietary antioxidants matter? Allergy 62:714–715
12. Ellwood P, Asher MI, Garcia-Marcos L, Williams H, Keil U,
Robertson C et al (2013) Do fast foods cause asthma, rhinocon-
junctivitis and eczema? Global findings from the International
Study of Asthma and Allergies in Childhood (ISAAC) phase
three. Thorax 68:351–360
13. Mallol J, Crane J, von Mutius E, Odhiambo J, Keil U, Stewart A
et al (2013) The International Study of Asthma and Allergies in
Childhood (ISAAC) Phase Three: a global synthesis. Allergol
Immunopathol 41:73–85
14. Ellwood P, Asher MI, Beasley R, Clayton TO, Stewart AW,
Committee IS (2005) The international study of asthma and
allergies in childhood (ISAAC): phase three rationale and
methods. Int J Tuberc Lung Dis 9:10–16
15. Julia V, Macia L, Dombrowicz D (2015) The impact of diet on
asthma and allergic diseases. Nat Rev Immunol 15:308–322
16. Organisation WH (2000) Global strategy on diet, physical
activity and health. WHO, Geneva
17. Hall JN, Moore S, Harper SB, Lynch JW (2009) Global vari-
ability in fruit and vegetable consumption. Am J Prev Med
36(402–9):e5
18. Nagel G, Weinmayr G, Kleiner A, Garcia-Marcos L, Strachan
DP, Group IPTS (2010) Effect of diet on asthma and allergic
sensitisation in the International Study on Allergies and Asthma
in Childhood (ISAAC) Phase Two. Thorax 65:516–522
19. Garcia-Larsen V, Del Giacco SR, Moreira A, Bonini M, Reeves
T, Charles D, Carlsen K-H, Haahtela T, Bonini S, Fonseca J,
Agache I, Papadopoulos NG, Delgado L (2016) Asthma and food
intake: an overview of systematic review. Allergy 71(4):433–442
20. Tanaka T (2014) Flavonoids for allergic diseases: present evi-
dence and future perspective. Curr Pharm Des 20:879–885
21. Moreno-Macias H, Romieu I (2014) Effects of antioxidant sup-
plements and nutrients on patients with asthma and allergies.
J Allergy Clin Immunol 133:1237–1244
22. von Hertzen L (2015) Plant microbiota: implications for human
health. Br J Nutr 114:1531–1532
23. Arrieta MC, Stiemsma LT, Dimitriu PA, Thorson L, Russell S,
Yurist-Doutsch S et al (2015) Early infancy microbial and
metabolic alterations affect risk of childhood asthma. Sci Trans
Med 7:307ra152
24. West CE, Ryden P, Lundin D, Engstrand L, Tulic MK, Prescott
SL (2015) Gut microbiome and innate immune response patterns
in IgE-associated eczema. Clin Exp Allergy 45:1419–1429
25. Waterlander WE, de Boer MR, Schuit AJ, Seidell JC, Steenhuis
IH (2013) Price discounts significantly enhance fruit and veg-
etable purchases when combined with nutrition education: a
randomized controlled supermarket trial. Am J Clin Nutr
97:886–895
26. Uauy R, Albala C, Kain J (2001) Obesity trends in Latin
America: transiting from under- to overweight. J Nutr 131:893S–
899S
27. Scaling Program Investments for Young Children Globally
(2015) Evidence from Latin America and the Caribbean: sum-
mary of a joint workshop by the Institute of Medicine, the
National Research Council, and Fundacao Maria Cecilia Souto
Vidigal, Sao Paolo. The National Academies Collection: Reports
funded by National Institutes of Health. Washington (DC)
692 Lung (2017) 195:683–692
123
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

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