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

Authors:
  • Fundación Hospital Universitario Metropolitano, Barranquilla, Colombia
  • TEMT Project - Swiss TPH

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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.
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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
[13]. 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.
684 Lung (2017) 195:683–692
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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.
Lung (2017) 195:683–692 687
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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
688 Lung (2017) 195:683–692
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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.
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... countries in children aged 6-7 years (18). A systematic review of 16 observational studies reported that asthma was associated with the consumption of fast foods (OR: 1.34; 95% CI: 1.23-1.46). ...
... Despite this heterogeneity, we found an association similar to that reported in studies with older children. The proinflammatory effect of consuming a high-carbohydrate diet is consistent throughout childhood, as shown by the evidence in children under 2 years of age, children over 6 years of age, and our evidence in children between 2 and 6 years of age (9,18). In our study the proportion of patients with obesity were higher in patients with severe exacerbation than moderate or mild exacerbation, but this difference was not statistically significant may be due to small sample size; however we adjust all variables in the multivariate regression with the weight due previous literature on the topic. ...
Article
Full-text available
Introduction: Over the last decades, dietary habits in developing countries have been characterized by low intake of fruits and vegetables and high consumption of sweetened drinks. Most of the evidence linking carbohydrate intake and asthma comes from children over 6 years of age. The aim of this study was to examine the association between macronutrient intake and the severity of asthma exacerbations in children aged 2 to 6 years. Methods: We performed a cross-sectional study that included all children aged 2 to 6 years hospitalized due to an asthma exacerbation. Dietary data were collected using a food frequency questionnaire (FFQ) validated in the Colombian population. The GINA classification of acute asthma was used to define the severity. To identify factors independently associated with asthma exacerbation severity, we fit the data to ordinal logistic regression. Results: During the study period, 228 cases of patients with asthma exacerbation were included. Asthma severity was dose-dependently associated with protein and carbohydrate-rich intake. The variables included in the multivariable analysis included reactive C protein (OR 1.05, CI 95% (1.03-1.07)), smoking at home (OR 3.92 (1.82-8.44)), atopic dermatitis (OR 3.82 (1.59-9.21)), and protein and carbohydrate-rich food intake (OR 0.11 (0.03-0.33)) and (OR 2.42 (1.09-5.80)), respectively. Conclusion: High carbohydrate-rich food intake is associated with the severity of asthma exacerbation adjusted by other known risk factors such as atopy, smoking, and reactive C protein. This evidence should motivate the development of public health policies to control the consumption of sugar-rich products in children under 6 years.
... [14][15][16] Similarly, higher consumption of vegetables was found to be inversely associated with allergic asthma and moderate/severe airway hyper-responsiveness 17 and a recent multicenter epidemiologic study revealed that a higher frequency intake of fruits or vegetables was negatively associated with current wheeze. 18 Diet diversity may also be associated with reduced allergy outcomes in infancy, whose role in food allergy has been clearer than other allergies. 19,20 In this context, additional studies are required to define more clearly the role of this quality measure in asthma and related outcomes. ...
... 45 Evidence has shown that patients with atopy and asthma have increased FeNO compared with healthy individuals, 44 CI 0.80, 1.00, respectively). 18 Furthermore, a prospective cohort involving primary schools from Japan found that higher amount of fruit intake was significantly associated with lower prevalence of asthma (OR = 0.44; 95% CI 0.02, 0.85) and allergic (OR = 0.31; 95% CI 0.14, 0.68) symptoms. 14 Our study has a few limitations. ...
Article
Full-text available
Background A diet rich in fruits and vegetables has been suggested to counteract the oxidative stress and inflammation that characterize asthma. We aimed to assess the association between vegetable and fruit diversity consumption and asthma and its related outcomes in school‐aged children. Methods Participants included 647 children (49% females, aged 7 to 12 years) recruited from 20 public schools across the city of Porto, in Portugal. Vegetable and fruit intake were ascertained using a single self‐reported 24‐hour recall questionnaire. A diversity score was built taking into account the different number of individual vegetables and fruits consumed, and categorized into two groups based on the total reported median consumption , which was rounded to the nearest whole number (≤3 and >3, for vegetables, and ≤1 and >1, for fruits). A questionnaire was used to enquire about self‐reported medical diagnosis of asthma and respiratory symptoms. Airway inflammation was assessed measuring exhaled fractional nitric oxide concentration (eNO) and was categorized into two groups (<35 and ≥35ppb). The association between fruit and vegetable diversity and respiratory outcomes was examined using logistic regression models, adjusting for confounders. Results A higher vegetable diversity consumption per day was negatively associated with having self‐reported asthma (OR= 0.67, 95%CI 0.47; 0.95), while having a vegetable diversity consumption superior than 3 items per day was negatively associated with levels of eNO ≥35ppb (OR= 0.38, 95%CI 0.16; 0.88) and breathing difficulties (OR= 0.39, 95%CI 0.16; 0.97). Conclusion Eating a greater variety of vegetables was associated with a lower chance of airway inflammation and prevalence of self‐reported asthma in school children.
... Moreover, a multicenter cross-sectional study of 143,967 children from 11 Latin American countries found that high consumption of fruits and vegetables was associated with lower prevalence of current wheeze, whereas fast food intake was associated with wheeze and symptoms of rhinoconjunctivitis and eczema. 20 In further support of potential protective effects of a healthy diet against asthma, a 6month pilot randomized clinical trial in 90 adults showed that a diet low in saturated fats and rich in fruits and vegetables was associated with improved asthma control. 21 Consistent with our findings in a longitudinal study of youth, an unhealthy diet was linked to asthma or asthma symptoms in prior cross-sectional studies. ...
Article
Background Poor diet quality may contribute to the disproportionate asthma burden in Puerto Rican youth. Objective To examine whether an unhealthy diet at one or two study visits conducted over ∼5 years is associated with asthma, severe asthma exacerbations, and worse lung function in Puerto Rican youth. Methods Prospective study of 406 Puerto Rican youth aged 6-14 years at a baseline visit and 9-20 years at a follow-up visit. As in prior work, diet was assessed using a dietary score ranging from -2 to +2. Our exposure of interest was an unhealthy diet, defined as a non-positive dietary score (0 to -2) at one or both visits. Our outcomes of interest were asthma (defined as physician-diagnosed asthma and ≥1 episode of wheeze in the year prior to the second visit), ≥1 severe asthma exacerbation in the year prior to the second visit, and change in percent predicted lung function measures (FEV1, FVC, and FEV1/FVC) between the first and second visits. Results In a multivariable analysis, an unhealthy diet at both visits was associated with increased odds of asthma (adjusted odds ratio [aOR]=3.38, 95% confidence interval [CI]=1.74 to 6.57) and severe asthma exacerbations (aOR=2.65, 95% CI=1.16 to 6.03), but not with change in lung function. Conclusions An unhealthy diet at both visits was associated with increased odds of asthma and severe asthma exacerbations compared with a healthy diet at both visits. Our findings support health policies promoting a healthy diet in Puerto Rican youth, a population at high risk for asthma.
... Finally, we found that a diet rich in fried and processed meats was associated with asthma and asthma-associated intestinal metabolites. Several prior studies have found positive associations between processed or fried meat consumption and asthma, [52][53][54] and one recent systematic review found that hamburger consumption had a particularly strong association with asthma. 55 Our findings support a causal pathway whereby intestinal metabolites mediate at least part of the association between fried and processed meat consumption and asthma. ...
Article
Background The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology. Objective We sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial. Methods Metabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other “omics”: the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires. Results Several intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = −6.3; 95% CI, −11.3 to −1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites. Conclusion Integrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies.
... More detailed information on each allergic disease is described in the eAppendix in the Supplement. [27][28][29][30] The Cronbach α coefficient of the ISAAC allergic questionnaire in the sampled children was 0.94. Validity determined by the Kaiser-Meyer-Olkin method was 0.94. ...
Article
Full-text available
Importance: Information on the association between maternal prepregnancy body weight, gestational weight change, and childhood allergies is not consistent. Little is known on whether there is a combined association with comprehensive childhood allergies. Objective: To examine the association of maternal prepregnancy body mass index and gestational weight gain (GWG) with the risk of childhood allergic diseases including asthma and/or wheezing, allergic rhinitis, eczema, and food and/or drug allergy. Design, setting, and participants: This cross-sectional study was conducted from April 12 to June 1, 2019, using the Shanghai Children Allergy Study (SCAS), a large, population-based survey. A multistage and multistrata sampling approach was applied to conduct the survey in 13 districts across Shanghai, China, with an enrollment of 15 145 mother-child pairs. Exposures: Reported maternal weight before pregnancy and at the time of delivery were requested in the survey; GWG was examined in absolute terms and with reference to the Institute of Medicine guideline. Main outcomes and measures: The ascertainment of allergic diseases was based on the International Study of Asthma and Allergies in Childhood questionnaire. Results: Among 15 145 children aged 3 to 14 years (7911 [52.2%] boys) within the SCAS, 8877 children (58.6%) were screened for allergic diseases. Multivariable log-binomial regression models suggested that excessive GWG was associated with risks of 19% for asthma/wheezing, 11% for allergic rhinitis, and 10% for eczema in the children. Gestational weight gain extremely above the Institute of Medicine guideline in women who were overweight/obese before pregnancy was associated with the highest risk of childhood asthma/wheezing (adjusted prevalence ratio, 1.42; 95% CI, 1.16-1.74; P = .001), allergic rhinitis (adjusted prevalence ratio, 1.32; 95% CI, 1.12-1.56; P = .001), and eczema (adjusted prevalence ratio, 1.24; 95% CI, 1.08-1.41; P = .002). Gestational weight gain below the Institute of Medicine guideline was associated with an attenuated risk of 13% for childhood asthma/wheezing, 11% for allergic rhinitis, 14% for eczema, and 15% food/drug allergy when mothers were of prepregnancy normal weight; similar associations were observed in underweight mothers, but there was no association in overweight mothers. Generally, the associations were similar in the stratified analysis according to children's age group. Moreover, the results were similar in the allergen test subgroup. Conclusions and relevance: The findings of this study suggest that excessive GWG may be a risk factor for childhood allergic diseases. Further studies on the long-term effects of the intrauterine environment on children's health may take maternal weight management during pregnancy into consideration since GWG could be a controllable and modifiable risk factor.
Chapter
Over the last 30 years, the role of diet in asthma prevention and management has gained interest in the international literature, and many papers have been published on these topics. Taken together, the literature is inconclusive, probably due to the complexity of both the exposures and outcomes and, consequently, their associations. Indeed, published epidemiological studies are very heterogeneous regarding diet assessment, diet estimation, a window of exposure (antenatal/childhood/adulthood diet), and asthma expression (primary/secondary prevention). In addition, being an essential part of lifestyle, diet is highly associated with obesity and other lifestyle factors, as well as social determinants. These factors may act in a more complicated way than simple confounders in the diet–asthma association. The chapter reviews studies on the topic and includes a discussion on the interrelations between diet, obesity, and physical activity in asthma prevention and management.
Article
Rationale: Protective effects of a high quality diet on respiratory health, particularly among youths exposed to environmental tobacco smoke (ETS), are unknown. Objectives: To assess if a higher quality diet is associated with improved respiratory symptoms and lung function among adolescents, and if these associations are modified by ETS exposure. Methods: This was a cross-sectional study on 7,026 nonsmoking adolescents of the 2003-2012 National Health and Nutrition Examination Survey. Diet quality was assessed using the Healthy Eating Index-2010 score (HEI-2010), categorized into quintiles. ETS exposure was measured using serum cotinine, dichotomized as high (>2.99 ng/ml) or low (≤2.99 ng/ml). Outcomes included the presence of wheezing and cough symptoms in the past 12 months, and in a sub-group, spirometric lung function. Survey-design adjusted logistic and linear models evaluated associations between diet and 1) respiratory symptoms and 2) lung function, respectively, and assessed the interaction between HEI-2010 and serum cotinine. Results: While there were no significant associations between diet quality and respiratory symptoms, there was a significant interaction between HEI-2010 and serum cotinine on wheezing (pint = 0.011). In models stratified by serum cotinine, adolescents with high serum cotinine and the healthiest diet (5th quintile HEI-2010) experienced lower wheezing odds (OR, 0.10; 95% CI, 0.02-0.61), compared to those with the poorest diet (1st quintile HEI-2010). In contrast, among adolescents with low serum cotinine, there were no significant differences in any respiratory symptoms between those with the highest, compared to the lowest diet quality. Of the sub-group with spirometry data (n = 3,166), there was a trend towards better lung function with improving diet quality, although this did not achieve statistical significance. There was no effect modification by ETS exposure on the relationship between diet quality and lung function. Conclusions: Consuming a higher quality diet was associated with lower wheezing odds in adolescents with substantial ETS exposure. While longitudinal studies are needed, public health interventions to improve diet quality in vulnerable, environmentally-exposed populations merit consideration.
Article
Background While the microbiome has an established role in asthma development, less is known about its contribution to morbidity in children with asthma. Objective In this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial (VDAART), we analyzed the gut microbiome and metabolome of wheeze frequency in children with asthma. Methods Bacterial 16s rRNA microbiome and untargeted metabolomic profiling were performed on fecal samples collected from three-year-old children with parent-reported physician-diagnosed asthma. We analyzed wheeze frequency by calculating the proportion of quarterly questionnaires between ages 3 and 5 years in which parents reported the child had wheezed (“wheeze proportion”). Taxa and metabolites associated with wheeze were analyzed by identifying log-fold changes with respect to wheeze frequency and correlation/linear regression analyses, respectively. Microbe-metabolite and microbe-microbe correlation networks were compared between subjects with high and low wheeze proportion. Results Specific taxa, including the genus Veillonella and histidine pathway metabolites, were enriched in subjects with high wheeze proportion. Amongst wheeze-associated taxa, Veillonella and Oscillospiraceae UCG-005, which was inversely associated with wheeze, were correlated with the greatest number of fecal metabolites. Microbial networks were similar between subjects with low vs. high wheeze frequency. Conclusion Gut microbiome features are associated with wheeze frequency in children with asthma, suggesting an impact of the gut microbiome on morbidity in childhood asthma.
Article
Full-text available
This study aimed to explore associations between non-cholesterol sterol concentrations in breast milk and allergic outcomes in children aged two. Data from the KOALA Birth Cohort Study, the Netherlands, were used. Non-cholesterol sterols were analyzed by gas–liquid chromatography–mass spectrometry in breast milk sampled one-month postpartum (N = 311). Sterols were selected for each allergic outcome, i.e., eczema, wheeze, and allergic sensitization, prior to analyses. Associations between the selected sterols with allergic outcomes were analyzed using multiple logistic regression to calculate odds ratios (ORs). The odds of eczema in the first two years of life were lower with higher concentrations of cholestanol (OR (95%CI): 0.98 (0.95; 1.00), p = 0.04), lanosterol (0.97 (0.95; 1.00), p = 0.02), lathosterol (0.93 (0.87; 0.99), p = 0.02), and stigmasterol (0.51 (0.29; 0.91), p = 0.02) in breast milk sampled one-month postpartum. None of the sterols were associated with wheeze in the first two years of life. The odds of allergic sensitization at age two were lower with higher concentrations of campesterol in breast milk (OR (95%CI): 0.81 (0.70; 0.95), p = 0.01). In conclusion, our data suggest that exposure to higher non-cholesterol sterol concentrations in breast milk may indeed be associated with the prevention of allergic outcomes in the first two years of life.
Article
Full-text available
Introduction: Diet and physical activity might be associated with the risk of allergic diseases in childhood. However, evidence in literature is sparse and diverse. We aim to examine the associations between four healthy dietary consumption pattern drinks, plus the adherence to a physically active lifestyle with atopic diseases (asthma, allergic rhinitis and eczema) in adolescence and their relative importance. Methods: A total of 1934 adolescents (921 boys, 47.5%) and their parents completed a validated questionnaire assessing atopic diseases' symptoms prevalence in the past 12 months, as well as nutritional and physical activity information. Four healthy dietary and one physical active lifestyle patterns were identified and logistic regression was applied to assess their relation with allergic diseases. Results: A high weekly consumption of fruits, vegetables and pulses and low consumption of unhealthy foods was negatively associated with all atopic symptoms while adherence to a physical active lifestyle was inversely associated with asthma and allergic rhinitis symptoms and dairy products with asthma and eczema symptoms in the past 12 months after adjustment for several confounders (all p < 0.05). Fruits, vegetables and pulses consumption per week emerged as the most important lifestyle pattern negatively associated for all atopic diseases, after the adjustment for all the remaining lifestyle patterns and confounders (all p < 0.05) Conclusions: Our findings suggest that a high fruit, vegetable and pulse intake should be the first lifestyle intervention every clinician and public health care worker evolving in the management of atopic adolescents should encourage and promote.
Article
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Epidemiological research on the relationship between diet and asthma has increased in the last decade. Several components found in foods have been proposed to have a series of antioxidant, anti-allergic and anti-inflammatory properties, which can have a protective effect against asthma risk. Several literature reviews and critical appraisals have been published to summarise the existing evidence in this field. In the context of this EAACI Lifestyle and asthma Task Force, we summarise the evidence from existing systematic reviews on dietary intake and asthma, using the PRISMA guidelines. We therefore report the quality of eligible systematic reviews and summarise the results of those with an AMSTAR score ≥32. The GRADE approach is used to assess the overall quality of the existing evidence. This overview is centred on systematic reviews of nutritional components provided in the diet only, as a way to establish what type of advice can be given in clinical practice and to the general population on dietary habits and asthma. This article is protected by copyright. All rights reserved.
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Plant microbiota: implications for human health - Volume 114 Issue 9 - Leena von Hertzen
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About 334 million people worldwide suffer from asthma, and this figure may be an underestimation. It is the most common chronic disease in children. Asthma is among the top 20 chronic conditions for global ranking of disability-adjusted life years in children; in the mid-childhood ages 5–14 years it is among the top 10 causes. Death rates from asthma in children globally range from 0.0 to 0.7 per 100 000. There are striking global variations in the prevalence of asthma symptoms (wheeze in the past 12 months) in children, with up to 13-fold differences between countries. Although asthma symptoms are more common in many high-income countries (HICs), some low- and middle-income countries (LMICs) also have high levels of asthma symptom prevalence. The highest prevalence of symptoms of severe asthma among children with wheeze in the past 12 months is found in LMICs and not HICs. From the 1990s to the 2000s, asthma symptoms became more common in some high-prevalence centres in HICs; in many cases, the prevalence stayed the same or even decreased. At the same time, many LMICs with large populations showed increases in prevalence, suggesting that the overall world burden is increasing, and that therefore global disparities in asthma prevalence are decreasing. The costs of asthma, where they have been estimated, are relatively high. The global burden of asthma in children, including costs, needs ongoing monitoring using standardised methods.