Journal of Agromedicine

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Rural Dwelling and Temporal Trends in Relation

to Childhood Asthma and Related Conditions in
Belarus: A Repeated Cross-sectional Survey

Grzegorz Brozek, Andrei Shpakou, Joshua Lawson & Jan Zejda

To cite this article: Grzegorz Brozek, Andrei Shpakou, Joshua Lawson & Jan Zejda (2015) Rural
Dwelling and Temporal Trends in Relation to Childhood Asthma and Related Conditions in
Belarus: A Repeated Cross-sectional Survey, Journal of Agromedicine, 20:3, 332-340, DOI:
10.1080/1059924X.2015.1042616

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 Journal of Agromedicine, 20:332–340, 2015
Copyright © Taylor & Francis Group, LLC
ISSN: 1059-924X print/1545-0813 online
DOI: 10.1080/1059924X.2015.1042616

Rural Dwelling and Temporal Trends in Relation to

Childhood Asthma and Related Conditions in Belarus:
A Repeated Cross-sectional Survey
Grzegorz Brozek,1 Andrei Shpakou,2 Joshua Lawson,3 and Jan Zejda1
1 Department
of Epidemiology, School of Medicine in Katowice,
Medical University of Silesia, Katowice, Poland
2 Department of Sport Medicine and Rehabilitation, Yanka Kupala State University of Grodno,
Downloaded by [University of Lethbridge] at 19:32 10 November 2015

Grodno, Belarus
3 Department of Medicine and Canadian Centre for Health and Safety in Agriculture,

University of Saskatchewan, Saskatoon, Saskatchewan, Canada

ABSTRACT. There is a lack of asthma research in Belarus, with no investigation of temporal trends.
The purpose of the study was to determine the prevalence of asthma and related conditions compar-
ing urban and rural children while investigating temporal changes in the region of Grodno, Belarus.
A repeated cross-sectional survey design was used. Parents completed surveys on behalf of the child.
Data collection was based on the International Study of Asthma and Allergies in Children (ISAAC)
survey and included 5020 urban and rural children aged 7–15 years in 2009–2010 and 4953 chil-
dren in 2014 from the Grodno Region. Asthma prevalence in 2009 was 1.4% compared with 1.8%
in 2014, whereas spastic bronchitis prevalence was higher (2009: 6.8%; 2014: 8.5%). After adjustment
for confounders, rural dwelling showed a statistically significant inverse association with each of the
allergic conditions or symptoms. However, asthma (odds ratio [OR] = 1.01, 95% confidence interval
[CI] = 0.69–1.50) was not associated with rural dwelling. A diagnosis of asthma was more likely in
2014 compared with 2009 (OR = 1.57, 95% CI = 1.05–2.33), as was spastic bronchitis (OR = 1.26,
95% CI = 1.06–1.51). Maternal smoking was associated with the presence of respiratory symptoms.
The data showed that the prevalence of diagnosed asthma was comparable between urban and rural
areas but lower than other regions, there was generally an increase in the prevalence of asthma and
related conditions, and that temporal changes did not vary by urban-rural status. The prevalence of
spastic bronchitis was over 3 times higher than that of asthma. These findings also suggest that the
presence of undiagnosed asthma in children is occurring in the Grodno Region.

KEYWORDS. Asthma, child health, epidemiology, international health, temporal trends

INTRODUCTION Study of Asthma and Allergies in Children

(ISAAC), with an overall trend towards increas-
Asthma is a common childhood condition, ing prevalence.1 However, there is a great
with a global prevalence of asthma symptoms deal of geographic variation in asthma preva-
around 11%–13% based on the International lence between regions, including urban-rural
Address correspondence to: Joshua Lawson, PhD, Department of Medicine and Canadian Centre for
Health and Safety in Agriculture, University of Saskatchewan, 1218 Health Sciences E-Wing, 104 Clinic
Place, Saskatoon, Saskatchewan S7N 5E5, Canada (E-mail: josh.lawson@usask.ca).

332
 Brozek et al.
and international differences. The results of
several studies suggest that farming or rural
exposure is protective of asthma and allergic
disease.2–5 Also, asthma prevalence is typi-
cally higher in Westernized nations (between
6% and 26%) compared with non-Westernized
nations.1,6,7 Relatively low prevalence of aller-
gic diseases in Eastern Europe was reported in
the ISAAC study1 and confirmed in a study of
urban centers in Eastern and Central Europe
that showed high between-country variation.8
Reasons for geographic variation may include
differences in diagnostic labeling, health care
access, or the environment.
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In the past, Westernized nations have had a
rapid increase in asthma prevalence over a rel-
atively short time period. Recently, there has
been some evidence that areas with higher
asthma prevalence have begun to stabilize,1,9
whereas some areas of traditionally low asthma
prevalence have begun to rise.1 Since the mid-
1990s, asthma symptom prevalence has risen
in Eastern Europe, including in Poland and
Ukraine.1,7,10–12 Although asthma prevalence
is lower in Eastern European nations, these
increases could result in asthma emerging as
a major health burden in the region. This has
implications for future burden on health care
systems and patient well-being. To plan for
appropriate management of asthma and improve
the well-being of children with asthma, investi-
gation of trends and identification of risk factors
must be completed.
Belarus is a country in Eastern Europe that
borders Russia, Ukraine, and the European
Union. Information on childhood asthma
prevalence from this country is limited to
one cross-sectional study,13 where it was
observed that asthma prevalence was lower
than Western nations, with a high likelihood
of underdiagnosis.13 There has never been an
investigation of temporal trends in Belarus.
Additionally, the difference in changes over
time between urban and rural settings has rarely
been considered. As such, we completed a
repeat of the cross-sectional study conducted
in 2009 in order to (1) identify changes in the
prevalence of asthma and related conditions
between 2009 and 2014; (2) determine if there
were differences in the prevalence of asthma
333
and related conditions between urban and rural
dwellers; and (3) determine if any temporal
trends were consistent between urban and rural
dwellers.
METHODS
Study Design and Population
This study consisted of two repeated cross-
sectional surveys (2009 and 2014) in the same
location, using the same methodology. This
methodology has been described previously
for the Belarus Ukraine Poland Asthma Study
(BUPAS).13–15 In brief, study subjects were
children aged 7 to 15 years, attending schools
in the city of Grodno and its surrounding rural
area of the Grodno Region in Belarus.
Using a cluster sampling approach with
schools as the sampling unit, we selected
3000 children from 10 schools in the city
of Grodno and 3000 children from 20 rural
schools in the Grodno Region. These schools
and students were selected from 36 eligi-
ble schools with approximately 28,199 attend-
ing students in the city of Grodno and from
32 schools with 4842 attending students in the
rural area surrounding Grodno. In 2014, the
same schools were included in order to remove
any bias that may occur by resampling. All
children attending selected schools were eli-
gible for inclusion. Questionnaires were sent
home to parents/guardians through the schools.
Upon completion of the questionnaire, they
were returned to the school where they were
picked up by the research team. The ques-
tionnaire was returned for 2606 urban chil-
dren and 2422 rural children in 2009, whereas
in 2014 it was returned for 2187 urban chil-
dren and 2766 rural children. This results
in response rates of 87.9% and 80.7% in
2009 and 84.3% and 88.3% in 2014, respec-
tively. To maintain equal age inclusion between
the years, only 7–15-year-old children were
included (2009: urban = 2565, rural = 2412;
2014: urban = 2095, rural = 2642).
The study protocol was approved by
the Ethics Committee at Yanka Kupala
University (Grodno, Belarus). Informed
 334 RURAL DWELLING AND CHILDHOOD ASTHMA IN BELARUS
consent was included as part of the returned
questionnaire.
Study Questionnaire
The questionnaire was composed of stan-
dard questions included in the ISAAC respira-
tory questionnaire.16 All questions were trans-
lated from English to Russian, and their syntax
was verified by back-translation. The ISAAC
questionnaire has been used internationally on
repeated occasions with multiple languages,
including Russian.16–18 Although translation
can be difficult, a previous assessment of trans-
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lation in the ISAAC study found that there were
few major translation deviations for questions so
long as careful attention was made.18 The ques-
tionnaire included questions about established
diagnoses, symptoms, family history of respira-
tory and allergic disorders, and socioeconomic
status. Location of dwelling was classified as
urban or rural based on whether the child lived
in the city of Grodno or the surrounding agricul-
tural area.
A history of asthma was based on the ques-
tion “Has this child ever had asthma?” in addi-
tion to the question “Was asthma diagnosed by
a doctor?” Current asthma was based on a pos-
itive response to physician-diagnosed asthma
as well as a report of asthma attacks in the
past 12 months. An additional list of analyzed
allergic and respiratory diseases included diag-
noses established during the child’s lifetime by
a physician and reported by subjects’ parents
for atopic eczema, allergic rhinitis, unspecified
allergy, and spastic bronchitis. Spastic bronchi-
tis is a traditional diagnosis of the region and is
used to describe chronic or recurrent asthmatic
symptoms such as “wheezy bronchitis.”
Respiratory symptoms in the past 12 months
were assessed by “Has your child had wheez-
ing or whistling in the chest in the past
12 months?”(chest wheeze); “Has your child
had an attack of shortness of breath that came
on during the day when she/he was at rest at any
time in the past 12 months?” (attack of dyspnea);
“Has your child ever had any nasal allergies,
including hay fever?” (hay fever); “Has your
child had a problem with sneezing or a runny or
blocked nose when she/he did not have a cold
or the flu in the past 12 months?” (noninfectious
rhinitis); and “Has your child ever had an itchy
rash which was coming and going for at least
6 months?” (recurrent itchy rash).
Several variables were considered as poten-
tial correlates of respiratory outcomes. Parental
asthma was defined as a positive history
of physician-diagnosed asthma by either the
mother or father. The highest level of educa-
tion was categorized as high school or greater
than high school. Exposure to tobacco smoke
was classified based on the smoking status of the
mother and father.
Statistical Analysis
Initially we completed descriptive analy-
ses to examine differences in the population
between 2009 and 2014. Statistical significance
was assessed using the independent-samples t
test and independent-samples chi-square test for
continuous and categorical variables, respec-
tively. We then reported the prevalence of each
respiratory related outcome by study year and
location of dwelling (urban or rural) using the
independent-samples chi-square test to statisti-
cally test differences. Multiple logistic regres-
sion analyses with each respiratory outcome
were used to examine the association with
the personal and environmental characteristics
and to account for potential confounding. The
strength of association was based on the odds
ratios (ORs) and 95% confidence intervals (CIs).
The primary independent variables of inter-
est were location of residence and study year.
Adjustments were also made for sex, maternal
smoking, weight status, maternal education sta-
tus, paternal education status, maternal history
of asthma, smoking during pregnancy, and age.
Interaction between study year and location of
dwelling was tested using the likelihood-ratio
test.
RESULTS
A higher proportion of children were from
rural areas in 2014 than in 2009 (55.8% vs.
48.5%; P < .001). Table 1 includes a descrip-
tion of the personal characteristics of the study
 Brozek et al. 335

TABLE 1. Personal Characteristics of the Study Population by Year of Study

Characteristic 2009 2014 P value

(N = 4977) (N = 4737)

% Female 48.8 50.7 .06

% Mother with more than high school 33.9 35.3 .17
% Father with more than high school 27.7 28.7 .26
% Rural dwelling 48.5 55.8 <.001
Obesity status
% Not overweight or obese 86.4 85.0
% Overweight 11.5 12.6
% Obese 2.0 2.4 .18
% Maternal asthma 1.2 1.3 .62
% Maternal allergic rhinitis 3.1 3.2 .72
% Maternal atopic eczema 4.8 2.7 <.001
% Paternal asthma 1.3 1.0 .16
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% Paternal allergic rhinitis 2.2 2.0 .51

% Paternal atopic eczema 2.2 1.4 .005
% Maternal current smoking 11.0 8.4 <.001
% Paternal current smoking 49.5 49.0 .59
% Maternal smoking during pregnancy 2.3 2.2 .78
Mean age, years (SD) 11.0 (2.4) 10.0 (2.2) <.001
Mean reported height, cm (SD) 146.7 (15.0) 144.3 (13.7) <.001
Mean reported weight, kg (SD) 38.6 (11.9) 37.5 (11.5) <.001

population. Approximately half the population
were female. In addition to this, a lower propor-
tion of children in 2014 had a maternal history of
atopic eczema, had a paternal history of atopic
eczema, and reported current maternal smoking
compared with 2009. Children in 2014 were also
younger, shorter, and weighed less, on average.
In both 2009 and 2014, rural dwellers had
a significantly lower prevalence of eczema,
allergy, symptoms of allergic rhinitis or
hayfever, sneezing with congestion or intense
runny nose apart from a cold, and skin allergy
or itching (Table 2). In 2014, the prevalence
of diagnosed spastic bronchitis and rhinitis
was significantly higher among urban dwellers
compared with rural dwellers (Table 2). Neither
asthma nor current asthma prevalence differed
between urban and rural locations. After adjust-
ment for potential confounders, rural dwelling
showed a statistically significant inverse asso-
ciation with each of the allergic conditions or
symptoms (Table 3). However, ever asthma
(OR = 1.01, 95% CI = 0.69–1.50) and current
asthma (OR = 1.29, 95% CI = 0.71–2.38) did
not show statistically significant associ-
ations with rural dwelling. There was a
trend towards lower likelihood of spastic
bronchitis (OR = 0.84, 95% CI = 0.70–1.01;
P = .06) and productive cough (OR = 0.85,
95% CI = 0.72–1.01; P = .07) among rural
dwellers compared with urban dwellers.
The prevalence of ever asthma was similar
between 2009 and 2014 (1.4% vs. 1.8%) as
was the prevalence of current asthma (2009:
0.6% vs. 2014: 0.8%). Overall, there were sta-
tistically significant increases in the prevalence
of being woken by asthma attacks in the past
3 months; ever chest wheeze and nocturnal
shortness of breath in the past 12 months; diag-
nosis of eczema, diagnosis of allergy, symptoms
of allergic rhinitis or hay fever, sneezing with
congestion or intense runny nose apart from a
cold, along with a lower prevalence of shortness
of breath with exercise in the past 12 months;
cough in the past 12 months; and productive
cough in the past 12 months between 2009 and
2014 (Table 2). These increases were seen
among both urban dwellers and rural dwellers.
Among urban dwellers, there was a statistically
significant increase in spastic bronchitis diagno-
sis between 2009 and 2014 (Table 2). Among
rural dwellers, there was a statistically signifi-
cant reduction in the prevalence of chest wheeze
in the past 12 months (Table 2).
 336 RURAL DWELLING AND CHILDHOOD ASTHMA IN BELARUS

TABLE 2. Distribution of Asthma, Asthma-Like Conditions, and Allergic Conditions by Year and
Location of Dwelling

Symptoms and conditions Overall Urban Rural

2009 2014 2009 2014 2009 2014

(N = 4977) (N = 4737) (N = 2565) (N = 2095) (N = 2412) (N = 2642)
% % % % % %

Ever asthma 1.4 1.8 1.4 1.7 1.4 1.9

Asthma attacks in the past 12 months 0.6 0.8 0.6 0.6 0.7 0.9
Woken by asthma attacks in the past 0.4 1.0∗ 0.4 1.3∗ 0.3 0.8†
3 months
Spastic bronchitis 6.8 8.5∗ 7.4 10.5∗ 6.2 7.0‡
Ever had chest wheeze 9.8 24.5∗ 9.3 24.8∗ 10.3 24.3∗
Chest wheeze in the past 12 months 9.7 7.3∗ 9.2 8.1 10.2 6.7∗
Shortness of breath with exercise in 4.0 1.4∗ 4.2 1.1∗ 3.7 1.6∗
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the past 12 months

Nocturnal shortness of breath in the 1.2 3.7∗ 1.4 3.8∗ 1.0 3.6∗
past 3 months
Cough in the past 12 months 28.4 11.2∗ 27.3 11.6∗ 29.4 10.9∗
Productive cough in the past 12.7 5.2∗ 13.1 5.5∗ 12.3 5.0∗
12 months
Ever diagnosed with rhinitis 3.9 4.2 5.5 6.0 2.2‡ 2.8‡
Ever diagnosed with eczema 10.3 16.6∗ 12.2 19.4∗ 8.3‡ 14.3∗‡
Ever diagnosed with any allergy 14.5 27.8∗ 18.6 36.1∗ 10.2‡ 21.2∗‡
Ever had symptoms of allergic rhinitis 2.5 4.2∗ 3.8 6.0∗ 1.0‡ 2.8∗‡
or hayfever
Ever had sneezing with congestion or 8.6 20.0∗ 10.2 22.2∗ 6.9‡ 18.2∗‡
intense runny nose apart from a
cold
Ever had skin allergy or itching 13.5 16.6∗ 15.0 19.4∗ 12.0‡ 14.3†‡
∗P < .005 comparing 2009 with 2014 within dwelling strata.
†P < .05 comparing 2009 with 2014 within dwelling strata.
‡ P < .05 comparing urban with rural within the same year.

After adjustment for confounders, a previ-
ous diagnosis of asthma was more likely in
2014 compared with 2009 (OR = 1.57, 95%
CI = 1.05–2.33), but no association between
current asthma and study year (OR = 1.53, 95%
CI = 0.83–2.82). Additional adjusted associa-
tions are presented in Table 3. There was an
increased likelihood of being woken by asthma
attacks in the past 3 months; spastic bronchi-
tis, ever chest wheeze, and nocturnal shortness
of breath in the past 12 months; and diagno-
sis of eczema, diagnosis of allergy, symptoms
of allergic rhinitis or hay fever, sneezing with
congestion or intense runny nose apart from
a cold, and eczema symptoms associated with
2014 compared with 2009. There was also a
reduced likelihood of current wheeze, shortness
of breath with exercise, cough, and productive
cough associated with 2014 after adjustment for
confounders.
Although there were some changes over time
that were statistically significant among either
rural dwellers or urban dwellers separately,
there was no statistically significant interac-
tion observed between location of dwelling and
study year, suggesting that the temporal trends
over time did not differ between urban or rural
children.
With the exception of being woken by asthma
attacks in the past 3 months, productive cough,
and eczema, a maternal, but not paternal, his-
tory of asthma showed strong (OR ranging from
1.66 to 7.17), statistically significant associa-
tions with each of the outcomes of interest.
Being female was generally protective of hav-
ing each outcome (Table 3). Current maternal
 Brozek et al. 337

TABLE 3. Adjusted∗ Associations Between Study Year, Location of Dwelling, and Personal
Factors With Asthma, Asthma-Related Symptoms, and Allergic Conditions

Symptoms and conditions Study year 2014 Rural Female Current maternal
(Ref: 2009) (Ref: Urban) (Ref: Male) smoking
OR (95% CI) OR (95% CI) OR (95% CI) (Ref: Not current)
OR (95% CI)

Ever asthma 1.57 (1.05–2.33) 1.01 (0.69–1.50) 0.58 (0.40–0.85) 1.65 (0.92–2.94)
Current asthma 1.53 (0.83–2.82) 1.29 (0.71–2.38) 0.39 (0.21–0.72) 1.47 (0.57–3.79)
Nocturnal asthma 3.14 (1.59–6.19) 0.69 (0.39–1.23) 0.82 (0.47–1.41) 2.06 (0.94–4.51)
Spastic bronchitis 1.26 (1.06–1.51) 0.84 (0.70–1.01) 0.71 (0.60–0.85) 1.18 (0.86–1.61)
Ever wheeze 2.88 (2.51–3.31) 1.06 (0.93–1.20) 0.87 (0.77–0.98) 1.29 (1.04–1.60)
Current wheeze 0.70 (0.59–0.83) 1.02 (0.85–1.21) 0.83 (0.70–0.98) 1.44 (1.09–1.90)
Shortness of breath with exercise 0.38 (0.28–0.52) 1.10 (0.81–1.48) 1.04 (0.78–1.38) 2.06 (1.36–3.12)
Nocturnal shortness of breath 2.40 (1.71–3.36) 0.93 (0.69–1.25) 0.73 (0.55–0.98) 1.47 (0.92–2.36)
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Cough 0.31 (0.27–0.35) 0.97 (0.85–1.10) 0.99 (0.88–1.12) 1.30 (1.06–1.60)

Productive cough 0.36 (0.30–0.43) 0.85 (0.72–1.01) 0.95 (0.81–1.12) 1.25 (0.95–1.65)
Rhinitis 1.15 (0.91–1.46) 0.50 (0.39–0.64) 0.55 (0.44–0.69) 1.05 (0.69–1.62)
Eczema 1.78 (1.55–2.06) 0.79 (0.69–0.91) 0.96 (0.84–1.10) 1.12 (0.88–1.42)
Allergy 2.28 (2.02–2.57) 0.58 (0.51–0.65) 1.02 (0.91–1.14) 1.15 (0.94–1.42)
Rhinitis symptoms 1.80 (1.38–2.34) 0.46 (0.35–0.60) 0.49 (0.38–0.63) 0.87 (0.53–1.44)
Sneezing 3.07 (2.65–3.57) 0.75 (0.65–0.86) 0.79 (0.70–0.90) 1.24 (0.98–1.56)
Eczema symptoms 1.25 (1.09–1.42) 0.83 (0.72–0.94) 0.92 (0.81–1.05) 1.11 (0.88–1.40)

∗ Adjusted for study year, location of dwelling, sex, maternal smoking, weight status, maternal education status, paternal

education status, maternal history of asthma, smoking during pregnancy, and age.

smoking was associated with the respiratory
symptoms of ever wheeze, current wheeze,
shortness of breath with exercise, and cough
(Table 3).
DISCUSSION
In our study, we found that allergic condi-
tions and symptoms were less prevalent in rural
dwelling children compared with urban chil-
dren, although this was not true for asthma.
We also found that most conditions increased
in prevalence between 2009 and 2014, although
there were some discrepancies, including reduc-
tions in prevalence over the past 12 months
for wheeze, shortness of breath with exercise,
cough, and productive cough. Finally, we found
that temporal patterns did not differ significantly
between urban and rural children.
It has generally been recognized that the
prevalence of asthma and allergic diseases are
lower in rural compared with urban areas,19,20
with more consistent associations generally seen
with farm dwelling, including results from
Belarus’s neighbors in Poland.21,22 Results from
our study support previous research suggest-
ing that allergic conditions are less frequent in
rural compared with urban areas. Reasons for
this could be due to environmental differences,
including endotoxin, which has been associated
inversely with asthma and allergy23 and has also
been shown to be higher in farm compared with
nonfarm locations.24 Other reasons for the dif-
ferences between urban and rural populations
could include patient presenting or health access
differences. Although we found the differences
we expected to see for allergic diseases other
than asthma, we did not find the association with
lower asthma prevalence in the rural areas com-
pared with urban areas. Previous research has
more consistently found these associations with
allergic conditions other than asthma, whereas
these associations have more inconsistent with
asthma. Generally, the associations with asthma
are with farms and livestock farms specifically.
However, we lacked this information, preventing
further investigation of this issue. Also, asthma
is a disease with several phenotypes. Although
it is strongly associated with allergy, there are
nonallergic mechanisms as well, which may
explain some of the more inconsistent results
 338 RURAL DWELLING AND CHILDHOOD ASTHMA IN BELARUS
with asthma compared with other allergic condi-
tions. Another explanation of the lack of a “rural
protective effect” is that in Belarus, differences
in lifestyle between rural and urban areas are not
as defined as in Western countries. For exam-
ple, it is very popular among people living in
towns to farm and cultivate potatoes and other
vegetables for their own purposes in gardens,
backyards, or school gardens.
After adjusting for confounders, children in
2014 were at an increased likelihood of hav-
ing a doctor’s diagnosis of asthma compared
with 2009. This was in spite of the actual
prevalence between years being similar and not
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statistically different. Most of the other condi-
tions also showed increased likelihood of hav-
ing an allergic condition in 2014 compared
with 2009. Interestingly, although the propor-
tion of children reporting ever wheeze increased,
the proportion of children with current wheeze
decreased, along with reductions in the preva-
lence of shortness of breath with exercise and
cough. Although we do not know the reason
for these unexpected findings (current wheeze,
cough, shortness of breath with exercise), we
can speculate that some of these children have
had a diagnosis of asthma or spastic bronchi-
tis resulting in treatment or may be treated
for breathing problems, resulting in a reduc-
tion in current symptoms. This represents an
area of future research. Also, these nonspecific
symptoms may result from pollen or infec-
tious disease and may have been less common
in the 12 months under study due to a very
mild winter experienced in Eastern Europe over
2013–2014.25
This study is the first from Belarus to investi-
gate time trends in the prevalence of asthma and
allergic conditions. Similar to other areas in the
region1,7,10–12 that have experienced relatively
low prevalence of these conditions, there has, in
general, been an increase in recent years. It is,
therefore, important to monitor these patterns
and to investigate reasons for these changes,
as this will have implications for understand-
ing the in etiology, diagnosis, and management.
Regardless of year, asthma prevalence was lower
than seen in Westernized nations,1 although
spastic bronchitis prevalence in this population
was over 4 times higher than asthma prevalence.
Given the relatively high prevalence of spastic
bronchitis compared with asthma and symp-
tom prevalence, which is comparable to other
regions, it is likely that asthma is underdiag-
nosed in Belarus, confirming other studies from
Eastern and Central Europe.8,13,15,26
We also examined associations with fam-
ily history of asthma, sex, and exposure to
environmental tobacco smoke (ETS). We con-
sistently found relatively strong associations
between family history of asthma and the out-
comes under study. Asthma and allergic disease
have a strong familial component, so this result
is not surprising and is consistent with the previ-
ous literature. In this study, family history was
often the strongest predictor of the outcome.
Being female consistently resulted in reduced
risk of the outcomes under study. Again, this
is consistent with previous literature, where in
childhood, boys typically have a lower preva-
lence of asthma and related conditions, until the
mid-teens when there appears to be a gender
switch, and females have a higher prevalence of
asthma. Lastly, our results considering maternal
smoking were also consistent with the literature,
where the presence of ETS, based on report of
current maternal smoking, was associated with
an increased risk of respiratory symptoms.
Some limitations should be considered. Data
were collected through repeated cross-sectional
studies, resulting in inherent limitations of
using the cross-sectional design such as lack of
an ability to investigate temporal associations.
However, cross-sectional designs are appropri-
ate for investigation of prevalence, which was
a key focus of our study. Also, the same
schools, sampling methods, and key survey
questions were used to reduce bias in our
comparisons. Information about children was
obtained through parent-completed question-
naires. Although there may be some recall bias,
parents are generally good at self-report of
previous diagnoses. Lack of diagnoses made
by a study physician is also a limitation.
However, given the practicality required in large
population-based studies, questionnaire report
is generally accurate, especially when we con-
sider asthma where there is not a gold standard
objective measure. In addition to this, we con-
sider trends in symptom report as well as trends
 Brozek et al.
in diagnoses in order to remove problems of
labeling. It is possible that there can be cluster-
ing within families resulting in correlated data.
Unfortunately, due to lack of family identifiers,
we were unable to assess this or control for it
through methods such as generalized estimating
equations. Although this is a more appropriate
statistical analysis, the strengths of association
would not be changed and the width of the
confidence intervals would likely be increased
slightly. It may be possible that some children
were included in both the 2009 and 2014 sur-
veys. However, we lacked the identifying infor-
mation to link these people between surveys.
Downloaded by [University of Lethbridge] at 19:32 10 November 2015
Finally, we lacked a great deal of information
specific to rural environments, which may have
helped our investigation of rural-urban associa-
tions. This was done in order to keep the survey
short and increase the participation rate to allow
more accurate assessments.
There are several strengths to this study.
We experienced excellent participation rates and
included a large sample size of children. Our
intentional sampling of a rural population of
children allowed for adequate sample sizes to
investigate associations in stratified analyses.
We were also able to collect a large amount of
information on respiratory conditions and symp-
toms along with important confounders. Data
were collected using well-established and stan-
dardized survey questions. Finally, we address
a large gap in knowledge by investigating the
prevalence of asthma and related conditions in
this understudied region.
We expect that in the future, the prevalence of
asthma will increase in Belarus. At present, it is
still a relatively closed country where life is still
relatively traditional. We would anticipate that
through gradual Westernization and application
of standardized diagnostic procedures and label-
ing, asthma prevalence will increase. Though
small, evidence of an increase is already begin-
ning to be seen. Future investigation in Belarus
should include investigation of labeling prac-
tices as well as subsequent management prac-
tices to determine if children with respiratory
conditions are adequately controlled. In addition
to this, monitoring environmental changes will
help account for the environment in the etiology
of asthma and related conditions.
339
We found that asthma prevalence was low, but
the prevalence of spastic bronchitis, respiratory
symptoms, and allergic conditions was much
higher; rural children were less likely to have
allergic conditions; and respiratory and aller-
gic conditions were typically increasing. This
study adds important information to the scien-
tific literature by investigating time trends in a
largely understudied region and further estab-
lishing consistency in the relationship between
rural living and lower prevalence of allergic
disease. Efforts should be made to investi-
gate the discrepancy between asthma prevalence
and the prevalence of respiratory and allergic
conditions.
REFERENCES
1. Asher MI, Monteforte S, Bjorksten B, et al., and
the ISAAC Phase Three Study Group. Worldwide time
trends in the prevalence of symptoms of asthma, aller-
gic rhinoconjunctivitis, and eczema in childhood: ISAAC
Phases One and Three repeat multicountry cross-sectional
surveys. Lancet. 2006;368:733–743.
2. Ernst P, Cormier Y. Relative scarcity of asthma and
atopy among rural adolescents raised on a farm. Am J
Respir Crit Care Med. 2000;161:1563–1566.
3. Riedler J, Braun-Fahrlander C, Eder W, et al.
Exposure to farming in early life and development of
asthma and allergy: a cross-sectional survey. Lancet.
2001;358:1129–1133.
4. Riedler J, Eder W, Oberfeld G, Schreuer M.
Austrian children living on a farm have less hay fever,
asthma and allergic sensitization. Clin Exp Allergy.
2000;30:194–200.
5. Midodzi WK, Rowe B, Majaesic CM, Senthilselvan
A. Reduced risk of physician-diagnosed asthma among
children dwelling in a farming environment. Respirology.
2007;12:692–699.
6. The International Study of Asthma and Allergies
in Childhood (ISAAC) Steering Committee. Worldwide
variations in the prevalence of asthma symptoms: the
International Study of Asthma and Allergies in Childhood
(ISAAC). Eur Respir J. 1998;12:315–35.
7. The International Study of Asthma and Allergies
in Childhood (ISAAC) Steering Committee. Worldwide
variation in prevalence of symptoms of asthma, allergic
rhinoconjunctivitis, and atopic eczema: ISAAC. Lancet.
1998;351:1225–1232.
8. Leonardi GS, Houthuijs D, Nikiforov B, et al.
Respiratory symptoms, bronchitis, and asthma in chil-
dren of Central and Eastern Europe. Eur Resp J. 2002;
20:890–898.
 340 RURAL DWELLING AND CHILDHOOD ASTHMA IN BELARUS
9. Senthilselvan A, Lawson JA, Rennie DC,
Dosman JA. Stabilization of an increasing trend in
physician-diagnosed asthma prevalence in Saskatchewan,
1991–1998. Chest. 2003;124:438–448.
10. Lis G, Breborowicz A, Cichocka-Jarosz E, et
al., International Study of Asthma and Allergy in
Childhood. Increasing prevalence of asthma in school
children—ISAAC Study. Pneumono Alergo Pol. 2003;71:
336–343.
11. Breborowicz A, Lis G, Cichocka-Jarosz E,
Alkiewicz J, Pietrzyk JJ. Prevalence and severity of asthma
symptoms in schoolchildren in Poland (ISAAC Study).
Pediatr Pol. 2005;80:866–873.
12. Brozek G, Zejda JE, Kowalska ML, Gebus M, Kepa
K, Igielski M. Opposite trends of allergic disorders and
Downloaded by [University of Lethbridge] at 19:32 10 November 2015
respiratory symptoms in children over a period of large-
scale ambient air pollution decline. Pol J Environ Stud.
2010;19:1133–1138.
13. Shpakou A, Brozek G, Stryzhak A, Neviartovich
T, Zejda J. Allergic disease and respiratory symptoms
in urban and rural children in Grodno Region (Belarus).
Pediatr Allergy Immunol. 2012;23:339–346.
14. Fedortsiv O, Brozek GM, Luchyshyn N, et al.
Prevalence of childhood asthma, rhinitis, and ecema in
the Ternopil region of Ukraine—results of BUPAS study.
Adv Med Sci. 2012;57: 282–289. doi:10.2478/v10039-012-
0034-6.
15. Zejda JE, Brozek GM, Farnik M, Smolka I. Social
and family-related correlates of medical care utilization
by asthmatic children in Upper Silesia, Poland. Ann Agric
Environ Med. 2012;19:141–145.
16. Asher MI, Anderson HR, Beasley R, et al.
International study of asthma and allergies in child-
hood (ISAAC): rationale and methods. Eur Respir J.
1995;8:483–491.
17. Bjorksten B, Dumitrascu D, Foucard T, et al.
Prevalence of childhood asthma, rhinitis, and eczema
in Scandanavia and Eastern Europe. Eur Respir J.
1998;12:432–437.
18. Ellwood P, Williams H, Ait-Khaled N, Bjorksten B,
Robertson C, ISAAC Phase III Study Group. Translation of
questions: the International Study of Asthma and Allergies
in Childhood (ISAAC) experience. Int J Tuberc Lung Dis.
2009;13:1174–1182.
19. Lawson JA, Janssen I, Bruner MW, Madani K,
Pickett W. Urban-rural differences in asthma prevalence
among young people in Canada: the roles of health
behaviours and obesity. Ann Allergy Asthma Immunol.
2011;10:220–228.
20. Priftis KN, Anthracopoulos MB, Nikolaou-
Papanagiotou A, et al. Increased sensitization in urban
vs. rural environment-rural protection or an urban living
effect. Pediatr Allergy Immunol. 2007;18:209–216.
21. Majkowska-Wojciechowska B, Pelka J, Korzon L,
et al. Prevalence of allergy, patterns of allergic sensitization
and allergy risk factors in rural and urban children. Allergy.
2007;62:1044–1050.
22. MacNeill SJ, Sozanska B, Danielewicz H, et al.
Asthma and allergies: is the farming environment (still)
protective in Poland? The GABRIEL Advanced Studies.
Allergy. 2013;68:771–779.
23. Braun-Fahrlander C, Riedler J, Herz U, et al.
Environmental exposure to endotoxin and its relation
to asthma in school-age children. N Engl J Med.
2002;347:869–877.
24. von Mutius E, Braun-Fahrlander C, Schierl R, et al.
Exposure to endotoxin or other bacterial components might
protect against the development of atopy. Clin Exp Allergy.
2000;30:1230–1234.
25. World Meteorological Organization. Meteoro-
logical summer/winter sees many extremes. Available
at: http://www.wmo.int/pages/mediacentre/news/Meteo
rologicalsummerwinterseesmanyextremes_en.html. Pub-
lished 2014. Accessed November 21, 2014.
26. Brozek G, Farnik M, Lawson J, Zejda J.
Underdiagnosis of childhood asthma: a comparison of sur-
vey estimates to clinical evaluation. Int J Occup Med
Environ Health. 2013;26:900–909.