Prevalence and risk factors of airflow limitation in a Mongolian population in Ulaanbaatar: Cross-sectional studies
Prevalence and risk factors of airflow limitation in a Mongolian population in Ulaanbaatar: Cross-sectional studies
Motoyuki Nakao 1 2 3
Keiko Yamauchi 1 2 3
Yoko Ishihara 1 2 3
Hisamitsu Omori 0 1 3
Bandi Solongo 1 3
Dashtseren Ichinnorov 1 3
0 Department of Biomedical Laboratory Sciences, Faculty of Life Sciences, Kumamoto University , Kumamoto , Japan , 3 Department of Respiratory Medicine, Mongolian National University of Medical Sciences , Ulaanbaatar , Mongolia
1 of Education , Culture, Sports, Science , and Technology (B)20406001 YI; Ministry of Education , Culture, Sports, Science , and Technology (B) 23406001 to YI; Ministry of Education , Culture, Sports, Science , and Technology (C)26340053 to YI; Ministry of Education , Culture, Sports, Science , and Technology MEXT-Supported Program for the
2 Department of Public Health, School of Medicine, Kurume University , Kurume, Fukuoka , Japan
3 Editor: Kevin Mortimer, Liverpool School of Tropical Medicine , UNITED KINGDOM
The burden of chronic obstructive pulmonary disease (COPD) is expected to increase in the coming decades. In Ulaanbaatar, Mongolia, air pollution, which has been suggested to correlate with COPD, is a growing concern. However, the COPD prevalence in Ulaanbaatar is currently unknown. This study aims to estimate the prevalence of airflow limitation and investigate the association between airflow limitation and putative risk factors in the Mongolian population. Five cross-sectional studies were carried out in Ulaanbaatar. Administration of a self-completed questionnaire, body measurements, and medical examination including spirometry were performed in 746 subjects aged 40 to 79 years living in Ulaanbaatar. The age- and sex-standardized prevalence of airflow limitation in Ulaanbaatar varied widely from 4.0 to 10.9% depending on the criteria for asthma. Age, body mass index (BMI), and smoking habit were independent predictors for airflow limitation while residential area and household fuel type were not significant. In conclusion, prevalence of putative COPD was 10.0% when subjects with physician-diagnosed asthma were excluded from COPD. Older age, lower BMI, and current smoking status were putative risk factors for airflow limitation. This prevalence was consistent with reports from Asian countries.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Chronic obstructive pulmonary disease (COPD) is characterized by persistent airflow
limitation caused by a mixture of small airway disease and parenchymal destruction [
to WHO estimates, COPD is the third leading cause of death globally . There were 3.1
million COPD deaths in 2012, corresponding to 5% of all deaths worldwide. The morbidity and
mortality of COPD, and its associated economic and social burdens, are increasing globally
even in the low- and middle-income countries [
]. The most evident risk factor for COPD is
cigarette smoking, with COPD prevalence correlating with tobacco smoking prevalence. In
developing countries, outdoor and indoor air pollution is also a major risk factor of COPD .
Strategic Research Foundation at Private
Universities to YI. The funders had no role in study
design, data collection and analysis, decision to
publish, or preparation of the manuscript.
The prevalence and burden of COPD are expected to increase in the coming decades due to
high smoking rates and severe air pollution in developing countries, and population aging in
COPD prevalence varies according to survey methods, diagnostic criteria, and analytical
methods. The prevalence of physiologically defined COPD in adult subjects over 40 years has
been reported to be 9±10% although there are regional or methodological differences [
Amongst Asian countries, COPD prevalence has been reported to be 10.9% in Japan [
13.7% in Korea (data from the Korea National Health and Nutrition Examination Survey) [
8.2% and 11.4% in China [
], and 13.9% in Manila, Philippines [
Ulaanbaatar, the Mongolian capital, is one of the world's worst air-polluted cities and
concerns about air pollution are growing . Coal and biomass fuel consumption is the major
cause of indoor and outdoor air pollution in Ulaanbaatar [
], and increased coal
consumption in winter is attributed to increased household use of coal-fired stoves. This increase in
household coal consumption is partly due to population influx from rural areas to
Ulaanbaatar, leading to the development of districts comprised of traditional tents with poor
infrastructure (termed ªgerº in Mongolia). People living in ger districts use smoke-rich fuel for
household use, resulting in frequent smog and indoor air pollution in Ulaanbaatar. Indoor air
pollution is a known important risk factor for COPD development [13±15], while other
reports suggest that outdoor air pollution also affects lung function and respiratory symptoms
although the effect seems to be small [1, 16±18].
The COPD prevalence in Ulaanbaatar is currently unknown. Here, we have conducted
cross-sectional studies to assess the determinants and estimated prevalence of airflow
limitation among Mongolian subjects aged 40±79 years living in Ulaanbaatar.
We conducted five cross-sectional studies among Mongolian adults aged 40 to 79 years at
eight facilities (two hospitals and six community clinics) in Ulaanbaatar from 2012 to 2013
(May and September, 2012 and March, July, December, 2013). Participants were recruited by
announcements advertising the health survey. Subjects received a self-completed
questionnaire containing questions pertaining to age, gender, occupation, respiratory symptoms, and
medical history. At the time of questionnaire administration, height and body weight were
measured, and medical interviews, auscultations, and pulmonary function tests by respiratory
specialists were conducted. Each survey included different sets of subjects and no duplicative
The present study included an initial 1,030 male and female community volunteers. Of these,
29 (2.8%) and 3 (0.3%) subjects were excluded due to ineligible age (< 40 or 80 years old)
and lack of gender information, respectively. The remaining 998 (96.9%) were subjected to
pulmonary function tests, however, the physician diagnosed that 71 (6.9%) subjects were
contraindicated for spirometry due to conditions such as active tuberculosis,
postpneumonectomy, or high blood pressure. Furthermore, spirometry on 24 (2.3%) subjects could not be
performed due to a facility electric outage, and 57 (5.5%) subjects were excluded from analysis
due to other reasons such as poor reproducibility, inappropriate spirograms, and/or
mechanical issues. Lastly, 100 (9.7%) subjects were excluded due to restrictive ventilatory impairment
(FEV1/FVC > 0.7 and FVC < 80% of predicted value). Characteristics of those subjects with
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restrictive ventilatory impairment was shown in S1 Table. Consequently, 746 (72.4%) subjects
were eligible for further analysis.
Pulmonary function test
A pre-bronchodilator pulmonary function test using the HI-105 spirometer (CHEST M.I.,
Inc., Tokyo, Japan) was conducted by the respiratory specialists. Spirometers were calibrated
before each survey. At least three spirograms were obtained, and the highest forced expiratory
volume in one second (FEV1) and forced ventilatory capacity (FVC) values were applied for
diagnosis. Mongolian and Japanese respiratory specialists assessed the reproducibility and
quality of spirograms (volume-time curve and flow-volume loop) and the invalid spirograms,
which showed artefacts, insufficient inspiration, or blow-out, were excluded from analysis.
Severity of airflow limitation was classified by the GOLD criteria (FEV1/FVC<0.7) with the
predicted FEV1 defined by GLI2012 reference equations for North East Asians [
Data handling and statistical analyses
All data were anonymized, and managed as electronic data for the analysis. Prevalence of
airflow limitation was age- and sex-standardized by direct standardization using Mongolian
national population data published by the United Nations [
]. Multiple logistic regression
analyses were carried out by forced inclusion procedure for all the variables. Odds ratios (ORs)
for presenting airflow limitation were adjusted for age group, sex (coded as 0 for female and 1
for male), body mass index (BMI) (coded as 0 for BMI 25.0 and 1 for BMI < 25.0), smoking
status (coded as 0 for non-smokers, 1 for former smokers, and 2 for current smokers),
household fuel (coded as 0 for smoke-free fuels such as gas and electricity and 1 for smoke-rich fuels
such as coal, wood and dry animal dung fuel), and residential district (coded as 0 for urban
areas and 1 for ger districts). The omnibus tests of model coefficient were shown to be
significant (P < 0.01) for all models. Correlation coefficients (r) among predictive values were tested,
and all r-values were less than 0.55, showing no multicollinearity. Statistical analyses including
Welch's t-test for parametric analysis of two groups, χ2-test for analysis of categorical data,
and multiple logistic regression analysis were performed using the statistical software package
JMP version 11 (SAS Institute Inc., Cary, NC, USA). P values less than 0.05 on both sides were
considered to be statistically significant.
Ethics, consent, and permissions
The present study was approved by the Clinical Ethical Review Board of Kurume University
School of Medicine. Before investigation, the participants were provided with explanations in
person as to the purpose and method of the study, as well as information regarding the
handling of the results. The study was carried out upon receipt of written consent.
Characteristics of participants
Mongolian subjects (n = 1,030) were recruited from the general population in Ulaanbaatar.
There were 746 (72.4%) eligible subjects for this study after excluding subjects who were out of
the age range, unknown gender, invalid spirometry, in poor physical condition, or with
restrictive ventilatory impairment. Characteristics of participants are presented in Table 1. Mean ages
of males and females were similar. Male-to-female ratio was 0.53 (258: 488), and BMI, smoking
status, residential district, and severity of airflow limitation according to GOLD criteria were
significantly different between sexes. When subjects were compared with the general Mongolian
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population of the same age group in 2012 to 2013 [
], the age characteristic of this study
population was slightly older with a significantly lower percentage of male subjects (34.6% of the
study subjects) than the general population (47.4% of the general population) (Table 2).
Expected prevalence of airflow limitation
Based on spirometry data, the unadjusted prevalence of airflow limitation in the study subjects
was 11.5% (Table 2). Severity of airflow limitation according to the GOLD criteria using the
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GLI 2012 reference equations for North East Asians was: mild, 43.9% (n = 18, male) and 22.2%
(n = 10, female); moderate, 46.3% (n = 19, male) and 73.3% (n = 33, female); and severe or
higher, 9.8% (n = 4, male) and 4.4% (n = 2, female). No females were classified as having very
severe airflow limitation. Crude and sex-standardized prevalence of airflow limitation were
increased with increasing age, and crude and age-standardized prevalence of airflow limitation
in males were higher than in females (Table 2). Age- and sex-standardized prevalence of
airflow limitation was 10.9%. The prevalence of airflow limitation stratified by subgroup is shown
in Table 3. Multiple logistic regression analyses to estimate odds ratios for presenting airflow
limitation were performed using age, sex, BMI, smoking status, household fuel type, and
residential district as predictive variables. Crude ORs were significant higher in older subjects,
males, the lower BMI group (< 25), and in current smokers. Of these, an older age, a lower
BMI, and current smoking status maintained significance after adjustment (Table 3). The
prevalence for subjects living in ger districts was higher than those in urban area but OR was
Differentiation of asthma from putative COPD
To assess the possibility of asthma, the study population was stratified by the number of
affirmative responses to four asthma-related questions; self-reported history of asthma, history of
wheezing in the past 12 months, frequent or occasional wheezes, and physician-diagnosed
asthma (Table 4). The number of subjects with physician-diagnosed asthma was 17 (4 male; 13
female) (data not shown). There were 8 subjects (2 male; 6 female) with physician-diagnosed
asthma also had airflow limitation. The crude prevalence of airflow limitation ranged from
4.3% to 11.5% depending on the number of affirmative responses to asthma-related questions.
The prevalence ranged from 4.0% to 10.9% when they were standardized by age and sex.
When subjects with physician-diagnosed asthma were excluded from putative COPD, the
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a Criteria for asthma diagnosis: self-reported history of asthma; history of wheezing in the past 12 months; frequent or occasional wheezes;
crude prevalence of putative COPD was 10.5% (age- and sex-adjusted prevalence: 10.0%) in
the study population.
This is the first study on the prevalence of airflow limitation in Mongolia. We investigated
lung function in Mongolian subjects aged 40 to 79 years living in Ulaanbaatar and found that
the crude prevalence of airflow limitation was 11.5%. Multiple logistic regression analysis
revealed that an older age, lower BMI, and current smoking status were independent
predictive variables for airflow limitation. In this study, COPD may be confounded by the presence
of asthma as post-bronchodilator spirometry was not conducted. When subjects with airflow
limitation were stratified according to different criteria for asthma, putative COPD prevalence
varied between 4.3 to 11.5%.
The prevalence of COPD shows interstudy variation depending on the diagnostic criteria.
Halbert et al. reported that the pooled prevalence of 37 estimates for COPD was 7.6% (95%
Confidence interval (CI): 6.0±9.5) [
]. Of these 37 estimates, the differences based on criteria
were relatively large, for example, spirometric criteria indicated 9.2% prevalence while
patientreported diagnosis resulted in 4.9%. The most popular criteria using spirometric results were
based on the GOLD criteria [
]. The crude prevalence of airflow limitation (GOLD stage I
(FEV1/FVC < 0.7)) in the present study was 11.5% when the possibility of asthma was not
considered and 10.5% when subjects with physician-diagnosed asthma were excluded from
putative COPD (Table 4). Furthermore, the age- and sex-standardized prevalence excluding
subjects with physician-diagnosed asthma was 10.0%. When criterion used in BOLD study
(GOLD stage II or higher (FEV1/FVC < 0.7 and FEV1 < 80% of predicted value)) was
employed, the crude prevalence of airflow limitation was 7.8% and standardized prevalence
was 7.3% (S2 Table) . Age- and sex-standardized prevalence excluding physician-diagnosed
asthma was 6.6% (S3 Table). Our results are comparable with other prevalence studies [6±9].
BMI was significantly lower in subjects with airflow limitation than those with normal lung
function (28.1 ± 5.0 (Normal) vs. 25.7 ± 2.9 (Airflow limitation), P < 0.001). Due to the
crosssectional design of the present study, it is not clear whether the low BMI is a risk factor or
secondary to airflow limitation, although low BMI has been reported to be a risk factor for COPD
]. The present study also showed that lower BMI was one of the
independent predictive variables for presenting airflow limitation, suggesting that low BMI is strongly
associated with COPD development. Smoking and second-hand smoke have been reported to
be the most important risk factors for COPD development [
1, 24, 25
]. Smoking rates in Asian
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countries are high especially for males , and in the present study (Table 1). Crude OR for
airflow limitation was significantly higher in males (Table 3), but significance was lost when
OR was adjusted, reflecting the high smoking prevalence in male subjects. A current smoking
status was found to be a significant risk factor for airflow limitation even after the adjustment
(Table 3). Smoking cessation or repeated attempts at smoking cessation has been reported to
be effective in preventing lung function decline and decreasing the prevalence of respiratory
symptoms even with subsequent cessation failure [27±31]. In contrast to current smokers,
former smoking was not significant risk factor for airflow limitation although the number of
former smokers in the present study was small (Table 3). Therefore, we can speculate that
smoking cessation is effective in Mongolia for preventing lung function deterioration.
Furthermore, for the subjects with airflow limitation of GOLD stage II or higher, both current and
former smoking were not significant risk factors for airflow limitation (S4 Table). These results
suggest that smoking does not have large impact on the risk for moderate to severe airflow
limitation (GOLD stage II or higher) but for mild (GOLD stage I) airflow limitation in this
population. It is consistent with the higher prevalence of mild airflow limitation (GOLD stage I) in
male which showed higher smoking prevalence than in female. In general, people using
smoke-rich fuel such as wood and coal for household use were exposed to indoor air pollution.
Exhausted smoke from gers is a primary cause of ambient air pollution in ger districts. Thus,
people living in ger districts are exposed to ambient air pollution for longer periods than
people living in urban area although air pollution covers urban areas as well, depending on time
and direction of the wind. Since indoor and outdoor air pollution is reported to be a cause of
airflow limitation [1, 13±18], we included the residential district and household fuel type as
independent variables in the multivariate analysis. Here, residential area and household fuel
type was not a significant predictor of airflow limitation (Table 3). Since actual exposure to air
pollution was not measured in the present study, subject responses accurately reflect exposure
to air pollution cannot be validated. The prevalence of airflow limitation in ger districts was
higher than that in urban areas but did not reach significance (Table 3). This result suggests
that the effect of air pollution on airflow limitation is relatively small in the present study. Our
previous study suggested that subjects living in ger districts with ventilatory impairment
showed significantly higher prevalence of respiratory symptoms, and decreased health status
in the cold season (unpublished data). Therefore, we can speculate that the effect of air
pollution was one of the risk factor for the exacerbation of symptoms and health status rather than
for the decline in lung function.
Since patients do not present themselves to the physician for examination until they have
severe symptoms or significant impairment, COPD is likely underestimated [
]. We assessed
the multivariate model for predicting airflow limitation using respiratory symptoms as
independent variables to encourage subjects with certain symptoms to consult a physician for early
detection of COPD. In this study, subjects presenting with the symptom ªusually cough up
sputum first thing in the morningº were liable to develop airflow limitation even after
adjustment (S1 Fig). Our result is consistent with a report by Kessler et al., where the fluctuation of
COPD symptoms over the day in COPD patients and all COPD-related symptoms including
phlegm were most predominant upon waking in the morning [
]. Encouraging subjects who
suffer respiratory symptoms in the morning to consult a physician would be effective for early
diagnosis of COPD and reduction of its associated burdens.
There are several limitations in this study. First, whether the putative risk factors found in
the present study indicates a risk of airflow limitation or its consequences is unclear due to the
cross-sectional design of this study. Second, in the present study, postbronchodilator
spirometry to distinguish asthma from COPD could not be performed as this study was conducted as a
screening. Since the biggest concern about accuracy of the estimation in this study was how
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many subjects with pure asthma without COPD were included in the subjects with airflow
limitation, we considered the possibility of bronchial asthma in Table 4 using differential
diagnostic criteria. As shown in Table 4, the standardized prevalence ranged 4.0% to 10.9%
corresponding the proportion of false positive ranged 63.3% to 0%. In Mongolia, asthma prevalence
was reported to be 4.7% based on symptoms [
], and Viinanen et al. reported the prevalence
of asthma in Ulaanbaatar to be 2.1% based on spirometry data although both studies did not
show COPD prevalence [
]. It is difficult to distinguish asthma from COPD in smokers and
older adults [
], as some patients may have clinical features of both asthma and COPD
known as asthma-COPD overlap syndrome (ACOS). In the present study, 2.3% of subjects
were diagnosed with asthma by respiratory specialists based on the symptoms and medical
history (Table 4). This is comparable to asthma prevalence in Ulaanbaatar based on spirometry
]. Lastly, the age distribution and male-to-female ratio of subjects were biased in the
present study as study subjects were older and with a lower male-to-female ratio compared to
the general Mongolian population. The overall prevalence of airflow limitation in this study
might be affected by the lower male-to-female ratio because the proportion of smokers was
much higher in males than in females. Nonetheless, this study population covered
approximately 0.1% of the Mongolian population aged 40 to 79 years [
] and the direct
standardization by age and sex were carried out using population data . Furthermore, multivariate
analyses adjusted for age, sex, and other factors potentially affecting airflow limitation were
carried out. Hence, the results obtained in this study reflect the actual situation in Mongolia
although generalizations are limited.
We investigated the prevalence of airflow limitation in subjects aged 40 to 79 in Ulaanbaatar,
Mongolia. The age- and sex-standardized prevalence of putative COPD ranged from 4.0 to
10.9% depending on the asthma criteria and the age- and sex-standardized prevalence was
10.0% when patients with physician-diagnosed asthma were excluded from COPD. An older
age, lower BMI, and current smoking status were independent risk factors for airflow
limitation. The putative COPD prevalence in this study was consistent with other reports from
S1 Fig. Respiratory symptoms associated with airflow limitation. Multiple logistic
regression analyses were carried out by a stepwise selection procedure used with forced inclusion of
specific variables. Respiratory symptoms were added as additional predictive variables as
follows; 1. Does the weather affect your cough? (Yes/No or No cough); 2. Have you ever coughed
up sputum from your chest when you do not have a cold? (Yes/No); 3. Do you usually cough
up sputum from your chest first thing in the morning? (Yes/No); 4. How frequently do you
wheeze? (Occasionally or more often/Never); 5. Do you have or have you had any allergies?
(Yes/No); 6. Do you suffer from any infectious disease? (Yes/No). Odds ratios were adjusted
for age group, sex, BMI, smoking status, household fuel, and residential district. The vertical
short line represents odds ratios; the horizontal line represents 95% confidence interval. The
omnibus tests of model coefficient were shown to be significant (P < 0.01) for all models.
Correlation coefficients (r) among predictive values were tested, and all r-values were less than
0.55, indicating no multicollinearity. P values less than 0.05 were considered to be statistically
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S1 Table. Characteristics of the subjects with restrictive ventilatory impairment.
S2 Table. Prevalence of airflow limitation in study population standardized by Mongolian
population when the cutoff value of airflow limitation was set at FEV1/FVC < 0.7 and
FEV1 < 80% of predicted value (GOLD stage II or higher).
S3 Table. Prevalence of putative COPD (GOLD stage II or higher) by diagnostic category
Conceptualization: MN YI.
Data curation: MN YI.
Formal analysis: MN YI.
Funding acquisition: YI.
Investigation: MN KY YI HO BS DI.
Methodology: MN YI.
Project administration: MN YI.
Resources: MN YI BS DI.
Validation: MN KY.
Writing ± original draft: MN.
Writing ± review & editing: MN KY YI.
S4 Table. Factors affecting the prevalence of airflow limitation (GOLD stage II or higher).
We would like to thank all staff at the Embassy of Japan in Mongolia for their cooperation
during our study in Mongolia. We also thank Dr. Go Hasegawa, Ms. Midori Yamaguchi, Ms.
Tomoe Terasaki, and Ms. Ayumi Narumi of Kurume University.
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