Participants and residential areas

The participants were 1200 children (age 6–12 years) from five public elementary schools. The schools were located in three urban districts (Sukhbaatar, Khan-Uul, and Bayanzurkh) and a suburban district (Nalaikh) in Ulaanbaatar. The districts were named A, B, C, and D, respectively. Figure ​Figure11 shows the locations of the study areas in Ulaanbaatar. District A is located in the center of the city. Two public schools in district A were included in this study. District B is located adjacent to district A, and industrial activity takes place in this district. District C is located at the eastern end of the urban area, and most residents live in “gers”. For comparative analysis, we selected suburban area D, which is located 40 km southeast of the urban area. It is the nearest suburban area to the capital and has increased rapidly in size, as internal migrants have moved from rural areas; therefore, approximately 70% of the residents live in “gers”.

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Fig. 1

a Map of Ulaanbaatar. b The locations of the urban study sites; A, B: apartments (white), C: “gers” (black). c The location of the suburban site; D: apartments (white), “gers” (black)

In each of these districts, the targeted school was close to traffic major road within 200 m. In the urban areas, outdoor air pollutant levels were measured by ambient air quality-monitoring stations. However, such systems have not yet been installed in district D (the suburban area; Fig. ​Fig.11).

Distance from each subject’s residence to the nearest major road and traffic volume

We estimated the distance between each subject’s residence and the nearest major road using the GeoNET 9.7.107 GPS navigator for mobile mapping software. Then, we categorized the subjects into ≤100 m and >100 m groups, depending on the distance from their residence to the nearest major road. Also, we measured the daily traffic volume at the major road nearest to each school four times in 2015. The mean daily traffic volume was determined using a vehicle counter (Tempomat CRM, IV, Radarlux).

Questionnaire

The survey about respiratory symptoms was based on a questionnaire adapted from the American Thoracic Society Epidemiologic Standardization Project questionnaire [19]; i.e., the ATS DLD 78 C questionnaire for children, which has been used in previous studies [8, 20–24]. The questionnaire was translated into Mongolian and then distributed to the participants via their schools. It was completed by their parents at home after obtaining written parental consent. The participants were given a week to return the questionnaire. All of the questionnaires were given ID numbers prior to the analysis.

The items included in the questionnaire were age, sex, residential address, whether the subject was bottle-fed in infancy, how long they had lived at their current residence, the heating system used in their home, their parents’ smoking habits at home, and their history of respiratory disease and current respiratory symptom status. The questionnaire covered the following respiratory symptoms: persistent cough, persistent phlegm, current wheezing, and asthma-like symptom. Respiratory symptoms were recorded as being present if a participant answered, “Yes”, to a relevant question. The participants were provided with explanations about each respiratory symptom [see Additional file 1: Table S1].

Passive sampling of air pollutants near schools

We selected NO₂ and SO₂ as indicators of outdoor air pollution. The ambient air concentrations of NO₂ and SO₂ were measured near the schools. The concentrations of these pollutants were measured in February, April, August, and November in 2015 and in January, April, July, and October in 2016. The two field blanks used for the concentration analysis and the filters for NO₂ and SO₂ were exchanged five times each at intervals of approximately 48 h. The samplers were installed for 10 days (14,400±5 min). We measured the mean air temperature and relative humidity during the same period as the NO₂ and SO₂ measurements were obtained. The levels of NO₂ and SO₂ were assessed using co-located Ogawa passive samplers (Ogawa & Co., Ltd., Kobe, Japan), which were used in previous studies [4, 25–28]. The passive samplers were installed at two sites, which were located ≤100 m and >100 m from the nearest major road, respectively, at a height of approximately 2.5 m.

Statistical analyses

All statistical analyses were performed using the PASW Statistics software, v.18 (Chicago, IL, USA). All questionnaire data were analyzed based on the ID numbers assigned to the questionnaires. The associations between respiratory symptoms and personal and environmental factors were analyzed statistically via multinomial logistic regression analysis. The respiratory symptoms were used as dependent variables, and potential confounding factors were used as independent variables. The following variables were considered to be potential confounding factors: gender, age, how long the subject had lived at their current residence (years), history of asthma diagnosed by a doctor, history of allergies or respiratory disease before the age of 2 years, history of pneumonia, being bottle-fed in infancy, parental smoking habits, and the distance between the subject’s residence and the nearest major road. We also analyzed the associations between the concentrations of air pollutants and respiratory symptoms; i.e., logistic regression was used to calculate odds ratio (OR) and 95% confidence interval (CI) values. P-values of <0.05 (two-tailed) were considered statistically significant. Adjusted OR were estimated and scaled to represent a 1-ppb increase in the NO₂ or SO₂ concentration, based on the mean 2-year concentrations and traffic volume data for each district. The paired t-test was used to examine the significance of differences in the seasonal concentrations of SO₂ and NO₂, and changes in the NO₂ concentration due to the distance from the main road. We evaluated the statistical significance of differences in the frequency of respiratory symptoms between the residential areas using one-way analysis of variance (ANOVA). P-values of <0.05 (two-tailed) were considered to be statistically significant.

Analytical method for NO₂

The NO₂ collection filters (14.5 mm) were placed in 25-ml glass vials. Then, 8 ml distilled water was added to the filter-containing vials, and each vial was subjected to shaking for extraction. After 30 min of extraction, the vials were refrigerated at 4–5 °C for 30 min. Then, 2 ml of sulfanilamide solution and 1-naphthyl-ethylenediamine dihydrochloride (NEDA; 0.56 g dissolved in 100 ml distilled water, stored at −4 °C) solution were added in a 10:1 ratio. The resultant mixture was simultaneously shaken and cooled for 30 min. After that, the vials were returned to room temperature. The absorbance of the samples was determined with a spectrophotometer at a wavelength of 545 nm.

Prevalence of respiratory symptoms among children

The survey was carried out in 2015. The questionnaire was completed by 1130 children, and 21 children were excluded because they were living in other districts or did not fill out more than half of the questionnaire. Table ​Table33 shows the personal and environmental data obtained via the questionnaire alongside the prevalence of respiratory symptoms by district. The ATS DLD questionnaire was correctly completed by 1109 (92.4%) participants. Among the subjects aged 6–12 years, the most common respiratory symptom was persistent cough (28.5%). In addition, 20.2% of the subjects reported persistent phlegm, 5.8% had current wheezing, and 0.7% reported asthma-like symptom. Furthermore, the following findings were obtained regarding the frequency of other background factors: being bottle-fed in infancy: 18.4%, a history of respiratory disease before the age of 2 years: 26%, a history of diagnosed asthma: 2.4%, a history of diagnosed pneumonia: 6.2%, history of residence year for >3 years: 65.6%, parents smoke at home: 43.1%, coal being used for heating at home: 33.5%, and living ≤100 m from the nearest major road: 37.4%. In particular, in districts C and D, high prevalence of subjects had persistent cough (32% and 37%, respectively). However, the prevalence of asthma-like symptoms was low.

Table 3

Descriptive characteristics of the subjects and the prevalence of respiratory symptoms based on the questionnaire

Residential area	Apartment				Ger dwelling				Total
District	A urban		B urban		C urban		D suburban
	n	%	n	%	n	%	n	%	n	%
Response rate	238	79	273	91	300	100	298	99	1109	92.4
Sex
Female	129	54	123	45	122	41	141	47	594	53.6
Male	109	46	150	55	178	59	157	53	515	46.4
Age
6–8 years	135	57	161	59	146	49	176	59	618	55.7
9–12 years	103	43	112	41	154	51	122	41	491	44.3
Feeding in infancy (bottle milk)	52	22	47	17	57	19	48	16	204	18.4
History of respiratory diseases before 2 years old	68	29	89	33	65	22	66	22	288	26.0
History of diagnosed asthma	12	5.0	2	0.7	6	2.0	7	2.3	27	2.4
History of allergic diseases	52	22	57	21	38	12	29	10	176	15.9
History of pneumonia	16	7	25	9	16	5	12	4	69	6.2
Parental smoking habit at home	87	37	103	38	146	49	142	48	478	43.1
History of residence years	150	63	170	62	187	62	220	74	727	65.6
Heating type (coal using)	6	3	11	4	141	47	214	72	372	33.5
Distance from major road <100 m	119	50	126	46	99	33	69	23	413	37.4
Daily traffic volume	16,842		16,985		19,473		7187		60,487
Respiratory symptoms
Persistent cough	60	25	50	18	95	32	111	37	316	28.5
Persistent phlegm	50	21	50	18	63	21	61	21	224	20.2
Asthma-like symptom	4	2	0	0	2	1	2	1	8	0.7
Current wheezing	22	9	14	5	17	6	11	4	64	5.8

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Respiratory health outcomes

This study confirmed that Mongolian schoolchildren have high prevalence rates of persistent cough (28.5%), persistent phlegm production (20.2%), current wheezing (5.8%), and asthma-like symptoms (0.7%). When the prevalence was examined by district, the prevalence of persistent cough was high in the suburban compared to the urban district which has similar many gers dwellings (37% vs. 32%, respectively). Conversely, the concentration of SO₂ was higher in district C than in the suburban (district D). The survey indicated that there are several possible reasons for this first, more children in district D (72%) than in district C (47%) lived in a household in which coal was used. So, it is considered that these children were affected by emissions from coal. Another possible reason is that the children in district D had lived in the same place for a longer period than those in district C; i.e., 74% of the children in district D had lived in the same residence place for >3 years, whereas the equivalent figure for district C was 62% (data shown in Table ​Table3).3). In a previous study, in which the subjects had a similar age distribution to those in our study, it was concluded that outdoor air pollution is the major source of black carbon (BC) and fine particulate matter (PM_2.5) exposure for children living in Ulaanbaatar. Also, it was reported that the children living in a district containing many “gers” were exposed to the highest levels of outdoor air pollution [37]. In our study, persistent cough was significantly more common in the areas containing many “gers” (districts C and D) than in the areas containing large numbers of apartments (districts A and B, p<0.001) [see Additional file 1: Table S6]. In particular, the prevalence rate of persistent cough was significantly higher in the suburban district (district D) than in the urban areas (districts A, B, and C, p<0.000). Even in the suburbs, the use of coal has led to a high prevalence of persistent cough in children. We were reported that on an isolated island without major artificial sources of air pollutants, changes in the concentrations of air pollutants acutely influenced the pulmonary function of healthy subjects [38]. On the other hand, the increased prevalence of respiratory symptoms may also affect the burning of solid waste at the open dumpsites in the gers districts. There still has a problem with solid waste, coal ash and other rubbish, and also low-income households burn old tires, plastic bottles [39, 40]. Das B et al. reported that open burning of municipal solid waste is a poorly characterized and frequently underestimated source of air pollution. It is can trigger health impacts such as acute and chronic respiratory disease [41]. Boadi K. O et al. reported also that inadequate solid waste facilities result in indiscriminate burning and burying of solid waste. There is an association between waste burning and the incidence of respiratory health symptoms among children [42].

In the statistical analysis, we confirmed that the prevalence of persistent cough among children was associated with the concentration of SO₂. Some Chinese studies have reported that children exhibit enhanced sensitivity to the harmful effects of air pollution. In addition, it was confirmed that genetic susceptibility and/or exposure to common environmental factors have a strong influence on respiratory health [8, 43].

In our study, the current wheezing symptom among children associated an increase in NO₂ concentration (data shown in Table ​Table4).4). Nicolai T et al.reported that the frequency of current wheezing among children increased with the NO₂ concentration [44]. Also, in our study, the children who were bottle-fed in infancy displayed an increased prevalence of current wheezing. Other studies have demonstrated that being breastfed was associated with a lower risk of lung function problems and reduced children’s susceptibility to the respiratory effects of pollutants [45, 46].

The prevalence of persistent cough and phlegm were reported to be more common among children in Mongolia than among children in the north and north-eastern cities of China and Thailand, but the frequencies of current wheezing and asthma-like symptom were similar in all of these places [8, 21, 22, 43]. It is considered that other than the geographical features mentioned above and the temperature inversion layer phenomenon that occurs in winter, meteorological features also have a great influence, as Ulaanbaatar has a longer heating period than China; i.e., it lasts for 8 months from mid-September to mid-May [47]. In winter, when coal consumption increases, the concentrations of air pollutants are expected to rise markedly, which might induce respiratory symptoms in children. However, a previous Japanese study found that persistent cough and phlegm were less common among Japanese children than among Mongolian children, although current wheezing and asthma-like symptom were more common among Japanese children [22]. One possible reason for this is that since the 1970s, the atmospheric concentration of SO₂ in Japan has reduced owing to the introduction of emission-control technologies. On the other hand, NO₂ concentrations decreased from 1970 to 1985, but increased from 1985 to 1995. NO₂ concentrations are notably higher at roadside air-monitoring stations [48].

Highlights of this study

We conducted a survey of respiratory symptoms among children and measured the air pollution levels in Ulaanbaatar, including in a suburban area. No previous studies have examined the prevalence of respiratory symptoms among children in suburban areas. Furthermore, outdoor air pollutants were being measured at ambient air quality monitoring stations in the urban areas of Ulaanbaatar. However, such systems have not been installed in the suburban areas surrounding the city. Moreover, traffic volume was assessed in a suburban area for the first time in this study.

We are grateful to the teachers and parents of the schoolchildren for their cooperation and support. Traffic volume was assessed in cooperation with the Ulaanbaatar Intelligent Traffic Center. The authors thank Ogawa & Co., Ltd., Japan, for analyzing the SO₂ samples and for their assistance with the data collection. The authors would like to thank Enago (www.enago.jp) for reviewing the English language.