Science of the Total Environment 408 (2010) 754–759

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Science of the Total Environment

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s c i t o t e n v

Asian Dust Storm and pulmonary function of school children in Seoul

Yun-Chul Hong a, Xiao-Chuan Pan b, Su-Young Kim c, Kwangsik Park d, Eun-Jung Park d, Xiaobin Jin b,
Seung-Muk Yi e, Yoon-Hee Kim f, Choong-Hee Park g, Sanghwan Song g, Ho Kim f,⁎
a
Institute of Environmental Medicine, Seoul National University Medical Research Centre, Republic of Korea
b
Department of Occupational and Environmental Health, Peking University School of Public Health, China
c
Department of Preventive Medicine, College of Medicine, Cheju National University, Republic of Korea
d
College of Pharmacy, Dongduk Women's University, Republic of Korea
e
Department of Environmental Health, Graduate School of Public Health, Seoul National University, Republic of Korea
f
Department of Biostatistics and Epidemiology, Graduate School of Public Health, Seoul National University, Republic of Korea
g
Environmental Epidemiology Division, Environmental Health Research Department, National Institute of Environmental Research, Republic of Korea

a r t i c l e i n f o a b s t r a c t

Article history: Health effects of the Asian Dust Storm (ADS) have not been evaluated adequately, even though it may affect
Received 12 July 2009 health of people in East Asia. This study was conducted to evaluate whether the ADS affects particulate air
Received in revised form 1 October 2009 pollution and pulmonary function of children. We studied 110 school children in Seoul, Korea with daily
Accepted 9 November 2009
measurement of peak expiratory flow rate (PEFR) from May 13 to June 15, 2007. PM2.5, PM10 and metals bound to
Available online 24 November 2009
the particles were also determined daily during the study period in Ala Shan and Beijing (China) as well as in
Keywords:
Seoul (Korea). Three-day back trajectories showed that air parcels arrived at Seoul mostly from the desert areas in
Dust storms China and Mongolia through eastern China during ADS event affecting levels of particulate pollutants in the areas.
Air pollution Analysis of metals bound to the particulates showed that natural metal levels were much higher than the
Lung function anthropogenic metal levels. We found that ambient concentrations of PM2.5 and PM10 were not significantly
Metals associated with PEFR in school children except asthmatics during the study period (P N 0.05). However, most of
Particles the metal concentrations bound to the particulates were significantly associated with decrease of the children's
PEFR (P b 0.05). The effect of anthropogenic metals was not different from natural components of metals for
reduction of PEFR. This result indicates that exposure to the metals bound to particles during the ADS period
reduces children's pulmonary function, but there was no difference of potency for reduction of the pulmonary
function between natural and anthropogenic metal components.
© 2009 Elsevier B.V. All rights reserved.

1. Introduction of kilometres, the composition of particulate pollutants may change due

Epidemiologic studies have shown impact of particulate air
pollutants on the respiratory system, including increased emergency
room visits and hospital admissions as well as decrement of pulmonary
function (Schwartz et al., 1993; Burnett et al., 1995; Boezen et al., 1998).
With increasing evidence of health effects imposed by particulate
matter in ambient air, threat to neighbouring communities from
transboundary particulate air pollution emerges as a challenging issue
because air pollutants cannot be contained within national boundaries
and often travel long distances before deposition occurs. Transboundary
particulate air pollution frequently originates from natural sources, such
as forest fires or sandstorms. The Asian Dust Storm (ADS) is one of the
transboundary air pollution composed of particles originating from the
Chinese or Mongolian desert areas. However, as ADS travels thousands
⁎ Corresponding author. Graduate School of Public Health, Seoul National University, 28
Yunkeon-Dong, Chongro-Gu, Seoul, Republic of Korea. Tel.: +82 2 740 8874; fax: +82 2
745 9104.
E-mail address: hokim@snu.ac.kr (H. Kim).
to addition of local pollutants from urban or industrial emissions along
the path of the sandstorm (Chang and Lee, 2007). Because particle size,
surface area and chemical composition determine the health risk and
these characteristics vary depending on the geographical locations and
the path of the ADS, simple calculation of health risk based on the same
impact per unit change of particulate matter (PM) or their components
could undermine both understanding the health effects of ADS and
establishing abatement strategies. In fact, there have been no consistent
findings of adverse health effect from exposure to ADS. Previous reports
from Kwon et al. (2002) and Chen et al. (2004) showed that ADS were
weakly, but not significantly, associated with risk of death from circu-
latory and respiratory causes. In contrast, Chan et al. (2008) reported
significantly increased cardiopulmonary emergency visits during ADS
periods. Therefore, the health effect of ADS may be different from
adverse health effects due to urban particulate pollution because of
different size and chemical composition of the particles. ADS may con-
tain metals or chemical components predominantly from natural
sources such as sand, but typical urban air pollution contains predom-
inantly particles from anthropogenic sources such as diesel exhaust.

0048-9697/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2009.11.015
 Y.-C. Hong et al. / Science of the Total Environment 408 (2010) 754–759
Since the literature increasingly supports the assumptions that particles
from combustion sources, particularly engine exhaust particles, are
associated with greater health risks than natural sources, natural
components of particulates during the ADS period could cause health
problem less severely than anthropogenic components. Therefore, this
study was conducted to evaluate whether ADS affects the pulmonary
function of children, and then compared the effect between natural and
anthropogenic components of metals bound to particles to evaluate the
different potency of metal components from the two sources (Forsberg
et al., 2005).
2. Methods
2.1. Study population
We surveyed a total of 110 school children (56 boys and 54 girls) of
9 years old from an elementary school in Seoul, Korea between May 13
and June 15, 2007. We collected information from questionnaire filled
up by their parents about past medical history of asthma, rhinitis
and eczema symptoms; environmental tobacco exposure at home; and
residential environment. Most of the students lived in apartments, and
their socioeconomic status was regarded as middle class. The study
protocol was approved by the institutional review boards at Seoul
National University, and written informed consent was obtained from
parents of all study participants.
2.2. Peak expiratory flow rate
The peak expiratory flow rate (PEFR) measures the maximum speed
of expiration that is an instantaneous rate that occurs near the beginning
of a forced expiration. The PEFR monitoring has been used for
assessment of particulate air pollutant effects on airways because it is
easy to perform, and allows for a large number of measurements during
the study period. Each student was provided with a peak expiratory flow
meter (Clement Clarke International Ltd., Essex, UK) to measure PEFR
three times per day at 09:00, 12:00, and 20:00 daily during the study
period. Each student recorded the best of three PEFR values for each
measurement and the daily mean PEFR data were used for the final
analysis. The PEFR data from the first 3 days were not used for data
analysis because of the training period to learn the PEFR measurement.
Because we did not measure PEFR on Sunday, the data used for the
analysis were from 26 measurement days.
2.3. Measurement of PM2.5, PM10 and metal components
We measured daily ambient concentrations of PM2.5 and PM10 in
Ala Shan and Beijing in China and Seoul in Korea during the study
period to evaluate transport patterns of particles during the ADS
event. We defined ADS event day in Seoul when PM10 is 130 mg/m3
or more during the study period. The other days were defined as non-
ADS event days. To obtain concentrations of PM2.5 and PM10, we
gravimetrically analyzed dusts on the polytetrafluoroethylene filters.
Metals from the collected PM2.5 and PM10 were determined by
inductively coupled plasma-mass spectrometer (Perkin-Elmer, USA).
Metal concentrations were calculated as the ratio of the metal amount
in the PM2.5 or PM10 sample to the air volume collected during the
sampling. Aluminum (Al), manganese (Mn), calcium (Ca), iron (Fe),
silica (Si), cadmium (Cd), lead (Pb), zinc (Zn), molybdenum (Mo) and
arsenic (As) were measured. Data for temperature and relative humidity
were obtained from the Korea Meteorological Administration.
2.4. Analysis of trajectories
Three-day back trajectories were analyzed to identify the transport
patterns of air parcels arriving at the sampling site of Seoul during the
ADS event. The HYSPLIT (Hybrid Single-Particle Lagrangian Integrated
755
Trajectory) model was used in this study to obtain three-dimensional
three-day backward trajectories (Draxler and Hess, 1998). Trajecto-
ries were calculated every 4 h and arrival height of 1000 m was used
at the receptor location in Seoul.
2.5. Statistical analysis
Rotated factor analysis was employed to categorize metals bound
to particulates into natural and anthropogenic components. We also
performed analysis using linear mixed-effects model to estimate
particulates or metal effects on the daily PEFR. Health effects were
estimated after adjusting for individual variables such as age, sex,
height, weight, asthma history, and environmental tobacco exposure
at home; meteorological variables such as daily mean temperature,
mean relative humidity, and air pressure; and the linear time trend.
We treated each student as random effects while other variables as
fixed effects in the models. We separately analyzed for asthmatics and
non-asthmatics to compare the effects of particulates on PEFR. In
addition, the effects of particulates were compared between ADS and
non-ADS event days.
3. Results
The three-day back trajectories show that air parcels arrived at Seoul
mostly from the desert areas in China and Mongolia during the ADS
event (Fig. 1). The figure also shows the levels of PM2.5 and PM10 in the
three areas. Particulate levels in these three cities may reflect distances
from the origin of ADS and appear to be linked together. Peak
concentrations in Ala Shan seem to be preserved in Beijing after several
days and preserved at successively lower concentrations in Seoul a few
days later. Mean concentrations of PM2.5 and PM10 were 177.52 and
361.66 μg/m3 in Ala Shan, 101.35 and 217.39 μg/m3 in Beijing, and 36.20
and 61.85 μg/m3 in Seoul. We classified metals bound to PM2.5 and PM10
into two factors. Table 1 showed that Si, Mn, Fe, Ca and Al belong to the
same group while Mo, Cd, Zn, Pb and As belong to another group.
Considering main sources of the metals, we grouped Si, Mn, Fe, Ca and Al
as natural components and Mo, Cd, Zn, Pb and As as anthropogenic
components. The proportion of natural metal components bound to the
particulates was much higher than the anthropogenic metal compo-
nents (Table 2). Particularly, the proportion of natural metals was
highest in Ala Shan which is closest to the origin of ADS whereas the
proportion of anthropogenic metals was highest in Beijing.
We studied 56 male and 54 female students at an elementary school
in Seoul. The mean age was 9.3 years old and the number of participants,
who had asthma history and second-hand smoke exposure, stood at 18
(16.8%) and 20 (18.7%), respectively. Their mean PEFR levels were
267.6 L/min (Table 3). Table 4 shows the means and distributions of
concentrations for PM2.5, PM10 and metals bound to the particulates in
Seoul. The metals in the descending order of concentrations were Si, Ca,
Fe, Al, Zn, Pb, Mn, As, Mo and Cd. After analysis of the lag distribution of
the PEFR change associated with concentrations of PM2.5 and PM10 from
the current day to the 4 previous days, we chose the current day model
for further analysis of association because reduction of PEFR was largest
on the current day. Table 5 shows the estimated effects of PM2.5 and
PM10, and their metal elements on the children's lung function. The
outdoor concentrations of PM2.5 or PM10 were not significantly
associated with change of the PEFR (P N 0.05). However, the metal
concentrations of the particulates were significantly associated with
decrease of the children's PEFR (P b 0.05) with the exception of
molybdenum (Mo). After Bonferroni correction based on the number
of metals (P = 0.005), we found the same results for PM10-bound metals
whereas Mn, Cd, Pb and Zn remained significant among PM2.5-bound
metals. When we separately analyzed the effect of particulate
concentrations on PEFR of asthmatics from non-asthmatics from the
current day to the 4 previous days, we found that asthmatics have
significant and larger effects than non-asthmatics on the current day
756 Y.-C. Hong et al. / Science of the Total Environment 408 (2010) 754–759

Fig. 1. Three-day backward trajectories of ADS arriving at Seoul, and PM2.5 and PM10 levels in Ala Shan, Beijing, and Seoul during the study period.

(Fig. 2). To compare the effect of the metal components of the
particulates, we evaluated PEFR change by an interquartile increase of
each sum of the five natural and anthropogenic metal components
during ADS and non-ADS event days separately (Fig. 3). However, we
did not find a significant difference of PEFR reduction between natural
and anthropogenic metal components regardless of ADS event
(P N 0.05).
4. Discussion
Transboundary air pollution becomes a regional or global prob-
lem beyond a local issue. Due to the travelling nature of transbound-
ary air pollution, attempts to deal with the problem locally will yield
only limited success. ADS originate from the Chinese or Mongolian
desert area such as the Loess Plateau, the Gobi and the Taklamakan
desert. They are carried by the wind to neighbouring countries such
as Korea, Japan and Taiwan, even reaching the western coast of the
USA and Canada (Chang and Lee, 2007). In addition to ADS, air
pollution levels in Seoul are affected considerably by long-range
transport of emissions from coastal China (Kang et al., 2006; Kim et
al., 2007).
Particulate air pollutants can be derived from crustal and anthro-
pogenic sources, resulting in complex chemical mixture (Schlesinger,
2007). Fine particulates (PM2.5) are reported to come primarily from
combustion of fossil fuel, while coarse particulates (PM2.5–10) are from
crustal sources (Schwartz et al., 1999). However, concentrations of
PM2.5 in this study changed correspondingly with PM10 levels, making
this simple classification invalid in some circumstances.
In this panel study, PEFR was monitored to assess the pulmonary
effects of particulate air pollutants for school children. Particulate
air pollutants may lead to acute decrement of pulmonary function by
generation of free radicals, subsequently causing epithelial damage,
increased permeability and inflammation (Bergamaschi et al., 2001;
Prahalad et al., 2001; Becker et al., 2005). We found that PEFR of
asthmatics were significantly reduced with an increase of PM10
concentrations on the current day, but could not find significant
associations between PEFR and concentrations of PM10 or PM2.5 for non-
asthmatics during the study period. Compared to the previous
studies which showed that the decrements of the daily mean PEFR for

Table 1
Factor analysis.
Table 2
Factor 1 Factor 2 Mean concentration of particulates and proportions of natural and anthropogenic metal
components.
PM10 Si 0.3111 − 0.2112
Mn 0.2703 − 0.1508 Ala Shan Beijing Seoul
Fe 0.2823 − 0.1704
Mean (SD) Mean (SD) Mean (SD)
Ca 0.2315 − 0.0927
Al 0.1811 − 0.0285 PM10 Mass concentration 361.66 (249.40) 217.39 (111.05) 61.85 (45.36)
Mo − 0.3160 0.5328 (µg/m3)
Cd − 0.1003 0.3116 Natural metal 18.05 (12.01) 10.99 (8.48) 7.67 (5.79)
Zn − 0.0649 0.2733 components (%)
Pb 0.0016 0.1940 Anthropogenic metal 0.05 (0.02) 0.51 (0.37) 0.43 (0.32)
As − 0.0666 0.2410 components (%)
PM2.5 Mo 0.2949 − 0.2062 PM2.5 Mass concentration 177.52 (122.65) 101.35 (50.59) 36.20 (25.56)
Zn 0.2197 − 0.0670 (µg/m3)
Cd 0.2291 − 0.0976 Natural metal 9.31 (6.24) 3.03 (3.64) 4.08 (2.40)
Pb 0.1597 0.0302 components (%)
As 0.2454 − 0.1509 Anthropogenic metal 0.04 (0.02) 0.36 (0.28) 0.29 (0.21)
Si − 0.2738 0.4713 components (%)
Ca − 0.0251 0.2542
Natural metal components (%) = mean and standard deviation of natural metal
Al − 0.0952 0.2929
concentration/mass concentration ⁎ 100.
Fe 0.0429 0.1803
Anthropogenic metal components (%) = mean and standard deviation of anthropogenic
Mn 0.0491 0.1737
metal concentration/mass concentration⁎ 100.
 Y.-C. Hong et al. / Science of the Total Environment 408 (2010) 754–759 757

Table 3 storm such as metals, organic chemicals and inorganic pollutants.

Characteristics of study subjects and summary statistics.
Mean (SDa) or N (%)
Male/female 56/54
Age (year) 9.3 (0.5)
Height (cm) 138.1 (6.0)
Weight (cm) 34.9 (6.4)
Asthma history 18 (16.8)
Second-hand smoke exposure 20 (18.7)
PEFR (L/min) 267.6 (49.8)
a
SD, standard deviation.
1 μg/m3 PM2.5 were − 0.05 to − 0.54 L/min (Ward and Ayres,
2004; Hong et al., 2007), the decrement of PEFR, −0.03 L/min for
1 μg/m3 PM2.5, in this study participants was small. This difference
indicates that composition of particulates, especially metals bound to
particulates, is different depending on locations and study period, and
the particulate levels during this study period affect respiratory function
less severely than conventional urban air pollution.
Metal components of particulates may be responsible at least in
part for the effects of particulate air pollutants on respiratory health
(Valavanidis et al., 2008). We also reported that some metals such as
lead and manganese in particulate pollutants reduce PEFR of school-
children in the previous study (Hong et al., 2007). In the present
study, we found a significant decrease of the PEFR with metal
concentrations of particles except molybdenum.
Because the ADS usually reaches Seoul after crossing western China
where economic activity has grown rapidly with a significant amount
of industrial emission, we believe certain chemical components
contained in the particles of ADS comes from urban or industrial
pollutant emissions (Chan et al., 2008). Therefore, the health effects
due to ADS are not attributable only to dust storms that originated
from deserts in China and Mongolia. The effects would also be
attributable to urban or industrial pollutants picked up in the dust
When ADS mixes with locally generated pollutants, it may cause
different health effects depending on the interaction among local
pollutant emissions, particle concentrations of the ADS and dilution of
windstorm.
To differentiate origin of metals bound to particles, we classified
metal components into two major contributing sources after factor
analysis: aluminum (Al), manganese (Mn), calcium (Ca), iron (Fe)
and silica (Si) as metals of natural sources and cadmium (Cd), lead
(Pb), zinc (Zn), molybdenum (Mo) and arsenic (As) as anthropogenic
components. This classification was consistent with previous reports
(Kim et al., 2003; Park et al., 2007). We found that there was no
significant difference of potency to reduce pulmonary function of the
children between metals of natural and anthropogenic sources
regardless of ADS event. This finding suggests that metals bound to
particles were responsible for reported health effects during the ADS
period irrespective of sources.
To the best of our knowledge, this is the first study to compare health
effects from natural and anthropogenic components during the ADS
period. However, the limitations of this study should be considered.
First, we used area monitoring data instead of measuring personal PM2.5
or PM10 exposure. This might have caused measurement error for
exposures to particulate air pollutants, but is likely to cause a bias
toward the null hypothesis and to underestimate their effects (Zeger
et al., 2000). Second, we did not measure daily exposure to gaseous
pollutants or chemicals other than metals, which also may be
responsible for changes of PEFR in school children. Third, urban air
pollution levels were affected by local pollution sources as well as by the
ADS during the study period. Therefore, effect estimates based on
particle concentrations during the study period may be mixed results
from exposure to the ADS and local sources.
In conclusion, our results show that airborne particulates move
from the desert areas to Seoul, which influence on particulate concen-
trations in the cities along the path. However, outdoor particulate
concentrations during the ADS period were not significantly associ-

Table 4
Concentration of the particulate-bound metal levels in Seoul.

Natural elements Anthropogenic elements

Al Mn Ca Fe Si Sum Cda Pb Zn Moa As Sum

PM2.5 (µg/m3) Mean 0.192 0.022 0.358 0.264 1.493 2.329 0.114 0.037 0.101 0.121 0.008 0.149
SDb 0.122 0.016 0.351 0.170 1.289 1.801 0.057 0.023 0.060 0.052 0.006 0.086
IQRc 0.144 0.014 0.324 0.172 2.143 2.109 0.091 0.024 0.060 0.077 0.010 0.093
PM10 (µg/m3) Mean 0.414 0.043 1.576 0.563 2.405 5.001 0.145 0.053 0.153 0.217 0.017 0.227
SD 0.503 0.043 2.333 0.529 2.823 6.060 0.083 0.037 0.129 0.094 0.035 0.194
IQR 0.188 0.020 0.643 0.322 2.492 3.099 0.113 0.039 0.116 0.127 0.010 0.159
a
Presented values are actual value ⁎ 100.
b
SD, standard deviation.
c
IQR, interquartile range.

Table 5
Estimated regression coefficients of PM2.5, PM10 and metals bound to the particles on PEFR (L/min) of school children in Seoul.

Mass Natural elements Anthropogenic elements

concentrations
Al Mn Ca Fe Si Sum Cd Pb Zn Mo As Sum

PM2.5 βa − 0.03 − 14.33 − 127.12 − 5.10 − 10.32 − 1.31 − 1.08 − 3148.00 − 99.34 − 37.09 − 2171.97 − 250.26 − 26.08
(µg/m3) SEb 0.02 5.08 40.55 1.84 3.80 0.57 0.40 1069.63 27.64 10.51 1267.81 97.49 7.25
β ⁎ IQRc − 0.66 − 2.07 − 1.75 − 1.65 − 1.77 − 2.81 − 2.28 − 2.86 − 2.42 − 2.24 − 1.68 − 2.42 − 2.42
P-value 0.229 0.005 0.002 0.006 0.007 0.021 0.006 0.003 b 0.001 b 0.001 0.087 0.010 b0.001
PM10 Β − 0.03 − 4.90 − 50.54 − 1.04 − 3.77 − 0.84 − 0.40 − 2569.12 − 65.42 − 21.83 − 1275.33 − 71.56 − 14.65
(µg/m3) SE 0.01 1.30 15.41 0.28 1.23 0.25 0.11 727.99 17.50 5.10 674.76 19.04 3.41
β ⁎ IQR − 1.07 − 0.92 − 1.00 − 0.67 − 1.21 − 2.09 − 1.25 − 2.90 − 2.55 − 2.54 − 1.62 − 0.73 − 2.33
P-value 0.062 b 0.001 0.001 b0.001 0.002 0.001 b0.001 b0.001 b 0.001 b 0.001 0.059 b 0.001 b0.001
a
β, regression coefficients of particles or metal components on PEFR.
b
SE, standard error.
c
IQR, interquartile range.
758 Y.-C. Hong et al. / Science of the Total Environment 408 (2010) 754–759

Fig. 2. PEFR change by 1 μg/m3 increase of PM2.5 and PM10 for all subjects, non-asthmatics and asthmatics from the current day to the 4 previous days. Estimated decrements of PEFR
(dots) and 95% confidence intervals (error bars) controlling for age, sex, height, weight, asthma history, and environmental tobacco exposure at home; meteorological variables such
as daily mean temperature, mean relative humidity, and air pressure; and the linear time trend.

ated with PEFR change in school children except asthmatics. Acknowledgments

Nevertheless, metals bound to the particulates during the ADS period
affect pulmonary function in school children, but there was no This work was supported by the National Institute of Environ-
difference of potency for reduction of the pulmonary function mental Research, Korea (2007). We wish to thank Dr So-Yeon Park
between natural and anthropogenic metal components. and Mr Gi-Moon Kim and Bo-Won Seo for their technical assistance.

Fig. 3. PEFR change by an interquartile increase of each sum of the five natural and anthropogenic metal components bound to PM10 and PM2.5 during ADS and non-ADS event days.
Estimated decrements of PEFR (dots) and 95% confidence intervals (error bars) controlling for age, sex, height, weight, asthma history, and environmental tobacco exposure at home;
meteorological variables such as daily mean temperature, mean relative humidity, and air pressure; and the linear time trend.
 Y.-C. Hong et al. / Science of the Total Environment 408 (2010) 754–759
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