Yonago Acta medica 2012;55:41–48

Influence of Asian Desert Dust on Lower Respiratory Tract
Symptoms in Patients with Asthma over 4 Years
Masanari Watanabe*, Jun Kurai*, Tadashi Igishi*, Akira Yamasaki*, Naoto Burioka†,
Hiromi Takeuchi‡, Takanori Sako§, Hirokazu Touge*, Masaki Nakamoto*, Yasuyuki
Hasegawa*, Hiroki Chikumi*, Shingo Matsumoto*, Chie Yamasaki*, Sayaka Minato#,
Yutaka Ueda#, Kazunori Horasaki#, Tetsushi Watanabe¶ and Eiji Shimizu**Division of Medical Oncology and Molecular Respirology, Department of Multidisciplinary Internal Medicine,
School of Medicine, Tottori University Faculty of Medicine, Yonago 683-8054, Japan, †Department of Pathological Science and Technology, School of Health Science, Tottori University Faculty of Medicine, Yonago 683-8053,
Japan, ‡Division of Otolaryngology, Head and Neck Surgery, Department of Medicine of Sensory and Motor Organs, School of Medicine, Tottori University Faculty of Medicine, Yonago 683-8054, Japan, §Clinic of Respiratory
Medicine, Obase Hospital, Miyako-gun Kanda-machi 800-0300, Japan, #Tottori Prefectural Institute of Public
Health and Environmental Science, Yurihama-cho 682-0704, Japan and ¶Laboratory of Public Health, Divisionof Biological Sciences, Kyoto Pharmaceutical University, Kyoto 607-8414, Japan

The Asian Dust Storm (ADS) aggravates symptoms and pulmonary dysfunction in adultasthma patients. Our objective was to investigate the association of air pollutants and metals
in desert dust with worsening of asthma symptoms during the ADS. A telephone survey was
performed to investigate the upper and lower respiratory tract symptoms, ocular symptoms
and skin symptoms of asthma patients during the ADS in March between 2007 and 2010.
Four surveys were conducted in 46 patients. Two patients noted worsening of lower respiratory tract symptoms in all four surveys, as well as 2 patients in three surveys, 7 patients in
two surveys, and 9 patients in one survey. There was no worsening of lower respiratory tract
symptoms in 26 patients. In each patient, the influence of the ADS on lower respiratory tract
symptoms varied between surveys. In 2010, the level of suspended particulate matter was
highest in all four years, but the smallest number of patients noted worsening of lower respiratory tract symptoms. Among pollutants, only the maximum concentration of nitrogen dioxideduring the ADS was significantly associated with the worsening of lower respiratory tract
symptoms. The influence of the ADS on lower respiratory tract symptoms of adult asthma patients is variable.
Key words: air pollution; Asian Dust Storm; asthma; lower respiratory tract symptom; telephonesurveyDust storms originating in the deserts of Mongolia,
northern China and Kazakhstan are collectively
known as the Asian Dust Storm (ADS). It is a seasonal phenomenon that affects much of East Asia,and the ADS occasionally even reaches the east
coast of the United States (Duce et al., 1980; Taylor,2002). Recently, many studies have identified healthproblems related to the ADS, along with an increasein the frequency and duration of these storms (Hanet al., 2004). In patients with asthma, some studies have found that exposure to the ADS increases
hospitalization and emergency room visits, exacerbates symptoms, and impairs respiratory function(Kwon et al., 2002; Yoo et al., 2008; Kanatani et al.,2010). Our previous studies have also revealed that
the ADS is associated with deterioration of symptoms and respiratory function in adults with asthma

Abbreviations: ADS, Asian Dust Storm; PEF, peak expiratory flow; PEFR, PEF rate; PM, particulate matter; SPM,
suspended PM

41

M. Watanabe et al.

the telephone survey every March between 2007
and 2010. Asthma was diagnosed according to thecriteria in the Global Initiative for Asthma guidelines (GINA, 1995). All patients had a history ofintermittent wheezing and airway hyperresponsiveness to methacholine or > 20% diurnal fluctuationof peak expiratory flow (PEF). They satisfied thedefinition of moderate asthma according to National
Institute of Child Health and Human Development
and the National Heart, Lung, and Blood Institutewhen assessed during February in every year of thesurvey (Schatz et al., 2003). Their inhaled corticosteroid dosages were classified as low, medium, or
high according to the Japanese guideline for adultasthma (Ohta et al., 2011). All patients gave written
informed consent.

(Watanabe et al., 2011a, 2011b).
Dust from deserts in Mongolia and northern
China has been reported to cause pulmonary andbronchial inflammation in animals (Lei et al., 2004;
Hiyoshi et al., 2005; Ichinose et al., 2006), but themechanism through which the ADS causes exacerbation of asthma has not been fully clarified. In
addition, the optimum methods for prevention andtreatment of asthma attacks during ADS are notwell understood. Aggravation of asthma symptoms
during ADS may not be due to dust alone, because
Asian desert dust contains natural and man-mademetal components, fungi and lipopolysaccharide,and because the levels of various air pollutants
such as SO and NO2 increase during ADS (Choiet al., 2001; Mori et al., 2003; Hong et al., 2010;
Watanabe et al., 2011a, 2011b). According to Honget al. (2010), the concentrations of most of the metals bound to dust were significantly associated witha decrease of the peak expiratory flow rate (PEFR)
in nonasthmatic school children, while the concentrations of particulate matter (PM) ≤ 2.5 μm and ≤10 µm in diameter were not significantly associatedwith the PEFR. We previously reported that pollen combined with the ADS led to augmentation ofsymptoms and pulmonary dysfunction in patientswith asthma (Watanabe et al., 2011b).
Between 2007 and 2011, we investigatedwhether patients with asthma experienced worsening of symptoms and pulmonary dysfunction during ADS. The present study was performed to assess the relations between asthma symptoms during
ADS, and air pollutants and metals found in desert
dust based on the results of our 4-year survey.

Definition of the ADS and measurement of
air pollutants, airborne pollen and metals
In Japan, ADS days are defined as days when visibility is less than 10 km due to dust arising from thedeserts of East Asia. In the present study, the ADS
events were defined according to information provided by the Japan Meteorological Agency and theMinistry of the Environment. Suspended PM (SPM)
and the levels of SO2, NO and NO2 were measured
by Tottori Prefectural Institute of Public Health andEnvironmental Science. Natural and anthropogenic
metal components such as Fe, Al, Ca, Cd, Mn, Ni,
Cu, Pb and Cr, were also measured.
Airborne pollen was measured with a Durham sampler placed on the roof of a building (10 mabove ground level) at a location with free air movement on all sides. Slides covered with glycerine jelly
containing fuchin were exposed for 24 h. Then thepollen grains in an 18 × 18 mm area on each slidewere counted after staining with Calbela’s solution.
The total daily pollen count was expressed as thenumber of pollen particles/cm2.

Materials and Methods
Patients
In each year between 2007 and 2010, we performed
a telephone survey 3 days after the 1st ADS event
and inquired whether asthma patients had experienced exacerbation of upper and lower respiratory
tract symptoms, ocular symptoms or skin symptoms(Watanabe et al., 2011a, 2011b). The present study
focused on 46 asthma patients who participated in

Telephone survey
As in our previous surveys (Watanabe et al., 2011a,
2011b), we asked about the following symptoms
during ADS days compared with a week before the42Asian dust and asthma

Table 1. Patient characteristics in 2007

ADS: i) worsening cough, sputum, wheezing, dyspnea and use of short-acting 2-agonists and hospital attendance for lower respiratory tract symptoms;ii) tearing, itching, mucus and pain as ocular symptoms; iii) stuffiness, sneezing, pharyngalgia anditching as upper respiratory tract symptoms and iv)
itching, redness and pain as skin symptoms. We defined exacerbation of symptoms as worsening of atleast one symptom, but excluded patients who had
confirmed or suspected respiratory tract infection.
We defined respiratory tract infection as existing in
any of the following patient groups: i) patients with
pyrexia, trachyphonia, or sore throat; ii) patients
who concluded that they had respiratory tract infection based on their own interpretation of symptoms
and iii) patients whose family members and/or colleagues also had cold-related symptoms.

Number46
63.4 ± 15.2
Age (yr)
Gender (male/female)
23/23
109.3 ± 102.4
Disease duration (mo)Presence of other allergic diseases
22
Allergic rhinitis
8
Cedar pollen and/or cypress pollen allergy
Perennial allergic rhinitis
14
2
Allergic conjunctivitis
Atopic dermatitis
33
Non-allergic rhinitis
Data are presented as the mean ± SD.

maintenance treatment on deterioration of lower respiratory tract symptoms during ADS. Significancewas accepted at P < 0.05 for all analyses. The present study was approved by the Ethics Committeeof Tottori University (permission number: 771 and1082). All procedures were performed in accordance with the principles defined in the Declarationof Helsinki.

Data analysis
Results are shown as the mean ± SD. SPSS software(Japanese version 16.0 for windows; IBM Japan, Tokyo, Japan) was used for statistical analysis. The 2
test was employed to estimate differences between
the surveys with respect to maintenance treatment,
as well as differences in the frequency of patientswith exacerbation of upper and lower respiratory
tract symptoms, ocular symptoms, skin symptoms,
and multiple classes of symptoms. Multivariate logistic regression analysis was performed to compare
the effects of weather conditions, air pollutants, andResults
Patient characteristics

Table 1 shows the characteristics of the patients in
February in 2007. Forty-six patients (23 male and23 female) participated in the study. There were 22
patients with allergic rhinitis, 3 with non-allergic
rhinitis, 2 with allergic conjunctivitis and 3 withatopic dermatitis. In all of thetelephone surveys, none of theTable 2. Comparison of maintenance treatment during March inpatients complained of other aleach year
lergic diseases. Table 2 shows the
2007
2008
2009
2010
maintenance treatment for asthma
surveysurveysurveysurveyduring March of each year. Use
47 (100) 47 (100) 47 (100) 47 (100)Inhaled corticosteroid
of intranasal corticosteroids inLow dose
11 (23.9)
8 (17.4) 7 (15.2) 7 (15.2)
Medium dose18 (39.1) 18 (39.1) 14 (30.4) 15 (32.6)
creased every year of the survey
17 (37.0) 20 (43.5) 25 (54.3) 24 (52.2)
High dosefrom no patients (0%) in 2007 to 1
19 (41.3) 21 (45.7) 25 (54.3) 26 (56.5)
Long-acting 2-agonists
patient (2.2%) in 2008, 6 patients
Leukotriene receptor antagonist 18 (39.1) 18 (39.1) 22 (47.8) 20 (43.5)(13.0%) in 2009 and 10 patients
Teophylline
10 (21.7)
9 (19.6) 9 (19.6) 8 (17.4)
5 (10.9)
6 (13.0) 8 (17.4) 8 (17.4)
Antihistamine(21.7%) in 2010. There were sigNasal corticosteroid*0 (0)1 (2.2)6 (13.0) 10 (21.7)
nificant differences between the( ), %.
surveys according to the 2 test.
* P < 0.05: differences were estimated by the 2 test.
Apart from the use of intranasal
43

M. Watanabe et al.

ADS days in 2010 (around 1/cm2/day). In contrast,
pollen levels were high on ADS days in the otheryears, especially in 2009. The levels of air pollutants (SO2, NO and NO2) and those of natural andanthropogenic metals varied widely. Most of themetal components identified were natural metals
such as Fe, Al and Ca.

steroids, there were no significant differences ofmaintenance treatment between each survey.
Air pollutants, airborne pollen and metalcomponents
Eight ADS days were identified during Marchbetween 2007 and 2010, including March 28 and
29 in 2007; March 4 in 2008; March 16 and 17 in
2009; and March 13, 16 and 21 in 2010. Table 3
shows the daily average or maximum values forweather conditions, air pollutants, pollen and natural and man-made metals. SPM levels were highest in 2010, but airborne pollen levels were low on

Telephone surveys
The results of the telephone surveys are displayed inTable 4. Worsening of lower respiratory tract symptoms was reported by 12 out of the 46 patients (26.1%)
in the 2007 survey, 8 out of the 46 patients (17.4%)
in the 2008 survey, 12 out of the 46 patients (26.1%)
in the 2009 survey and 5 out of the 46 patients (10.9%)
in the 2010 survey. The frequency of worsening
symptoms did not differ significantly between thesurveys. Worsening of upper respiratory tract symptoms was reported by 7 patients (15.2%) in 2007
and 2008, 10 patients (21.7%) in 2009 and 1 patient(2.2%) in 2010, with a significant difference by the
2 test. Worsening of ocular symptoms was reported
by 4 out of the 46 patients (8.7%) in the 2007 survey,
2 out of the 46 patients (4.3%) in the 2008 survey,
9 out of the 46 patients (19.6%) in the 2009 survey
and 1 out of the 46 patients (2.2%) in the 2010 survey. There were significant differences between thesurveys by the 2 test. Although the SPM level was
highest in 2010, the number of patients with worsening of upper respiratory tract and ocular symptoms
was markedly lower than that in other years. Noneof the patients was hospitalized for exacerbation ofasthma in any of the years investigated.
Table 5 shows the number of patients withworsening of lower respiratory tract symptoms on
ADS days across the four surveys. There were 9of the 46 patients with worsening of lower respiratory tract symptoms in only one survey, including
2 patients in 2007, 5 patients in 2009 and 2 patientsin 2010. All patients with deterioration of lower
respiratory tract symptoms in 2008 also experienced worsening of symptoms in other years. Seven
patients had worsening of lower respiratory tract
symptoms in two surveys, including 3 patients inboth 2007 and 2008, 3 patients in both 2007 andTable 3. Weather conditions and concentrationof air pollutants, air pollution levels, pollen, andnatural and anthropogenic metal components on
ADS day(s) in March of each year
March March
29–30
4
2007
2008

March
16–17
2009

March
21
2010

12.9
6.3
15.0
9.2
Temperature* (˚C)
Humidity* (%)
72.0
78.0
50.3
60.6
Atmosphericpressure* (hPa) 1009.3 1011.0 1014.1 1015.3
SPM(mg/m3)
42.0
41.3
151.0
Average		 32.0
136.0
69.7
602.0
Maximum		 55.5
SO2
(ppb)
1.0
1.0
2.7
1.0
Average		
2.5
4.0
8.7
3.0
Maximum		
(ppb)
NO
3.0
2.0
1.0
0
Average		Maximum		
9.5
6.0
3.3
1.0
NO2
(ppb)
6.0
7.0
5.0
Average		 10.0
21.0
25.0
17.0
Maximum		 26.5
Pollen (/cm2/day)
46
20
165
1
(µg/m3)
Fe
2.4
2.0
7.6
16.7
(µg/m3)
Al
1.6
1.0
9.0
8.3
(µg/m3)
Ca
2.9
2.2
9.1
11.1
(µg/m3)Cd
0.001 > 0.001
0.002 0.002(µg/m3)
Mn
0.037
0.047
0.234
0.718
(µg/m3)Ni
0.004 0.003
0.026
0.036
(µg/m3)Cu
0.006 0.006 0.161
0.043(µg/m3)Cr
0.007 0.005
0.030
0.048
(µg/m3)
Pb
0.003
0.016
0.071
0.064
ADS, Asian Dust Storm; SPM, suspended particulatematter.
Average, average concentration on ADS days; maximum, highest concentration on ADS days.
* Average.

44

Asian dust and asthma

2009 and 1 patient in both 2008 Table 4. Results of the annual telephone surveys
and 2009. Two patients had wors2007
2008
2009
2010
surveysurveysurveysurveyening of lower respiratory tract
symptoms in three surveys (2007, Patients with any symptoms
33 (71.7) 35 (76.1) 31 (67.4) 40 (87.0)
2008, 2009 for 1 patient and 2007, Patients with worsening ofeither symptom
14 (30.4) 12 (26.1) 16 (34.8) 7 (15.2)
2008, 2010 for another). Finally, 2 Patientswith worsening ofpatients noted worsening of their
8 (17.4) 12 (26.1) 5 (10.9)
lower respiratory tract symptom 12 (26.1)
9 (19.6)
7 (15.2) 8 (17.4) 4 (8.7)
Coughlower respiratory tract symptoms
8 (17.4)4 (8.7)8 (17.4) 3 (6.5)
Sputumin all four surveys. Even in the
1 (2.2)1 (2.2)4 (8.7)0 (0)Wheezingsame patient, the influence ofDyspnea
5 (10.9)
5 (10.9) 5 (10.9) 1 (2.2)
ADS on lower respiratory tract Patients with worsening ofupper respiratory tract symptom* 7 (15.2)
7 (15.2) 10 (21.7) 1 (2.2)
symptoms often varied widely.
Sneezing
6 (13.0)
6 (12.8) 7 (15.2) 0 (0)Twenty-six out of the 46 patients2 (4.3)2 (4.3)3 (6.5)
1 (2.2)
Stuffiness
0 (0)1 (2.2)0 (0)0 (0)Itching(56.5%) did not complain of worswith worsening ofening of lower respiratory tract Patients4 (8.7)2 (4.3)9 (19.6) 1 (2.2)
ocular symptom*
symptoms throughout the four
Tearing
1 (2.2)0 (0)0 (0)1 (2.2)Itching
3 (6.5)2 (4.3)9 (19.6) 0 (0)surveys (Table 6), and 22 patientsMucus
1 (2.2)0 (0)1 (2.2)1 (2.2)(47.8%) did not have worsening of
Pain
0 (0)
0 (0)
0 (0)
0 (0)
any symptoms on ADS days.
Patients with worsening of
0 (0)
0 (0)
0 (0)
0 (0)
skin symptom
Multiple logistic regression
Hospitalization foranalysis using the forward selec0 (0)
0 (0)
0 (0)
0 (0)
exacerbation of asthma
tion method and calculation of the( ), %.
likelihood ratio was performed * P < 0.05: the 2 test was used to assess differences among the surveys in theto investigate the association of
frequency of patients with worsening of any symptoms, upper or lower respiratory tract symptoms, ocular symptoms or skin symptoms.
worsening of lower respiratory
tract symptoms with air pollutants,
pollen, metal components and maintenance therapy
Table 5. Patients with worsening of lower respirafor asthma (Table 7). As a result, worsening of tory tract symptoms on ADS days in each survey
lower respiratory tract symptoms was significantly
Numberassociated with the maximum hourly concentration2007 survey
2of NO2 on ADS days and the daily dose of inhaled02008 survey
5
corticosteroids, but not with the levels of SPM, pol- 2009 survey
2
survey2010len, SO2, NO and natural or anthropogenic metal
2007 and 2008 survey
3components.
32007 and 2009 survey
2007 and 2010 survey
2008 and 2009 survey
2008 and 2010 survey
2009 and 2010 survey
2007, 2008 and 2009 survey
2007, 2008 and 2010 survey
2007, 2009 and 2010 survey
2008, 2009 and 2010 survey
2007, 2008, 2009 and 2010 survey

Discussion
The present study showed that the influence of ADS
on lower respiratory tract symptoms, upper respiratory tract symptoms, ocular symptoms and skin
symptoms was often different for each ADS day inpatients with asthma. Only 4% of the patients consistently showed exacerbation of lower respiratory
tract symptoms on every ADS day. Also, 48% of
the patients were completely unaffected by the ADS

0
1
0
0
1
1
0
0
2

ADS, Asian Dust Storm.
Nine patients had worsening of lower respiratory tract symptoms on ADS days in one survey as well as 7 patients in two
surveys, 2 patients in three surveys and 2 patients in all four
surveys.

45

M. Watanabe et al.

Table 6. Patients without worsening of symptoms on ADS days in any survey

and worsening of symptoms was unrelated to the
SPM level, suggesting that other factors may haveaggravated the symptoms of asthma patients in addition to Asian dust.
We previously reported that some asthma
patients had worsening of lower respiratory tract
symptoms on ADS days and that pollen augmented
the influence of ADS on symptoms (Watanabe etal., 2011a, 2011b). Dust from deserts in Mongolia
and northern China has been found to exacerbate
pulmonary and bronchial inflammation in animals(Let et al., 2004; Hiyoshi et al., 2005; Ichinose et al.,2006). However, it was not clear that the worseningof symptoms on ADS days was only due to desert
dust, because the levels of anthropogenic metals(such as Cd, Mn and Ni) and SO2 were significantly
higher on ADS days than non-ADS days in Tottori(Watanabe et al., 2011a, 2011b). It has been reported
that Cd, Mn, Ni and SO2 can induce airway inflammation and/or bronchoconstriction (Lazarus et al.,
1997; Lison et al., 1997; Gavett et al., 2003; Zhang
et al., 2003; Jakubowski et al., 2004; Liu et al.,2009).
Our previous study revealed that the daily PEF
was significantly associated with the SPM level inpatients with worsening of upper and/or lower respiratory tract symptoms during ADS (Watanabe etal., 2011). In contrast, the present study showed thatthe influence of ADS on asthma symptoms varied
even in the same patient. In 2010, the SPM level was
the highest among all four surveys, but the smallest
percentage of patients with exacerbation of lower
respiratory tract symptoms was found in the 2010
survey. It is known that SO2 itself induces airway
inflammation and/or bronchoconstriction (Lazarus
et al., 1997). Therefore, our findings suggest that the

Number (%)
Patients without worsening of
any symptoms		
Patient without worsening oflower respiratory symptoms		

22 (47.8)
26 (56.5)

ADS, Asian Dust Storm.
Four patients did not experience of worsening of lower respiratory tract symptoms, but had worsening of upper respiratory tract symptoms or ocular symptoms.

worsening of lower respiratory tract symptoms during ADS was not only due to desert dust.
According to Hong et al. (2010), exposure tometals bound to dust particles during ADS reduced
the pulmonary function of children, but we could
not find any association between worsening of lower respiratory tract symptoms in asthma patients on
ADS days and the levels of natural and/or anthropogenic metals. In this study, the maximum concentration of NO2 was significantly associated withworsening of lower respiratory tract symptoms according to multiple logistic regression analysis, but
the levels of metals did not show any association.
Many studies have indicated that NO2 is associatedwith airway inflammation and bronchoconstrictionin asthma patients after even short-term exposure(Mann et al., 2010; Di Giampaolo et al., 2011). Accordingly, the deterioration of lower respiratory
tract symptoms during ADS in asthma patients wasprobably not only related to dust, but also to otherair pollutants such as NO2.
The results of our study differed from thoseof Hong et al. (2010) possibly because the levels of
PM and metal components during ADS are lower

Table 7. Adjusted odds ratio for the influence of weather conditions, air pollutants, maintenance treatment on worsening of lower respiratory tract symptoms during ADS (multiple logistic regression
analysis)

NO2 (maximum)
Daily dosage of inhaled corticosteroids

Partial regression
coefficient

Odds
ratio

95%
confidence interval

P value

0.135
0.801

1.15
2.23

1.008–1.248
1.252–3.969< 0.05< 0.01

ADS, Asian Dust Storm.
NO2 (maximum) is the maximum hourly concentration of NO2 on ADS days.

46

Asian dust and asthma

veys, even in the same patient. The reason for thisfinding may be differences in the levels of natural or
anthropogenic metals air pollutants, and pollen oneach ADS day. The level of NO2 was significantly
associated with the exacerbation of lower respiratory tract symptoms during ADS, and the dust storms
had more influence on symptoms in patients using
higher daily doses of inhaled corticosteroids whose
asthma may have been poorly controlled. The desert dust itself may influence airway inflammationin Japanese asthma patients, but further studies areneeded to define the role of other air pollutants andmaterials bound to the dust such as natural and anthropogenic metals.

in Tottori than in Korea. However, the most important difference may be related to the age of thesubjects. Some studies reported an increased risk of
hospitalization during ADS in children with asthma(Kanatani et al., 2010; Ueda et al., 2010), so the
influence of ADS or other air pollutants may differ
between adults and children. According to Devalia
et al. (1994), exposure to a combination of SO2 andNO2 enhances the airway response to inhaled allergens compared with the effect of SO2 or NO2 alone
in patients with asthma. Thus, allergens may induce
bronchoconstriction more easily on ADS days thannon-ADS days, because SO2 levels were significantly higher on ADS days than non-ADS days in
Tottori (Watanabe et al., 2011b).
A higher daily dosage of inhaled corticosteroids was also a risk factor for deterioration of lower
respiratory tract symptoms during ADS. If patientsneed high doses of inhaled corticosteroids to control
asthma, their airway inflammation may not be fully
suppressed even though they were classified as having moderate asthma. This means that desert dust
and/or air pollutants could readily induce bronchoconstriction and aggravate airway inflammation inpatients on high-dose inhaled corticosteroids.
In this study, 22 of the 46 patients (47.8%) also
had allergic rhinitis and 3 of the 46 patients (6.5%)
had non-allergic rhinitis. However, the ratio of useof antihistamines was below 18%, and that of nasal
corticosteroids were below 22% through the four
surveys. Especially in 2007 and 2008, the numberof patients using intranasal steroids was 0 and 1, respectively. Thus, the asthma patients with rhinitis in
this study may have had poorly controlled rhinitis,
although leukotriene receptor antagonists were usedby 39.1% to 47.8%. In patients with rhinitis, dry airand PM can easily reach the lower airways, because
the ability of the nasal passages to warm and humidify air is impaired (Ingelstedt and Ivstam, 1951;
Togias, 2003). To prevent the exacerbation of lower
respiratory tract symptoms on ADS days in asthma
patients using high-dose inhaled corticosteroids,
treatment of upper airway conditions may be more
beneficial than more intensive therapy for asthma.
In conclusion, the influence of ADS on thesymptoms of asthma patients differed between sur-Acknowledgments: Conception and design, MW, JK, ES;analysis and interpretation, MW, TI; drafting the manuscript for important intellectual content, MW, TI, NB, ES.
This research was supported by the Environment Research and Technology Development Fund (C-1154) of theJapanese Ministry of the Environment.
Reference
1 Choi JC, Lee M, Chun Y, Kin J, Oh S. Chemical composition and source signature of spring aerosol in Seoul,
Korea. J Geophys Res 2001;106:18067–18074.
2 Devalia JL, Rusznak C, Herdman MJ, Trigg CJ, Tarraf
H, Davies RJ. Effect of nitrogen dioxide and sulphur
dioxide on airway response of mild asthmatic patients toallergen inhalation. Lancet 1994;344:1668–1671.
3 Di Giampaolo L, Quecchia C, Schiavone C, Cavallucci
E, Renzetti A, Braga M, et al. Environmental pollution
and asthma. Int J Immunopathol Pharmacol. 2011;24(1Suppl):31S–38S.
4 Duce RA, Unni CK, Ray BJ, Prospero JM, Merrill JT.
Long-range atmospheric transport of soil dust from Asia
to the tropical north pacific: temporal variability. Science 1980;209:1522–1524.
5 Gavett SH, Haykal-Coates N, Copeland LB, HeinrichJ, Gilmour MI. Metal composition of ambient PM2.5
influences severity of allergic airways disease in mice.
Environ Health Perspect 2003;111:1471–1477.
6 Global Initiative for Asthma (GINA). Global strategy forasthma management and prevention: NIH Publication No.
02-3629. Bethesda: National Institutes of Health, National
Heart, Lung, and Blood Institute; 1995 (update 2002).
7 Han YJ, Holsen TM, Hopke PK, Cheong JP, Kim H, Yi
SM. Identification of source locations for atmospheric
dry deposition of heavy metals during yellow-sandevents in Seoul, Korea in 1998 using hybrid receptor
models. Atmos Environ 2004;38:5353–5361.
8 Hiyoshi K, Ichinose T, Sadakane K, Takano H,

47

M. Watanabe et al.

Nishikawa M, Mori I, et al. Asian sand dust enhances
ovalbumin-induced eosinophil recruitment in the alveoli
and airway of mice. Environ Res 2005;99:361–368.
9 Hong YC, Pan XC, Kim SY, Park K, Park EJ, Jin X, etal. Asian Dust Storm and pulmonary function of school
children in Seoul. Sci Total Environ 2010;408:754-759.
10 Ichinose T, Sadakane K, Takano H, Yanagisawa R,
Nishikawa M, Mori I, et al. Enhancement of mite allergen-induced eosinophil infiltration in the murine airway
and local cytokine/chemokine expression by Asian sanddust. J Toxicol Environ Health A 2006;69:1571–1585.
11 Ingelstedt S, Ivstam B. Study in the humidifying capacity of the nose. Acta Otolaryngol 1951;39:286–290.
12 Jakubowski M, Abramowska-Guzik A, Szymczak W,
Trzcinka-Ochocka M. Influence of long-term occupational exposure to cadmium on lung function tests results. Int J Occup Med Environ Health 2004;17:361–368.
13 Kanatani KT, Ito I, Al-Delaimy WK, Adachi Y,
Mathews WC, Ramsdell JW; Toyama Asian Desert
Dust and Asthma Study Team. Desert dust exposure isassociated with increased risk of asthma hospitalizationin children. Am J Respir Crit Care Med 2010;182:1475–
1481.
14 Kwon HJ, Cho SH, Chun Y, Lagarde F, Pershagen G.
Effects of the Asian dust events on daily mortality inSeoul, Korea. Environ Res 2002;90:1–5.
15 Lazarus SC, Wong HH, Watts MJ, Boushey HA, Lavins
BJ, Minkwitz MC. The leukotriene receptor antagonist
zafirlukast inhibits sulfur dioxide-induced bronchoconstriction in patients with asthma. Am J Respir Crit Care
Med 1997;156:1725–1730.
16 Lei YC, Chan CC, Wang PY, Lee CT, Cheng TJ. Effectsof Asian dust event particles on inflammation markers
in peripheral blood and bronchoalveolar lavage in pulmonary hypertensive rats. Environ Res 2004;95:71–76.
17 Lison D, Lardot C, Huaux F, Zanetti G, Fubini B. Influence of particle surface area on the toxicity of insoluble
manganese dioxide dusts. Arch Toxicol 1997;71:725–
729.
18 Liu L, Poon R, Chen L, Frescura AM, Montuschi P,
Ciabattoni G, et al. Acute effects of air pollution on pulmonary function, airway inflammation, and oxidative
stress in asthmatic children. Environ Health Perspect
2009;117:668–74.

19 Mann JK, Balmes JR, Bruckner TA, Mortimer KM,
Margolis HG, Pratt B, et al. Short-term effects of air
pollution on wheeze in asthmatic children in Fresno,
California. Environ Health Perspect 2010;118:1497–
1502.
20 Mori I, Nishikawa M, Tanimura T, Quan H. Change
in size distribution and chemical composition of Kosa
(Asian dust) aerosol during long-range transport. Atmos
Environ 2003;37:4253–4263.
21 Ohta K, Yamaguchi M, Akiyama K, Adachi M,
Ichinose M, Takahashi K, et al. Japanese guideline for
adult asthma. Allergol Int 2011;60:115–145.
22 Schatz M, Dombrowski MP, Wise R, Thom EA,
Landon M, Mabie W, et al. Asthma morbidity during
pregnancy can be predicted by severity classification. J
Allergy Clin Immunol 2003;112:283–288.
23 Taylor DA. Dust in the wind. Environ Health Perspect
2002;110:A80–A87.
24 Togias A. Rhinitis and asthma: evidence for respiratory system integration. J Allergy Clin Immunol
2003;111:1171–1183.
25 Ueda K, Nitta H, Odajima H. The effects of weather, air
pollutants, and Asian dust on hospitalization for asthma
in Fukuoka. Environ Health Prev Med 2010;15:350–357.
26 Watanabe M, Yamasaki A, Burioka N, Kurai J, Yoneda
K, Yoshida A, et al. Correlation between Asian dust
storms and worsening asthma in Western Japan. Allergol Int 2011a;60:267–275.
27 Watanabe M, Igishi T, Burioka N, Yamasaki A, Kurai J,
Takeuchi H, et al. Pollen augments the influence of desert dust on symptoms of adult asthma patients. Allergol
Int 2011b;60:517–524.
28 Yoo Y, Choung JT, Yu J, Kim do K, Koh YY. Acute effects of Asian dust events on respiratory symptoms andpeak expiratory flow in children with mild asthma. J
Korean Med Sci 2008;23:66–71.
29 Zhang Q, Kusaka Y, Zhu X, Sato K, Mo Y, Kluz T, etal. Comparative toxicity of standard nickel and ultrafine
nickel in lung after intratracheal instillation. J Occup
Health 2003;45:23–30.
Received May 11, 2012; accepted May 16, 2012
Corresponding author: Masanari Watanabe, MD

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