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Sensitization and exposure to house dust and

storage mites in high-altitude areas of Ecuador


Rommel Valdivieso, MD*; Victor Iraola, PhD; Monica Estupinan, MD*; and
Enrique Fernandez-Caldas, PhD

Background: Few studies have addressed exposure and sensitization to mite allergens in Andean countries.
Objectives: To identify the main mite species in 3 locations at different altitudes in Ecuador and to verify skin test reactivity
to various mite species in allergic individuals in Quito, Ecuador.
Methods: Mattress dust samples were collected in Quito (2,800 m above sea level), Cuenca (2,500 m above sea level), and
Guayaquil (sea level). Mite species present in the samples were isolated, identified, and counted. Der p 1 and Der f 1 levels were
measured using monoclonal antibody based enzyme immunoassays. Four hundred thirty-five patients in Quito diagnosed as
having allergic rhinitis or asthma underwent skin testing with commercial extracts of Dermatophagoides pteronyssinus,
Dermatophagoides farinae, Blomia tropicalis, Tyrophagus putrescentiae, and Lepidoglyphus destructor. In addition, Glycyphagus domesticus, Acarus siro, and Aleuroglyphus ovatus were tested in 362, 262, and 279 patients, respectively.
Results: Twenty-one mite species were identified. Large populations of mites were detected above 2,500 m of altitude. All
the dust samples contained detectable levels of Der p 1 or Der f 1. Positive skin prick test reactions to D pteronyssinus, D farinae,
B tropicalis, L destructor, T putrescentiae, A ovatus, A siro, and G domesticus were obtained in 60.9%, 56.8%, 17.0%, 19.3%,
10.6%, 15.8%, 8.8%, and 11.0% of the patients, respectively.
Conclusions: Most analyzed mattresses contained several species of mites. Mite allergen levels were high. This study confirms
the importance of house dust and storage mite allergens in Ecuador in areas above 2,500 m of altitude, where humidity remains
high year round.
Ann Allergy Asthma Immunol. 2006;97:532538.

INTRODUCTION
The importance of house dust mites in respiratory allergic
diseases has been recognized since 1964. Multiple studies,
conducted worldwide, have shown strong associations between exposure to mites, sensitization, and exacerbation of
allergic respiratory diseases.1 House dust mites are considered ubiquitous arthropods, although studies conducted in the
Alps in Europe have shown a scarce presence of these arthropods above 1,000 m of altitude2; no mites have been
found in this region above 1,600 m above sea level
(m.a.s.l.).3,4 Similar findings have been reported in the Rocky
Mountains.5 In a study6 conducted in 10 neighboring states of
the Rocky Mountains, no mites were found in 48 of 55
homes. The presence of large quantities of mites in 2 homes
was associated with the use of humidifiers. The scarce presence of mites in Europe and the United States above a certain
altitude is in contrast with reports for high-altitude areas of
some South American countries, especially in the Andes,
including Colombia,713 Peru,14 and Venezuela.15 This discrepancy in the prevalence of mites among high-altitude areas
in Europe, North America, and Andean regions could be
explained by climatic differences, especially by the ambient

* Centro de Alergia y Dermatologa, Centro Medico Meditropoli, Quito,


Ecuador.
Laboratorios LETI, SL, Tres Cantos Madrid, Spain.
Received for publication December 13, 2005.
Accepted for publication in revised form March 12, 2006.

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humidity. Cities and villages in Andean countries in which


mite surveys have been conducted are close to the equator, in
the tropics. These cities have a moderate year-round temperature, high humidity, and abundant rainfall. These characteristics, which are good for the growth of mites, are not encountered in the Rockies in North America or in the Alps in
Europe. Other characteristics, such as the reduced use of
heating and cooling systems and the absence of extreme
temperatures in the winter and summer, have a positive effect
on mite growth.
Sensitization to mites is common in Latin American countries, as shown in numerous publications. A multinational
study16 conducted in Argentina, Brazil, Colombia, Mexico,
and Venezuela analyzed skin test reactivity to 6 different mite
species. Overall, skin test reactivity among asthmatic patients
ranged from 93.7% to Blomia tropicalis in Sao Paulo, Brazil,
to 30.0% to Lepidoglyphus destructor in Mexico City, Mexico.16 Skin test reactivity to Dermatophagoides pteronyssinus
ranged from 91.2% in Sao Paulo to 60.7% in Cartagena,
Colombia. Other studies conducted in Argentina,17 Brazil,18
Colombia,19,20 Mexico,21,22 Venezuela,15,23 and Guatemala24
have shown similar results.
To our knowledge, no studies have been conducted in
Ecuador to identify the domestic mite fauna, although previous studies25 in Quito (2,800 m.a.s.l.) suggested that D pteronyssinus and Dermatophagoides farinae are important sensitizing agents in patients with allergic rhinoconjunctivitis and
bronchial asthma. Its significance is greater than that of

ANNALS OF ALLERGY, ASTHMA & IMMUNOLOGY

Table 1. Characteristics of the Houses and Mattresses in the 3 Main Cities in Ecuador in Which Dust Samples Were Collected
City
Quito
Guayaquil
Cuenca

Samples,
No.

Signs of
humidity,
%

Carpet in
bedroom,
%

Age of
mattresses,
y

Spring

Foam

20
23
24

25
13
8

40
65
4

7.7
6.9
6.0

90
83
70

10
17
30

pollens and other allergens.26 The objectives of this study


were to identify the mite fauna in house dust samples collected in different cities and at different altitudes in Ecuador
and to determine the rate of sensitization to house dust and
storage mites in allergic patients in Quito.
MATERIALS AND METHODS
Collection of Dust Samples, Identification of Mite Species,
and Determination of Allergen Levels
To verify the presence of house dust mites, we conducted a
random mite survey in mattresses in the 3 main cities in
Ecuador. A total of 67 mattress dust samples were collected
during 2003: 20 samples were collected during August in
Quito (2,800 m.a.s.l.; mean relative humidity, 62%; mean
temperature, 17.3C), 23 samples during November in
Cuenca (2,500 m.a.s.l.; mean relative humidity, 66%; mean
temperature, 16C), and 24 during October in Guayaquil (5
m.a.s.l.; mean relative humidity, 71.5%; mean temperature,
24C). The characteristics of the houses and mattresses are
given in Table 1. All the dust samples were collected from the
entire surface of the mattress during 2 minutes in the homes
of 10 allergic and 57 nonallergic volunteers by the same
trained technician using a 1.4-kW portable vacuum cleaner
(Trio 2; Electrolux do Brasil SA, Curitiba, Brazil) and the
Mitest Dust Collector (Indoor Biotechnologies Inc, Charlottesville, VA). All the samples were frozen for at least 48
hours to avoid mite proliferation.
Dust samples were weighed and recorded. Twenty-milligram aliquots were suspended in saturated saline solution and
analyzed using a stereoscope following previously described
methods.27 All the mites in each sample were collected using
a fine needle and were placed in 2 drops of Hoyer medium on
a microscope slide. The slide was then covered and allowed
to dry at 50C for 24 hours. Slides were inspected using a

Mattress type, %

microscope, and mite species were identified following specialized keys28 and counted. Der p 1 and Der f 1 levels were
quantified using an enzyme-linked immunosorbent assay
technique following the instructions of the manufacturer (Indoor Biotechnologies Inc). The results are expressed in micrograms of allergen per gram of dust.
Patient Population
The prevalence of sensitization to house dust and storage
mites was evaluated in 435 consecutive patients (53.6%
males and 46.4% females; mean age, 16.2 years; age range,
1 80 years) in Quito who were diagnosed as having allergic
respiratory diseases: 7.6% had asthma only, 67.1% had rhinoconjunctivitis only, and 25.3% had allergic asthma and
rhinoconjunctivitis. The diagnosis of allergic rhinitis was
established following recent guidelines.29 The diagnosis of
asthma was made according to Global Initiative for Asthma
recommendations. Patients with symptoms such as cough,
episodic breathlessness, wheezing, and chest tightness who
had at least a 12% improvement in forced expiratory volume
in 1 second after inhalation of a bronchodilator (1 mg of
terbutaline turbuhaler) were diagnosed as having asthma
(http://www.ginasthma.org). Patients were divided into 5
groups according to age: 1 to 5 years, 6 to 11 years, 12 to 19
years, 20 to 39 years, and 40 years and older. The characteristics of each age group are given in Table 2.
Skin Tests
Skin tests were conducted on the volar surface of the forearms using a sterile lancet (Laboratorios LETI, SL) and a
standard battery of skin tests, including standardized extracts
of the following mite species: D pteronyssinus, D farinae, B
tropicalis, L destructor, Tyrophagus putrescentiae (435 patients for all), Glycyphagus domesticus (362 patients), Acarus
siro (262 patients), and Aleuroglyphus ovatus (279 patients)

Table 2. Characteristics of the Patient Population According to Age Groups


Sex, %
Age
group, y
15
611
1219
2039
40
Total

Diagnosis, %

Patients,
No.

Asthma

Rhinitis

Asthma and
rhinitis

126
110
73
91
35
435

56.3
62.7
46.6
50.5
37.1
53.6

43.7
37.3
53.4
49.5
63.9
46.4

7.9
5.5
8.2
5.5
17.1
7.6

69.8
65.5
64.4
70.3
60.0
67.1

22.2
29.5
27.4
24.2
22.9
25.3

VOLUME 97, OCTOBER, 2006

533

Table 3. Presence and Abundance of Mite Species in 67 Dust Samples Collected in the 3 Main Cities in Ecuador
% positive samples; GM mites/g
Mite species*
Total
Dermatophagoides pteronyssinus
Dermatophagoides farinae
Euroglyphus maynei
Blomia tropicalis
Blomia kulagini
Blomia tjibodas
Lepidoglyphus destructor
Glycyphagus privatus
Chortoglyphus. arcuatus
Tyrophagus putrescentiae
Suidasia medanensis
Histiostoma feroniarum
Lynxacarus radovsky
Cheyletus species
Tarsonemus species

Quito

Cuenca

Guayaquil

100; 840.4
95; 715.1
15; 696.2
20; 259.7
30; 107
5; 250
0
15; 126
5; 50
5; 300
10; 86.6
0
0
0
50; 79.9
15; 50

95.7; 894.7
95.7; 686.2
17.4; 305.8
30.4; 185.4
8.7; 50
8.7; 1,431.8
4.3; 1,250
17.4; 206
0
8.7; 50
0
0
4.3; 50
0
21.7; 223.9
21.7; 90.1

100; 4,586.3
100; 1,119.7
64; 1,100.9
28; 1,582.6
76; 1,266
12; 540
0
8; 86.6
0
0
8; 50
12; 135.7
0
4; 300
72; 175.3
4; 150

* Mites of the families Tydeidae, Tetranychidae, Tenuipalpidae, Stigmaeidae, Oribatida, and Mesostigmata were also identified.
GM mites/g indicates the geometric mean number of mites per gram of mattress dust.

(Laboratorios LETI, SL). Allergen extracts were standardized


in histamine equivalent in prick test units following the rules
of the Nordic Council on Medicines.30 Other test allergens
included cockroach mix, Cypress, Eucalyptus, grasses, dog
and cat dander, weeds, feathers, and molds. Skin prick tests
were performed according to international recommendations,
and the reactions were read after 15 minutes.31 Reactions of 3
mm or greater were considered positive. Histamine hydrochloride, 10 mg/mL, and a glycerinated saline solution were
used as positive and negative controls, respectively.
Statistical Analysis
The statistical analyses of the results, including descriptive
statistics and parametric and nonparametric methods, were
performed using a computer program (StatView version 4.53;
Abacus Concept Inc, Berkeley, CA).
RESULTS
Frequency and Abundance of House Dust and Storage
Mite Species in 3 Cities in Ecuador
The frequency and abundance of mite species are given in
Table 3. Twenty-one mite species were identified in the
survey. In all 3 cities, members of the families Pyroglyhidae

(D pteronyssinus, D farinae, and Euroglyphus maynei), Glycyphagidae (L destructor), Echimyopodidae (B tropicalis and
Blomia kulagini), Cheyletidae (Cheyletus species), and Tarsonemidae (Tarsonemus species) were identified. The largest
mite population was detected in Guayaquil (geometric mean:
4,586.3 mites/g of dust), being significantly greater than the
counts detected in Quito (840.4/g) and Cuenca (894.7/g) (P
.001). The samples in Guayaquil contained larger quantities
(P .001) and more frequently D farinae and B tropicalis
than samples in Quito and Cuenca. No significant differences
were detected in the mite fauna in Quito and Cuenca.
Risk Factors Associated With Larger Mite Populations
Several risk factors were associated with a greater presence of
mites. The presence of obvious signs of humidity in the house
was correlated with higher levels of B tropicalis and L destructor (P .001) in Cuenca. The age of the mattress was
also positively correlated with greater numbers of D farinae
in Cuenca and of B tropicalis in Guayaquil (P .03). The
other analyzed variables, including type of mattress, the presence of carpet in the bedroom, the area of the city in which
the samples were collected, and the age of the owners of the
mattress, did not show any significant correlations.

Table 4. Der p 1 and Der f 1 Levels in 67 Dust Samples and the Percentage of Homes With Levels Greater Than 2 and 10 g/g of Dust
Der p 1

534

Der f 1

City

Geometric
mean, g/g
of dust

>2 g/
g, %

>10 g/
g, %

Geometric
mean, g/g of
dust

>2 g/g,
%

>10 g/g,
%

Quito
Cuenca
Guayaquil

9.7
13.6
8.3

93.8
96.6
80.0

43.8
65.2
76.0

5.5
1.7
12.7

18.8
8.7
52.0

12.5
4.3
48.0

ANNALS OF ALLERGY, ASTHMA & IMMUNOLOGY

* Statistically significant differences (P .05) compared with the age group with the lowest values for skin test for each mite species by age.
The lowest values for percentage of sensitization and mean wheal sizes for each mite species.

6; 4.0 0.7 (n 83)


19.1; 4.3 1.8* (n 68)
30.6*; 4.4 2.8* (n 49)
11.0; 5.1 1.7 (n 57)
4.5; 6 (n 22)
15.8; 4.5 2.0
1.4; 3.0 (n 72)
8.1; 3.7 0.5 (n 74)
19.6*; 4.6 1.6* (n 46)
6.6*; 4.5 1* (n 49)
4.8; 4 (n 21)
8.8; 4.2 1.2
7.9; 3.8 1.0
10.0; 4.1 2.4
19.2; 4.4 1.2*
9.9; 4.8 1.1
5.7; 4.5 0.7
10.6; 4.3 1.5
1.9; 3.5 0.7 (n 104)
8.9; 3.9 1.2* (n 90)
27.4*; 4.1 1.3* (n 62)
9.9*; 4.7 1.0* (n 75)
12.9*; 4.5 0.6* (n 31)
11.0; 4.2 1.2
15 (n 126)
611 (n 110)
1219 (n 73)
2039 (n 91)
40 (n 35)
Total

51.6*; 7.2 3.2*


74.5*; 8.7 4.1*
82.2*; 9.8 4.5*
56.0*; 7.7 4.3*
20.0; 6.0 1.7
60.9; 8.3 4.1

43.7*; 6.2 2.3*


72.7*; 6.4 2.6*
75.3*; 7.9 3.3*
53.8*; 6.6 2.8*
22.9; 5 1.5
56.8; 6.7 2.8

9.5; 4.3 1.4


25.5*; 6 2.5*
26*; 6.5 3*
22*; 5.3 2*
14.3; 7.2 4.5
19.3; 5.8 2.6

5.6; 4.0 1.2


24.5*; 5 1.6*
31.5*; 4.9 2.0*
15.4*; 5.2 1.2*
8.6; 8.7 5.5
17.0; 5.1 2.0

Aleuroglyphus
ovatus
Acarus
siro
Tyrophagus
putrescentiae
Blomia
tropicalis
Glycyphagus
domesticus

Sensitization, %; wheal size, mean SD, mm

Lepidoglyphus
destructor
Dermatophagoides Dermatophagoides
pteronyssinus
farinae
Age
group, y

Table 5. Sensitization to All Mite Species, Wheal Size by Age Group, and Number of Patients Tested

VOLUME 97, OCTOBER, 2006

Figure 1. Percentage of patients sensitized to a variable number of mite


species in Quito, Ecuador. Five different age groups were analyzed: 1 to 5
years, 6 to 11 years, 12 to 19 years, 20 to 39 years, and 40 years and older.

Der p 1 and Der f 1 Allergen Levels in Dust Samples


Der p 1 and Der f 1 levels are given in Table 4. All the dust
samples contained detectable amounts of Der p 1 or Der f 1.
No significant differences were detected in Der p 1 levels in
the dust samples collected in the 3 cities and in the percentage
of homes with more than 2 and 10 g/g. However, in Guayaquil, the number of mattresses with more than 2 and 10 g/g
of Der f 1 was greater than in Cuenca (P .002) and Quito
(P .01). Der f 1 levels in Guayaquil were significantly
greater than those in Cuenca (P .005).
Skin Test Results
Of 435 patients who underwent skin testing with a battery of
mite extracts, 144 (33.1%) had negative reactions to mites
and 291 (66.9%) had positive reactions to at least 1 mite
species. The sensitization rates to all the species and the
respective mean wheal sizes are given in Table 5. Overall,
60.9% of the patients were positive to D pteronyssinus,
56.8% to D farinae, 19.3% to L destructor, and 17.0% to B
tropicalis. The greatest wheal sizes were also recorded for
these species. Twenty-three individuals (5.3%) were exclusively sensitized to D pteronyssinus, 10 (2.3%) to D farinae,
1 (0.2%) to L destructor, 2 (0.5%) to G domesticus, 3 (0.7%)
to T putrescentiae, 1 (0.2%) to A siro, and 1 (0.2%) to A
ovatus. Patients with asthma and rhinoconjunctivitis have a
significantly (P .05) higher prevalence of sensitization and
a bigger wheal size than patients with rhinitis only to D
pteronyssinus, D farinae, L destructor, B tropicalis, and T
putrescentiae.
Table 5 also provides the results according to age groups.
In all cases, the greatest prevalence of positive skin test
results was recorded in the group aged 12 to 19 years. In all
the age groups, the highest prevalence of positive skin test
results corresponded to Dermatophagoides species. For most

535

storage mites, excluding A siro, the largest mean skin test


reactions were obtained in patients older than 19 years. We
also analyzed in each age group the percentage of patients
sensitized to a variable number of mite species (Fig 1). In
total, 27.5% of the patients were sensitized to 2 mite species,
mainly D pteronyssinus and D farinae. The greatest prevalence of sensitization to these 2 species was detected in the
age groups younger than 40 years.
DISCUSSION
In the present study, we described, for the first time, the mite
fauna present in mattress dust samples in Ecuador. We also
analyzed skin test reactivity to different mite species in a
large group of patients in Quito, which is located at 2,800
m.a.s.l. Previous studies25,26 had suggested the importance of
Dermatophagoides species but without any scientific evidence that these species were present in house dust. In the
present study, we confirmed a high prevalence of skin test
reactivity to Dermatophagoides species in patients in all age
groups. These results were corroborated by the high prevalence of these 2 species in mattress dust, especially of D
pteronyssinus in Quito and of D farinae in Guayaquil. Exposure to more than 2 g of group 1 allergens (Der p 1 Der
f 1) per gram of dust of the Dermatophagoides species is
considered a risk factor for mite allergic sensitization; more
than 10 g represents a greater risk for sensitization and
asthma. In this study, 63.6% of the mattresses in Quito had
more than 10 g of group 1 (65.2% in Cuenca and 72.0% in
Guayaquil). Although skin tests were not conducted in
Guayaquil, we would expect a slightly greater prevalence of
sensitization to mites there than in the 2 other cities because
of the high levels of mites encountered. In Quito, the prevalence of sensitization to D pteronyssinus was 60.9%, which is
similar to the percentage of homes with more than 10 g of
group 1 per gram of dust. In general, the percentage of
mattresses with more than 10 g of group 1 per gram of dust
in Ecuador can be considered very high and significantly
greater than in the United States.32
We confirmed that the prevalence of sensitization to Dermatophagoides species depends on the age of the individual
in Ecuador. Comparing data from the age groups 1 to 5 years,
6 to 11 years, and 12 to 19 years, we detected a steady
increase in the percentage of sensitized individuals and in the
size of the skin test reactions. The highest prevalence and the
largest wheal sizes were detected in the group aged 12 to 19
years. Afterward, there was a decline in the prevalence and in
the size of the reactions, reaching the smallest values in the
group older than 40 years.
The prevalence of sensitization to other mite species was
analyzed to investigate whether these newly described species could play a role in allergic sensitization in people with
allergic respiratory diseases in Quito. The percentages of
positive skin prick test reactions to L destructor and B tropicalis were lower than those described in other Andean cities,
such as Bogota, Colombia,16 which is situated at 2,640

536

m.a.s.l., and similar to those described in allergic children in


Mexico City22 (2,240 m.a.s.l.). The highest prevalence of
sensitization to storage mites was also detected in the group
aged 12 to 19 years. For G domesticus, B tropicalis, L
destructor, and A siro, the lowest rates of sensitization were
detected in the group aged 1 to 5 years, whereas for A ovatus
and T putrescentiae it was detected in patients older than 40
years. In contrast to D pteronyssinus and D farinae, the mean
size of the skin test reaction to all storage mite species was
greater in patients older than 20 years, except for the storage
mite A siro. Although the reason for this finding remains
unknown, it is possible that sensitization to storage mites
requires longer periods of exposure than to the Dermatophagoides species. Another explanation could be the greater
presence of Dermatophagoides species in mattress dust.
Cross-reactivity is a common feature among mite allergens, especially in those from taxonomically related species.
Whereas the allergenicity of the house dust mites D pteronyssinus, D farinae, and E maynei is well documented, the
extent to which their allergens are unique or cross-react with
other mite allergens has not been completely delineated.
Euroglyphus maynei, D pteronyssinus, and D farinae show
significant allergenic cross-reactivity. In vitro cross-reactivity
studies33 between Dermatophagoides species and extracts of
other mite species have demonstrated that, in general, mites
share common and species-specific allergens.
In the present study, we identified several mite species in
mattresses in cities situated at 2,500 m.a.s.l. and high levels
of Der p 1 and Der f 1. In most cases, allergen levels and mite
counts exceeded the concentrations that have been proposed
for sensitization and respiratory symptoms.34 A total of 21
different mite species were identified, with a geometric mean
of greater than 800 mites per gram in Quito and Cuenca and
greater than 4,500 per gram in the coastal city of Guayaquil.
The numbers and species of domestic mites in this coastal
city are similar to the results obtained in coastal cities in
Venezuela35 and approximately 5 times greater than those in
Quito and Cuenca. The domestic mite fauna in Quito and
Cuenca is similar to that in other Andean cities in Colombia
or Peru, except for the presence and abundance of B tropicalis. Overall, the main identified species were D pteronyssinus, D farinae, E maynei, and B tropicalis, which is similar
to what has been described in the United States.36 Blomia
tropicalis was present in 30% of the samples collected in
Quito. Up to now, B tropicalis had been described in relatively large quantities only in low-altitude and high-humidity
areas.37 The fact that we identified 17% of individuals sensitized to B tropicalis in Quito is in agreement with the relatively frequent presence of this mite species in mattress dust.
Similar results were obtained for L destructor and T putrescentiae, suggesting that these species could have clinical
significance in Ecuador.
This study, and those previously mentioned, support the
idea that altitude is not the major determinant regarding the
abundance or even presence of house dust mites in the tropics. Other climatic conditions that play a role are temperature

ANNALS OF ALLERGY, ASTHMA & IMMUNOLOGY

and humidity, which regulate reproduction and growth in dust


mites. Therefore, at these altitudes, with high absolute humidity values, mites may play an important role in the pathogenesis of allergic respiratory diseases in cities at 2,000 to
3,000 m of altitude in South America. More studies are
needed in cities located above 3,000 m, where the climatic
conditions may vary significantly.
In conclusion, we identified a rich domestic mite fauna in
3 different locations in Ecuador and verified that some of
these species may play a role in allergic respiratory diseases.
These results suggest that in addition to the Dermatophagoides species, species such as E maynei, B tropicalis, L
destructor, and T putrescentiae should be included in the
standard battery of skin tests owing to their common presence
in house dust and the prevalence of positive skin test reactions.

16.

17.

18.
19.

20.

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Requests for reprints should be addressed to:


Rommel Valdivieso, MD
Av. Mariana de Jesus y Occidental
Centro Medico Meditropoli
Consultorio 113
Quito, Ecuador
E-mail: rommelva@andinanet.net

ANNALS OF ALLERGY, ASTHMA & IMMUNOLOGY

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