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(Chest. 2002;121:347-353.)
© 2002 American College of Chest Physicians

Levels of House Dust Mite-Specific IgE and Cockroach-Specific IgE and Their Association With Lower Pulmonary Function in Taiwanese Children*

Ying-Chu Lin, MSc; Huey-Jen Su, ScD; Tzuen-Ren Hsiue, MD; Cheng-Hung Lee, MD; Chang-Wen Chen, MD and Yueliang Leon Guo, MD, PhD

* From the Department of Environmental and Occupational Health (Mr. Lin, and Drs. Su and Guo), and the Division of Chest Medicine, Department of Internal Medicine (Drs. Hsiue, Lee, and Chen), National Cheng Kung University Hospital, Tainan, Taiwan.

Correspondence to: Yueliang Leon Guo, MD, PhD, Department of Environmental and Occupational Health, National Cheng Kung University, 138 Sheng-Li Road, Tainan, Taiwan 704; e-mail: leonguo{at}mail.ncku.edu.tw


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: Sensitization to an aeroallergen is known to diminish pulmonary function in young children and adults; however, it remains unclear whether it produces similar effects in adolescents. This study, therefore, examined the relationship between serum allergen-specific IgE levels and pulmonary function in adolescents.

Design: Middle-school children were invited for a physician’s evaluation and pulmonary function test when not experiencing an asthma attack and for the determination of serum levels of specific IgE to common allergens.

Setting: National Cheng Kung University Hospital, Taiwan.

Subjects: Middle-school children in southern Taiwan, who had completed both a nationally administered Chinese version of the International Study of Asthma and Allergies in Childhood questionnaire and a pulmonary function test in October 1996.

Results: Forty-two then currently asthmatic children, 38 children with asthma in remission (no reported attack for > 12 months), and 69 children without asthma completed the study. Children with asthma had a significantly lower adjusted forced expiratory flow between 25% and 75% of FVC (FEF25–75%) and FEV1/FVC than children without asthma. A greater percentage of children with asthma were more sensitized to Dermatophagoides pteronyssinus (Der p), Dermatophagoides farinae (Der f), and German cockroach but not cat dander or dog dander. Children with asthma with Der f-specific IgE > 100 IU/mL, or cockroach-specific IgE > 0.7 IU/mL showed lower pulmonary function. No such association was found in children without asthma.

Conclusion: Our findings suggest that sensitization to Der f and German cockroach was a critical factor for the lower pulmonary function observed in middle-school children with asthma.

Key Words: asthma • cockroach • dust mite • pulmonary function • radioallergosorbent test • sensitization


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
In adults, FEV1 declines with an increase in age.1 One longitudinal study with a 15-year follow-up showed that greater reduction in lung function was found in people with asthma than in people without asthma.2 In children, those who had wheezing attacks between 1 years and 6 years of age were found to have lower FEV1 despite showing healthy lung function at 1 year of age.3 Although reduced lung function is the key phenomenon presented by a person with asthma during an attack,4 5 the degree of reduction is less obvious in an adolescent with asthma who is not having an attack.

Several reports6 7 8 9 10 have also suggested that sensitization to aeroallergens, including house dust, pollen, house dust mites, and cat and dog dander, is associated with diminished lung function in adults, particularly for people with asthma >= 60 years old; however, this is not true for sensitization to grass. In addition, a study in the United States reported that sensitization to dust mites, dog dander, and oak among children with asthma 6 to 12 years old was associated with reduced FEV1.11 A study in Australia demonstrated that an increased serum level of IgE against Aspergillus fumigatus was a significant risk factor for lower FEV1 and forced expiratory flow between 25% and 75% of FVC (FEF25–75%).12

Although an association between aeroallergens and reduced lung function has been demonstrated in several studies, it remains unclear what corresponding levels of serum IgE to allergen exposures could have induced the observed difference in lung function. The present study was conducted: (1) to measure the levels of specific IgE to house dust mites, German cockroach, and dog and cat dander in children with and without asthma in Taiwan; (2) to determine the levels of serum IgE to specific allergens associated with lower lung function; and (3) to statistically analyze the relationship between items 1 and 2.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Population and Subjects
In 1996, a national survey of respiratory health for middle school children was conducted in Taiwan.13 A Chinese version of the International Study of Asthma and Allergies in Childhood questionnaire was used to identify children with asthma. After the survey, a random sampling of 10% from each population of school children received a pulmonary function test. We conducted the present study focusing on eighth-grade and ninth-grade middle school children in the Tainan area who had completed the pulmonary function test in October 1996. Based on criteria established from questionnaire information, 4,154 children without asthma, 1,058 children who were suspected of having asthma, and 546 children with asthma received a diagnosis. Of this population, a random sample of 20% of the children without asthma, 50% of the children suspected of having asthma, and all of the children with asthma were selected for this study. After excluding those who reported a smoking habit on the questionnaire and those who reported no mailing address, there were 800 children without asthma, 500 children suspected of having asthma, and 543 children with asthma. All selected study subjects were invited to National Cheng Kung University Hospital, Tainan, Taiwan, for a complete examination in our clinic. The examinations and diagnoses were performed by specialized physicians, and the subjects were categorized as children with asthma, children with asthma in remission, children suspected of having asthma, and children without asthma. Children with asthma were those who were confirmed as having asthma by a physician, or who reported having typical wheezing witnessed by parents. Those who had had no attack for >= 12 months were considered in remission. Children suspected of having asthma were those who had self-reported wheezing or episodic shortness of breath. Pulmonary function tests and blood collections were preformed for all subjects after informed consent was obtained from their parents.

Pulmonary Function Test
The pulmonary function test was conducted on each subject when the subject was symptom free and without auscultatory wheezing on the physical examination. The subject was tested while standing and using a spirometer (Model 2130; SensorMedics; Yorba Linda, CA) connected to a computer. Quality control consisted of a 3-L syringe calibration and a leak test before the test. The ambient temperature and atmospheric pressure were measured during the pulmonary function test. The measurements were performed according to the criteria of the American Thoracic Society.14 FEV1, FEV1/FVC, and FEF25–75% were recorded for analysis. FEV1 and FEF25–75% were adjusted for age, sex, height, and weight.

Determination of Specific IgE to Allergens
A commercial Pharmacia CAP system, radioallergosorbent (RAST) FEIA (Pharmacia Diagnostics, Uppsala, Sweden) test was used to determine the allergen-specific IgE antibodies in serum levels of five common allergens in Taiwan, including Dermatophagoides pteronyssinus (Der p), Dermatophagoides farinae (Der f), German cockroach (Blatella germanica, cockroach), cat dander, and dog dander. The results were categorized into level 1 (specific IgE < 0.7 IU/mL), level 2 (specific IgE 0.7 to 17.5 IU/mL), level 3 (specific IgE 17.5 to 100 IU/mL), and level 4 (specific IgE > 100 IU/mL). Values >= 0.7 IU/mL were regarded as a positive response to the specific allergens.

Statistical Analysis
Data analysis was performed using version 3.2.6 for Windows 98 (SAS Institute; Cary, NC). Statistical analysis consisted of determinations of mean and SE of serum levels of specific IgE. Group differences were compared by analysis of variance (ANOVA) and Tukey tests. The unpaired Student’s t test was used to determine the difference between two groups. If the variables were not normally distributed, we used the Kruskal-Wallis test and Dunnett’s posttest to examine the difference, and the Wilcoxon rank sum test to compare the difference between two groups. The Pearson {chi}2 test was used to determine the difference of frequency for two or more groups. If conditions were not suitable for the {chi}2 test, Fisher’s Exact Test was used. Spearman correlation coefficients were computed to assess bivariate relationships. All p values were determined by a two-tailed test, and p < 0.05 was regarded statistically significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Demography of Subjects in Clinical Diagnosis
After the clinic visit and physicians’ evaluation, the children in the study included 43 children with current asthma, 40 children with asthma in remission, 20 children with suspected asthma, and 113 children without asthma. The children with suspected asthma were excluded from further study. Of the 196 children remaining, blood was drawn for serum analysis from 149 subjects: 42 children with current asthma, 38 children with asthma in remission, and 69 children without asthma. Table 1 shows the distributions of these subjects by age, gender, and status of clinical diagnosis.


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  		Table 1.. Demographic Characteristics of Study Subjects (n = 149)*

 
Telephone interviews of 1,027 randomly sampled candidates who did not visit our clinic were conducted. Six hundred forty-six subjects (62.9%) reported that they had not received the invitation letter, 42 subjects (4.1%) reported that they were healthy and not willing to join the study, 143 subjects (13.9%) reported that they were too busy, and 10 subjects (1.0%) reported that they had rejected the invitation for other reasons. Thirty-three candidates (3.2%) refused the phone interview.

Lung Function
The adjusted FEV1 and adjusted FEF25–75% were normally distributed, but FEV1/FVC was not. No difference in adjusted FEV1, adjusted FEF25–75%, and FEV1/FVC was found between children with asthma and those with asthma in remission (Table 2 ). We combined children with current asthma and children with asthma in remission into one group, children with asthma, for the following analysis. Compared with children without asthma, children with asthma had a significantly lower FEV1/FVC (p < 0.05) and adjusted FEF25–75% (p < 0.05), but a similar trend without statistical significance was found in adjusted FEV1.


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  		Table 2.. Differences in Adjusted FEV1, Adjusted FEF25–75%, and FEV1/FVC Between Asthmatic Children and Nonasthmatic Children*

 
Serum Levels of Specific IgE
Table 3 demonstrates that the prevalence of positive RAST response was different among children with asthma, those with asthma in remission, and those without asthma by Pearson {chi}2 test or Fisher’s Exact Test. Prevalence rates of sensitization to Der p (p < 0.0001), Der f (p < 0.0001), and cockroach (p < 0.05) were statistically different among these three groups. No difference in frequency was found among these groups in IgE against cat dander and dog dander. Children with asthma had higher prevalence rates of sensitization to Der p (p < 0.0001), Der f (p < 0.0001), and cockroach (p < 0.05) than did those without asthma. Children with asthma in remission had higher prevalence rates of sensitization to Der p (p < 0.001) and Der f (p < 0.01) than did those without asthma. Prevalence rates of sensitization to common allergens were not different between those with asthma and those with asthma in remission. We combined children with current asthma and those with asthma in remission into one group, children with asthma, for the following analysis.


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  		Table 3.. Frequency of Positive RAST Results Among Asthmatics, Asthmatics in Remission, and Nonasthmatics

 
Adjusted FEV1, FEV1/FVC, Adjusted FEF25–75%, and Specific IgE
In children without asthma, no difference in adjusted FEV1, adjusted FEF25–75%, or FEV1/FVC was found among subjects with different serum levels of IgE against Der p, Der f, cockroach, cat dander, and dog dander. In children with asthma, significant differences in adjusted FEV1, adjusted FEF25–75%, and FEV1/FVC were found among subjects with different serum specific IgE levels by ANOVA or Kruskal-Wallis test (Tables 4 5 6) . Further tests on the difference by Dunnett’s post-test or the Tukey test showed that children with level 4 of Der f-specific IgE had lower FEV1/FVC (p < 0.05) and lower adjusted FEF25–75% (p < 0.05) than children with level 1. Children with level 2 of specific IgE to cockroach had lower adjusted FEV1 (p < 0.01), lower FEV1/FVC (p < 0.01), and lower adjusted FEF25–75% (p < 0.01) than children with level 1. No difference in adjusted FEV1, adjusted FEF25–75%, or FEV1/FVC was found between children with level 2 and level 1 of IgE against cat and dog dander.


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  		Table 4.. Difference in Adjusted FEV1 in Liters Among Asthmatic Children With Different Serum Levels of Allergen-Specific IgE*

 

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  		Table 5.. Difference in FEV1/FVC Percentage Among Asthmatic Children With Different Serum Levels of Allergen-Specific IgE*

 

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  		Table 6.. Difference in Adjusted FEF25–75% in Liters per Second Among Asthmatic Children With Different Serum Levels of Allergen-Specific IgE*

 
Correlation Between Lung Function and Allergen-Specific IgE
In children without asthma, no correlation was found between lung function and serum levels of allergen-specific IgE. In children with asthma (Table 7 ), a decrease in FEV1 correlated with an increase in serum level of Der f-specific IgE (p < 0.05). The decrease in adjusted FEF25–75% correlated with the increase in IgE against Der f (p < 0.05) and cockroach (p < 0.01). Falling FEV1/FVC correlated with the rising serum-specific IgE levels to Der f (p < 0.05) and cockroach (p < 0.01). A separate analysis was also conducted to examine whether there was a difference in this correlation between children with asthma and those with asthma in remission. In children with asthma, a decrement in adjusted FEV1 (p < 0.01), FEV1/FVC (p < 0.01), and adjusted FEF25–75% (p < 0.05) correlated with an increment of IgE against cockroach. The decrease of adjusted FEV1 correlated with the increase of IgE against Der f (p < 0.05). In children with asthma in remission, a similar trend was found between lung function and levels of sensitization, but the correlation was not statistically significant.


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  		Table 7.. Correlation Coefficients Between Lung Function and Allergen-Specific IgE Found in Asthmatic Children*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Our study demonstrated that children in Taiwan with asthma or asthma in remission had higher prevalence rates of sensitization to Der p, Der f, and cockroach. There was no difference in the rates of sensitization to these allergens between children with asthma and those in remission. Children with asthma had lower adjusted FEF25–75% and FEV1/FVC than children without asthma, but no difference in adjusted FEV1 was found. The decline of lung function in children with asthma was associated with serum levels of Der f-specific and cockroach-specific IgE. In children without asthma, however, lung function was not different among children with different serum levels of allergen-specific IgE.

Der p, Der f, cockroach, house dust mites, cat dander, and dog dander are well recognized as important aeroallergens.15 The findings of Hsieh16 showed that exposure to house dust mite allergen is the most important factor for the occurrence of asthma in Taiwan. The rates of sensitization to dust mite varied notably between different places in the world. According to the RAST results, our study demonstrated that sensitization rates of Der p and Der f in those with asthma were much higher than results from Los Alamos (dust mite, 17.4%), Albermarle (dust mite, 42.7%), Central and North Swiss (dust mite, 22%), Helsingborg (dust mite, 54%), and Linkoping (Der p, 34%; Der f, 55%) but similar to results from South Florida (Der p, 89.6%), Singapore (Der p, 79.2%; Der f, 75%) and to results in previous studies in Taiwan.17 18 19 20 21 22 Increased temperature (up to 30°C) and relative humidity might have favored the development of dust mites.23 In areas with lower humidity, indoor dampness is probably more important than outdoor humidity in the domestic development of dust mites.24 However, the high outdoor humidity in Taiwan (68 to 80% monthly average) could have been an important determinant of the indoor humidity,13 which may in part explain the high sensitization rate to dust mites even in those without asthma (50.7%; Table 3 ). When a student was sensitized to two or more allergens, it was difficult to determine exactly which allergen was responsible for the observed asthmatic symptoms.

Children with asthma are known to have abnormal lung function measurements in FEV1,25 FEV1/FVC,26 or FEF25–75%,27 even when not having an asthma attack. A study in The Netherlands28 also supports the hypothesis that sensitization to allergens such as Der p could cause reduced FEV1. However, information is lacking on the threshold serum level of specific IgE at which lung function change can be detected. Our study illustrated that there were thresholds of serum levels of IgE against common allergens for children with asthma or with asthma in remission. It seemed that sensitization to common allergens, as indicated by increased serum-specific IgE, was not associated with a decline of FEV1, FEV1/FVC, and FEF25–75% in children without asthma. The results summarized in Tables 4 5 6 suggest that the relationship between adjusted FEF25–75% and serum levels of allergen-specific IgE antibodies is more readily detectable than that between FEV1 and allergen-specific IgE or FEV1/FVC and allergen-specific IgE. This finding is consistent with the report by Hamid et al,29 who showed that small airways (internal perimeter < 2 mm) were a major site of airway inflammation in asthmatics. Our data also suggest that sensitization to cockroach is at least equally capable of inducing lung function change as sensitization to dust mite for Taiwanese middle school children with asthma or with asthma in remission.

IgE against Der p and Der f are highly cross-reactive. However, there was still some unique specific IgE to Der p or to Der f.30 Shen et al31 reported that serum from children with asthma had different degrees of IgE binding to Der f 7 (46%) and Der p 7 (30%). This observation could partially explain why we found lung function change associated only with a high level of IgE against Der f-specific IgE, but not with Der p-specific IgE.

Children sensitized to cat dander or dog dander had no lung function change compared with those who were not sensitized to these allergens. Two plausible explanations for this are that there was a lack of exposure among the susceptible individuals in the study, and that there were no susceptible individuals in the study. One report from Taiwan implied that the presence of the human leukocyte antigen DPB1*0201 allele was associated with lower serum levels of IgE against house dust mite.32 It is possible that middle school children who lived in the Tainan area had some human leukocyte antigen class II genes involved that could not induce IgE against cat dander or dog dander. These relationships, however, still need to be confirmed.

FEV1 and FEV1/FVC are known to be indicators of the state of airway disease.33 Decreased FEV1/FVC and FEV1 were found in patients with airway constriction. Patients with pulmonary fibrous changes or respiratory muscle weakness had an FEV1 reduction but had normal FEV1/FVC. In our study, the results in Tables 4 5 6 demonstrate that sensitivity of specific IgE to Der f and cockroach was associated with lower lung function in adjusted FEV1, adjusted FEF25–75%, and FEV1/FVC, but that the relationship was not consistent. It is possible that these three specific IgEs played different roles in the pathology of lung function change. However, the interactions among different kinds of allergen- specific IgEs and their mechanisms for causing reduced lung function warrant further investigation.

In conclusion, we found a high prevalence of sensitization to dust mites in Taiwanese adolescents. Children with asthma had higher prevalence of sensitization to dust mites and cockroach than did children without asthma. Sensitization to Der f or to German cockroach was related to lower lung function among middle-school children with asthma or with asthma in remission.


   Acknowledgements
 
We extend our heartfelt appreciation to all of the children, parents, teachers, and school staff who participated in the study, and to the field workers who supported data collection.


   Footnotes
 
Abbreviations: ANOVA = analysis of variance; Der p = Dermatophagoides pteronyssinus; Der f = Dermatophagoides farinae; FEF25–75% = forced expiratory flow between 25% and 75% of FVC; RAST = radioallergosorbent test

This study was funded by grant EPA-86-FA05-09-A2 from the Environmental Protection Administration, Taiwan.

Received for publication October 11, 2000. Accepted for publication September 6, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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