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PEDIATRICS Vol. 107 No. 5 May 2001, p. e80
, §,
,,, ¶,, §,
From the * Channing Laboratory, Department of Medicine, Brigham
and Women's Hospital, Boston, Massachusetts; Division of Pulmonary
and Critical Care Medicine, Beth Israel Deaconess Medical Center,
Boston, Massachusetts; § Harvard Medical School, Boston, Massachusetts;
Program of Population Genetics, Harvard School of Public Health,
Boston, Massachusetts; and ¶ Anhui Medical University Center for
Ecogenetics and Disease Control, Anqing, China.
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ABSTRACT |
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Abstract
Methods
Results
Discussion
Conclusion
References
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Objective. Sensitization to perennial aeroallergens is associated with asthma in industrialized countries with a Western lifestyle. Because silk products are commonly used in Chinese society, we were interested in examining the relation between sensitization to silk and asthma.
Design. Cross-sectional study of 871 children in 503 families living in Anqing, a predominantly rural province of China.
Results. After adjustment for age, gender, familial correlations, and sensitization to other aeroallergens, skin test reactivity to silk was an independent predictor of asthma (odds ratio = 2.6; 95% confidence interval = 1.2-5.7). This association became stronger after inclusion of the eosinophil count and history of parasitic diseases of the participants in the multivariate model (odds ratio = 3.6; 95% confidence interval = 1.4-8.9).
Conclusion. Because sericulture is an important activity in China and other countries throughout the world, sensitization to silk may influence the pathogenesis and severity of asthma in people living in these nations. Key words: asthma, sensitization to silk, rural China.
The silk production industry began in China ~2640 BC,
when the Empress Hsi-ling Shih is credited with learning how to raise silkworms and unwind the silk filaments from their cocoons. Although sericulture then spread to Japan and later westward over India and
Central Asia, China is the main producer of raw silk in the world
today.
Skin test reactivity to perennial aeroallergens, such as the house dust
mite, animal dander, and mold, is strongly associated with asthma in
countries with a Western lifestyle.1-6 Because silk is an
aeroallergen that is ubiquitous in Chinese society,7 we
were interested in examining the relation between sensitization to silk
and asthma among 871 children living in Anqing, a predominantly rural
province of China.
Anqing stretches for ~80 km along the northern bank of
the Yangtze river. The annual temperature is 15°C. Anqing has 3 urban areas and 8 rural counties, with a total area of 15 000
km.2 The population in 1990 was 5.8 million (urban, 9%;
rural, 91%). Families were selected from the general population. All
families were selected by a 2-stage random sampling technique using
1992 census records. The sample unit at the first stage was the
administrative unit (eg, the village). At the second stage, the unit
was the household. The following criteria were used for inclusion of
families in the study: 1) 2 or more siblings in the family; 2) age of
the youngest sibling Procedures
Informed consent was obtained from the parents of all
participating children <12 years old and from all participating
children >12 years old. Local officials and health centers arranged
for appointments to take place at a central office at a time convenient for the participants. Data were collected by faculty members from Anhui
Medical University and by trained interviewers between July 1, 1994, and January 26, 1998.
The following procedures were conducted: 1) completion of a modified
American Thoracic Society Division of Lung Diseases questionnaire including questions on respiratory symptoms, respiratory health status,
occupational history, tobacco use, home environment, family history of
asthma and other chronic diseases, and current status and history of
parasitic diseases; 2) skin testing of reactivity to 10 allergens along
with a positive and a negative control; 3) collection of blood samples
for measurement of eosinophil count; and 4) examination of a single
stool specimen for ova and parasites. The study was approved by the
institutional review boards of the Brigham and Women's Hospital, the
Anhui Medical University Center for Ecogenetics and Disease Control,
and the Harvard School of Public Health.
Peripheral Blood Eosinophil Count
Eosinophil count in peripheral blood, henceforth referred to as
eosinophil count, was measured by Coulter-counter techniques at the
Hematology Laboratory of Anhui Medical University. Because the values
obtained did not follow a normal distribution, they were transformed to
a log10 scale for analysis.
Allergy Skin Testing
Skin testing was performed with a slightly modified version of
the semiquantitative puncture method developed by Santilli et
al.8 In addition to histamine and saline controls, the
following antigens were applied to the skin of the forearm: cockroach,
house dust, mixed trees, mixed grasses, tobacco leaf, polyvalent molds,
Dermatophagoides pteronyssinus, Dermatophagoides farinae,
Artemisia vulgaris, and mulberry silk waste (henceforth referred
to as silk). The silk, A vulgaris, polyvalent molds, and
house dust antigens were provided by the Department of Allergy of
Peking Union Medical College (Beijing, China); the remaining antigens
were purchased from Bayer Corp (Spokane, WA). The preparation of the
silk antigen has been described elsewhere.7 A test was
considered positive if the diameter of the skin wheal was Stool Examination for Ova and Parasites
Microscopic examination of wet mounts of stool specimens for ova
and parasites was performed at the Parasitology Laboratory of Anhui
Medical University Center.
Definition of Asthma
Our definition of asthma was based on affirmative answers to the
questions "Do you have asthma?" and "Has your asthma been confirmed by a doctor?" as well as a history of either Definition of Other Predictor Variables
Age, a potential confounder of the relationship between
sensitization to allergens and asthma, was treated as a continuous variable. There was no reporting of current smoking in any of the
participating children, and they were all presumed to be nonsmokers for
study purposes.
Statistical Methods
Bivariate relationships between predictor and outcome variables
were analyzed by Participant Characteristics
The study originally included 923 participants The characteristics of the 871 participating children are summarized in
Table 1. The mean and standard deviation of the age of the 871 study participants were 10.6 ± 2 years; the
age range of these participants was 6 to 14 years. The geometric mean
eosinophil count of the study participants was
146/mm3. Information on history of past parasitic
diseases and results of a single stool examination for ova and
parasites were available for 677 of the 871 study participants
(77.7%). Ninety of these 677 participants (13.3%) had a history of
parasitic diseases (n = 55) and/or a positive
examination for ova and parasites (n = 54).
TABLE 1
METHODS
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Abstract
Methods
Results
Discussion
Conclusion
References
6 years; and 3) both parents available.
3 mm after
subtracting the negative control.
1
respiratory symptoms (cough, wheezing, or nocturnal cough/wheezing) or
asthma attacks in the preceding 12 months.
2 or Fisher's exact tests in
the case of pairs of categorical variables or 2-tailed t
tests in the case of a categorical and a continuous variable. To
account for correlations among individuals from the same household,
methods developed by Zeger and Liang9 with generalized
estimating equations for the logistic case were used to evaluate the
relationship between the dependent and independent variables. All of
the analyses were performed with the SAS statistical software package
(SAS Institute, Inc, Cary, NC).
RESULTS
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Abstract
Methods
Results
Discussion
Conclusion
References
14 years in 539 families in Anqing, China. The present analyses were limited to the 871 children who had complete information on peripheral blood eosinophil
count and skin test reactivity to aeroallergens. No statistically
significant differences in age; gender; physician-diagnosed asthma;
wheezing, cough, or nocturnal symptoms in the preceding 12 months; skin
test reactivity to 1 aeroallergen; or peripheral blood eosinophil
count were found between participants included in the analysis
(n = 871) and those excluded (n = 52).
Characteristics of 871 Study Participants in Anqing,
China
Predictors of Asthma on Univariate Analysis
No statistically significant difference was found between the mean ages of asthmatic and nonasthmatic children (10.1 ± 2.2 years vs 10.6 ± 2.0 years; P = .14). There was a statistically significant association between skin test reactivity to silk and asthma (Table 2). However, sensitization to any of the other 9 aeroallergens examined was not significantly associated with asthma (P > .2 in all cases).
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Participants whose eosinophil count was in the upper 2 quartiles of the log10 distribution of eosinophil count had significantly higher odds of having asthma than did those in the bottom quartile (Table 2).
Asthma and Sensitization to Silk
Table 3 summarizes the results of multivariate analyses of the relation between asthma and skin test reactivity to aeroallergens. After adjustment for age, gender, familial correlations, and skin test reactivity to other aeroallergens using generalized estimating equations, children who were sensitized to silk had 2.6 times higher odds of having asthma than did nonreactors (model 1). This association between sensitization to silk and asthma became stronger and of greater statistical significance after inclusion of the eosinophil count of the participants in the multivariate model, as either a categorical variable (model 2) or a linear term (model 3).
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DISCUSSION |
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Abstract
Methods
Results
Discussion
Conclusion
References
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To our knowledge, this is the first population-based study to demonstrate an association between sensitization to silk and childhood asthma. After adjustment for age, gender, familial correlations, and sensitization to other aeroallergens, skin test reactivity to silk was an independent predictor of asthma among 871 children living in rural China (odds ratio [OR] = 2.6; 95% confidence interval [CI] = 1.2-5.7).
In a study of 737 children living in San Bu, a rural province of southeast China, Leung and collaborators10 found no association between sensitization to any of 4 aeroallergens (pollen, cockroach, mold, and animal dander) and asthma. Although sensitization to house dust mite was associated with asthma, this association was of borderline statistical significance (OR = 5.6; 95% CI = 1.0-30.2). Skin testing to silk was not performed in this study.
Matsumura and colleagues11 reported 4 cases of childhood
asthma attributable to silk inhalation. In 2 of their study
participants, provocative tests with inhalation of silk extract
resulted in strong asthmatic attacks. Chaoming and
collaborators7 reported 64 cases of silk-induced asthma
among children 15 years of age who were evaluated at an allergy
clinic in Beijing. The diagnosis of asthma related to silk exposure was
based on history, skin prick testing, and conjunctival or nasal
provocation testing with silk extract. Of the 64 children included in
this series, 60 (93.7%) were classified as having moderate to severe
asthma. Johansson and colleagues12 reported a series of 50 patients diagnosed with asthma caused by allergy to bed quilts filled
with silk waste at the Department of Dermatology and Allergy at the
University Hospital in Zurich. On an average, the first symptoms
appeared 7 months after exposure to silk. The study participants were
10 to 58 years old, and 49 of the 50 patients (98%) improved with
avoidance of exposure to silk. Sensitization to silk and occupational
asthma have long been known to be hazards of
sericulture.13-15
China is the homeland of silk. The allergenicities of the 2 groups of silk used in China, mulberry and wild, are very similar.12 However, allergy to mulberry silk is more frequent in China than is allergy to wild silk because mulberry silk is more commonly used.7 Silk is obtained from the cocoon of the silkworm.14,15 Each cocoon consists of a single thread secreted by the worm. Because the emerging moth would break the thread, the pupae are killed by steaming the cocoons. The steamed cocoons are boiled, and then the threads are rolled over reels. Each thread is a double filament of protein material (fibroin) glued together with sericin, an allergenic gummy substance that is extracted during processing of the silk threads.14,15 The final textile products of silk, however, are most often nonallergenic.7 Sensitization to mulberry silk can be attributable to allergens in the silk cocoon, silkworm pupae, and unprocessed silk threads. Silk workers involved in sorting or boiling the cocoons and in reeling, rearranging, or degumming the threads can be sensitized to silk by inhalation of airborne allergens.14,15 Unprocessed silk threads that are broken during reeling (silk waste) are used by the Chinese to fill bed quilts, clothes, toys, and mattresses.7 Children can also be exposed to silk if their parents work in sericulture.7 Although exposure to silk waste may be more intense during the winter months, when children often use blankets filled with this material, perennial exposure to silk waste is likely to occur in some children. Given the pervasive presence of silk products in Chinese culture, avoidance of exposure to silk waste may be difficult unless its use is greatly reduced.
Peripheral blood eosinophilia is associated with asthma and increased airway responsiveness in Western countries with low prevalence of parasitic diseases.16,17 The role of peripheral blood eosinophil count as a marker of asthma in the Far East, however, has not been adequately studied. Our findings suggest that the eosinophil count in peripheral blood may be a useful marker of asthma in areas of the Far East with a low to moderate prevalence of parasitic illnesses.
We recognize several limitations to our findings. First, this is a cross-sectional study, and a temporal relationship between sensitization to silk and the development of asthma, thus, cannot be demonstrated. Second, our definition of asthma was based on responses to a standardized questionnaire, because we did not measure airway responsiveness to bronchoconstrictors in the study participants. However, our definition of asthma has been found to be adequate for use in population-based studies. Third, we examined only a single stool specimen for ova and parasites. Significant underestimation of the true prevalence of parasitic disease in Anqing is unlikely, however, because the geometric mean eosinophil level in our study population is far lower than that of heavily parasitized groups.17 Fourth, we did not examine skin test reactivity to cat or dog allergens. However, ownership of these pets is exceedingly rare among people living in Anqing. Fifth, because the prevalence of childhood asthma in Anqing is low (3.9%), our statistical power may not have been adequate to detect a modest association between any of the aeroallergens examined and asthma.
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CONCLUSION |
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Abstract
Methods
Results
Discussion
Conclusion
References
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Sensitization to silk is an independent predictor of childhood asthma in rural China. Because sericulture is a very important activity in China and other countries (eg, India and Japan), sensitization to silk may influence the pathogenesis and severity of asthma in children living in these nations. Additional research is needed to examine whether sensitization to silk in early life precedes the development of asthma among children living in silk-producing nations and to assess whether avoidance of exposure to silk products (eg, silk waste) results in symptomatic improvement of silk-induced asthma.
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ACKNOWLEDGMENTS |
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This study was supported in part by Grant AI56371 from the National Institutes of Health and by Millennium Research.
Dr Celedón is supported by a Charles A. King Trust Fellowship Award. Dr Palmer is a Winston Churchill Memorial Trust Fellow and an Australian-American Educational Foundation Fulbright Fellow.
We thank the study participants; the staffs of Anhui Medical University and the Anqing Health Bureau; Jaylyn Olivo for her editorial assistance; and Dr Frank E. Speizer for his helpful comments on the manuscript.
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FOOTNOTES |
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Received for publication Nov 7, 2000; accepted Dec 21, 2000.
Reprint requests to (J.C.C.) Channing Laboratory, 181 Longwood Ave, Boston, MA 02115. E-mail: juan.celedon{at}channing.harvard.edu
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ABBREVIATIONS |
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OR, odds ratio; CI, confidence interval.
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REFERENCES |
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