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Allergic Diseases Attributable to Atopy in a Population Sample of Asian

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Allergic Diseases Attributable to Atopy in a Population Sample of Asian www.nature.com/scientificreports OPEN Allergic diseases attributable to atopy in a population sample of Asian children Chao‑Yi Wu1,3, Hsin‑Yi Huang1, Wen‑Chi Pan2, Sui‑Ling Liao3,4,5, Man‑Chin Hua3,4,5, Ming‑Han Tsai3,4,5, Shen‑Hao Lai3,4,6, Kuo‑Wei Yeh1,3,4, Li‑Chen Chen3,4,7, Jing‑Long Huang3,4,7* & Tsung‑Chieh Yao1,3,4* The proportion of allergic diseases attributable to atopy remains a subject of controversy. This study aimed to estimate the population risk of physician‑diagnosed asthma, rhinitis and eczema attributed to atopy among a population sample of Asian school‑age children. Asian children aged 5–18 years (n = 1321) in the Prediction of Allergies in Taiwanese CHildren (PATCH) study were tested for serum allergen‑specifc immunoglobulin E. Physician‑diagnosed asthma, rhinitis and eczema were assessed by a modifed International Study of Asthma and Allergies in Childhood questionnaire. Atopy was defned as the presence of serum allergen‑specifc immunoglobulin E. In this population‑based study, 50.4% of the subjects with asthma, 46.3% with rhinitis, and 46.7% with eczema were attributable to atopy. The population attributable risk (PAR) of atopy for three allergic diseases was higher in adolescents (asthma, 54.4%; rhinitis, 59.6%; eczema, 49.5%) than younger children aged less than 10 years (asthma, 46.9%; rhinitis, 39.5%; eczema, 41.9%). Among the seven allergen categories, sensitization to mites had the highest PARs for all three allergic diseases (51.3 to 64.1%), followed by sensitization to foods (asthma, 7.1%; rhinitis, 10.4%; eczema 27.7%). In conclusion, approximately half (46.3 to 50.4%) of Asian children in Taiwan with allergic diseases are attributable to atopy. Abbreviations BMI Body mass index CI Confdence interval IgE Immunoglobulin E ISAAC​ International Study of Asthma and Allergies in Childhood NC Not computed OR Odds ratio PAR Population attributable risk PATCH Prediction of Allergies in Taiwanese CHildren RR Relative risk SD Standard deviation Te prevalence of allergic diseases, including asthma, rhinitis and eczema, is increasing worldwide1–3. Children with allergic diseases may have signifcantly impaired quality of life and higher healthcare utilization, represent- ing a substantial health burden4–8. A clear understanding of the spectrum of etiologies contributing to allergic diseases may lead to improved strategies for prevention and management of these conditions. Atopy, defned as the genetic propensity to develop immunoglobulin E (IgE) antibodies in response to expo- sure to allergen, is a well-known risk factor for allergic diseases9,10. Most treatment and prevention strategies nowadays thus focused on mechanisms of allergic sensitization and emphasized on the importance of allergen 1Division of Allergy, Asthma, and Rheumatology, Department of Pediatrics, Chang Gung Memorial Hospital, 5 Fu-Hsin Street, Kweishan, Taoyuan, Taiwan. 2Institute of Environmental and Occupational Health Sciences, National Yang-Ming University, Taipei, Taiwan. 3School of Medicine, Chang Gung University College of Medicine, Taoyuan, Taiwan. 4Community Medicine Research Center, Chang Gung Memorial Hospital At Keelung, Keelung, Taiwan. 5Department of Pediatrics, Chang Gung Memorial Hospital At Keelung, Keelung, Taiwan. 6Division of Pediatric Pulmonology, Department of Pediatrics, Chang Gung Memorial Hospital, Taoyuan, Taiwan. 7Department of Pediatrics, New Taipei Municipal TuCheng Hospital, 6 Sec. 2 Jinchen Road, Tucheng District, New Taipei, Taiwan. *email: [email protected]; [email protected] Scientifc Reports | (2021) 11:16052 | https://doi.org/10.1038/s41598-021-95579-2 1 Vol.:(0123456789) www.nature.com/scientificreports/ Figure 1. Schematic presentation of the recruitment process of the study subjects. avoidance. However, some physicians have argued that the proportion of allergic diseases attributable to atopy may have been overestimated, challenging the concept that there are allergic and non-allergic forms of asthma, rhinitis and eczema10–13. However, the exact proportion of allergic diseases truly attributable to atopy remains a subject of debate. Previous studies have demonstrated ethnic diferences in the prevalence of atopy as well as allergic diseases14,15. Although previous studies in Western countries suggested that 4 to 63% of asthma cases10,11,16–18, 37.3 to 80.7% of rhinitis cases 10,12 and 32% of eczema cases were attributable to atopy 10, there is limited data available on the proportion of allergic diseases attributable to atopy among Asian children. Te objective of this study was to estimate the population risk of physician-diagnosed asthma, rhinitis and eczema attributed to atopy among a population sample of Asian school-age children in Taiwan. Methods Study subjects. Te schematic presentation of the recruitment process of study subjects is presented in Fig. 1. Study participants were recruited from a population-based cohort of 5351 children (2616 boys, 48.9%; age, 10.4 ± 2.9 years), participating in the Prediction of Allergies in Taiwanese CHildren (PATCH) study3,19–24. Among the subjects, 1900 children were randomly invited and 1717 of them agreed to participate the study. Blood samples were successfully obtained from 1321 children to determine allergen-specifc IgE. Parents of the recruited subjects answered pre-designed questionnaires modifed from the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire 25, regarding subject’s general health information, demographic data, and questions on clinical symptoms and diagnosis of allergic diseases. Tere were no signifcant diferences between the 1321 study subjects and the original 5351 cohort members in terms of gender, age, and prevalence of allergic diseases. Te study was approved by the Institutional Review Board of Chang Gung Medical Foundation (96-0370B) and written inform consents were provided by the parents of each subject. All experiments in this study were performed in accordance with the relevant guidelines and regulations. Allergen‑specifc serum immunoglobulin E. Atopy was defned as positive Phadiatop Infant test result (≧ 0.35 PAU/L) (Phadia, Uppsala, Sweden), a commercial assay to detect allergen-specifc IgE against a mix of common inhalant and food allergens26. Allergen-specifc IgEs against 40 common allergens divided in 7 categories were measured by an automated microfuidic-based multiplexed immunoassay system (BioIC TM Allergen-specifc IgE Detection Kit- AD40 Panel; Agnitio Science and Technology, Hsinchu, Taiwan). As previ- ously reported27, the allergen-specifc IgEs includes: (1) mites: Dermatophagoides pteronyssinus, Dermatopha- goides farinae, and Blomia tropicalis; (2) animals: dog dander, cat dander, chicken feather and skin, and duck feather and skin; (3) cockroaches: German cockroach and Oriental cockroach; (4) mold: Candida albicans, Cla- dosporium herbarum, Aspergillus fumigatus, Penicillium notatum, and Alternaria alternata; (5) pollen: timothy grass, bermuda grass, ragweed, mugwort, and goldenrod; (6) foods: cow’s milk, goat’s milk, egg white, egg yolk, crab, shrimp, codfsh, salmon, blue mussel, soybean, wheat, potato, peanut, almond, garlic, cheese, baker’s yeast, kiwi, tomato, and carrot; and (7) latex. However, latex was excluded from the analysis of the estimate for popula- tion attributable risk (PAR) because its low prevalence resulted in non-convergence of the model 28. Defnitions of allergic diseases. Tis study evaluated 3 allergic diseases, including asthma, rhinitis and eczema. Te diagnosis of allergic diseases were assessed using the modifed ISAAC questionnaire25. Cases were subjects whose parents provided afrmative answers to the questions, ‘‘Has a doctor ever told you that you had asthma?’’, ‘‘Has a doctor ever told you that you had allergic rhinitis?’’ or ‘‘Has a doctor ever told you that you had eczema?’’. Scientifc Reports | (2021) 11:16052 | https://doi.org/10.1038/s41598-021-95579-2 2 Vol:.(1234567890) www.nature.com/scientificreports/ All subjects Atopy Non atopy p Age, years (mean ± SD) 10.3 ± 2.7 10.3 ± 2.7 10.4 ± 2.7 0.625 Gender, male, n (%) 644/1321 (48.8%) 410/757 (54.2%) 234/564 (41.5%) < 0.001* Body mass index, kg/m2 (mean ± SD) 18.7 ± 3.6 18.8 ± 3.7 18.5 ± 3.4 0.087 Body mass index category 0.199 Underweight, n (%) 107/1321 (8.1%) 53/757 (7.0%) 54/564 (9.6%) Normal weight, n (%) 858/1321 (65.0%) 491/757 (64.9%) 367/564 (65.1%) Overweight, n (%) 271/1321 (20.5%) 158/757 (20.9%) 113/564 (20.0%) Obesity, n (%) 85/1321 (6.4%) 55/757 (7.3%) 30/564 (5.3%) Asthma, n (%) 146/1304 (11.2%) 113/743 (15.2%) 33/561 (5.9%) < 0.001* Rhinitis, n (%) 487/1293 (37.7%) 360/738 (48.8%) 127/555 (22.9%) < 0.001* Eczema, n (%) 253/1297 (19.5%) 188/741 (25.4%) 65/556 (11.7%) < 0.001* Parental allergic diseases, n (%) 462/986 (46.9%) 282/550 (51.3%) 180/436 (41.3%) 0.002* Paternal allergic diseases, n (%) 319/972 (32.8%) 192/542 (35.4%) 127/430 (29.5%) 0.052 Maternal allergic diseases, n (%) 253/974 (26.0%) 163/541 (30.1%) 90/433 (20.8%) 0.001* Household passive smoking, n (%) 696/1284 (54.2%) 402/736 (54.6%) 294/548 (53.7%) 0.730 Season of birth 0.884 Spring, n (%) 312/1321 (23.6%) 183/757 (24.2%) 129/564 (22.9%) Summer, n (%) 348/1321 (26.3%) 194/757 (25.6%) 154/564 (27.3%) Autumn, n (%) 349/1321 (26.4%) 199/757 (26.3%) 150/564 (26.6%) Winter, n (%) 312/1321 (23.6%) 181/757 (23.9%) 131/564 (23.2%) Table 1. Characteristics of study subjects. SD standard deviation. *P < 0.05 is bold. Statistical analysis. Diferences in the prevalence of subject characteristics were analyzed using Chi- squared test or Student’s t-test. Logistic regression models were applied where odds ratios (ORs) and 95% con- fdence intervals (CIs) were estimated for atopy on the risk of asthma, rhinitis or eczema, respectively. Models were adjusted for age, gender, body mass index (BMI), household passive smoking, and season of birth, which were similar to previous studies 17.
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