Prevalence, risk factors and comorbidities of allergic rhinitis in South Korea: The Fifth Korea National Health and Nutrition Examination Survey Chae-Seo Rhee, M.D., Ph.D.,1 Jee Hye Wee, M.D.,1 Jae-Cheul Ahn, M.D.,1 Woo Hyun Lee, M.D.,1 Keng Lu Tan, M.D.,1 Soyeon Ahn, Ph.D.,2 Ju Hyun Lee, M.S.,2 Chul-Hee Lee, M.D., Ph.D.,1 Yang-Sun Cho, M.D., Ph.D.,3 Kyoung Ho Park, M.D., Ph.D.,4 Kun Hee Lee, M.D., Ph.D.,5 Kyung-Su Kim, M.D., Ph.D.,6 Ari Lee, M.S.,7 and Jeong-Whun Kim, M.D., Ph.D.1
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ABSTRACT
Background: There has been no nationwide epidemiological investigation of allergic rhinitis (AR) that was diagnosed by both questionnaires and laboratory tests in Korea. This study investigated the prevalence, risk factors, and comorbidities of AR in South Korea. Methods: The Korean National Health and Nutritional Examination Survey examined a representative sample of the Korean population. A total of 2305 participants underwent immunoradiometric assay for specific IgE antibodies against common indoor allergens. Healthy, atopy only, and AR groups were defined according to the results of allergen test. The weighted prevalence for each group was calculated. Risk factors including food and comorbidities were identified using univariate or multivariate analyses. The patients were also categorized into four subgroups according to the Allergic Rhinitis and Its Impact on Asthma (ARIA) classification and associated comorbidities were analyzed. Results: The prevalence of atopy only and AR was 30.0 ⫾ 1.2% and 16.2 ⫾ 1.0%, respectively. The multivariate analysis showed that the prevalence was influenced by sex (p ⬍ 0.01) for atopy only and sex (p ⫽ 0.09), age (p ⫽ 0.02), marital status (p ⫽ 0.24), and stress level (p ⫽ 0.30) for AR. Compared with the healthy group, asthma (odds ratio [OR] ⫽ 4.77), nasal polyp (NP; OR ⫽ 3.44), chronic rhinosinusitis (OR ⫽ 13.93), and olfactory dysfunction (OR ⫽ 4.88) were more prevalent in the AR group. Based on the ARIA guideline, intermittent mild rhinitis was most common (58.1%). Asthma was correlated to severity and atopic dermatitis and NPs was associated with persistency. Daily intake of less mackerel and more carrots, bread, and bean curd were associated with the increased risk of AR. Conclusion: Prevalence, risk factors, and comorbidities of AR were evaluated in the general Korean population, which will contribute to prevention and treatment of AR and its comorbidities in Koreans. (Am J Rhinol Allergy 28, e107–e114, 2014; doi: 10.2500/ajra.2014.28.4040)
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llergic rhinitis (AR) is a common chronic respiratory illness. Epidemiological studies have provided valuable information to develop its effective prevention and treatment of the disease.1 Large international studies, including the European Community Respiratory Health Survey, National Health and Nutrition Examination Survey (NHANES), and International Study of Asthma and Allergies of Childhood, have studied AR prevalence worldwide. The cumulative incidence of AR was 12% in the European Community Respiratory Health Survey II2 and the prevalence of current allergies was 23.5% of the general U.S. population in the NHANES 2005–2006.3 AR prevalence has varied from region to region, probably because of differences in the From the 1Department of Otorhinolaryngology–Head and Neck Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, South Korea, 2Medical Research Collaborating Center, Seoul National University Bundang Hospital, Seongnam, South Korea, 3Department of Otorhinolaryngology–Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, South Korea, 4Department of Otorhinolaryngology– Head and Neck Surgery, The Catholic University of Korea School of Medicine, Seoul, South Korea, 5Department of Otorhinolaryngology–Head and Neck Surgery, Kyung Hee University School of Medicine, Seoul, South Korea, 6Department of Otorhinolaryngology–Head and Neck Surgery, Yonsei University College of Medicine, Seoul, South Korea, and 7Division of Chronic Disease Surveillance, Korea Centers for Disease Control and Prevention, Chung Won, South Korea Presented and received the Young Scientist Award at the 20th World Congress of the International Federation of Otorhinolaryngological Societies (IFOS), Seoul, Korea, June 1–5, 2013 The authors have no conflicts of interest to declare pertaining to this article C-S Rhee and JH Wee contributed equally to this article Address correspondence to Jeong-Whun Kim, M.D., Ph.D., Department of Otorhinolaryngology–Head and Neck Surgery, Seoul National University College of Medicine , Seoul National University Bundang Hospital, 166, Kumiro, Bundang-gu, Seongnam 463-707, South Korea E-mail address: [email protected]; alternative: [email protected]; alternative: [email protected] Copyright © 2014, OceanSide Publications, Inc., U.S.A.
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subjects included and the diagnostic criteria used. In an Asia-Pacific Survey, the AR prevalence ranged from 2.5 to 13.2%.4 Although interand intraregional differences of the prevalence were investigated in the International Study of Asthma and Allergies of Childhood, the study samples were mainly children.5 Furthermore, most studies were based on questionnaires or clinical diagnosis and focused on the relationship between AR and asthma. There have been few studies for the prevalence and risk factors of AR in the general population of South Korea. The first epidemiological study on AR based on a nationwide survey was reported in 1991,6 which included questionnaires and nasal examinations, and perennial AR prevalence was 1.14%. Recently, a nationwide study reported that its prevalence was 28.01% in 2008, diagnosed only by nasal symptoms without an allergen test.7 The Korean NHANES (KNHANES), which is a government-driven survey of the Korea Center for Disease Control and Prevention, has been conducted since 1998. The Korean Society of Otorhinolaryngology– Head and Neck Surgery (KORL) participated in this project and interviews and examinations were performed by trained ear, nose, and throat (ENT) residents. KNHANES V-1 (2010) was the first population-based study to assess specific IgE to major perennial allergens in the noninstitutionalized civilian population of South Korea. The aim of this study was to analyze the prevalence of AR and its risk factors including food and laboratory test results, using KNHANES V-1 data. In addition, its association with comorbidities was also evaluated based on the Allergic Rhinitis and Its Impact on Asthma (ARIA) criteria in South Korea.
METHODS Study Population and Data Collection We used data from KNHANES V-1, which was conducted in 2010. The survey was performed using a rolling sampling design that involves a complex, stratified, multistage, probability cluster survey
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of a representative sample of the noninstitutionalized civilian population of South Korea. A total of 192 sampling units were randomly selected from primary sampling units encompassing the target population with 20 households per sampling unit, including a total of 3840 households. The KNHANES was conducted by four survey teams consisting of three components: a health interview, a nutrition interview, and health examination. Each survey team had one ENT resident, one ophthalmologist, one dentist, one radiologist, two interviewers, three nurses, and one coordinator. Each team moved in a mobile examination vehicle and performed surveys for 4 consecutive days per sampling unit. All participants provided written consents. This study was approved by the Institutional Review Board of Seoul National University Bundang Hospital.
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Demographic Characteristics The questionnaires were administered by the physicians or interviewers face to face. All data have been converted to appropriate categories for analysis. Age was stratified into seven subgroups and then categorized into younger (⬍30–39 years old) and older (⬎40–49 years old) age groups. Body mass index was categorized into normal (⬍25 kg/m2) or obese (ⱖ25 kg/m2). The socioeconomic status (residency, household income, education, and occupation) was categorized as previously described.8 Marital status was divided into single or married. The number of family members (crowding) was divided into two groups: three or less or four or more family members. The type of dwelling was categorized into detached houses or apartments. Smoking status was classified into never smoker (persons who have never smoked), exsmoker (persons who smoked in the past but do not smoke currently), and current smoker (persons who smoke currently). The urine cotinine level was used as a marker of exposure to smoking and was categorized by the following criteria: ⬍20 ng/mL, “nonsmoker”; 20–100 ng/mL, “passive smoker”; and ⬎100 ng/mL, “active smoker”.9 Current alcohol use was assessed by questioning the participants about their average frequency per week of alcohol consumption during the month before their interview. Sleep time was divided into two categories by the mean value: under mean, mean, or more. Stress level assessed by questionnaire was categorized into low (none or small amount) or high (some or extreme). Eating out frequency was rated on a seven-point scale and classified into low (less than once a day) or high (once a day or more). Serum vitamin D of ⬍20 ng/mL was defined as vitamin D deficiency and ⬍10 ng/mL as severe deficiency.10
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Evaluation of ENT Findings and Comorbidities A total of 87 ENT residents from 45 training hospitals were recruited and trained for this survey. The Epidemiologic Survey Committee of the KORL verified the quality control of the survey. Endoscopic examinations were performed according to standardized protocols. Chronic rhinosinusitis (CRS), septal deviation, and olfactory loss were defined as previously described.8 Asthma, atopic dermatitis, and tuberculosis were defined as a self-reported physician’s diagnosis.
Diagnosis of AR
Participants were interviewed for their nasal symptoms by ENT residents and underwent blood tests for allergen-specific IgE. The allergen test was performed for the subjects aged ⱖ10 years old. Serum samples were analyzed using an immunoradiometric assay (ImmunoCAP 100, Phadia, Sweden). Three common indoor allergens such as Dermatophagoides farinae, cockroach, and dog were tested. Atopy was defined as being positive for at least one specific IgE.11 The detection limit was 0.35 kU/L. AR was defined as being atopic and reporting at least one subjective allergic symptom such as sneezing, watery rhinorrhea, nasal obstruction, and itching without fever
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Figure 1. Adjusted odds ratios (ORs; 95% confidence intervals [CIs]) for the association between dietary intake and allergic rhinitis (AR), compared with the healthy group. The multiple regression models are adjusted for sex, age, marital status, the number of family members, stress level, and eatingout frequency.
or sore throat within the last year. The participants without atopy and allergic symptoms were defined as healthy. According to the ARIA guidelines,12 AR was categorized into intermittent mild, intermittent moderate/severe, persistent mild, and persistent moderate/severe.
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Table 1 The prevalence of healthy, atopy only, and AR and characteristics among the KNHANES 2010 population aged >10 yr Characteristics Overall Sex Male Female Age, yr 10–19 20–29 30–39 40–49 50–59 60–69 ⱖ 70 Body mass index Normal(⬍25 kg/m2) Obese (ⱖ25 kg/m2) Missing Residency Rural Urban Marital status Single Married Missing Family no. (crowding) ⱕ3 ⱖ4 Dwelling type Detached house Apartment Missing Quartile of household income Low, midlow Midhigh, high Missing Educational level Low High Missing Occupation White collar Blue collar Missing Smoking status Never smoker Exsmoker Current smoker Missing Urine cotinine Nonsmoker Passive smoker Active smoker Missing Current alcohol use ⬍2/wk ⱖ2/wk Missing Sleep time* Under mean Mean or more Missing
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Unweighted Total No.
Weighted, % (SE)#
2305
Healthy, % (SE)#
Atopy Only, % (SE)#
AR, % (SE)#
41.4 (1.3)
30.0 (1.2)
16.2 (1.0) 17.5 (1.5) 14.9 (1.4)
1140 1165
50.0 (0.8) 50.0 (0.8)
34.4 (1.6)§ 48.6 (2.0)
36.7 (1.8)§ 23.2 (1.6)
394 360 381 390 396 327 57
15.2 (0.7) 15.4 (0.9) 18.0 (0.9) 19.1 (0.7) 15.2 (0.7) 9.0 (0.6) 7.9 (1.2)
34.4 (3.1)§ 33.6 (2.8) 36.9 (3.1) 48.6 (2.7) 47.1 (3.1) 50.8 (3.6) 41.9 (7.3)
29.5 (3.2) 30.5 (2.9) 26.4 (2.4) 30.1 (2.6) 31.8 (2.8) 33.8 (3.9) 29.7 (7.2)
1641 659 5
69.7 (1.3) 30.3 (1.3)
41.4 (1.6) 41.7 (2.6)
27.9 (1.3)§ 34.4 (2.5)
17.2 (1.2) 14.1 (1.8)
1226 1079
54.7 (2.3) 45.3 (2.3)
42.3 (1.7) 40.4 (2.0)
30.6 (1.6) 29.2 (1.8)
15.1 (1.5) 17.6 (1.3)
766 1537 2
32.6 (1.2) 67.4 (1.2)
33.8 (2.1)§ 45.2 (1.6)
29.8 (1.9) 30.1 (1.6)
23.9 (1.8)§ 12.4 (1.3)
1135 1170
46.4 (1.6) 53.6 (1.6)
41.5 (2.0) 41.4 (1.6)
31.3 (2.0) 28.8 (1.5)
14.2 (1.5) 18.0 (1.3)
850 1447 8
47.8 (2.7) 52.2 (2.7)
40.1 (2.1) 42.9 (1.7)
32.7 (2.0)§ 27.4 (1.4)
15.4 (1.6) 16.7 (1.4)
971 1306 28
46.4 (1.7) 53.6 (1.7)
40.2 (2.0) 42.7 (1.7)
31.4 (2.0) 28.5 (1.5)
16.3 (1.6) 16.4 (1.2)
904 1384 17
39.3 (1.4) 60.7 (1.4)
43.2 (2.0) 40.4 (1.6)
29.6 (2.1) 30.0 (1.5)
15.1 (1.8) 17.0 (1.1)
1532 746 27
68.1 (1.3) 31.9 (1.3)
39.7 (1.5) 45.4 (2.1)§
30.8 (1.6) 27.7 (1.7)
16.1 (1.2) 16.7 (1.6)
1378 409 507 11
58.1 (1.0) 17.4 (1.0) 24.6 (1.0)
45.1 (1.8)§ 40.1 (2.6) 34.3 (3.0)
25.8 (1.5)§ 31.2 (2.9) 38.1 (3.0)
15.8 (1.3) 18.2 (2.8) 15.8 (2.0)
1478 163 540 124
63.8 (1.5) 8.7 (0.9) 27.5 (1.2)
44.8 (1.6)§ 39.7 (4.3) 33.9 (2.7)
27.6 (1.5)§ 27.2 (4.4) 38.8 (2.8)
16.1 (1.4) 17.3 (4.2) 15.6 (1.8)
1842 437 26
79.5 (0.9) 20.5 (2.1)
43.0 (1.5) 37.0 (2.6)
28.1 (1.4)§ 36.7 (2.9)
16.1 (1.1) 16.5 (2.1)
849 1351 105
39.3 (1.3) 60.7 (1.3)
42.3 (2.3) 41.5 (1.6)
29.8 (2.0) 29.6 (1.6)
16.2 (1.7) 16.3 (1.2)
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22.7 (2.6)§ 22.9 (2.2) 21.0 (2.7) 11.5 (2.1) 9.9 (1.8) 8.2 (1.7) 12.3 (4.7)
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Table 1 Continued Characteristics Stress level* Low High Missing Eating-out frequency Low (⬍1/day) High (ⱖ1/day) Missing Serum vitamin D deficiency ⬍20 ng/ml ⱖ20 ng/mL Serum vitamin D severe deficiency ⬍10 ng/mL ⱖ10 ng/mL
Unweighted Total No.
Weighted, % (SE)#
Healthy, % (SE)#
Atopy Only, % (SE)#
AR, % (SE)#
1632 576 97
72.2 (1.4) 27.8 (1.4)
43.1 (1.6) 38.3 (2.6)
29.1 (1.4) 31.3 (2.6)
15.0 (1.1)§ 19.6 (2.3)
1661 489 155
78.0 (1.2) 22.0 (1.2)
43.1 (1.5) 37.1 (3.0)
30.3 (1.5) 25.9 (2.1)
1585 720
68.8 (1.9) 31.2 (1.9)
42.0 (1.7) 40.2 (2.3)
27.9 (1.5)§ 34.6 (2.3)
16.4 (1.2) 15.9 (1.8)
167 2138
7.6 (1.0) 92.4 (1.0)
38.5 (4.8) 41.7 (1.3)
29.4 (4.7) 30.0 (1.2)
18.8 (3.7) 16.0 (1.0)
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14.8 (1.2)§ 21.3 (2.3)
*Subjects aged ⱖ12 yr. #Weighted for the multistage sampling design of the KNHANES. §p ⬍ 0.05 for the chi-square test of differences between subjects’ weighted prevalence (missing data not tested) across the characteristic categories. AR ⫽ allergic rhinitis; KNHANES ⫽ Korean National Health and Nutritional Examination Survey.
Dietary Intake The information of dietary intake was collected using a food frequency questionnaire, which is generally used in large-scale epidemiological studies.13–15 Fifty-eight foods were included as shown in Fig. 1. The frequency of food intake was rated on a 10-point scale and the median value was calculated. Then, the participants were divided into low (below median value) or high (median value or above) frequency.
Statistical Analysis
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RESULTS
Risk Factors and Comorbidities Table 2 shows adjusted ORs for associations between risk factors and each of atopy only and AR compared with the healthy group. The significant risk factors in multiple logistic regression analyses after adjusting for variables with p ⬍ 0.20 in univariate analyses were male gender (OR ⫽ 1.98; p ⬍ 0.001) for atopy only; male gender (OR ⫽ 1.63; p ⫽ 0.09), younger age (OR ⫽ 1.96; p ⫽ 0.02), single (OR ⫽ 1.61; p ⫽ 0.24), and high stress level (OR ⫽ 1.55; p ⫽ 0.31) for AR, compared with the healthy group. The weighted prevalence and OR of comorbidities in atopy only and AR groups relative to the healthy group are shown in Table 3. When compared with the healthy group, the OR of having asthma, nasal polyps (NPs), CRS, and olfactory dysfunction was 4.77, 3.44, 13.99, and 4.88 (p ⬍ 0.05), respectively for AR after adjustment for AR risk factors.
ARIA Classification
Demographic Characteristics Specific IgE level was available in a total of 2305 participants. Their mean age was 40.0 ⫾ 17.7 (10–83 years) years. The weighted charac-
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The KNHANES sampling weight variable was used along with a masked variance primary sampling unit and stratum variables. This adjustment allows for extrapolation from the samples to the noninstitutionalized civilian Korean population as a whole. The survey sample weights were used in all of the analyses. The subjects’ characteristics were summarized as unweighted number of observations and weighted percentages ⫾ SE for categorical variables. The weighted prevalence for atopy only, AR, and healthy was calculated in the Korean population after adjustment for strata and clustering at primary sampling unit level. The chi-square test was used to analyze the differences in the prevalence across the categories. Logistic regression models were created to identify risk factors independently associated with atopy only or AR compared with the healthy. Unadjusted odds ratios (ORs) and their 95% confidence intervals (CIs) were calculated. The multiple logistic regression analyses were performed including variables with values of p ⬍ 0.20 in the univariate analysis to estimate their adjusted ORs and CIs. The association between dietary intake and AR was also evaluated using the multiple logistic regression analyses. The prevalence of comorbidities was presented as weighted percentages ⫾ SE for each group. A binary logistic regression model was used to study the relationship between the presence of comorbidities and each group was compared with the healthy group. A value of p ⬍ 0.05 was considered as significant. Missing data were considered to be missing completely at random. The data were analyzed with SPSS (Version 18.0; SPSS, Inc., Chicago, IL).
teristics of the subjects are shown in Table 1. The weighted prevalence of atopy only and AR was 30.0 ⫾ 1.2% and 16.2 ⫾ 1.0%, respectively. AR prevalence was higher in the younger group than in the older group (p for trend, ⬍0.001). The significantly higher prevalence of atopy only was found in the following categories: male participants (p ⬍ 0.001), obese participants (p ⫽ 0.16), living in a detached house (p ⫽ 0.28), current and exsmoker (p for trend, 0.01), high urine cotinine level (p for trend, 0.01), frequent alcohol use (p ⫽ 0.07), and normal serum vitamin D level (p ⫽ 0.15). The significantly higher AR prevalence was found in the following categories: single (p ⬍ 0.001), high stress level (p ⫽ 0.49), and frequent eating out (p ⫽ 0.08). The prevalence of a healthy condition was significantly higher in women compared with men (Fig. 2 A) and that of atopy only was significantly higher in men than in women (Fig. 2 B). AR prevalence peaked at 25.4% in the 20- to 29-year age group in women, and it was highest at 25.3% in the 10- to 19-year age group in men. The prevalence decreased with age in both genders (test for trend, p ⫽ 0.11 in men; p ⫽ 0.13 in women). There was no significant gender difference in the AR prevalence (Fig. 2 C).
According to the ARIA guidelines, the weighted prevalence of intermittent mild, intermittent moderate/severe, persistent mild, and persistent moderate/severe AR were 58.1 ⫾ 3.2%, 18.0 ⫾ 3.0%, 9.1 ⫾ 1.7%, and 14.8 ⫾ 2.3%, respectively. Asthma prevalence was higher in
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Figure 2. Age and gender differences in prevalence of (A) healthy, (B) atopy only, and (C) allergic rhinitis (AR) groups. (A) The prevalence of a healthy condition was significantly higher in women compared with men and (B) that of atopy only was significantly higher in men than in women. (C) The prevalence of AR decreased with age in both genders (test for trend, p ⫽ 0.11 in men and p ⫽ 0.13 in women). There was no significant gender difference in the AR prevalence.
Risk Factors* Atopy only vs healthy Sex (male) Body mass index (ⱖ25) Marital status (single) Dwelling type (detached house) Occupation (white collar) Smoking status Never smoker Exsmoker Current smoker Current alcohol use (ⱖ2/wk) Serum Vitamin D deficiency (ⱖ20 ng/mL) AR vs healthy Sex (male) Age (younger, ⬍40 yr) Marital status (single) Family no., crowding (⬍3) Stress level (high) Eating-out frequency (ⱖ1/day)
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p Value#
Adjusted OR (95% CI)
⬍0.001 0.123 0.105 0.129 0.055 0.523
1.98 (1.46–2.71) 1.26 (0.94–1.69) 1.30 (0.95–1.77)
0.318 0.452
0.009 0.002 0.024 0.612 0.030 0.393
1.64 (1.13–2.36) 1.96 (1.30–2.96) 1.61 (1.07–2.44) 1.09 (0.78–1.53) 1.55 (1.05–2.30) 1.20 (0.79–1.80)
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*Risk factors with values of p ⬍ 0.20 in the univariate analysis. #The p values from multivariate analysis stratified by variables with values of p ⬍ 0.20 in the univariate analysis. AR ⫽ allergic rhinitis; OR ⫽ odds ratio; CI ⫽ confidence interval.
the subgroups with moderate/severe AR than in those with mild AR (p ⫽ 0.27). NP prevalence was higher in the subgroups with persistent AR than in those with intermittent AR (p ⫽ 0.13). On the contrary, atopic dermatitis prevalence was higher in the subgroups with intermittent AR than in those with persistent AR (p ⫽ 0.04). The odds of having CRS were significantly greater in all of the AR subgroups relative to the healthy group (p ⬍ 0.001; Table 4).
Dietary Intake Frequent intake of mackerel (OR ⫽ 0.63; CI, 0.43–0.92; p ⫽ 0.16) was significantly associated with reduced AR risk while frequent intake of carrots (OR ⫽ 2.01; CI, 1.01–1.43; p ⫽ 0.10), bread (OR ⫽ 2.68; CI, 1.14–1.75; p ⫽ 0.11), and bean curd (OR ⫽ 2.82; CI, 1.16–1.81; p ⫽ 0.42) were significantly associated with the increased risk of AR, after adjusting for risk factors (Fig. 1).
Our epidemiological research may be unique in several aspects. First, AR prevalence was calculated from a study including a representative sample of the entire Korean population based on laboratory tests and questionnaires. Second, this study investigated not only the proportions of ARIA subgroups, but the prevalence of comorbidities according to the guidelines and correlations between comorbidities and ARIA subgroups. Third, the present study evaluated the association between AR and dietary habits after adjusting for AR risk factors. None of the previous Asia-Pacific population-based studies have examined AR prevalence by using both allergen tests and symptoms. Although there was a study showing AR prevalence based on symptoms and allergen-specific IgE in Japan,16 subjects were not representative of the general population. Our KNHANES V-1 provided nationally representative data of serum allergen–specific IgE level and questionnaires. In addition, our study can be more professional because both the questionnaires and the ENT examinations were conducted by ENT residents who were trained and validated. The AR prevalence was higher than what was previously reported in South Korea. The difference might be explained by an actual increase of AR patients during the past 10 years as in the other countries of AsiaPacific area4 or by different diagnostic criteria and study population. The specific IgE positivity of 46.2% in our study is comparable with 44% in the U.S. population-based study of 2005–2006.11 Our study suggested that AR prevalence is influenced by risk factors such as male gender, younger age, single, and high stress levels. With regard to male predominance to AR, previous studies showed conflicting results.6,7,11 The other factors were consistent with previous studies that reported an age-dependent decrease in nasal allergic symptoms6,7,17 and exacerbation of allergy by psychological stress.18,19 As for the single individuals, they might be less organized in terms of cleanliness and own pets. The accumulation of dust and animal allergen might, in turn, result in a higher prevalence of AR. However, additional studies are needed to verify this assumption. In a population-based study conducted in six Western Europe countries,20 70% of AR patients had intermittent diseases. Although the study exhibited the proportion of ARIA subgroups, they only showed the persistency without severity. There have been a few studies identifying correlations between AR and comorbidities according to the ARIA guidelines.21–23 Even if they showed the relationships between AR and asthma prevalence, the study was not based on general population. In our study, more than one-half (58.1%) of the population had intermittent mild AR. This result was in accordance with previous findings from a population-based study in South Korea, although AR was diagnosed only by their symptoms without allergen tests.7 Other studies have shown that the most prevalent type of AR is persistent moderate/severe AR.24,25 We attribute this difference to the fact that their subjects were recruited from hospital visit-
T
1.26 (0.99–1.61) 1.00 (reference) 0.94 (0.63–1.42) 1.21 (0.79–1.85) 1.20 (0.84–1.71) 1.13 (0.83–1.53)
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DISCUSSION
Table 2 Adjusted ORs for the association between risk factors and atopy only and AR, compared with the healthy group
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Table 3 Prevalence and ORs of comorbidities in atopy only and AR compared with the healthy control
Asthma, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Atopic dermatitis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Tuberculosis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Septal deviation,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Purulent rhinorrhea,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# NP,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Chronic sinusitis*, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Middle ear effusion, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Olfactory dysfunction, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)#
Healthy
Atopy Only vs Healthy
AR vs Healthy
2.0 (0.6) 1.00 1.00 3.9 (0.8) 1.00 1.00 4.6 (1.0) 1.00 1.00 45.1 (2.4) 1.00 1.00 2.9 (0.8) 1.00 1.00 1.6 (0.5) 1.00 1.00 1.6 (0.5) 1.00 1.00 0.4 (0.2) 1.00 1.00 1.8 (0.5) 1.00 1.00
1.7 (0.5) 0.87 (0.42–1.80) 0.71 (0.31–1.62) 3.4 (0.8) 0.87 (0.48–1.58) 0.83 (0.46–1.49) 2.5 (0.7) 0.54 (0.26–1.15) 0.58 (0.28–1.19) 52.1 (2.4) 1.33 (1.04–1.70)§ 1.18 (0.91–1.53) 2.5 (0.7) 0.83 (0.41–1.70) 0.80 (0.35–1.85) 1.5 (0.5) 0.97 (0.41–2.28) 0.82 (0.32–2.06) 2.5 (0.8) 1.59 (0.68–3.75) 1.36 (0.54–3.40) 0.0 (0.0) — — 3.1 (0.8) 1.74 (0.76–3.95) 1.45 (0.56–3.78)
7.1 (1.6) 3.81 (1.74–8.33)§ 4.77 (1.92–11.82)§ 8.3 (1.7) 2.24 (1.30–3.86)§ 1.54 (0.87–2.72) 4.1 (1.4) 0.91 (0.38–2.14) 1.65 (0.64–4.25) 56.0 (3.7) 1.55 (1.14–2.12)§ 1.32 (0.94–1.86) 2.6 (1.1) 0.89 (0.32–2.47) 1.27 (0.42–3.88) 4.3 (1.4) 2.84 (1.19–6.79)§ 3.44 (1.29–9.17)§ 18.4 (2.6) 13.96 (7.06–27.59)§ 13.93 (6.69–29.01)§ 0.5 (0.3) 1.19 (0.20–7.01) — 7.2 (1.9) 4.28 (2.05–8.91)§ 4.88 (1.88–12.66)§
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*Subjects aged ⱖ12 yr. #Adjustment for sex, BMI, marital status, dwelling type, occupation, smoking status, current alcohol use, and serum vitamin D deficiency in atopy only/for sex, age, marital status, family no. (crowding), stress level, and eating-out frequency in AR. §p ⬍ 0.05 for the test (missing data not tested). AR ⫽ allergic rhinitis; BMI ⫽ body mass index; OR ⫽ odds ratio; NP ⫽ nasal polyp; CI ⫽ confidence interval.
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ing people, not from the general population. For this reason, there is a chance for a selection bias. Asthma prevalence was correlated to the severity of AR. This result is consistent with the previous data in France22 and supports that patients with severe rhinitis should be evaluated for asthma. On the other hand, atopic dermatitis and NP prevalence were correlated to the persistency of AR. Additional studies are needed to understand the mechanisms. There was no significant correlation between olfactory dysfunction and ARIA classification. In a previous study, olfactory dysfunction was found most commonly in persistent moderate/severe AR.24 Although there have been a few studies about relationship between nutrients or antioxidant-containing food and asthma,26–28 the literature relating food or dietary habits with AR is still limited. Furthermore, findings are still conflicting. Although there was a study showing the effects of dietary habits on AR,29 it was based on reports on children. Although there was a study about associations between nutrients and AR prevalence in a general population,30 only antioxidant nutrients such as carotenoids, tocopherols, and vitamin C were evaluated. Our data showed a positive correlation between intake of carrots containing -carotene and AR prevalence, but it is controversial for the relationship between -carotene and allergic diseases. -Carotene intake is associated with a higher prevalence of hay fever in a European cohort study,31 whereas other studies found an inverse association or no association.30,32,33 We found an inverse association between intake of mackerel containing ␣-tocopherol and AR. There was a study showing that atopic dermatitis was associated with reduced erythrocyte ␣-tocopherol concentrations,34 but other studies could not find any association between consumption of ␣-tocopherol and risk of having allergic diseases.30,35 In addition, a few authors
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reported that the Mediterranean diet containing high antioxidant contents such as fruits, vegetables, legumes, and nuts was protective for AR,28,36 whereas other studies showed no association.29 In our study, we could not find any association between consumption of fruits or vegetables and the risk of having AR. Our study also had several limitations. First, the present study was cross-sectional. Although the causal relationship of risk factors with atopy only and AR is inconclusive, the results may be reliable because this is a population-based study all around the country. Second, we tested only indoor allergens and included only three common allergens. However, there are some studies showing that these indoor allergens are predominant among Koreans.37,38 In a study including patients from Seoul, they reacted more commonly to indoor allergens, especially to dust mites and cockroaches in skin-prick tests.37 In addition, a previous study of Korean AR patients revealed that dust mites were the most common allergic sensitization with a positive reactivity of 70–80%.38 Although three indoor allergens were perennial allergens, many AR patients are sensitized to both perennial and seasonal allergens simultaneously in Korea.39 In addition, some patients sensitized to seasonal allergens have symptoms throughout the year and some patients sensitized to perennial allergens have symptoms during specific seasons.39 Interestingly, although all of the AR patients had perennial allergen sensitivities in our study, patients with intermittent symptoms (76.1%) had persistent symptoms much more than the other patients (23.9%). Third, there may be some response bias on reporting of several parameters such as smoking, stress level, and olfactory dysfunction, because the KNHANES was conducted by using self-administered questionnaires. Finally, there may be recall bias on reporting frequency of dietary intake, because
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Table 4 Prevalence and ORs of comorbidities in each ARIA group of AR patients compared with the healthy control
Asthma, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Atopic dermatitis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Tuberculosis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Septal deviation,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Purulent rhinorrhea,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# NP,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Chronic sinusitis,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Middle ear effusion, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Olfactory dysfunction, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)#
Healthy
Intermittent Mild vs Healthy
Intermittent Moderate/ Severe vs Healthy
2.0 (0.6) 1.00 1.00 3.9 (0.8) 1.00 1.00 4.6 (1.0) 1.00 1.00 45.1 (2.4) 1.00 1.00 2.9 (0.8) 1.00 1.00 1.6 (0.5) 1.00 1.00 1.6 (0.5) 1.00 1.00 0.4 (0.2) 1.00 1.00 1.8 (0.5) 1.00 1.00
4.6 (1.7) 2.40 (0.93–6.20) 2.82 (0.89–8.93) 9.9 (2.6) 2.72 (1.41–5.27)§ 2.05 (1.04–4.03)§ 2.5 (1.0) 0.53 (0.19–1.44) 0.94 (0.30–2.95) 53.4 (4.4) 1.40 (0.97–2.01) 1.18 (0.79–1.75) 3.6 (1.8) 1.22 (0.38–3.98) 1.64 (0.46–5.80) 2.3 (1.2) 1.51 (0.47–4.87) 2.24 (0.69–7.26) 6.8 (2.0) 4.55 (1.99–10.38)§ 5.85 (2.34–14.60)§ 0.3 (0.2) 0.75 (0.13–4.39) — 4.7 (1.7) 2.69 (1.03–7.03)§ 3.05 (1.06–8.75)§
12.7 (5.0) 7.19 (2.42–21.38)§ 8.76 (2.27–33.83)§ 11.3 (4.1) 3.15 (1.31–7.58)§ 2.45 (1.02–5.90)§ 4.5 (3.3) 0.99 (0.21–4.82) 1.86 (0.34–10.28) 58.0 (7.3) 1.68 (0.90–3.15) 1.34 (0.71–2.54) 0.0 (0.0) — — 0.8 (0.8) 0.50 (0.06–4.13) 0.98 (0.12–7.86) 19.9 (7.0) 15.38 (5.40–43.85)§ 17.92 (7.84–40.99)§ 1.6 (1.6) 4.21 (0.40–44.08) — 1.9 (1.4) 1.06 (0.21–5.29) 2.20 (0.41–11.75)
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Persistent Mild vs Healthy
Persistent Moderate/ Severe vs Healthy
0.0 (0.0) — — 4.4 (2.7) 1.13 (0.31–4.20) 1.22 (0.25–5.98) 11.0 (8.8) 2.59 (0.41–16.55) 2.35 (0.51–10.72) 75.8 (7.5) 3.82 (1.82–8.48)§ 3.14 (1.23–8.02)§ 1.1 (1.1) 0.37 (0.05–2.95) 0.49 (0.06–4.19) 11.0 (6.9) 7.85 (1.70–36.21)§ 13.57 (2.12–86.74)§ 20.6 (8.1) 16.15 (4.94–52.80)§ 21.28 (5.06–89.50)§ 0.0 (0.0) — — 8.0 (4.4) 4.76 (1.23–18.52)§ 4.33 (0.98–19.11)
11.5 (5.9) 6.43 (1.72–24.06)§ 7.14 (1.98–25.78)§ 0.9 (0.9) 0.22 (0.03–1.76) 0.18 (0.22–1.51) 6.2 (4.2) 1.38 (0.30–6.25) 1.65 (0.35–7.86) 51.9 (9.0) 1.32 (0.65–2.65) 1.00 (0.49–2.07) 3.2 (2.3) 1.08 (0.24–4.87) 1.34 (0.28–6.46) 12.3 (6.8) 8.92 (2.35–33.79)§ 13.17 (4.02–43.11)§ 60.0 (7.7) 92.96 (39.61–218.14)§ 147.88 (65.26–335.09)§ 0.0 (0.0) — — 23.4 (7.3) 16.77 (7.51–37.44)§ 30.95 (14.00–68.39)§
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*Subjects aged ⱖ12 yr. #Adjustment for sex, age, marital status, family member (crowding), stress level, and eating-out frequency. §p ⬍ 0.05 for the test (missing data not tested). AR ⫽ allergic rhinitis; ARIA ⫽ Allergic Rhinitis and Its Impact on Asthma; OR ⫽ odds ratio; NP ⫽ nasal polyp; CI ⫽ confidence interval.
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the information was retrospectively collected using a 24-hour recall method. Even if there are several shortcomings, the present study is the first population-based study to assess the levels of IgE specific to indoor allergens in the general Korean population. For further studies, a longitudinal design is needed to understand complex relationships between allergen exposures and development of allergic sensitization and diseases. In conclusion, KNHANES V-1 indicated that almost one-half of the population was sensitized to at least one indoor allergen and almost one-third of them had rhinitis symptoms. Risk factors such as sex, age, marital status, and stress level were associated with AR. Additional studies are needed to understand complex relationships between allergic disease and development of comorbidities. The general population–based study results on the prevalence, risk factors, and comorbidities of AR will contribute to prevention and treatment of AR and its comorbidities in the Korean population.
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ACKNOWLEDGMENTS
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The authors express their gratitude and appreciation to 87 residents of the Department of Otorhinolaryngology–Head and Neck Surgery from 45 training hospitals in South Korea and the members of the Korea Centers for Disease Control and Prevention who participated in this survey.
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REFERENCES 1.
Meltzer EO, Blaiss MS, Naclerio RM, et al. Burden of allergic rhinitis: Allergies in America, Latin America, and Asia-Pacific adult surveys. Allergy Asthma Proc 33(suppl 1):S113–S141, 2012.
10.
11.
Radon K, Gerhardinger U, Schulze A, et al.; Occupational Group of the ECRHS study. Occupation and adult onset of rhinitis in the general population. Occup Environ Med 65:38–43, 2008. Salo PM, Calatroni A, Gergen PJ, et al. Allergy-related outcomes in relation to serum IgE: Results from the National Health and Nutrition Examination Survey 2005–2006. J Allergy Clin Immunol 127:1226– 1235.e7, 2011. Katelaris CH, Lai CK, Rhee CS, et al. Nasal allergies in the AsianPacific population: Results from the Allergies in Asia-Pacific Survey. Am J Rhinol Allergy 25(suppl 1):S3–S15, 2011. Katelaris CH, Lee BW, Potter PC, et al. Prevalence and diversity of allergic rhinitis in regions of the world beyond Europe and North America. Clin Exp Allergy 42:186–207, 2012. Min YG, Jung HW, Kim HS, et al. Prevalence and risk factors for perennial allergic rhinitis in Korea: Results of a nationwide survey. Clin Otolaryngol Allied Sci 22:139–144, 1997. Cho YS, Choi SH, Park KH, et al. Prevalence of otolaryngologic diseases in South Korea: Data from the Korea national health and nutrition examination survey 2008. Clin Exp Otorhinolaryngol 3:183–193, 2010. Lee WH, Wee JH, Kim DK, et al. Prevalence of subjective olfactory dysfunction and its risk factors: Korean national health and nutrition examination survey. PLoS One 8:e62725, 2013. Haufroid V, and Lison D. Urinary cotinine as a tobacco-smoke exposure index: A minireview. Int Arch Occup Environ Health 71:162–168, 1998. Frieri M, and Valluri A. Vitamin D deficiency as a risk factor for allergic disorders and immune mechanisms. Allergy Asthma Proc 32:438–444, 2011. Hoppin JA, Jaramillo R, Salo P, et al. Questionnaire predictors of atopy in a US population sample: Findings from the National Health and Nutrition Examination Survey, 2005–2006. Am J Epidemiol 173: 544–552, 2011.
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12.
13.
14.
15. 16.
17.
18. 19.
20. 21.
22.
23.
24.
25.
Bachert C, van Cauwenberge P, and Khaltaev N; World Health Organization. Allergic Rhinitis and Its Impact on Asthma. In collaboration with the World Health Organization. Executive summary of the workshop report. 7–10 December 1999, Geneva, Switzerland. Allergy 57:841–855, 2002. Ahn Y, Kwon E, Shim JE, et al. Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. Eur J Clin Nutr 61:1435–1441, 2007. Na YJ, and Lee SH. Development and validation of a quantitative food frequency questionnaire to assess nutritional status in Korean adults. Nutr Res Pract 6:444–450, 2012. Lee JY, Jun N, and Baik I. Associations between dietary patterns and screen time among Korean adolescents. Nutr Res Pract 7:330–335, 2013. Sakashita M, Hirota T, Harada M, et al. Prevalence of allergic rhinitis and sensitization to common aeroallergens in a Japanese population. Int Arch Allergy Immunol 151:255–261, 2010. Singh K, Axelrod S, and Bielory L. The epidemiology of ocular and nasal allergy in the United States, 1988–1994. J Allergy Clin Immunol 126:778–783.e6, 2010. Mo¨sges R, and Klimek L. Today’s allergic rhinitis patients are different: New factors that may play a role. Allergy 62:969–975, 2007. Trueba AF, Rosenfield D, Oberdo¨rster E, et al. The effect of academic exam stress on mucosal and cellular airway immune markers among healthy and allergic individuals. Psychophysiology 50:5–14, 2013. Bauchau V, and Durham SR. Epidemiological characterization of the intermittent and persistent types of allergic rhinitis. Allergy 60:350–353, 2005. Antonicelli L, Micucci C, Voltolini S, et al. Allergic rhinitis and asthma comorbidity: ARIA classification of rhinitis does not correlate with the prevalence of asthma. Clin Exp Allergy 37:954–960, 2007. Bousquet J, Annesi-Maesano I, Carat F, et al. Characteristics of intermittent and persistent allergic rhinitis: DREAMS study group. Clin Exp Allergy 35:728–732, 2005. Bousquet J, Neukirch F, Bousquet PJ, et al. Severity and impairment of allergic rhinitis in patients consulting in primary care. J Allergy Clin Immunol 117:158–162, 2006. Lee CH, Jang JH, Lee HJ, et al. Clinical characteristics of allergic rhinitis according to Allergic Rhinitis and Its Impact on Asthma guidelines. Clin Exp Otorhinolaryngol 1:196–200, 2008. Bousquet PJ, Combescure C, Neukirch F, et al. Visual analog scales can assess the severity of rhinitis graded according to ARIA guidelines. Allergy 62:367–372, 2007.
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26. 27.
28. 29.
30.
31.
32.
33.
34.
35. 36.
Devereux G, and Seaton A. Diet as a risk factor for atopy and asthma. J Allergy Clin Immunol 115:1109–1117, 2005. Rosenkranz RR, Rosenkranz SK, and Neessen KJ. Dietary factors associated with lifetime asthma or hayfever diagnosis in Australian middle-aged and older adults: A cross-sectional study. Nutr J 11:84, 2012. Allan K, Kelly FJ, and Devereux G. Antioxidants and allergic disease: A case of too little or too much? Clin Exp Allergy 40:370–380, 2010. Tamay Z, Akcay A, Ergin A, and Guler N. Effects of dietary habits and risk factors on allergic rhinitis prevalence among Turkish adolescents. Int J Pediatr Otorhinolaryngol 77:1416–1423, 2013. Kompauer I, Heinrich J, Wolfram G, and Linseisen J. Association of carotenoids, tocopherols and vitamin C in plasma with allergic rhinitis and allergic sensitisation in adults. Public Health Nutr 9:472–479, 2006. Nagel G, Nieters A, Becker N, and Linseisen J. The influence of the dietary intake of fatty acids and antioxidants on hay fever in adults. Allergy 58:1277–1284, 2003. Oh SY, Chung J, Kim MK, et al. Antioxidant nutrient intakes and corresponding biomarkers associated with the risk of atopic dermatitis in young children. Eur J Clin Nutr 64:245–252, 2010. Allen S, Britton JR, and Leonardi-Bee JA. Association between antioxidant vitamins and asthma outcome measures: Systematic review and meta-analysis. Thorax 64:610–619, 2009. Hozyasz KK, Chełchowska M, Laskowska-Klita T, et al. Low concentration of alpha-tocopherol in erythrocytes of atopic dermatitis patients. Med Wieku Rozwoj 8:963–969, 2004. Rosenlund H, Magnusson J, Kull I, et al. Antioxidant intake and allergic disease in children. Clin Exp Allergy 42:1491–1500, 2012. Li J, Huang Y, Lin X, et al.; China Alliance of Research on Respiratory Allergic Disease (CARRAD). Factors associated with allergen sensitizations in patients with asthma and/or rhinitis in China. Am J Rhinol Allergy 26:85–91, 2012. Sener O, Kim YK, Ceylan S, et al. Comparison of skin tests to aeroallergens in Ankara and Seoul. J Investig Allergol Clin Immunol 13:202–208, 2003. Bang JH, Kim YJ, Shin HS, and Lee BJ. Clinical analysis of allergic rhinitis in Seoul. Korean J Rhinol 3:130–134, 1996. Chung YJ, Cho IK, Lee KI, et al. Seasonal specificity of seasonal allergens and validation of the ARIA classification in Korea. Allergy Asthma Immunol Res 5:75–80, 2013. e
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ABSTRACT
Background: There has been no nationwide epidemiological investigation of allergic rhinitis (AR) that was diagnosed by both questionnaires and laboratory tests in Korea. This study investigated the prevalence, risk factors, and comorbidities of AR in South Korea. Methods: The Korean National Health and Nutritional Examination Survey examined a representative sample of the Korean population. A total of 2305 participants underwent immunoradiometric assay for specific IgE antibodies against common indoor allergens. Healthy, atopy only, and AR groups were defined according to the results of allergen test. The weighted prevalence for each group was calculated. Risk factors including food and comorbidities were identified using univariate or multivariate analyses. The patients were also categorized into four subgroups according to the Allergic Rhinitis and Its Impact on Asthma (ARIA) classification and associated comorbidities were analyzed. Results: The prevalence of atopy only and AR was 30.0 ⫾ 1.2% and 16.2 ⫾ 1.0%, respectively. The multivariate analysis showed that the prevalence was influenced by sex (p ⬍ 0.01) for atopy only and sex (p ⫽ 0.09), age (p ⫽ 0.02), marital status (p ⫽ 0.24), and stress level (p ⫽ 0.30) for AR. Compared with the healthy group, asthma (odds ratio [OR] ⫽ 4.77), nasal polyp (NP; OR ⫽ 3.44), chronic rhinosinusitis (OR ⫽ 13.93), and olfactory dysfunction (OR ⫽ 4.88) were more prevalent in the AR group. Based on the ARIA guideline, intermittent mild rhinitis was most common (58.1%). Asthma was correlated to severity and atopic dermatitis and NPs was associated with persistency. Daily intake of less mackerel and more carrots, bread, and bean curd were associated with the increased risk of AR. Conclusion: Prevalence, risk factors, and comorbidities of AR were evaluated in the general Korean population, which will contribute to prevention and treatment of AR and its comorbidities in Koreans. (Am J Rhinol Allergy 28, e107–e114, 2014; doi: 10.2500/ajra.2014.28.4040)
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llergic rhinitis (AR) is a common chronic respiratory illness. Epidemiological studies have provided valuable information to develop its effective prevention and treatment of the disease.1 Large international studies, including the European Community Respiratory Health Survey, National Health and Nutrition Examination Survey (NHANES), and International Study of Asthma and Allergies of Childhood, have studied AR prevalence worldwide. The cumulative incidence of AR was 12% in the European Community Respiratory Health Survey II2 and the prevalence of current allergies was 23.5% of the general U.S. population in the NHANES 2005–2006.3 AR prevalence has varied from region to region, probably because of differences in the From the 1Department of Otorhinolaryngology–Head and Neck Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, South Korea, 2Medical Research Collaborating Center, Seoul National University Bundang Hospital, Seongnam, South Korea, 3Department of Otorhinolaryngology–Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, South Korea, 4Department of Otorhinolaryngology– Head and Neck Surgery, The Catholic University of Korea School of Medicine, Seoul, South Korea, 5Department of Otorhinolaryngology–Head and Neck Surgery, Kyung Hee University School of Medicine, Seoul, South Korea, 6Department of Otorhinolaryngology–Head and Neck Surgery, Yonsei University College of Medicine, Seoul, South Korea, and 7Division of Chronic Disease Surveillance, Korea Centers for Disease Control and Prevention, Chung Won, South Korea Presented and received the Young Scientist Award at the 20th World Congress of the International Federation of Otorhinolaryngological Societies (IFOS), Seoul, Korea, June 1–5, 2013 The authors have no conflicts of interest to declare pertaining to this article C-S Rhee and JH Wee contributed equally to this article Address correspondence to Jeong-Whun Kim, M.D., Ph.D., Department of Otorhinolaryngology–Head and Neck Surgery, Seoul National University College of Medicine , Seoul National University Bundang Hospital, 166, Kumiro, Bundang-gu, Seongnam 463-707, South Korea E-mail address: [email protected]; alternative: [email protected]; alternative: [email protected] Copyright © 2014, OceanSide Publications, Inc., U.S.A.
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subjects included and the diagnostic criteria used. In an Asia-Pacific Survey, the AR prevalence ranged from 2.5 to 13.2%.4 Although interand intraregional differences of the prevalence were investigated in the International Study of Asthma and Allergies of Childhood, the study samples were mainly children.5 Furthermore, most studies were based on questionnaires or clinical diagnosis and focused on the relationship between AR and asthma. There have been few studies for the prevalence and risk factors of AR in the general population of South Korea. The first epidemiological study on AR based on a nationwide survey was reported in 1991,6 which included questionnaires and nasal examinations, and perennial AR prevalence was 1.14%. Recently, a nationwide study reported that its prevalence was 28.01% in 2008, diagnosed only by nasal symptoms without an allergen test.7 The Korean NHANES (KNHANES), which is a government-driven survey of the Korea Center for Disease Control and Prevention, has been conducted since 1998. The Korean Society of Otorhinolaryngology– Head and Neck Surgery (KORL) participated in this project and interviews and examinations were performed by trained ear, nose, and throat (ENT) residents. KNHANES V-1 (2010) was the first population-based study to assess specific IgE to major perennial allergens in the noninstitutionalized civilian population of South Korea. The aim of this study was to analyze the prevalence of AR and its risk factors including food and laboratory test results, using KNHANES V-1 data. In addition, its association with comorbidities was also evaluated based on the Allergic Rhinitis and Its Impact on Asthma (ARIA) criteria in South Korea.
METHODS Study Population and Data Collection We used data from KNHANES V-1, which was conducted in 2010. The survey was performed using a rolling sampling design that involves a complex, stratified, multistage, probability cluster survey
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of a representative sample of the noninstitutionalized civilian population of South Korea. A total of 192 sampling units were randomly selected from primary sampling units encompassing the target population with 20 households per sampling unit, including a total of 3840 households. The KNHANES was conducted by four survey teams consisting of three components: a health interview, a nutrition interview, and health examination. Each survey team had one ENT resident, one ophthalmologist, one dentist, one radiologist, two interviewers, three nurses, and one coordinator. Each team moved in a mobile examination vehicle and performed surveys for 4 consecutive days per sampling unit. All participants provided written consents. This study was approved by the Institutional Review Board of Seoul National University Bundang Hospital.
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Demographic Characteristics The questionnaires were administered by the physicians or interviewers face to face. All data have been converted to appropriate categories for analysis. Age was stratified into seven subgroups and then categorized into younger (⬍30–39 years old) and older (⬎40–49 years old) age groups. Body mass index was categorized into normal (⬍25 kg/m2) or obese (ⱖ25 kg/m2). The socioeconomic status (residency, household income, education, and occupation) was categorized as previously described.8 Marital status was divided into single or married. The number of family members (crowding) was divided into two groups: three or less or four or more family members. The type of dwelling was categorized into detached houses or apartments. Smoking status was classified into never smoker (persons who have never smoked), exsmoker (persons who smoked in the past but do not smoke currently), and current smoker (persons who smoke currently). The urine cotinine level was used as a marker of exposure to smoking and was categorized by the following criteria: ⬍20 ng/mL, “nonsmoker”; 20–100 ng/mL, “passive smoker”; and ⬎100 ng/mL, “active smoker”.9 Current alcohol use was assessed by questioning the participants about their average frequency per week of alcohol consumption during the month before their interview. Sleep time was divided into two categories by the mean value: under mean, mean, or more. Stress level assessed by questionnaire was categorized into low (none or small amount) or high (some or extreme). Eating out frequency was rated on a seven-point scale and classified into low (less than once a day) or high (once a day or more). Serum vitamin D of ⬍20 ng/mL was defined as vitamin D deficiency and ⬍10 ng/mL as severe deficiency.10
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Evaluation of ENT Findings and Comorbidities A total of 87 ENT residents from 45 training hospitals were recruited and trained for this survey. The Epidemiologic Survey Committee of the KORL verified the quality control of the survey. Endoscopic examinations were performed according to standardized protocols. Chronic rhinosinusitis (CRS), septal deviation, and olfactory loss were defined as previously described.8 Asthma, atopic dermatitis, and tuberculosis were defined as a self-reported physician’s diagnosis.
Diagnosis of AR
Participants were interviewed for their nasal symptoms by ENT residents and underwent blood tests for allergen-specific IgE. The allergen test was performed for the subjects aged ⱖ10 years old. Serum samples were analyzed using an immunoradiometric assay (ImmunoCAP 100, Phadia, Sweden). Three common indoor allergens such as Dermatophagoides farinae, cockroach, and dog were tested. Atopy was defined as being positive for at least one specific IgE.11 The detection limit was 0.35 kU/L. AR was defined as being atopic and reporting at least one subjective allergic symptom such as sneezing, watery rhinorrhea, nasal obstruction, and itching without fever
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Figure 1. Adjusted odds ratios (ORs; 95% confidence intervals [CIs]) for the association between dietary intake and allergic rhinitis (AR), compared with the healthy group. The multiple regression models are adjusted for sex, age, marital status, the number of family members, stress level, and eatingout frequency.
or sore throat within the last year. The participants without atopy and allergic symptoms were defined as healthy. According to the ARIA guidelines,12 AR was categorized into intermittent mild, intermittent moderate/severe, persistent mild, and persistent moderate/severe.
March–April 2014, Vol. 28, No. 2
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Table 1 The prevalence of healthy, atopy only, and AR and characteristics among the KNHANES 2010 population aged >10 yr Characteristics Overall Sex Male Female Age, yr 10–19 20–29 30–39 40–49 50–59 60–69 ⱖ 70 Body mass index Normal(⬍25 kg/m2) Obese (ⱖ25 kg/m2) Missing Residency Rural Urban Marital status Single Married Missing Family no. (crowding) ⱕ3 ⱖ4 Dwelling type Detached house Apartment Missing Quartile of household income Low, midlow Midhigh, high Missing Educational level Low High Missing Occupation White collar Blue collar Missing Smoking status Never smoker Exsmoker Current smoker Missing Urine cotinine Nonsmoker Passive smoker Active smoker Missing Current alcohol use ⬍2/wk ⱖ2/wk Missing Sleep time* Under mean Mean or more Missing
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Unweighted Total No.
Weighted, % (SE)#
2305
Healthy, % (SE)#
Atopy Only, % (SE)#
AR, % (SE)#
41.4 (1.3)
30.0 (1.2)
16.2 (1.0) 17.5 (1.5) 14.9 (1.4)
1140 1165
50.0 (0.8) 50.0 (0.8)
34.4 (1.6)§ 48.6 (2.0)
36.7 (1.8)§ 23.2 (1.6)
394 360 381 390 396 327 57
15.2 (0.7) 15.4 (0.9) 18.0 (0.9) 19.1 (0.7) 15.2 (0.7) 9.0 (0.6) 7.9 (1.2)
34.4 (3.1)§ 33.6 (2.8) 36.9 (3.1) 48.6 (2.7) 47.1 (3.1) 50.8 (3.6) 41.9 (7.3)
29.5 (3.2) 30.5 (2.9) 26.4 (2.4) 30.1 (2.6) 31.8 (2.8) 33.8 (3.9) 29.7 (7.2)
1641 659 5
69.7 (1.3) 30.3 (1.3)
41.4 (1.6) 41.7 (2.6)
27.9 (1.3)§ 34.4 (2.5)
17.2 (1.2) 14.1 (1.8)
1226 1079
54.7 (2.3) 45.3 (2.3)
42.3 (1.7) 40.4 (2.0)
30.6 (1.6) 29.2 (1.8)
15.1 (1.5) 17.6 (1.3)
766 1537 2
32.6 (1.2) 67.4 (1.2)
33.8 (2.1)§ 45.2 (1.6)
29.8 (1.9) 30.1 (1.6)
23.9 (1.8)§ 12.4 (1.3)
1135 1170
46.4 (1.6) 53.6 (1.6)
41.5 (2.0) 41.4 (1.6)
31.3 (2.0) 28.8 (1.5)
14.2 (1.5) 18.0 (1.3)
850 1447 8
47.8 (2.7) 52.2 (2.7)
40.1 (2.1) 42.9 (1.7)
32.7 (2.0)§ 27.4 (1.4)
15.4 (1.6) 16.7 (1.4)
971 1306 28
46.4 (1.7) 53.6 (1.7)
40.2 (2.0) 42.7 (1.7)
31.4 (2.0) 28.5 (1.5)
16.3 (1.6) 16.4 (1.2)
904 1384 17
39.3 (1.4) 60.7 (1.4)
43.2 (2.0) 40.4 (1.6)
29.6 (2.1) 30.0 (1.5)
15.1 (1.8) 17.0 (1.1)
1532 746 27
68.1 (1.3) 31.9 (1.3)
39.7 (1.5) 45.4 (2.1)§
30.8 (1.6) 27.7 (1.7)
16.1 (1.2) 16.7 (1.6)
1378 409 507 11
58.1 (1.0) 17.4 (1.0) 24.6 (1.0)
45.1 (1.8)§ 40.1 (2.6) 34.3 (3.0)
25.8 (1.5)§ 31.2 (2.9) 38.1 (3.0)
15.8 (1.3) 18.2 (2.8) 15.8 (2.0)
1478 163 540 124
63.8 (1.5) 8.7 (0.9) 27.5 (1.2)
44.8 (1.6)§ 39.7 (4.3) 33.9 (2.7)
27.6 (1.5)§ 27.2 (4.4) 38.8 (2.8)
16.1 (1.4) 17.3 (4.2) 15.6 (1.8)
1842 437 26
79.5 (0.9) 20.5 (2.1)
43.0 (1.5) 37.0 (2.6)
28.1 (1.4)§ 36.7 (2.9)
16.1 (1.1) 16.5 (2.1)
849 1351 105
39.3 (1.3) 60.7 (1.3)
42.3 (2.3) 41.5 (1.6)
29.8 (2.0) 29.6 (1.6)
16.2 (1.7) 16.3 (1.2)
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American Journal of Rhinology & Allergy
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22.7 (2.6)§ 22.9 (2.2) 21.0 (2.7) 11.5 (2.1) 9.9 (1.8) 8.2 (1.7) 12.3 (4.7)
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Table 1 Continued Characteristics Stress level* Low High Missing Eating-out frequency Low (⬍1/day) High (ⱖ1/day) Missing Serum vitamin D deficiency ⬍20 ng/ml ⱖ20 ng/mL Serum vitamin D severe deficiency ⬍10 ng/mL ⱖ10 ng/mL
Unweighted Total No.
Weighted, % (SE)#
Healthy, % (SE)#
Atopy Only, % (SE)#
AR, % (SE)#
1632 576 97
72.2 (1.4) 27.8 (1.4)
43.1 (1.6) 38.3 (2.6)
29.1 (1.4) 31.3 (2.6)
15.0 (1.1)§ 19.6 (2.3)
1661 489 155
78.0 (1.2) 22.0 (1.2)
43.1 (1.5) 37.1 (3.0)
30.3 (1.5) 25.9 (2.1)
1585 720
68.8 (1.9) 31.2 (1.9)
42.0 (1.7) 40.2 (2.3)
27.9 (1.5)§ 34.6 (2.3)
16.4 (1.2) 15.9 (1.8)
167 2138
7.6 (1.0) 92.4 (1.0)
38.5 (4.8) 41.7 (1.3)
29.4 (4.7) 30.0 (1.2)
18.8 (3.7) 16.0 (1.0)
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14.8 (1.2)§ 21.3 (2.3)
*Subjects aged ⱖ12 yr. #Weighted for the multistage sampling design of the KNHANES. §p ⬍ 0.05 for the chi-square test of differences between subjects’ weighted prevalence (missing data not tested) across the characteristic categories. AR ⫽ allergic rhinitis; KNHANES ⫽ Korean National Health and Nutritional Examination Survey.
Dietary Intake The information of dietary intake was collected using a food frequency questionnaire, which is generally used in large-scale epidemiological studies.13–15 Fifty-eight foods were included as shown in Fig. 1. The frequency of food intake was rated on a 10-point scale and the median value was calculated. Then, the participants were divided into low (below median value) or high (median value or above) frequency.
Statistical Analysis
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RESULTS
Risk Factors and Comorbidities Table 2 shows adjusted ORs for associations between risk factors and each of atopy only and AR compared with the healthy group. The significant risk factors in multiple logistic regression analyses after adjusting for variables with p ⬍ 0.20 in univariate analyses were male gender (OR ⫽ 1.98; p ⬍ 0.001) for atopy only; male gender (OR ⫽ 1.63; p ⫽ 0.09), younger age (OR ⫽ 1.96; p ⫽ 0.02), single (OR ⫽ 1.61; p ⫽ 0.24), and high stress level (OR ⫽ 1.55; p ⫽ 0.31) for AR, compared with the healthy group. The weighted prevalence and OR of comorbidities in atopy only and AR groups relative to the healthy group are shown in Table 3. When compared with the healthy group, the OR of having asthma, nasal polyps (NPs), CRS, and olfactory dysfunction was 4.77, 3.44, 13.99, and 4.88 (p ⬍ 0.05), respectively for AR after adjustment for AR risk factors.
ARIA Classification
Demographic Characteristics Specific IgE level was available in a total of 2305 participants. Their mean age was 40.0 ⫾ 17.7 (10–83 years) years. The weighted charac-
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The KNHANES sampling weight variable was used along with a masked variance primary sampling unit and stratum variables. This adjustment allows for extrapolation from the samples to the noninstitutionalized civilian Korean population as a whole. The survey sample weights were used in all of the analyses. The subjects’ characteristics were summarized as unweighted number of observations and weighted percentages ⫾ SE for categorical variables. The weighted prevalence for atopy only, AR, and healthy was calculated in the Korean population after adjustment for strata and clustering at primary sampling unit level. The chi-square test was used to analyze the differences in the prevalence across the categories. Logistic regression models were created to identify risk factors independently associated with atopy only or AR compared with the healthy. Unadjusted odds ratios (ORs) and their 95% confidence intervals (CIs) were calculated. The multiple logistic regression analyses were performed including variables with values of p ⬍ 0.20 in the univariate analysis to estimate their adjusted ORs and CIs. The association between dietary intake and AR was also evaluated using the multiple logistic regression analyses. The prevalence of comorbidities was presented as weighted percentages ⫾ SE for each group. A binary logistic regression model was used to study the relationship between the presence of comorbidities and each group was compared with the healthy group. A value of p ⬍ 0.05 was considered as significant. Missing data were considered to be missing completely at random. The data were analyzed with SPSS (Version 18.0; SPSS, Inc., Chicago, IL).
teristics of the subjects are shown in Table 1. The weighted prevalence of atopy only and AR was 30.0 ⫾ 1.2% and 16.2 ⫾ 1.0%, respectively. AR prevalence was higher in the younger group than in the older group (p for trend, ⬍0.001). The significantly higher prevalence of atopy only was found in the following categories: male participants (p ⬍ 0.001), obese participants (p ⫽ 0.16), living in a detached house (p ⫽ 0.28), current and exsmoker (p for trend, 0.01), high urine cotinine level (p for trend, 0.01), frequent alcohol use (p ⫽ 0.07), and normal serum vitamin D level (p ⫽ 0.15). The significantly higher AR prevalence was found in the following categories: single (p ⬍ 0.001), high stress level (p ⫽ 0.49), and frequent eating out (p ⫽ 0.08). The prevalence of a healthy condition was significantly higher in women compared with men (Fig. 2 A) and that of atopy only was significantly higher in men than in women (Fig. 2 B). AR prevalence peaked at 25.4% in the 20- to 29-year age group in women, and it was highest at 25.3% in the 10- to 19-year age group in men. The prevalence decreased with age in both genders (test for trend, p ⫽ 0.11 in men; p ⫽ 0.13 in women). There was no significant gender difference in the AR prevalence (Fig. 2 C).
According to the ARIA guidelines, the weighted prevalence of intermittent mild, intermittent moderate/severe, persistent mild, and persistent moderate/severe AR were 58.1 ⫾ 3.2%, 18.0 ⫾ 3.0%, 9.1 ⫾ 1.7%, and 14.8 ⫾ 2.3%, respectively. Asthma prevalence was higher in
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Figure 2. Age and gender differences in prevalence of (A) healthy, (B) atopy only, and (C) allergic rhinitis (AR) groups. (A) The prevalence of a healthy condition was significantly higher in women compared with men and (B) that of atopy only was significantly higher in men than in women. (C) The prevalence of AR decreased with age in both genders (test for trend, p ⫽ 0.11 in men and p ⫽ 0.13 in women). There was no significant gender difference in the AR prevalence.
Risk Factors* Atopy only vs healthy Sex (male) Body mass index (ⱖ25) Marital status (single) Dwelling type (detached house) Occupation (white collar) Smoking status Never smoker Exsmoker Current smoker Current alcohol use (ⱖ2/wk) Serum Vitamin D deficiency (ⱖ20 ng/mL) AR vs healthy Sex (male) Age (younger, ⬍40 yr) Marital status (single) Family no., crowding (⬍3) Stress level (high) Eating-out frequency (ⱖ1/day)
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p Value#
Adjusted OR (95% CI)
⬍0.001 0.123 0.105 0.129 0.055 0.523
1.98 (1.46–2.71) 1.26 (0.94–1.69) 1.30 (0.95–1.77)
0.318 0.452
0.009 0.002 0.024 0.612 0.030 0.393
1.64 (1.13–2.36) 1.96 (1.30–2.96) 1.61 (1.07–2.44) 1.09 (0.78–1.53) 1.55 (1.05–2.30) 1.20 (0.79–1.80)
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*Risk factors with values of p ⬍ 0.20 in the univariate analysis. #The p values from multivariate analysis stratified by variables with values of p ⬍ 0.20 in the univariate analysis. AR ⫽ allergic rhinitis; OR ⫽ odds ratio; CI ⫽ confidence interval.
the subgroups with moderate/severe AR than in those with mild AR (p ⫽ 0.27). NP prevalence was higher in the subgroups with persistent AR than in those with intermittent AR (p ⫽ 0.13). On the contrary, atopic dermatitis prevalence was higher in the subgroups with intermittent AR than in those with persistent AR (p ⫽ 0.04). The odds of having CRS were significantly greater in all of the AR subgroups relative to the healthy group (p ⬍ 0.001; Table 4).
Dietary Intake Frequent intake of mackerel (OR ⫽ 0.63; CI, 0.43–0.92; p ⫽ 0.16) was significantly associated with reduced AR risk while frequent intake of carrots (OR ⫽ 2.01; CI, 1.01–1.43; p ⫽ 0.10), bread (OR ⫽ 2.68; CI, 1.14–1.75; p ⫽ 0.11), and bean curd (OR ⫽ 2.82; CI, 1.16–1.81; p ⫽ 0.42) were significantly associated with the increased risk of AR, after adjusting for risk factors (Fig. 1).
Our epidemiological research may be unique in several aspects. First, AR prevalence was calculated from a study including a representative sample of the entire Korean population based on laboratory tests and questionnaires. Second, this study investigated not only the proportions of ARIA subgroups, but the prevalence of comorbidities according to the guidelines and correlations between comorbidities and ARIA subgroups. Third, the present study evaluated the association between AR and dietary habits after adjusting for AR risk factors. None of the previous Asia-Pacific population-based studies have examined AR prevalence by using both allergen tests and symptoms. Although there was a study showing AR prevalence based on symptoms and allergen-specific IgE in Japan,16 subjects were not representative of the general population. Our KNHANES V-1 provided nationally representative data of serum allergen–specific IgE level and questionnaires. In addition, our study can be more professional because both the questionnaires and the ENT examinations were conducted by ENT residents who were trained and validated. The AR prevalence was higher than what was previously reported in South Korea. The difference might be explained by an actual increase of AR patients during the past 10 years as in the other countries of AsiaPacific area4 or by different diagnostic criteria and study population. The specific IgE positivity of 46.2% in our study is comparable with 44% in the U.S. population-based study of 2005–2006.11 Our study suggested that AR prevalence is influenced by risk factors such as male gender, younger age, single, and high stress levels. With regard to male predominance to AR, previous studies showed conflicting results.6,7,11 The other factors were consistent with previous studies that reported an age-dependent decrease in nasal allergic symptoms6,7,17 and exacerbation of allergy by psychological stress.18,19 As for the single individuals, they might be less organized in terms of cleanliness and own pets. The accumulation of dust and animal allergen might, in turn, result in a higher prevalence of AR. However, additional studies are needed to verify this assumption. In a population-based study conducted in six Western Europe countries,20 70% of AR patients had intermittent diseases. Although the study exhibited the proportion of ARIA subgroups, they only showed the persistency without severity. There have been a few studies identifying correlations between AR and comorbidities according to the ARIA guidelines.21–23 Even if they showed the relationships between AR and asthma prevalence, the study was not based on general population. In our study, more than one-half (58.1%) of the population had intermittent mild AR. This result was in accordance with previous findings from a population-based study in South Korea, although AR was diagnosed only by their symptoms without allergen tests.7 Other studies have shown that the most prevalent type of AR is persistent moderate/severe AR.24,25 We attribute this difference to the fact that their subjects were recruited from hospital visit-
T
1.26 (0.99–1.61) 1.00 (reference) 0.94 (0.63–1.42) 1.21 (0.79–1.85) 1.20 (0.84–1.71) 1.13 (0.83–1.53)
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DISCUSSION
Table 2 Adjusted ORs for the association between risk factors and atopy only and AR, compared with the healthy group
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Table 3 Prevalence and ORs of comorbidities in atopy only and AR compared with the healthy control
Asthma, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Atopic dermatitis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Tuberculosis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Septal deviation,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Purulent rhinorrhea,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# NP,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Chronic sinusitis*, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Middle ear effusion, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Olfactory dysfunction, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)#
Healthy
Atopy Only vs Healthy
AR vs Healthy
2.0 (0.6) 1.00 1.00 3.9 (0.8) 1.00 1.00 4.6 (1.0) 1.00 1.00 45.1 (2.4) 1.00 1.00 2.9 (0.8) 1.00 1.00 1.6 (0.5) 1.00 1.00 1.6 (0.5) 1.00 1.00 0.4 (0.2) 1.00 1.00 1.8 (0.5) 1.00 1.00
1.7 (0.5) 0.87 (0.42–1.80) 0.71 (0.31–1.62) 3.4 (0.8) 0.87 (0.48–1.58) 0.83 (0.46–1.49) 2.5 (0.7) 0.54 (0.26–1.15) 0.58 (0.28–1.19) 52.1 (2.4) 1.33 (1.04–1.70)§ 1.18 (0.91–1.53) 2.5 (0.7) 0.83 (0.41–1.70) 0.80 (0.35–1.85) 1.5 (0.5) 0.97 (0.41–2.28) 0.82 (0.32–2.06) 2.5 (0.8) 1.59 (0.68–3.75) 1.36 (0.54–3.40) 0.0 (0.0) — — 3.1 (0.8) 1.74 (0.76–3.95) 1.45 (0.56–3.78)
7.1 (1.6) 3.81 (1.74–8.33)§ 4.77 (1.92–11.82)§ 8.3 (1.7) 2.24 (1.30–3.86)§ 1.54 (0.87–2.72) 4.1 (1.4) 0.91 (0.38–2.14) 1.65 (0.64–4.25) 56.0 (3.7) 1.55 (1.14–2.12)§ 1.32 (0.94–1.86) 2.6 (1.1) 0.89 (0.32–2.47) 1.27 (0.42–3.88) 4.3 (1.4) 2.84 (1.19–6.79)§ 3.44 (1.29–9.17)§ 18.4 (2.6) 13.96 (7.06–27.59)§ 13.93 (6.69–29.01)§ 0.5 (0.3) 1.19 (0.20–7.01) — 7.2 (1.9) 4.28 (2.05–8.91)§ 4.88 (1.88–12.66)§
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*Subjects aged ⱖ12 yr. #Adjustment for sex, BMI, marital status, dwelling type, occupation, smoking status, current alcohol use, and serum vitamin D deficiency in atopy only/for sex, age, marital status, family no. (crowding), stress level, and eating-out frequency in AR. §p ⬍ 0.05 for the test (missing data not tested). AR ⫽ allergic rhinitis; BMI ⫽ body mass index; OR ⫽ odds ratio; NP ⫽ nasal polyp; CI ⫽ confidence interval.
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ing people, not from the general population. For this reason, there is a chance for a selection bias. Asthma prevalence was correlated to the severity of AR. This result is consistent with the previous data in France22 and supports that patients with severe rhinitis should be evaluated for asthma. On the other hand, atopic dermatitis and NP prevalence were correlated to the persistency of AR. Additional studies are needed to understand the mechanisms. There was no significant correlation between olfactory dysfunction and ARIA classification. In a previous study, olfactory dysfunction was found most commonly in persistent moderate/severe AR.24 Although there have been a few studies about relationship between nutrients or antioxidant-containing food and asthma,26–28 the literature relating food or dietary habits with AR is still limited. Furthermore, findings are still conflicting. Although there was a study showing the effects of dietary habits on AR,29 it was based on reports on children. Although there was a study about associations between nutrients and AR prevalence in a general population,30 only antioxidant nutrients such as carotenoids, tocopherols, and vitamin C were evaluated. Our data showed a positive correlation between intake of carrots containing -carotene and AR prevalence, but it is controversial for the relationship between -carotene and allergic diseases. -Carotene intake is associated with a higher prevalence of hay fever in a European cohort study,31 whereas other studies found an inverse association or no association.30,32,33 We found an inverse association between intake of mackerel containing ␣-tocopherol and AR. There was a study showing that atopic dermatitis was associated with reduced erythrocyte ␣-tocopherol concentrations,34 but other studies could not find any association between consumption of ␣-tocopherol and risk of having allergic diseases.30,35 In addition, a few authors
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reported that the Mediterranean diet containing high antioxidant contents such as fruits, vegetables, legumes, and nuts was protective for AR,28,36 whereas other studies showed no association.29 In our study, we could not find any association between consumption of fruits or vegetables and the risk of having AR. Our study also had several limitations. First, the present study was cross-sectional. Although the causal relationship of risk factors with atopy only and AR is inconclusive, the results may be reliable because this is a population-based study all around the country. Second, we tested only indoor allergens and included only three common allergens. However, there are some studies showing that these indoor allergens are predominant among Koreans.37,38 In a study including patients from Seoul, they reacted more commonly to indoor allergens, especially to dust mites and cockroaches in skin-prick tests.37 In addition, a previous study of Korean AR patients revealed that dust mites were the most common allergic sensitization with a positive reactivity of 70–80%.38 Although three indoor allergens were perennial allergens, many AR patients are sensitized to both perennial and seasonal allergens simultaneously in Korea.39 In addition, some patients sensitized to seasonal allergens have symptoms throughout the year and some patients sensitized to perennial allergens have symptoms during specific seasons.39 Interestingly, although all of the AR patients had perennial allergen sensitivities in our study, patients with intermittent symptoms (76.1%) had persistent symptoms much more than the other patients (23.9%). Third, there may be some response bias on reporting of several parameters such as smoking, stress level, and olfactory dysfunction, because the KNHANES was conducted by using self-administered questionnaires. Finally, there may be recall bias on reporting frequency of dietary intake, because
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Table 4 Prevalence and ORs of comorbidities in each ARIA group of AR patients compared with the healthy control
Asthma, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Atopic dermatitis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Tuberculosis, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Septal deviation,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Purulent rhinorrhea,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# NP,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Chronic sinusitis,* % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Middle ear effusion, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)# Olfactory dysfunction, % (SE) Unadjusted OR (95% CI) Adjusted OR (95% CI)#
Healthy
Intermittent Mild vs Healthy
Intermittent Moderate/ Severe vs Healthy
2.0 (0.6) 1.00 1.00 3.9 (0.8) 1.00 1.00 4.6 (1.0) 1.00 1.00 45.1 (2.4) 1.00 1.00 2.9 (0.8) 1.00 1.00 1.6 (0.5) 1.00 1.00 1.6 (0.5) 1.00 1.00 0.4 (0.2) 1.00 1.00 1.8 (0.5) 1.00 1.00
4.6 (1.7) 2.40 (0.93–6.20) 2.82 (0.89–8.93) 9.9 (2.6) 2.72 (1.41–5.27)§ 2.05 (1.04–4.03)§ 2.5 (1.0) 0.53 (0.19–1.44) 0.94 (0.30–2.95) 53.4 (4.4) 1.40 (0.97–2.01) 1.18 (0.79–1.75) 3.6 (1.8) 1.22 (0.38–3.98) 1.64 (0.46–5.80) 2.3 (1.2) 1.51 (0.47–4.87) 2.24 (0.69–7.26) 6.8 (2.0) 4.55 (1.99–10.38)§ 5.85 (2.34–14.60)§ 0.3 (0.2) 0.75 (0.13–4.39) — 4.7 (1.7) 2.69 (1.03–7.03)§ 3.05 (1.06–8.75)§
12.7 (5.0) 7.19 (2.42–21.38)§ 8.76 (2.27–33.83)§ 11.3 (4.1) 3.15 (1.31–7.58)§ 2.45 (1.02–5.90)§ 4.5 (3.3) 0.99 (0.21–4.82) 1.86 (0.34–10.28) 58.0 (7.3) 1.68 (0.90–3.15) 1.34 (0.71–2.54) 0.0 (0.0) — — 0.8 (0.8) 0.50 (0.06–4.13) 0.98 (0.12–7.86) 19.9 (7.0) 15.38 (5.40–43.85)§ 17.92 (7.84–40.99)§ 1.6 (1.6) 4.21 (0.40–44.08) — 1.9 (1.4) 1.06 (0.21–5.29) 2.20 (0.41–11.75)
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Persistent Mild vs Healthy
Persistent Moderate/ Severe vs Healthy
0.0 (0.0) — — 4.4 (2.7) 1.13 (0.31–4.20) 1.22 (0.25–5.98) 11.0 (8.8) 2.59 (0.41–16.55) 2.35 (0.51–10.72) 75.8 (7.5) 3.82 (1.82–8.48)§ 3.14 (1.23–8.02)§ 1.1 (1.1) 0.37 (0.05–2.95) 0.49 (0.06–4.19) 11.0 (6.9) 7.85 (1.70–36.21)§ 13.57 (2.12–86.74)§ 20.6 (8.1) 16.15 (4.94–52.80)§ 21.28 (5.06–89.50)§ 0.0 (0.0) — — 8.0 (4.4) 4.76 (1.23–18.52)§ 4.33 (0.98–19.11)
11.5 (5.9) 6.43 (1.72–24.06)§ 7.14 (1.98–25.78)§ 0.9 (0.9) 0.22 (0.03–1.76) 0.18 (0.22–1.51) 6.2 (4.2) 1.38 (0.30–6.25) 1.65 (0.35–7.86) 51.9 (9.0) 1.32 (0.65–2.65) 1.00 (0.49–2.07) 3.2 (2.3) 1.08 (0.24–4.87) 1.34 (0.28–6.46) 12.3 (6.8) 8.92 (2.35–33.79)§ 13.17 (4.02–43.11)§ 60.0 (7.7) 92.96 (39.61–218.14)§ 147.88 (65.26–335.09)§ 0.0 (0.0) — — 23.4 (7.3) 16.77 (7.51–37.44)§ 30.95 (14.00–68.39)§
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*Subjects aged ⱖ12 yr. #Adjustment for sex, age, marital status, family member (crowding), stress level, and eating-out frequency. §p ⬍ 0.05 for the test (missing data not tested). AR ⫽ allergic rhinitis; ARIA ⫽ Allergic Rhinitis and Its Impact on Asthma; OR ⫽ odds ratio; NP ⫽ nasal polyp; CI ⫽ confidence interval.
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the information was retrospectively collected using a 24-hour recall method. Even if there are several shortcomings, the present study is the first population-based study to assess the levels of IgE specific to indoor allergens in the general Korean population. For further studies, a longitudinal design is needed to understand complex relationships between allergen exposures and development of allergic sensitization and diseases. In conclusion, KNHANES V-1 indicated that almost one-half of the population was sensitized to at least one indoor allergen and almost one-third of them had rhinitis symptoms. Risk factors such as sex, age, marital status, and stress level were associated with AR. Additional studies are needed to understand complex relationships between allergic disease and development of comorbidities. The general population–based study results on the prevalence, risk factors, and comorbidities of AR will contribute to prevention and treatment of AR and its comorbidities in the Korean population.
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ACKNOWLEDGMENTS
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The authors express their gratitude and appreciation to 87 residents of the Department of Otorhinolaryngology–Head and Neck Surgery from 45 training hospitals in South Korea and the members of the Korea Centers for Disease Control and Prevention who participated in this survey.
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REFERENCES 1.
Meltzer EO, Blaiss MS, Naclerio RM, et al. Burden of allergic rhinitis: Allergies in America, Latin America, and Asia-Pacific adult surveys. Allergy Asthma Proc 33(suppl 1):S113–S141, 2012.
10.
11.
Radon K, Gerhardinger U, Schulze A, et al.; Occupational Group of the ECRHS study. Occupation and adult onset of rhinitis in the general population. Occup Environ Med 65:38–43, 2008. Salo PM, Calatroni A, Gergen PJ, et al. Allergy-related outcomes in relation to serum IgE: Results from the National Health and Nutrition Examination Survey 2005–2006. J Allergy Clin Immunol 127:1226– 1235.e7, 2011. Katelaris CH, Lai CK, Rhee CS, et al. Nasal allergies in the AsianPacific population: Results from the Allergies in Asia-Pacific Survey. Am J Rhinol Allergy 25(suppl 1):S3–S15, 2011. Katelaris CH, Lee BW, Potter PC, et al. Prevalence and diversity of allergic rhinitis in regions of the world beyond Europe and North America. Clin Exp Allergy 42:186–207, 2012. Min YG, Jung HW, Kim HS, et al. Prevalence and risk factors for perennial allergic rhinitis in Korea: Results of a nationwide survey. Clin Otolaryngol Allied Sci 22:139–144, 1997. Cho YS, Choi SH, Park KH, et al. Prevalence of otolaryngologic diseases in South Korea: Data from the Korea national health and nutrition examination survey 2008. Clin Exp Otorhinolaryngol 3:183–193, 2010. Lee WH, Wee JH, Kim DK, et al. Prevalence of subjective olfactory dysfunction and its risk factors: Korean national health and nutrition examination survey. PLoS One 8:e62725, 2013. Haufroid V, and Lison D. Urinary cotinine as a tobacco-smoke exposure index: A minireview. Int Arch Occup Environ Health 71:162–168, 1998. Frieri M, and Valluri A. Vitamin D deficiency as a risk factor for allergic disorders and immune mechanisms. Allergy Asthma Proc 32:438–444, 2011. Hoppin JA, Jaramillo R, Salo P, et al. Questionnaire predictors of atopy in a US population sample: Findings from the National Health and Nutrition Examination Survey, 2005–2006. Am J Epidemiol 173: 544–552, 2011.
American Journal of Rhinology & Allergy
Delivered by Ingenta to: Economics Dept IP: 79.133.106.97 On: Tue, 28 Jun 2016 19:09:36 Copyright (c) Oceanside Publications, Inc. All rights reserved. For permission to copy go to https://www.oceansidepubl.com/permission.htm
e113
12.
13.
14.
15. 16.
17.
18. 19.
20. 21.
22.
23.
24.
25.
Bachert C, van Cauwenberge P, and Khaltaev N; World Health Organization. Allergic Rhinitis and Its Impact on Asthma. In collaboration with the World Health Organization. Executive summary of the workshop report. 7–10 December 1999, Geneva, Switzerland. Allergy 57:841–855, 2002. Ahn Y, Kwon E, Shim JE, et al. Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. Eur J Clin Nutr 61:1435–1441, 2007. Na YJ, and Lee SH. Development and validation of a quantitative food frequency questionnaire to assess nutritional status in Korean adults. Nutr Res Pract 6:444–450, 2012. Lee JY, Jun N, and Baik I. Associations between dietary patterns and screen time among Korean adolescents. Nutr Res Pract 7:330–335, 2013. Sakashita M, Hirota T, Harada M, et al. Prevalence of allergic rhinitis and sensitization to common aeroallergens in a Japanese population. Int Arch Allergy Immunol 151:255–261, 2010. Singh K, Axelrod S, and Bielory L. The epidemiology of ocular and nasal allergy in the United States, 1988–1994. J Allergy Clin Immunol 126:778–783.e6, 2010. Mo¨sges R, and Klimek L. Today’s allergic rhinitis patients are different: New factors that may play a role. Allergy 62:969–975, 2007. Trueba AF, Rosenfield D, Oberdo¨rster E, et al. The effect of academic exam stress on mucosal and cellular airway immune markers among healthy and allergic individuals. Psychophysiology 50:5–14, 2013. Bauchau V, and Durham SR. Epidemiological characterization of the intermittent and persistent types of allergic rhinitis. Allergy 60:350–353, 2005. Antonicelli L, Micucci C, Voltolini S, et al. Allergic rhinitis and asthma comorbidity: ARIA classification of rhinitis does not correlate with the prevalence of asthma. Clin Exp Allergy 37:954–960, 2007. Bousquet J, Annesi-Maesano I, Carat F, et al. Characteristics of intermittent and persistent allergic rhinitis: DREAMS study group. Clin Exp Allergy 35:728–732, 2005. Bousquet J, Neukirch F, Bousquet PJ, et al. Severity and impairment of allergic rhinitis in patients consulting in primary care. J Allergy Clin Immunol 117:158–162, 2006. Lee CH, Jang JH, Lee HJ, et al. Clinical characteristics of allergic rhinitis according to Allergic Rhinitis and Its Impact on Asthma guidelines. Clin Exp Otorhinolaryngol 1:196–200, 2008. Bousquet PJ, Combescure C, Neukirch F, et al. Visual analog scales can assess the severity of rhinitis graded according to ARIA guidelines. Allergy 62:367–372, 2007.
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26. 27.
28. 29.
30.
31.
32.
33.
34.
35. 36.
Devereux G, and Seaton A. Diet as a risk factor for atopy and asthma. J Allergy Clin Immunol 115:1109–1117, 2005. Rosenkranz RR, Rosenkranz SK, and Neessen KJ. Dietary factors associated with lifetime asthma or hayfever diagnosis in Australian middle-aged and older adults: A cross-sectional study. Nutr J 11:84, 2012. Allan K, Kelly FJ, and Devereux G. Antioxidants and allergic disease: A case of too little or too much? Clin Exp Allergy 40:370–380, 2010. Tamay Z, Akcay A, Ergin A, and Guler N. Effects of dietary habits and risk factors on allergic rhinitis prevalence among Turkish adolescents. Int J Pediatr Otorhinolaryngol 77:1416–1423, 2013. Kompauer I, Heinrich J, Wolfram G, and Linseisen J. Association of carotenoids, tocopherols and vitamin C in plasma with allergic rhinitis and allergic sensitisation in adults. Public Health Nutr 9:472–479, 2006. Nagel G, Nieters A, Becker N, and Linseisen J. The influence of the dietary intake of fatty acids and antioxidants on hay fever in adults. Allergy 58:1277–1284, 2003. Oh SY, Chung J, Kim MK, et al. Antioxidant nutrient intakes and corresponding biomarkers associated with the risk of atopic dermatitis in young children. Eur J Clin Nutr 64:245–252, 2010. Allen S, Britton JR, and Leonardi-Bee JA. Association between antioxidant vitamins and asthma outcome measures: Systematic review and meta-analysis. Thorax 64:610–619, 2009. Hozyasz KK, Chełchowska M, Laskowska-Klita T, et al. Low concentration of alpha-tocopherol in erythrocytes of atopic dermatitis patients. Med Wieku Rozwoj 8:963–969, 2004. Rosenlund H, Magnusson J, Kull I, et al. Antioxidant intake and allergic disease in children. Clin Exp Allergy 42:1491–1500, 2012. Li J, Huang Y, Lin X, et al.; China Alliance of Research on Respiratory Allergic Disease (CARRAD). Factors associated with allergen sensitizations in patients with asthma and/or rhinitis in China. Am J Rhinol Allergy 26:85–91, 2012. Sener O, Kim YK, Ceylan S, et al. Comparison of skin tests to aeroallergens in Ankara and Seoul. J Investig Allergol Clin Immunol 13:202–208, 2003. Bang JH, Kim YJ, Shin HS, and Lee BJ. Clinical analysis of allergic rhinitis in Seoul. Korean J Rhinol 3:130–134, 1996. Chung YJ, Cho IK, Lee KI, et al. Seasonal specificity of seasonal allergens and validation of the ARIA classification in Korea. Allergy Asthma Immunol Res 5:75–80, 2013. e
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