Trends in Allergic Sensitization and Diseases in the Korean General Population Over a 9-Year Period

Article information

Clin Exp Otorhinolaryngol. 2025;18(1):40-49

Publication date (electronic) : 2024 December 10

doi : https://doi.org/10.21053/ceo.2024.00209

Dong Hee Lee, Ji-Hyeon Shin

Department of Otolaryngology-Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul, Korea

Corresponding author: Ji-Hyeon Shin Department of Otolaryngology-Head and Neck Surgery, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 06591, Korea Tel: +82-31-820-3892 Email: shinjee79@catholic.ac.kr

Received 2024 July 25; Revised 2024 November 20; Accepted 2024 December 6.

Abstract

INTRODUCTION

Allergic sensitization, a critical step in the development of allergic diseases, requires exposure to specific allergens. However, the relationship between allergen exposure, sensitization, and the subsequent development of allergic diseases is influenced by a variety of factors, including age, sex, timing of exposure, environmental conditions, lifestyle, and socioeconomic status [1-3]. Population-based studies have documented variations in allergic sensitization across different regions and populations. Factors such as climate change, industrialization, and related environmental and lifestyle shifts are believed to contribute to increased sensitization to allergens and the rise of allergic diseases. Previous studies have reported changes in the prevalence of allergic sensitization in various populations [4-7]. However, to date, there have been no large-scale, population-based studies examining trends in allergic sensitization and related diseases in Korea.

In Korea, allergen-specific immunoglobulin E (IgE) levels in the general population, including house dust mites (HDM), dogs, and cockroaches, were measured in the 2010 Korea National Health and Nutrition Examination Survey (KNHANES). Recently, the 2019 KNHANES estimated the IgE levels specific to seven allergens: HDM, dogs, cats, birch, oak, Japanese hop, and ragweed. HDM- and dog-specific IgE levels were measured in 2010 and 2019. These are the representative indoor allergens in Korea, as well as worldwide. This study analyzed trends in sensitization to HDM and dogs, as well as allergic diseases, over approximately 10 years and explored the potential factors associated with these changes.

MATERIALS AND METHODS

Study population

This cross-sectional study used data from the KNHANES which is a nationwide, population based, cross-sectional health survey conducted by the Korea Centers for Disease Control and Prevention (KCDC). For sampling the representative participants, a total of twenty households were systematically selected from among 192 distinct regions, with a focus on about 10,000 individuals aged one year and older. The demographic cohort targeted by KNHANES comprises non-institutionalized citizens of Korea. The methodological framework employed for sampling adheres to a multi-stage clustered probability design. The KNHANES consists of a health interview, a nutritional survey, and a health examination survey. The KNHANES study has undergone annual ethical review and approval by the KCDC Research Ethics Review Committee since 2007. The committee adheres to the “KCDC Research Ethics Review Committee’s standard guidelines,” which are aligned with both domestic and international regulations, including the Declaration of Helsinki and the Bioethics and Safety Act. Prior to the survey, all participants provided written informed consent for use of their data. The survey was approved by the Institutional Review Board (IRB) of the KCDC (no. 2010–02CON-21-C in 2010 and 2018-01-03-2C-A in 2019) and was performed in accordance with relevant guidelines and regulations. IRB approval from the author’s institution (IRB No. UC24ZISI0131) was waived.

The KCDC provides de-identified data, processed to ensure the inability to identify individuals, in compliance with the Personal Information Protection Act and the Statistics Act. This data can be downloaded from the KNHANES website by any researcher for academic purposes. The original data included the necessary information for complex sample analysis: weights (like wt_itvex, wt_ntr), strata (kstrata), and clusters (psu). These weights were adjusted to accurately represent the Korean population, considering factors like complex sample design, survey non-response rates and post-stratification. We used this data to create a complex sample dataset.

The response rate based on health interview and health examination was 76.5% in 2010 and 71.0% in 2019. Four thousand eight hundred participants (≥10 years of age) had blood tests for measurement of allergen-specific IgE. After excluding incomplete results of specific IgE and any missing data, a total of 2,019 and 2,065 participants who successfully underwent measurement of specific IgE, a health interview, and examination in the years 2010 and 2019, respectively, were included in this study (Fig. 1). We also divided the participants into two age groups: adolescents (ages 10–18) and adults (ages 19 and older). This was done because the risk factors for allergic sensitization differ by age group.

Fig. 1.

Flowchart showing the selection of study participants. IgE, immunoglobulin E.

RESULTS

Clinicodemographic characteristics

The characteristics of the study population are summarized in Table 1. A total of 4,084 participants were included in this study. In 2010, 1,083 of 2,019 participants were women, and in 2019, 1,076 of 2,065 were women. The mean age in 2010 was lower than in 2019 (mean age±standard error: 40.8±0.6 years in 2010; 44.9±0.6 years in 2019; P<0.001). The proportion of adolescents in 2019 was lower than in 2010 (9.3% and 13.6%, respectively; P<0.001). A significantly higher proportion of participants in 2019 were apartment dwellers and a lower proportion were from low-income households. The prevalence of obesity among adolescents was higher in 2019 than in 2010. The proportion of adults with a low education level and who currently smoked in 2019 was lower than in 2010. Other factors showed no significant differences between the two years. The characteristics according to sensitization type are summarized in Supplementary Tables 1-3.

Table 1.

Clinical and demographic characteristics of the study population in 2010 and 2019

The mean level of HDM-specific IgE was significantly lower in 2019 (5.19±0.36 kU/L) than in 2010 (6.61±0.47 kU/L) (P=0.017). The mean dog-specific IgE levels showed no change between 2010 (0.21±0.05 kU/L) and 2019 (0.21±0.03 kU/L).

Prevalence of allergic sensitization and allergic diseases

The prevalence of sensitization to HDM and to dogs both decreased from 2010 to 2019; however, the differences were not significant. Among adolescents, dog sensitization in 2019 was significantly higher than in 2010 (8.7% in 2010 vs. 15.3% in 2019; P=0.027) (Fig. 2A). We also compared sensitization between the two years according to sex, with no significant differences observed (Fig. 2B). No significant differences in the prevalence of asthma, AD, or AR were observed between 2010 and 2019. In both adolescents and adults, the prevalence of allergic diseases showed no significant differences between the two years (Fig. 2C), nor when the participants were grouped by sex (Fig. 2D).

Fig. 2.

Prevalence of allergic sensitization and allergic diseases. (A) Sensitization to house dust mites (HDM) and dogs according to age group. (B) Sensitization to HDM and dogs according to sex. (C) Prevalence of allergic diseases according to age group. (D) Prevalence of allergic diseases according to sex. AD, atopic dermatitis; AR, allergic rhinitis. ^*P<0.05.

Prevalence of allergic sensitization in participants with allergic diseases

The prevalence of allergic sensitization according to the presence of allergic diseases is summarized in Table 2. In 2010, sensitization rates to HDM and dogs were significantly higher in participants with AR than in those without AR. In 2019, these rates were significantly higher in participants with all three allergic diseases than in those without allergies. The prevalence of allergic sensitization in 2019 was higher than in 2010, except for HDM sensitization in participants with AR. The rate of HDM sensitization in participants with AD significantly increased in 2019 (43.7% in 2010 vs. 70.1% in 2019; P=0.005) (Fig. 3A).

Table 2.

Prevalence of IgE sensitization according to the presence of allergic diseases

Fig. 3.

(A) Prevalence of allergic sensitization in participants with allergic diseases. (B) Prevalence of allergic diseases in allergen-sensitized participants. HDM, house dust mites; AD, atopic dermatitis; AR, allergic rhinitis. ^*P<0.05.

Prevalence of allergic diseases in allergen-sensitized participants

The prevalence of allergic diseases according to sensitization is shown in Table 3. In 2010, the prevalence of AR in HDM(+) participants was significantly higher than that in HDM(–) participants. Dog(+) participants also had a higher prevalence of AR than dog(–) participants. In 2019, HDM(+) and dog(+) participants showed a significantly higher prevalence of all three allergic diseases than HDM(–) and dog(–) participants. The prevalence of allergic diseases in 2019 was higher than in 2010, except for the prevalence of AR in HDM(+) participants; however, there was no significant difference between the two years (Fig. 3B).

Table 3.

Prevalence of allergic diseases according to sensitization to allergens

Association between clinicodemographic characteristics and IgE sensitization

In 2010, men were more likely to be sensitized to HDM than women (odds ratio [OR], 1.76; 95% CI, 1.38–2.24). Older age (OR, 0.83; 95% CI, 0.77–0.90), urban residence (OR, 0.76; 95% CI, 0.60–0.96), and apartment dwelling (OR, 0.78; 95% CI, 0.64–0.95) were associated with a lower risk of HDM sensitization. In 2019, men were still more likely to be sensitized to HDM than women (OR, 1.56; 95% CI, 1.27–1.90), and older age (OR, 0.79; 95% CI, 0.75–0.85) was still associated with a lower risk. However, living in urban areas or apartments was no longer linked to a lower risk of HDM sensitization.

In 2010, dog sensitization had more than a two-fold positive association with being male (OR, 2.37; 95% CI, 1.48–3.80) and in 2019, was negatively associated with older age (OR, 0.67; 95% CI, 0.59–0.77) (Fig. 4, Supplementary Table 4). Among adolescents in 2019, HDM sensitization was twice as high in obese adolescents (OR, 2.02; 95% CI, 1.04–3.91). In 2010, dog sensitization was eight times as high in urban residents (OR, 8.06; 95% CI, 1.53–42.49) (Fig. 5A, Supplementary Table 5).

Fig. 4.

Association between clinicodemographic characteristics and immunoglobulin E sensitization. HDM, house dust mites; OR, odds ratio.

Fig. 5.

(A) Association between clinicodemographic characteristics and immunoglobulin E (IgE) sensitization among adolescents. (B) Association between clinicodemographic characteristics and IgE sensitization among adults. HDM, house dust mites; OR, odds ratio.

For adults in both 2010 and 2019, HDM sensitization was positively associated with being male (2010: OR, 1.78; 95% CI, 1.31–2.43 vs. 2019: OR, 1.52; 95% CI, 1.19–1.94) and negatively associated with older age (2010: OR, 0.83; 95% CI, 0.73– 0.95 vs. 2019: OR, 0.81; 95% CI, 0.73–0.90). In 2019, heavy drinking showed a significantly positive association with HDM sensitization (OR, 1.44; 95% CI, 1.03–2.02). Dog sensitization was positively associated with heavy drinking (OR, 2.35; 95% CI, 1.20–4.62) in 2010 and negatively associated with older age (OR, 0.72; 95% CI, 0.59–0.87) in 2019 (Fig. 5B, Supplementary Table 6).

DISCUSSION

This study is the first to report changes in allergic sensitization to HDM and dogs as well as the prevalence of allergic diseases in a large-scale general Korean population. The prevalence of sensitization to HDM and dogs showed little change between 2010 and 2019. In line with our findings, two European studies found no increase in sensitization to HDM. The European Community Respiratory Health Survey (ECRHS) produced minimal evidence that the age-specific prevalence of HDM sensitization was significantly different between adults born in recent times and those born earlier (over a 20-year period) [13]. A Swedish study compared results from the ECRHS in 1991–1992 and the West Sweden Asthma Study in 2009–2012. The prevalence of sensitization to HDM and dogs remained unchanged [14]. Conversely, numerous studies conducted over several decades have demonstrated an increase in allergic sensitization and associated diseases correlating with urbanization, westernization, and lifestyle modifications [15,16]. A Danish review of health examination studies over a 25-year period in a Danish general adult population showed a substantial increase in the prevalence of aeroallergens, including HDM sensitization [16]. Therefore, results from one general population cannot be generalized to other populations.

Various factors, including genetic factors, indoor allergens, air pollutants, geographic factors, and microbial exposure, interact to complicate allergen exposure, sensitization, and allergic diseases [1,3,10,17]. In the current study, the small changes in sensitization to HDM and dogs could be related to increased awareness and preventive measures, changing patterns of allergen exposure, and shifts in the residential environment.

The current study showed that dog sensitization in adolescents significantly increased over 9 years. This pattern may be caused by increased pet ownership, closer contact with pets, or a changing immune response in adolescents [18-20]. Although the relationship between exposure to dogs and the development of sensitization remains controversial, recent studies suggest that environmental and genetic factors, such as the filaggrin mutation, influence sensitization [21-23]. Cross-reactive molecules between cat and dog allergens may also play a role in sensitization [24]. However, cat-specific IgE levels were not measured in 2010, and cross-reactivity by cat allergen was not considered in the current study. Nevertheless, the rising prevalence of dog sensitization highlights a need for prevention and management strategies in adolescents.

We found a significantly higher increase in HDM sensitization in participants with AD in 2019 than in 2010. In addition, sensitized participants had increased rates of asthma, AD, and AR, indicating higher symptomatic sensitization over time. Many factors influence the development of clinical symptoms associated with asymptomatic sensitization. These include family history of atopy, total or allergen-specific IgE levels, and the number of sensitized allergens (mono- or poly-sensitized). Over time, there may have been changes in their interplay [25].

Our study evaluated the association between allergic sensitization and related factors. Using multivariate analysis, we found that increasing age was negatively associated with sensitization (except for dog sensitization in 2010), especially in adults. These findings align with previous studies that reported increased allergic sensitization in children/adolescents and decreased (or minimally increased) sensitization in older adults [13,26], which may be the result of reduced allergen exposure and immunological changes during aging [26]. We also found changes in the factors associated with allergic sensitization over time. Males showed a positive association with HDM sensitization in both 2010 and 2019, similar to previous studies [21]. However, the association between male sex and dog sensitization, which was significant in 2010, disappeared in 2019. Thus, we can infer a potential shift in the sex factor over time.

In general, urbanization has been positively associated with allergic sensitization [27,28]. However, although our study showed that HDM sensitization was negatively associated with urban residences and apartment dwellings in 2010, these associations were not observed in 2019. Furthermore, urbanization in the United States general population was associated with sensitization to outdoor allergens but not with sensitization to indoor allergens, including HDM and dogs [21]. Our findings may be due to a reduction in the differences between urban and rural environments or to changes in lifestyle in urban areas.

Among adolescents, dog sensitization had a strong association with urban residence in 2010; however, this association was no longer significant in 2019. In 2010, dog-sensitized adolescents were more likely to live in urban areas than non-sensitized adolescents, whereas in 2019, there was no difference in living areas according to dog sensitization (Supplementary Table 2). Some studies showed a positive association between dog sensitization and urban environments [29], while others observed no association [30]. A Danish birth cohort study found that early exposure to animals could have harmful or protective effects on allergic diseases, depending on many factors such as the type of animal, timing and source of exposure, and parental history of allergies [31]. In 2019, obese adolescents were more than twice as likely to have a positive association with HDM sensitization; however, this association remains controversial. Some studies reported that obesity was associated with asthma and wheezing, not with allergic sensitization [32,33], while other studies found that overweight and obesity were associated with allergic sensitization [34,35]. A cross-sectional study of Korean adolescents showed that being overweight was significantly associated with atopy; however, the mechanisms remain unclear [36]. One possible explanation is that inflammatory adipokines such as leptin are released from adipose tissues and can have proinflammatory effects on the immune system of obese individuals [37].

In adults, heavy drinking was associated with dog sensitization in 2010; however, this association was no longer observed in 2019. In 2019, heavy drinkers had a 1.4-fold higher positive association with HDM sensitization. Although previous studies have reported inconsistent results regarding the association between alcohol consumption and IgE sensitization [38,39], heavy alcohol consumption does have known immunomodulatory effects, leading to allergic sensitization [40].

Nevertheless, the mechanisms by which environmental exposures influence allergic sensitization remain unclear. The epithelial barrier hypothesis [41] suggests that external exposomes (climate, air pollutants, biodiversity loss, dietary habit changes, and microbiome dysbiosis) facilitate damage to the epithelial barrier of skin, lung, and intestine [3,42,43]. The damaged epithelial cells then initiate allergic inflammation via the secretion of epithelial cell-derived cytokines like thymic stromal lymphopoietin, interleukin (IL)-25, and IL-33, which regulate type 2 immune responses and affect the development of allergic diseases [44]. Recently, an in vitro study using cultures of the nasal mucosa showed that exposure to air pollutants increased the expression of allergic inflammatory cytokines in nasal epithelial cells and fibroblasts [45]. Therefore, various environmental factors can potentially contribute to the development of allergic sensitization and allergic disease.

In addition, the biodiversity hypothesis suggests that reduced exposure to environmental biodiversity induces adverse effects on human commensal microbiota and related immune tolerance [46,47]. Finally, dysregulation of the gut, lung, and skin microbiomes, especially in young children, causes allergic sensitization and diseases by increasing T helper (Th) 2 and Th17 cell functions and decreasing Th1 and regulatory T cells [48-50].

This study had some limitations. First, due to the nature of the cross-sectional design, the causal relationship between allergic sensitization and associated factors remains unclear. Second, dependence on self-reported surveys for the assessment of clinicodemographic data may result in recall bias. Third, we only assessed IgEs specific to HDM and dogs. This study did not include other allergens like cats, pollen, and mold, limiting the ability to understand the broader spectrum of sensitization. Fourth, as cat-specific IgE levels were not measured in 2010, it was not possible to assess whether cross-reactivity with cats influenced the observed changes in dog-specific IgE levels. Based on the findings of this study, we hope to expand the range of allergens tested in the KNHANES in the future, which will enable the collection of national-level data on a broader range of allergens. Further studies with longitudinal research designs and diverse allergens may yield a more profound understanding of the mechanisms underlying allergic sensitization and the prevalence of allergic diseases.

Nevertheless, this study investigated changes in the prevalence of sensitization to common indoor allergens and their associated factors in the general Korean population. Our results emphasize the need for allergic disease prevention and management in dog-sensitized adolescents. Also, our findings suggest strategies to reduce allergic sensitization and control modifiable risk factors such as obesity in adolescents and heavy drinking in adults. The relationship between humans and companion animals, particularly dogs, has been steadily strengthening. Unlike in the past, dogs and cats are now regarded as companion animals rather than merely pets. Companion animals have become an integral part of human life, making it increasingly challenging to discuss human lifestyles without considering their role. Consequently, the findings of this study underscore the need for a public health-oriented approach to companion animal management, addressing issues such as allergies related to companion animals and the development of allergy testing for individuals who own them. This study contributes valuable medical evidence supporting the importance of such a public health perspective.

In conclusion, this study demonstrated trends in allergic sensitization and diseases and identified factors linked to these changes in a large-scale nationwide population over a 9-year period. We found the prevalence of HDM and dog sensitization remained stable over 9 years, while dog sensitization among adolescents increased. In addition, clinicodemographic factors associated with sensitization differed between age groups and years. Ultimately, understanding these changes and associated factors in the general population will help healthcare providers propose new strategies to reduce allergic sensitization and allergic diseases.

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