Introdution

Allergy and asthma, as immune system related disorders, are major health concerns. The allergic conditions are prevalent medical issues linked to immunological anomalies, characterized by the immune system’s hypersensitive reaction to substances in the environment that are typically viewed as innocuous, encompassing respiratory, skin, and food allergies [1]. As a common lung disease caused by swelling and narrowing of the tubes that carry air in and out of the lungs, asthma stands as a prevalent chronic ailment affecting children globally [2]. The global prevalence of allergic diseases and asthma were steadily increasing, with a notable rise in the complexity and severity, particularly among children and young adults, which have a reduced quality of life [3, 4]. These upward trends in allergic diseases and asthma had also led to a growing socioeconomic burden worldwide.

The relationship between allergic diseases and respiratory tract infections has always been the focus of pathological mechanism research [5, 6]. Respiratory infections, particularly viral infections, may trigger allergic reactions and exacerbate allergic diseases such as asthma and allergic rhinitis [5, 6]. The act of wearing a mask in community settings had been demonstrated effectiveness in potentially reducing the transmission of respiratory diseases [7], and the implementation of social distancing measures has also been found to decrease the spread of seasonal influenza within workplace environments [8]. Of note, a study had found that during early 2020, social distancing and other lockdown strategies were effective in slowing down the transmission of common respiratory viral illnesses and reducing the need for pediatric hospitalizations [9].

It is well known that since the end of 2019, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has caused a global pandemic. The measures implemented to control COVID-19 have greatly changed people’s daily habits and routines [10], including online classes or home-based working, keeping social distance, wearing a mask, have slowed the spread of not only just COVID-19, but other infectious diseases. Literature reported a significant decline in hospital admissions in the United States with the onset of the COVID-19 pandemic [11]. Asthma hospital visits and hospitalizations also decreased in many countries during the COVID-19 pandemic [11,12,13,14,15]. The incidence of food allergies and food allergic reaction in children were reported lower than pre-pandemic [16, 17]. The implementation of social isolation measures during the COVID-19 pandemic had a profound impact on the seasonality of childhood respiratory diseases [18]. It is also worth noting that the incidence of both atopic dermatitis and eczema increased among young children during this period [16, 19]. However, few large-scale studies have investigated the prevalence of allergic diseases and asthma among children and adolescents during the COVID-19 pandemic.

Therefore, we conducted this study using the nationally representative National Health Interview Survey (NHIS) data for analysis to compare the difference of the prevalence of allergies and asthma in a nationally representative sample of US children and adolescents during and before COVID-19 pandemic.

Methods

Study populations

Our study utilized 2018–2021 cross-sectional data from NHIS, a household survey conducted continuously throughout the year by the National Center for Health Statistics (NCHS), Centers for Disease Control and Prevention (CDC) [20, 21]. NHIS is a nationally representative survey that covers the U.S. civilian noninstitutionalized population and has been the primary source of information on health conditions in the U.S. population since 1957 [22]. NHIS collects data through in-person interviews, typically conducted in respondents’ homes, and follow-up interviews may be conducted over the telephone to complete the survey [23]. Information about the health of sample children is obtained through interviews with parents or adults responsible for their healthcare. NHIS has an annual sample size of approximately 30,000 households, which includes around 8,400 sample children. Between 2018 and 2021, the total household response rate for NHIS ranged from 50.7% to 64.2%, and the conditional response rate for the sample child component ranged from 86.9% to 93.5%. NHIS has been approved by the Research Ethics Review Board of the NCHS and the US Office of Management and Budget. All respondents provided oral informed consent prior to participation. Considering that the first COVID-19 case in United States was reported in January, 2020 [24], periods in 2020 and 2021 were defined as the COVID-19 pandemic period.

Ascertainment of variables

Our study included children and adolescents between the ages of 0 and 17 years that participated in the NHIS and had available information on allergies (including respiratory allergies, food allergies and skin allergies) and asthma.

The content and structure of the NHIS was updated in 2019, with content on respiratory, food and skin allergies in the children’s sample module rotating every three years starting in 2021. Therefore, there was content on allergies in 2018 and 2021, but not in 2019 and 2020, and the data from the questionnaire on allergies content was slightly different in 2018 and 2021. The three allergic types and asthma were defined based on an affirmative response to the questions showed in Table 1 [1, 4]. Any allergy was defined as having any one or more of the three types of allergies listed above.

Table 1 The questions on respiratory allergies, food allergies, skin allergies and asthma in NHIS 2018-2021a
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During the interview, a standardized questionnaire was used to collect demographic data, such as age, sex, race/ethnicity, highest educational level of family members, family income to poverty ratio and geographic region. Participants self-reported their race and Hispanic ethnicity, which were classified according to the 1997 Office of Management and Budget Standards. Family income to poverty ratio is the total family income divided by the poverty threshold.

Statistical analysis

To ensure that the results are representative of the US population, we applied survey sampling weights, strata, and primary sampling units that were created by the NCHS and provided with the NHIS data, which are available at NHIS online website. These were included in all of our analyses, unless otherwise stated.

Comparisons of baseline characteristics among children and adolescents with allergies and asthma were performed using the chi-square test for all categorical variables. We estimated the differences in the prevalence of allergy and asthma in children and adolescents during and before the COVID-19 pandemic using weighted logistic regression models, adjusting for age, sex, race/ethnicity, education, family income to poverty ratio and geographic region. Moreover, interaction analyses were performed by including multiplicative terms of each strata variable with survey cycle in the aforementioned logistic regression models to examine whether the secular differ across strata.

All statistical analyses were conducted using the survey modules of SAS software, version 9.4 (SAS Institute). A 2-sided P < 0.05 was considered statistically significant.

Results

Characteristics of participants and the prevalence of allergic conditions and asthma

The characteristics of participants according to their allergies and asthma status were described in Tables 2, 3 and 4. A total of 31,503 children and adolescents aged 0–17 years were included in our final analytical sample (weighted mean [SD] age, 8.64 [0.04] years; 16,265 boys [51.0%] and girls [49.0%]; 7485 Hispanic [25.7%], 16,723 non-Hispanic (NH) white [51.3%], 3364 NH black [12.7%], and 3931 other races [10.3%]).

Table 2 Characteristics of study population and numbers of allergies by characteristics before and during the COVID-19 pandemic from 2018 to 2021a
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Table 3 Characteristics of study population and numbers of allergies by characteristics before and during the COVID-19 pandemic, 2018 to 2021a
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Table 4 Characteristics of study population and numbers of asthma by characteristics before and during the COVID-19 pandemic, 2018 to 2021a
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In 2018 and 2021, the overall prevalence of any allergy, respiratory allergies, food allergies and skin allergies were 26.6% (95% CI 25.7%- 27.5%), 16.4% (95% CI 15.7%- 17.1%), 6.1% (95% CI 5.7%- 6.6%) and 11.7% (95% CI 11.0%- 12.3%), respectively. The overall prevalence of asthma was 10.4% (95% CI 10.0%- 10.9%) from 2018 to 2021.

Specifically, in 2018, among the 8269 participants, 2321(weighted prevalence, 26.1%) had any allergy, 1296 (weighted prevalence, 14.0%) had respiratory allergies, 560 (weighted prevalence, 6.5%) had food allergies, and 1097 (weighted prevalence, 12.6%) had skin allergies. The weighted prevalence of any allergy, respiratory allergies and skin allergies varied by race/ethnicity and highest educational level of family members. In 2021, among the 8259 participants, 2316 (weighted prevalence, 27.1%) had any allergy, 1599 (weighted prevalence, 18.8%) had respiratory allergies, 506 (weighted prevalence, 5.8%) had food allergies, and 932 (weighted prevalence, 10.7%) had skin allergies. Significant variations in the weighted prevalence of all three allergy types and any allergy were noted across different races/ethnicities.

In 2018–2019, among the 17,458 participants, 1995(weighted prevalence, 11.1%) had asthma, varied by all demographic and socioeconomic groups. In 2020–2021, among the 14,045 participants, 1468(weighted prevalence, 9.8%) had asthma, varied by age, sex and race/ethnicity.

Differences in the prevalence of allergies and asthma in children and adolescents during and before the COVID-19 pandemic

Children and adolescents during the COVID-19 pandemic, compared with those before the COVID-19 pandemic, were more prone to respiratory allergies (weighted prevalence, 18.8% vs 14.0%; P < 0.001), but less likely to suffer from skin allergies (weighted prevalence, 10.7% vs weighted prevalence, 12.6%; P = 0.005) and asthma (weighted prevalence, 9.8% vs weighted prevalence, 11.1%; P = 0.001), and there were no differences in any allergy (weighted prevalence, 26.1% vs 27.1%; P = 0.27) and food allergies (weighted prevalence, 5.8% vs prevalence, 6.5%; P = 0.12) (Table 5). After adjusting for age, sex, race/ethnicity, family highest education level, family income level, and geographical region, the above differences remained statistically significant (Table 5).

Table 5 Differences in the prevalence of allergies and asthma in children and adolescents before and during the COVID-19 pandemic, 2018 to 2021
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Logistic regression models and interaction analyses

Stratified analyses showed that there were differences in the prevalence of all three allergic types during and before the Covid-19 pandemic in NH White and those with family income to poverty ratio of 1.00–1.99. Among southern children and adolescents, variations in the prevalence of any allergy or asthma were observed during and before the Covid-19 pandemic. Moreover, there was a significant interaction between age and any allergy or asthma, between highest educational level of family members and food allergies, skin allergies or asthma, between geographic region and any allergy, respiratory allergies or asthma (Tables 6, 7 and 8).

Table 6 Prevalence of any allergies and respiratory allergies in US children and adolescents by characteristics before and during the COVID-19 pandemic from 2018 to 2021
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Table 7 Prevalence of food allergies and skin allergies in US children and adolescents by characteristics before and during the COVID-19 pandemic from 2018 to 2021
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Table 8 Prevalence of asthma in US children and adolescents by characteristics before and during the COVID-19 pandemic, 2018 to 2021
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Discussion

Based on a nationally representative sample from NHIS, we found that the prevalence of respiratory allergies increased and the prevalence of both skin allergies and asthma decreased among US children and adolescents during the COVID-19 pandemic compared with the pre-COVID-19 pandemic. The differences persisted after adjusting for demographic and socioeconomic variables.

The findings of the current study are partially consistent with the results observed in the earlier research segment, although not entirely identical. Similar studies have been conducted in Korea, showing a decline in the prevalence of allergic diseases and asthma among adolescents during the COVID-19 pandemic [25,26,27]. Our study also observed a decline in the prevalence of skin allergies and asthma during the COVID-19 pandemic. However, there was an increase in the prevalence of respiratory allergies during this period, while the prevalence of any allergy and food allergies remained constant.

It was supposed that the increased prevalence of respiratory allergies among children and adolescents during the COVID-19 pandemic may be attributed to several potential factors. The changes in lifestyle and behavior during the pandemic including reduced outdoor activities and increased time spent indoors were potentially one of the most important aspects [28, 29]. It may have led to greater exposure to indoor allergens and reduced exposure to beneficial outdoor environments. Qing et al. [30] found the children and youth groups exhibited an increasing positive rate for most common allergens, especially indoor inhalant allergens, during the COVID-19 epidemic than before the pandemic in China. Furthermore, the rapid and potent immune response against SARS-CoV-2 infection is the first line of defense against the invasion of the virus. However, excessive natural immune inflammation and impaired adaptive immune response may cause damage to both local and systemic tissues [31]. The COVID-19 virus may activate and disrupt the regulation of the immune system [32], and may lead to an enhanced response to allergens in the body. This may make children and adolescents more sensitive to respiratory allergens and increase the risk of allergic reactions and symptoms. There are also other reasons that may contribute to the increased prevalence of respiratory allergies among children and adolescents. Scientific research indicated that the COVID-19 pandemic had a negative impact on the mental health of children and adolescents [33]. High levels of stress and anxiety can potentially have adverse effects on the immune system [34], thereby potentially increasing the risk of allergic reactions. Additionally, the implementation of infection prevention measures, such as the utilization of face masks and adherence to social distancing, might have unintentionally affected the normal progression of immune tolerance, potentially resulting in an elevated risk of developing allergic sensitization.

The decreased prevalence of asthma among children and adolescents in the United States during the COVID-19 pandemic was observed in the study. A lot of attention has been paid to the reasons for the decline in the prevalence of asthma. The reduction in exposure to common environmental triggers of asthma among children and adolescents may have contributed to it. It was the result of the implementation of public health measures to control COVID-19 and other infectious diseases [26, 27]. These measures effectively limited the exposure of children and adolescents to outdoor allergens, air pollution and irritants, which may trigger or exacerbate asthma [35,36,37]. What’s more, the reduction in prevalence of asthma attacks may had been strongly influenced by the ongoing decrease in respiratory virus levels during the COVID-19 pandemic [38]. Viral respiratory tract infections are commonly associated with induced asthma exacerbations [39]. And the incidence of respiratory viral diseases and the detection of viruses declined significantly during the pandemic [38, 40]. Therefore, the incidence of asthma may be reduced as a result. In addition, reductions in vigorous physical activity during the COVID-19 pandemic may also have had an effect on the reduced prevalence of asthma [26]. It was reported that vigorous physical activity was positively associated with symptoms of asthma in adolescents [41]. During the epidemic, there was a decrease in physical activity among adolescents [42, 43], leading to a corresponding reduction in vigorous exercise, thus resulting in a decrease in the prevalence of asthma. What’s more, with less doctor visits during the COVID-19 pandemic, there were less instances of making a doctor’s diagnosis also influencing the results.

The decline in the prevalence of skin allergies among children and adolescents in the United States during the COVID-19 pandemic was likely due to decreased exposure to allergens [44]. Measures such as wearing masks, washing hands frequently, enhancing indoor ventilation, and maintaining social distance avoided the exposure of children and adolescents to allergens [44]. Also, the reduction in air pollutants may have contributed to the decline in the prevalence of skin allergies. Exposure to air pollutants can increases the risk of skin allergies [45, 46], but the implementation of lockdown measures resulted in a substantial improvement in air quality, marked by a significant reduction in the levels of air pollutants [47]. Thus it may be one of the reasons for the decline in the prevalence of skin allergies. Additionally, studies have pointed out that overexposure to ultraviolet radiation can cause skin irritation [48], and the lockdown policy had led to a reduction in sun exposure, which may have led to a decrease in the prevalence of skin allergies.

Previous studies had shown an increase in the prevalence of food allergies among children [25,26,27]. In contrast, we found the prevalence of food allergies in current study remained constant during the COVID-19 epidemic. Whether this was because COVID-19 primarily affects the respiratory system remains unknown [49]. During the epidemic, concerns were focused on respiratory symptoms and infection prevention rather than on issues related to food allergies.

This study has several notable strengths. Firstly, the study was a large-scale study to compare the differences in the prevalence of allergic diseases and asthma among US children and adolescents during the COVID-19 pandemic and preceding the pandemic. Moreover, it utilizes extensive nationwide population-based data, incorporating a large sample size and encompassing a diverse multiracial/multiethnic population. The adoption of a nationally representative sampling strategy through the NHIS enables the findings to be more broadly applicable to the general population. And the study benefits from a relatively high response rate in the NHIS [22], which helps mitigate concerns related to selection bias.

This study is subject to several limitations. First, the assessment of both allergic disease and asthma relied on self-reported and retrospectively reported information, which introduces the potential for recall bias and misreporting. And the NHIS underwent a planned redesign in 2019 and there was a lack of consistency on how questions on allergies were collected before and during pandemic for allergies. However, it is important to note that the prevalence rates of the allergic disease and asthma observed in this study align with those reported in other nationwide studies conducted during similar time periods. This suggests a degree of consistency and supports the reliability of the findings despite the reliance on self-reported data. Second, because this study was cross-sectional, we were unable to determine the long-term effects due to the COVID-19 pandemic. Therefore, longer-term observations are needed in the future to determine the specific effects of pandemics on allergic diseases and asthma. In addition, some of the results of our observations including the rising prevalence of respiratory allergies and the constant prevalence of any allergy and food allergies were inconsistent with other studies. Therefore, future explorations for specific allergy types are needed.

Conclusion

Based on nationally representative data in large cross-sectional surveys, we found significant differences in the prevalence of respiratory allergies, skin allergies and asthma in children and adolescents during and before the COVID-19 pandemic. More research is necessary to examine the relationship between the prevalence of allergic diseases and the COVID-19 pandemic time period using survey data representing that time period, especially focusing on the impact of lifestyle changes due to infection prevention measures.