Abstract
Background:
Despite the importance of influenza vaccination, its rates in subjects with asthma are suboptimal, especially in the young population.
Methods:
Among 72,843 adults aged ⩾18 years from the Korea National Health and Nutrition Examination Survey conducted between 2010 and 2019, 1643 with asthma were included. The yearly trends and factors associated with influenza vaccination were analyzed in subjects with asthma. In addition, stratified analyses were performed by age group (<65 versus ⩾65 years).
Results:
During the study period, the overall influenza vaccination rate among subjects with asthma fluctuated from 51.0% to 64.3%, with a consistently higher vaccination rate in elderly subjects than in young subjects. Among young subjects with asthma, factors positively associated with influenza vaccination were female sex [adjusted odds ratio (aOR) = 1.66, 95% confidence interval (CI) = 1.11–2.49], current asthma being treated (aOR = 1.69, 95% CI = 1.14–2.50), history of pulmonary tuberculosis (aOR = 2.01, 95% CI = 1.04–3.87), and dyslipidemia (aOR = 1.86, 95% CI = 1.05–3.30). However, unmarried subjects showed an inverse relationship (aOR = 0.50, 95% CI = 0.34–0.75). In elderly subjects, unmarried status (aOR = 0.52, 95% CI = 0.29–0.94), being underweight (aOR = 0.29, 95% CI = 0.09–0.97), and having a low income (aOR = 0.42, 95% CI = 0.18–0.97) were factors negatively associated with influenza vaccination.
Conclusion:
In the last 10 years, influenza vaccination rates have still been insufficient in subjects with asthma, particularly in young subjects. Considering the factors that are influencing the vaccination rates of young subjects, public policies to increase influenza vaccination rates in subjects with asthma need to be established urgently.
Keywords: asthma, epidemiology, influenza, prevalence, vaccination
Introduction
Asthma is a common inflammatory disorder of the airways characterized by airway hyperresponsiveness. 1 Acute exacerbation of asthma is an important factor associated with increased health care needs, including emergency department visits and hospital admissions.2,3 As a virulent respiratory virus, influenza is one of the common triggers for acute exacerbation of asthma. 4 Subjects with asthma are more susceptible to influenza infection due to impaired antiviral immunity.5,6 Consequently, asthmatics are at increased risk of acute exacerbation, often leading to hospitalization, attributable to influenza infection.7,8
Although there are antiviral treatments for influenza infection, vaccination is the most effective strategy for coping with influenza. 9 The effectiveness of vaccination has been demonstrated in subjects with asthma, which prevented nearly half of influenza infections and approximately 60–80% of asthma attacks.10,11 Accordingly, guidelines have recommended that subjects with asthma should be vaccinated against the influenza virus every year.12–14 However, the previous literature has consistently reported a suboptimal rate of influenza vaccination in this population.15–19 A study using Korean national data reported that the influenza vaccination rate for the general population more than 40 years of age was 45.2%, while it was 76.8% for those aged 65 years and older. 20 In patients with asthma, the influenza vaccination rate for those aged 65 years and older was higher at 81.5%, but the vaccination rate below 50 years of age was only 28.3%. 18 In addition, several factors have been suggested to be associated with low influenza vaccination rates, with young age contributing as a significant factor.16–18,21 Consequently, various methods, such as social marketing, were proposed to increase influenza vaccination rates in young subjects. 22
However, despite these efforts, there are no recent data on whether influenza vaccination rates have increased in subjects with asthma and whether younger age is no longer associated with the low influenza vaccination rates. Therefore, we aimed to investigate the recent yearly trends of influenza vaccination rates and the factors associated with influenza vaccination in subjects with asthma, with a focus on age.
Materials and methods
Study population and design
The Korea National Health and Nutrition Examination Survey (KNHANES) is a population-based nationwide survey that assesses the health and nutritional status of the non-institutionalized Korean population. The survey was conducted by the Korea Disease Control and Prevention Agency (KDCA). The study population was selected using a stratified multistage probability cluster sampling method. More detailed information on the KNHANES has been provided in a previous study. 23
We used data from the KNHANES V (2010–2012), VI (2014–2015), VII (2016–2018), and VIII (2019). In this study, data from the KNHANES 2013 were not included because the influenza vaccination data were not available to the public. A total of 93,338 subjects were included in the surveys over 9 years, and 72,843 agreed to participate (participation rate, 78.0%). Of the 72,843 participants, we excluded subjects aged <18 years (n = 14,659) or those who had missing data for influenza vaccination (n = 6,004). Of the remaining 52,180 subjects, we excluded 50,537 who did not have a history of physician-diagnosed asthma. Finally, 1,643 subjects with asthma were included in the analysis (Figure 1).
Figure 1.
Flow chart of the study population.
Outcomes
The outcomes were as follows: (1) influenza vaccination rate over the study period and (2) factors associated with influenza vaccination in subjects with asthma. Subject’s history of influenza vaccination was investigated using the following question: ‘Have you ever been vaccinated against influenza in the past year?’
Exposure
Subjects with asthma were defined as those with a history of physician-diagnosed asthma. Physician-diagnosed asthma was assessed by the question, ‘Have you ever been diagnosed with asthma by a doctor?’ For stratified analyses, subjects with asthma were further subdivided into (1) young subjects (age < 65 years) and (2) elderly subjects (age ⩾ 65 years).
Measurements and other definitions
Body mass index (BMI) was calculated by dividing an individual’s weight by the square of their height (kg/m2). Past smoking was defined as a person who smoked five or more cigarettes in their lifetime but who does not currently smoke. Single, separated, divorced, and widowed individuals were defined as unmarried. Monthly household income was defined as low for the lowest quartile, intermediate for the second to third quartiles, and high for the highest quartile. Regular walking was defined as walking at least five times a week for more than 30 min at a time. Chronic cough was defined as a cough symptom lasting 3 months or longer. Chronic sputum was defined as sputum accompanied by coughing for more than 3 months per year. Physical limitation was defined using the question, ‘Do you have limitations in your daily life?’ Hypertension was defined as a systolic blood pressure ⩾140 mmHg, diastolic blood pressure ⩾90 mmHg, or treatment with antihypertensive medication. Dyslipidemia was defined as low-density lipoprotein cholesterol level greater than 130 mg/dl, high-density lipoprotein cholesterol level less than 40 mg/dl, or treatment with lipid-lowering medications. Diabetes mellitus was defined as a fasting plasma glucose level of ⩾126 mg/dl or treatment with glucose-lowering medications. Other comorbidities were defined on the basis of a physician’s diagnosis. 24
Statistical analysis
Data are expressed as weighted percentages with standard errors. The p values for differences according to influenza vaccination history were calculated using Pearson’s chi-square test. Logistic regression analysis was performed to explore factors associated with influenza vaccination in subjects with asthma. In multivariable analysis, demographic profiles (age, sex, and BMI), personal habits (smoking status and regular walking), socioeconomic factors (marital status, income, and education), symptoms (any respiratory symptoms and physical limitation), asthma status (no asthma at present, not being treated for asthma, and currently being treated for asthma), and comorbidities were included. Income is included in the adjustment because subjects with asthma have to pay for influenza vaccination, whereas it is free for the elderly (⩾65 years) in Korea.
The sampling weights were adjusted for all analyses using the ‘survey’ package of R. Participants in the single primary survey unit stratum were centered at the sampled grand mean. Missing values were handled using the missing indicator method, which analyzes missing values by grouping them into missing categories. Statistical significance was defined as a two-sided p value of less than 0.05. All analyses were performed using R version 4.0.3 (R Core Team 2021; R Foundation for Statistical Computing, Vienna, Austria).
Results
Baseline characteristics
The baseline characteristics of the subjects with asthma are shown in Table 1. Among subjects with asthma, compared with unvaccinated subjects, those vaccinated against influenza were more likely to be older (58.1% versus 11.5%, p < 0.001) and female (67.5% versus 55.5%, p < 0.001). Vaccinated subjects were less likely to be current smokers (11.4% versus 24.2%, p < 0.001), unmarried (35.5% versus 48.6%, p < 0.001), college graduates (16.3% versus 34.4%, p < 0.001), and regular walker (33.7% versus 41.0%, p = 0.014), but had more respiratory symptoms (18.8% versus 9.6%, p < 0.001) and physical limitations (25.7% versus 12.9%, p < 0.001) and were more likely being treated for asthma (45.7% versus 21.5%, p < 0.001). However, there were no differences in BMI and income between the two groups.
Table 1.
Baseline characteristics of the study population.
| Total (n = 1,643) | Unvaccinated (n = 695) | Vaccinated (n = 948) | p value | |
|---|---|---|---|---|
| Age (years) | <0.001 | |||
| 18–64 | 61.8 (1.4) | 88.5 (1.3) | 41.9 (1.9) | |
| ⩾65 | 38.2 (1.4) | 11.5 (1.3) | 58.1 (1.9) | |
| Sex | <0.001 | |||
| Male | 37.7 (1.3) | 44.5 (2.1) | 32.6 (1.6) | |
| Female | 62.4 (1.3) | 55.5 (2.1) | 67.5 (1.6) | |
| BMI, kg/m2 | 0.096 | |||
| Underweight (<18.5) | 4.7 (1.3) | 6.2 (1.1) | 3.6 (0.7) | |
| Normal weight (18.5–24.9) | 57.6 (0.6) | 57.7 (1.9) | 57.6 (1.8) | |
| Overweight/obese (⩾25) | 37.2 (1.3) | 35.5 (1.9) | 38.5 (1.8) | |
| Smoking status | <0.001 | |||
| Non-smoker | 62.7 (1.3) | 61.0 (2.0) | 64.0 (1.7) | |
| Past smoker | 19.5 (1.1) | 14.1 (1.4) | 23.6 (1.6) | |
| Current smoker | 16.9 (1.1) | 24.2 (1.8) | 11.4 (1.2) | |
| Marital status | <0.001 | |||
| Unmarried | 41.1 (1.3) | 48.6 (2.1) | 35.5 (1.8) | |
| Married | 58.9 (1.3) | 51.4 (2.1) | 64.6 (1.8) | |
| Income | 0.956 | |||
| Low | 29.2 (1.3) | 29.2 (2.0) | 29.2 (1.6) | |
| Intermediate | 48.3 (1.4) | 48.7 (2.0) | 48.1 (1.8) | |
| High | 22.1 (1.2) | 21.6 (1.6) | 22.4 (1.5) | |
| Education | <0.001 | |||
| Elementary school graduate | 36.0 (1.4) | 16.4 (1.6) | 50.7 (1.8) | |
| Middle/high school graduate | 39.0 (1.3) | 48.9 (2.2) | 31.7 (1.7) | |
| College graduate | 24.1 (1.2) | 34.4 (2.0) | 16.3 (1.3) | |
| Regular walking | 36.9 (1.4) | 41.0 (2.1) | 33.7 (1.7) | 0.014 |
| Symptoms | ||||
| Any respiratory symptoms | 14.9 (1.0) | 9.6 (1.2) | 18.8 (1.4) | <0.001 |
| Cough | 9.9 (0.8) | 7.0 (1.1) | 12.0 (1.2) | <0.001 |
| Sputum | 12.3 (0.9) | 7.9 (1.1) | 15.7 (1.3) | <0.001 |
| Physical limitations | 20.2 (1.1) | 12.9 (1.5) | 25.7 (1.5) | <0.001 |
| Asthma status | <0.001 | |||
| No asthma at present | 42.0 (1.4) | 54.4 (2.0) | 32.7 (1.7) | |
| Not being treated for asthma | 22.7 (1.1) | 24.1 (1.8) | 21.6 (1.5) | |
| Currently being treated for asthma | 35.3 (1.3) | 21.5 (1.8) | 45.7 (1.8) | |
| Comorbidities | ||||
| Pulmonary tuberculosis | 9.0 (0.8) | 4.6 (0.9) | 12.3 (1.2) | <0.001 |
| Hypertension | 39.2 (1.4) | 22.6 (1.8) | 51.7 (1.8) | <0.001 |
| Diabetes mellitus | 13.9 (0.9) | 8.5 (1.2) | 18.0 (1.4) | <0.001 |
| Dyslipidemia | 34.3 (1.3) | 26.3 (1.9) | 40.4 (1.8) | <0.001 |
| Allergy | ||||
| Atopic dermatitis | 8.5 (0.8) | 13.3 (1.4) | 4.9 (0.8) | <0.001 |
| Allergic rhinitis | 19.5 (1.1) | 26.0 (1.7) | 14.7 (1.3) | <0.001 |
| Cardiovascular disease | 5.4 (0.7) | 3.3 (0.8) | 7.0 (0.9) | 0.002 |
Data are expressed as weighted percentages (standard errors).
Regarding comorbidities, compared to unvaccinated subjects, vaccinated subjects had more history of pulmonary tuberculosis (12.3% versus 4.6%, p < 0.001), hypertension (51.7% versus 22.6%, p < 0.001), diabetes mellitus (18.0% versus 8.5%, p < 0.001), dyslipidemia (40.4% versus 26.3%, p < 0.001), and cardiovascular disease (7.0% versus 3.3%, p = 0.002), but less atopic dermatitis (4.9% versus 13.3%, p < 0.001) and allergic rhinitis (14.7% versus 26.0%, p < 0.001).
Influenza vaccination rates and yearly trends
The overall influenza vaccination rates were 57.2% for all subjects with asthma, 38.7% for young subjects with asthma, and 87.1% for elderly subjects with asthma. The annual trends in influenza vaccination are shown in Figure 2. More than 10 years, the vaccination rate fluctuated in subjects with asthma, ranging from 51.0% to 64.3%. In younger subjects with asthma, the vaccination rate increased from 36.3% in 2010 to 46.6% in 2014 and then sharply decreased in 2015. This dropped vaccination rate was maintained until 2017 and started to increase in 2018. In elderly subjects with asthma, small fluctuations in vaccination rates were observed between 2010 and 2012, ranging from 80.0% to 88.1%. Thereafter, the vaccination rate increased steadily from 86.8% in 2014 and peaked in 2019 (92.6%).
Figure 2.
Influenza vaccination trends in subjects with asthma between 2010 and 2019.
Factors associated with influenza vaccination
Supplemental Table S1 and Table 2 show univariable and multivariable logistic regression analyses of influenza vaccination in the subjects with asthma, resprectively. In multivariable analysis, age was the factor most strongly associated with influenza vaccination [adjusted odds ratio (aOR) = 6.49, 95% CI (confidence interval) = 4.35–9.67 for ⩾65 years]. Other identified factors showing an association with influenza vaccination were female sex (aOR = 1.72, 95% CI = 1.21–2.44), unmarried state (aOR = 0.51, 95% CI = 0.37–0.71), current asthma being treated (aOR = 1.82, 95% CI = 1.32–2.51), hypertension (aOR = 1.47, 95% CI = 1.07–2.01), and dyslipidemia (aOR = 1.75, 95% CI = 1.07–2.85).
Table 2.
Factors associated with influenza vaccination in subjects with asthma.
| Total subjects (n = 1643) | Young subjects with asthma (n = 999) | Elderly subjects with asthma (n = 644) | ||||
|---|---|---|---|---|---|---|
| aOR (95% CI) | p value | aOR (95% CI) | p value | aOR (95% CI) | p value | |
| Age (years) | ||||||
| 18–64 | Ref. | - | - | - | - | |
| ⩾65 | 6.49 (4.35–9.67) | <0.001 | - | - | - | - |
| Sex | ||||||
| Male | Ref. | Ref. | Ref. | |||
| Female | 1.72 (1.21–2.44) | 0.002 | 1.66 (1.11–2.49) | 0.014 | 1.73 (0.75–4.03) | 0.201 |
| BMI (kg/m2) | ||||||
| Underweight | 0.77 (0.36–1.65) | 0.507 | 1.10 (0.56–2.17) | 0.781 | 0.29 (0.09–0.97) | 0.044 |
| Normal | Ref. | Ref. | Ref. | - | ||
| Overweight or obese | 0.90 (0.68–1.20) | 0.478 | 0.86 (0.61–1.20) | 0.370 | 0.92 (0.50–1.69) | 0.795 |
| Smoking status | ||||||
| Non-smoker | Ref. | Ref. | Ref. | |||
| Past smoker | 1.26 (0.85–1.86) | 0.252 | 1.14 (0.71–1.84) | 0.589 | 1.75 (0.78–3.95) | 0.174 |
| Current smoker | 0.69 (0.45–1.06) | 0.093 | 0.75 (0.46–1.21) | 0.235 | 0.68 (0.26–1.75) | 0.419 |
| Marital status | ||||||
| Unmarried | 0.51 (0.37–0.71) | <0.001 | 0.50 (0.34–0.75) | <0.001 | 0.52 (0.29–0.94) | 0.030 |
| Married | Ref. | Ref. | Ref. | |||
| Income | ||||||
| Low | 0.88 (0.59–1.31) | 0.536 | 1.14 (0.74–1.77) | 0.545 | 0.42 (0.18–0.97) | 0.042 |
| Intermediate | 0.79 (0.59–1.08) | 0.138 | 0.80 (0.56–1.13) | 0.202 | 0.76 (0.34–1.71) | 0.510 |
| High | Ref. | Ref. | Ref. | - | ||
| Education | ||||||
| Elementary school graduate | Ref. | Ref. | Ref. | - | ||
| Middle/high school graduate | 0.72 (0.48–1.08) | 0.114 | 0.66 (0.38–1.12) | 0.125 | 0.88 (0.42–1.86) | 0.736 |
| College graduate | 0.65 (0.41–1.03) | 0.068 | 0.64 (0.36–1.12) | 0.115 | 0.54 (0.15–1.99) | 0.352 |
| Regular walking | 0.93 (0.71–1.22) | 0.617 | 0.79 (0.57–1.08) | 0.140 | 1.76 (0.90–3.42) | 0.098 |
| Any respiratory symptoms | 1.11 (0.76–1.63) | 0.588 | 1.22 (0.76–1.96) | 0.407 | 0.93 (0.49–1.80) | 0.837 |
| Asthma status | ||||||
| No current asthma | Ref. | Ref. | Ref. | - | ||
| Current asthma being untreated | 0.93 (0.65–1.32) | 0.672 | 0.87 (0.58–1.31) | 0.499 | 0.99 (0.45–2.14) | 0.972 |
| Current asthma being treated | 1.82 (1.32–2.51) | <0.001 | 1.69 (1.14–2.50) | 0.009 | 1.80 (0.93–3.50) | 0.081 |
| Physical limitations | 1.11 (0.77–1.58) | 0.577 | 1.08 (0.68–1.71) | 0.743 | 1.26 (0.64–2.49) | 0.506 |
| Comorbidities | ||||||
| Pulmonary tuberculosis | 1.55 (0.92–2.63) | 0.100 | 2.01 (1.04–3.87) | 0.037 | 1.01 (0.47–2.13) | 0.987 |
| Hypertension | 1.47 (1.07–2.01) | 0.018 | 1.34 (0.90–1.98) | 0.151 | 1.70 (0.92–3.14) | 0.092 |
| Diabetes mellitus | 1.03 (0.64–1.66) | 0.912 | 1.23 (0.62–2.42) | 0.548 | 0.89 (0.42–1.91) | 0.767 |
| Dyslipidemia | 1.75 (1.07–2.85) | 0.026 | 1.86 (1.05–3.30) | 0.035 | 1.20 (0.35–4.14) | 0.770 |
| Allergy | ||||||
| Atopic dermatitis | 0.77 (0.45–1.34) | 0.355 | 0.86 (0.48–1.53) | 0.605 | 0.61 (0.15–2.46) | 0.486 |
| Allergic rhinitis | 0.92 (0.61–1.37) | 0.669 | 0.99 (0.62–1.56) | 0.954 | 0.73 (0.28–1.92) | 0.522 |
| Cardiovascular disease | 0.77 (0.40–1.48) | 0.433 | 0.73 (0.24–2.23) | 0.585 | 0.74 (0.29–1.86) | 0.518 |
OR, odds ratio; CI, confidence interval.
Bold font indicates statistical significance.
In the stratified analysis, young subjects with asthma, who are female (aOR = 1.66, 95% CI = 1.11–2.49), receiving current asthma treatment (aOR = 1.69, 95% CI = 1.14–2.50), and with a history of pulmonary tuberculosis (aOR = 2.01, 95% CI = 1.04–3.87) or dyslipidemia (aOR = 1.86, 95% CI = 1.05–3.30) were positively associated with influenza vaccination, whereas those with an unmarried status were negatively associated (aOR = 0.50, 95% CI = 0.34–0.75). Among elderly subjects with asthma, those who were underweight (aOR = 0.29, 95% CI = 0.09–0.97), unmarried (aOR = 0.52, 95% CI = 0.29–0.94), and had a low income (aOR = 0.42, 95% CI = 0.18–0.97) were less likely to be vaccinated against influenza.
Discussion
This study comprehensively investigated trends of and factors associated with influenza vaccination rate in subjects with asthma using recent nationwide population-based data of Korea. In the analysis of the trend between 2010 and 2019, the influenza vaccination rate among subjects with asthma has fluctuated at a suboptimal level without a significant increase. In addition, our results showed that lower influenza vaccination rate in subjects with asthma is mostly attributable to young subjects and revealed several important factors associated with vaccination uptake.
Previous studies from western countries have shown the low influenza vaccination rate in subjects with asthma. According to the 2007 Behavioral Risk Factor Surveillance System in the United States, influenza vaccination coverage was 39.9% for adult asthmatics (⩾16 years of age). 15 Influenza vaccination rates in European countries (⩾16 years of age) were 38.0% in the Spanish National Health Study 2006 17 and 35.2% in the European Health Survey 2009, 16 which is comparable to that in the United States. In Korea, the influenza vaccination rate was 61.1% for adults with asthma from 2010 Korean Community Health Survey (⩾19 years of age). 18 However, in another recent Korean study using 2017 Korea Youth Risk Behavior Web-Based Survey, the influenza vaccination rate was 41.8% in Korean adolescents (13–18 years of age) with asthma. 19
After the 2009 influenza pandemic, only a few studies have investigated the influenza vaccination rates in subjects with asthma,18,19 and studies that have evaluated the long-term trend of influenza vaccination are even scarcer. Previously, World Health Assembly recommended increasing influenza vaccination coverage up to at least 75% in subjects with underlying diseases. Surprisingly, contrary to expectations, the influenza vaccination rate in subjects with asthma remains suboptimal and has not increased over the last decade. This suggests that despite national and international asthma guidelines emphasizing the importance of influenza vaccination for asthmatics,12,13 the current vaccination strategies are insufficient to encourage them to be vaccinated. Moreover, given that coinfection with SARS-CoV-2 and influenza virus was associated with a higher risk of poor outcomes,26,27 it would be important to re-evaluate whether influenza vaccination for asthma is adequately implemented in each country.
Many factors are associated with influenza vaccination rates in subjects with asthma, and a well-known factor is age.16–18,21,28 In a pooled analysis of a national population-based survey of Canada, Guthrie et al. 29 reported the rate of ‘feeling that influenza vaccine was unnecessary’ was 1.6-fold higher in adult asthmatics aged 18–24 years than those aged 55–64 years. Our study showed that only 38% of young subjects with asthma were vaccinated, whereas almost 90% of elderly subjects with asthma were vaccinated. First, this large difference may be explained by public policies. The Korean government expanded the coverage for free influenza vaccination from 2005 to include elderly subjects (aged ⩾ 65 years), 30 which might have contributed to the results of our study. Second, it is known that many young adults are hesitant to be vaccinated against various diseases, including influenza. 31 The suggested reasons are unawareness of vaccination recommendations, mistrust of vaccination effects, and confidence in their health.17,28 Whether influenza infection in young subjects with asthma who had infrequent asthma symptoms is associated with severe outcomes remains unclear. However, it is well known that subjects with mild asthma are still at risk of severe asthma exacerbation, 32 and exposure to viruses that might trigger this is unpredictable. Thus, clinicians should evaluate the influenza vaccination status of young subjects with asthma and make greater efforts to vaccinate them against influenza.
In line with the previous studies in asthmatics,15,18,33 we found increased adherence to influenza vaccination in women and in subjects who were married. In addition, subjects who received asthma treatment and had a history of pulmonary tuberculosis and dyslipidemia were more likely to be vaccinated against influenza. It seems natural that subjects who have been treated in the past or are currently receiving treatment for respiratory diseases, such as asthma and pulmonary tuberculosis, are more prone to influenza vaccination. 16 Subjects with chronic diseases, such as diabetes and dyslipidemia, might have higher chances to interact with health care providers than those without chronic diseases. Moreover, physicians will probably pay more attention to influenza prevention in their patients. This is because patients with chronic diseases may be at a higher risk of serious influenza-related outcomes if they also have asthma. 34 These circumstances may lead to increased vaccination uptake. However, the exact social or biological mechanism of these factors leading to influenza vaccination remains an issue warranting future studies.
Moreover, being underweight, being unmarried, and having a low income were found to be related to decreased influenza vaccination rates among elderly subjects with asthma. The benefits from vaccination might be greater in this population, as these are known to be associated with various health issues.35–37 Nevertheless, misbeliefs caused by a lack of information, such as concerns about vaccine side effects, may prevent this population from becoming vaccinated. 28 Although the overall influenza vaccination rate is sufficient in elderly subjects with asthma, it is necessary to examine whether there are other underprivileged populations within the elderly.
The strength of this study is that recent influenza vaccination rates among subjects with asthma were analyzed using nationally representative survey data. Through a 10-year trend analysis, our study found that the asthma guidelines’ recommendations for influenza vaccination are not followed in the real world. Nonetheless, very few studies have reported influenza vaccination trends among asthmatic subjects after the 2009 influenza pandemic. Therefore, similar studies need to be conducted in each country to investigate and improve the national influenza vaccination rates in subjects with asthma. Another strength is that comprehensive factors were included to evaluate their association with influenza vaccination, which can help identify subgroups of subjects with asthma in whom to encourage vaccination. However, our study had some limitations. First, the causal relationship identified was uncertain because our study was conducted using cross-sectional data. Second, recall bias was possible because a history of asthma and influenza vaccination was assessed using a questionnaire. Third, common barriers to influenza vaccination among asthmatics, such as support for vaccination and worries about being sick after vaccination, 28 were not investigated in this study. Fourth, although we included the variable of current treatment status (being treated versus untreated) in the analysis, we could not include detailed information on treatment, such as asthma duration or treatment steps, because these data were not available in the KNHANES dataset. Fifth, in some categories, such as underweight elderly subjects, the number of subjects was relatively small. Findings in these categories require cautious interpretation. Finally, the uniqueness of the Korean medical system should be considered when interpreting the results because Korea implements the National Health Insurance System. Therefore, generalizations to other countries must be carefully made.
In conclusion, influenza vaccination rates have been insufficient in subjects with asthma in the last 10 years. The influenza vaccination rate was consistently lower in young subjects with asthma than that in the elderly. In young subjects with asthma, female sex, current asthma treatment, history of pulmonary tuberculosis, and dyslipidemia were positively associated with influenza vaccination, whereas an unmarried status was negatively associated. Public policies to increase influenza vaccination rates in subjects with asthma, considering the factors that are influencing the vaccination rates of young subjects, urgently need to be established.
Supplemental Material
Supplemental material, sj-docx-1-taj-10.1177_20406223221123979 for Trends and factors associated with influenza vaccination in subjects with asthma: analysis of the Korea National Health and Nutrition Examination Survey between 2010 and 2019 by Sang Hyuk Kim, Hye Yun Park, Hwasik Jung, Sungmin Zo, Saerom Kim, Dong Won Park, Tai Sun Park, Ji-Yong Moon, Sang-Heon Kim, Tae-Hyung Kim, Jang Won Sohn, Ho Joo Yoon, Hyun Lee and Sun Hye Shin in Therapeutic Advances in Chronic Disease
Acknowledgments
There are no acknowledgements to declare.
Footnotes
ORCID iDs: Sang Hyuk Kim 
https://orcid.org/0000-0002-0410-8524
Sang-Heon Kim
https://orcid.org/0000-0001-8398-4444
Hyun Lee
https://orcid.org/0000-0002-1269-0913
Sun Hye Shin
https://orcid.org/0000-0003-3164-889X
Supplemental material: Supplemental material for this article is available online.
Contributor Information
Sang Hyuk Kim, Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Internal Medicine, Hallym University Kangnam Sacred Heart Hospital, Seoul, Korea.
Hye Yun Park, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
Hwasik Jung, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
Sungmin Zo, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
Saerom Kim, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
Dong Won Park, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Tai Sun Park, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Ji-Yong Moon, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Sang-Heon Kim, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Tae-Hyung Kim, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Jang Won Sohn, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Ho Joo Yoon, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea.
Hyun Lee, Division of Pulmonary Medicine and Allergy, Department of Internal Medicine, Hanyang University College of Medicine, 222, Wangsimni-ro Seongdong-gu, Seoul 04763, Korea.
Sun Hye Shin, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81, Irwon-ro, Gangnam-gu, Seoul 06351, Korea..
Declarations
Ethics approval and consent to participate: We conducted this study following the Declaration of Helsinki. The Institutional Review Board (IRB) of the KDCA approved the study (IRB: 2010-02CON-21-C, 2011-02CON-06-C, 2012-01EXP-01-2C, 2013-12EXP-03-5C, 2018-01-03-P-A, and 2018-01-03-C-A). Written informed consent was obtained from all participants, and anonymized data were provided.
Consent for publication: Not applicable.
Author contributions: Sang Hyuk Kim: Data curation; Formal analysis; Visualization; Writing – original draft.
Hye Yun Park: Writing – original draft.
Hwasik Jung: Writing – review & editing.
Sungmin Zo: Writing – review & editing.
Saerom Kim: Writing – review & editing.
Dong Won Park: Writing – review & editing.
Tai Sun Park: Writing – review & editing.
Ji-Yong Moon: Writing – review & editing.
Sang-Heon Kim: Writing – review & editing.
Tae-Hyung Kim: Writing – review & editing.
Jang Won Sohn: Writing – review & editing.
Ho Joo Yoon: Writing – review & editing.
Hyun Lee: Conceptualization; Supervision; Validation; Writing – original draft.
Sun Hye Shin: Supervision; Validation; Writing – original draft.
Funding: The authors received no financial support for the research, authorship, and/or publication of this article.
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Availability of data and materials: Raw data of this study are publicly available in Korea Disease Control and Prevention Agency database (https://knhanes.kdca.go.kr/knhanes/sub03/sub03_02_05.do).
References
- 1. Huang K, Yang T, Xu J, et al. Prevalence, risk factors, and management of asthma in China: a national cross-sectional study. Lancet 2019; 394: 407–418. [DOI] [PubMed] [Google Scholar]
- 2. Ekström M, Nwaru BI, Wiklund F, et al. Risk of rehospitalization and death in patients hospitalized due to asthma. J Allergy Clin Immunol Pract 2021; 9: 1960–1968. [DOI] [PubMed] [Google Scholar]
- 3. Zein JG, Wu CP, Attaway AH, et al. Novel machine learning can predict acute asthma exacerbation. Chest 2021; 159: 1747–1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Veerapandian R, Snyder JD, Samarasinghe AE. Influenza in asthmatics: for better or for worse? Front Immunol 2018; 9: 1843–1843. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Wark PAB. Why are people with asthma more susceptible to influenza. Eur Respir J 2019; 54: 1901748. [DOI] [PubMed] [Google Scholar]
- 6. Wu Q, Jiang D, Smith S, et al. IL-13 dampens human airway epithelial innate immunity through induction of IL-1 receptor-associated kinase M. J Allergy Clin Immunol 2012; 129: 825–833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Papadopoulos NG, Christodoulou I, Rohde G, et al. Viruses and bacteria in acute asthma exacerbation—a GA2 LEN-DARE systematic review. Allergy 2011; 66(4)458–468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Trinh P, Jung TH, Keene D, et al. Temporal and spatial associations between influenza and asthma hospitalisations in New York City from 2002 to 2012: a longitudinal ecological study. BMJ Open 2018; 8: e020362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Brody H. Influenza. Nature 2019; 573: S49. [DOI] [PubMed] [Google Scholar]
- 10. Martínez-Baz I, Navascués A, Casado I, et al. Effect of influenza vaccination in patients with asthma. CMAJ 2021; 193: E1120–E1128. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Vasileiou E, Sheikh A, Butler C, et al. Effectiveness of influenza vaccines in asthma: a systematic review and meta-analysis. Clin Infect Dis 2017; 65: 1388–1395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Global Initiative for Asthma (GINA). Global strategy for asthma management and prevention, https://ginasthma.org/wp-content/uploads/2021/05/GINA-Main-Report-2021-V2-WMS.pdf (accessed 29 July 2022).
- 13. The Korean Academy of Tuberculosis and Respiratory Disease. Korean guideline for asthma: Updated 2020, https://lungkorea.org/bbs/?code=guide (accessed 29 July 2022).
- 14. British guideline on the management of asthma. Thorax 2008; 63(Suppl. 4): iv, 1–121. [DOI] [PubMed] [Google Scholar]
- 15. Lu PJ, Euler GL, Callahan DB. Influenza vaccination among adults with asthma findings from the 2007 BRFSS survey. Am J Prev Med 2009; 37: 109–115. [DOI] [PubMed] [Google Scholar]
- 16. Santos-Sancho JM, López-de Andrés A, Jimenez-Trujillo I, et al. Adherence and factors associated with influenza vaccination among subjects with asthma in Spain. Infection 2013; 41: 465–471. [DOI] [PubMed] [Google Scholar]
- 17. Jiménez-García R, Hernández-Barrera V, Carrasco-Garrido P, et al. Coverage and predictors of adherence to influenza vaccination among Spanish children and adults with asthma. Infection 2010; 38: 52–57. [DOI] [PubMed] [Google Scholar]
- 18. Chung JH, Kim TH, Han CH. Factors influencing influenza vaccination among South Korean adult asthma patients: a nationwide population-based cross-sectional study. J Asthma 2018; 55: 294–299. [DOI] [PubMed] [Google Scholar]
- 19. Kyung Y, Choi MH, Lee JS, et al. Influencing factors for influenza vaccination among South Korean adolescents with asthma based on a nationwide cross-sectional study. Int Arch Allergy Immunol 2020; 181: 434–445. [DOI] [PubMed] [Google Scholar]
- 20. Cha SH, Paik JH, Lee MR, et al. Influenza vaccination coverage rate according to the pulmonary function of Korean adults aged 40 years and over: analysis of the fifth Korean National Health and Nutrition Examination Survey. J Korean Med Sci 2016; 31: 709–714. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Kwon DS, Kim K, Park SM. Factors associated with influenza vaccination coverage among the elderly in South Korea: the Fourth Korean National Health and Nutrition Examination Survey (KNHANES IV). BMJ Open 2016; 6: e012618. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Lee Y-I, Jin Y, Nowak G. Motivating influenza vaccination among young adults: the effects of public service advertising message framing and text versus image support. Soc Market Quarter 2018; 24: 89–103. [Google Scholar]
- 23. Kweon S, Kim Y, Jang MJ, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 2014; 43: 69–77. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Lee H, Shin SH, Gu S, et al. Racial differences in comorbidity profile among patients with chronic obstructive pulmonary disease. BMC Med 2018; 16: 178. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Prevention and control of influenza pandemics and annual epidemics, https://apps.who.int/gb/archive/pdf_files/WHA56/ea56r19.pdf (accessed 29 July 2022). [Google Scholar]
- 26. Zheng J, Chen F, Wu K, et al. Clinical and virological impact of single and dual infections with influenza A (H1N1) and SARS-CoV-2 in adult inpatients. PLoS Negl Trop Dis 2021; 15: e0009997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Yue H, Zhang M, Xing L, et al. The epidemiology and clinical characteristics of co-infection of SARS-CoV-2 and influenza viruses in patients during COVID-19 outbreak. J Med Virol 2020; 92: 2870–2873. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Bigaj J, Czaicki N, Zielonka TM. Factors affecting influenza vaccination rate in adults with asthma. Adv Exp Med Biol 2020; 1279: 101–111. [DOI] [PubMed] [Google Scholar]
- 29. Guthrie JL, Fisman D, Gardy JL. Self-rated health and reasons for non-vaccination against seasonal influenza in Canadian adults with asthma. PLoS ONE 2017; 12: e0172117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Yun JW, Noh JY, Song JY, et al. The Korean influenza national immunization program: history and present status. Infect Chemother 2017; 49: 247–254 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Dratva J, Wagner A, Zysset A, et al. To vaccinate or not to vaccinate – this is the question among Swiss University Students. Int J Environ Res Public Health 2021; 18: 9210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32. Dusser D, Montani D, Chanez P, et al. Mild asthma: an expert review on epidemiology, clinical characteristics and treatment recommendations. Allergy 2007; 62: 591–604. [DOI] [PubMed] [Google Scholar]
- 33. Mazurek JM, White GE, Moorman JE, et al. Influenza vaccination among persons with work-related asthma. Am J Prev Med 2014; 47: 203–211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34. Mertz D, Kim TH, Johnstone J, et al. Populations at risk for severe or complicated influenza illness: systematic review and meta-analysis. BMJ 2013; 347: f5061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35. Dhindsa DS, Khambhati J, Schultz WM, et al. Marital status and outcomes in patients with cardiovascular disease. Trends Cardiovasc Med 2020; 30: 215–220. [DOI] [PubMed] [Google Scholar]
- 36. Yang B, Han K, Kim SH, et al. Being underweight increases the risk of non-cystic fibrosis bronchiectasis in the young population: a nationwide population-based study. Nutrients 2021; 13: 3206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Mendenhall E, Kohrt BA, Norris SA, et al. Non-communicable disease syndemics: poverty, depression, and diabetes among low-income populations. Lancet 2017; 389: 951–963. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplemental material, sj-docx-1-taj-10.1177_20406223221123979 for Trends and factors associated with influenza vaccination in subjects with asthma: analysis of the Korea National Health and Nutrition Examination Survey between 2010 and 2019 by Sang Hyuk Kim, Hye Yun Park, Hwasik Jung, Sungmin Zo, Saerom Kim, Dong Won Park, Tai Sun Park, Ji-Yong Moon, Sang-Heon Kim, Tae-Hyung Kim, Jang Won Sohn, Ho Joo Yoon, Hyun Lee and Sun Hye Shin in Therapeutic Advances in Chronic Disease