Abstract
The aim of the current study was to analyze the relationship between plant food (fruits, vegetables, and kimchi) and the prevalence of rhinitis among Korean adults using data from the 2011 and 2012 Korea National Health and Nutrition Examination Survey. A total of 7494 subjects aged from 19 to 64 years participated in a rhinitis morbidity survey, health behavior interview, and 24-h dietary recall test. Individuals with energy intakes less than 500 kcal or more than 5000 kcal were excluded. The results showed that kimchi intake was inversely associated with the prevalence of rhinitis. The prevalence of rhinitis decreased with increasing kimchi consumption. The quintile 4 (range of kimchi intake: 108.0–180.0 g) groups, compared with the reference of quintile 1 (0–23.7 g), showed a decrease of 18.9% (odds ratio [OR] = 0.811, 95% confidence interval [CI] = 0.672–0.979) in Model 4. In conclusion, consumption of kimchi lowers the risk of rhinitis, suggesting that its use should be encouraged among the Korean population.
Introduction
R
Kimchi is a fermented side dish rich in vitamins, minerals, dietary fibers, and other biological compounds, including lactic acid bacteria (LAB), in Korea. 6,7 Many studies have reported on the valuable effects of kimchi, including antimutagenic, 8 anticancer, 9 antioxidant, 10 antiaging, 11 antiatherogenic, 12 antiobesity, 13 antidiabetic activities, 14 and fibrinolytic effects. 15
Due to changes in dietary habits in recent decades, consumption of vegetables and fruits, including kimchi, has gradually decreased among the Korean population. Many researchers have reported on consumption trends and health effects of consuming vegetables and fruits. 16 –20 The National Health Plan 2020 of Korea aims to increase vegetable and fruit intake up to 50% in Koreans who consume 500 g and more of vegetables and fruits daily. 21 The typical serving size of kimchi was reported to be 40 g per meal based on the Baechu (Chinese cabbage) kimchi most consumed among Koreans, as reported for the dietary reference intakes for Koreans in 2015 legislated from the Ministry of Health and Welfare and the Korean Nutrition Society. 6,22 Previous studies examined the biological properties of LAB from fermented kimchi as well as sensory and physicochemical qualities of various ingredients. 23 –27 A few previous studies on the relationship between some allergic diseases such as atopic dermatitis and asthma and dietary factors have been reported. 28,29 Kim et al. 28 investigated the relationship between kimchi consumption and asthma in Korean adults. It was also reported that kimchi has beneficial effects on immune function for atopic dermatitis in mice. 29 Although rhinitis has shown a gradual increase in adults as well as infants and children in Korea, research on the relationship between dietary factors and the prevalence of rhinitis has never been reported.
The objective of the current study examined the relationship between plant food (fruits, vegetables, and kimchi) intake and the prevalence of rhinitis among Korean adults using data from the 2011 and 2012 KNHANES.
Materials and Methods
Study population
This study was based on the 2011 and 2012 KNHANES data (the Rhinitis Prevalence Survey was not conducted in 2010). A total of 7494 subjects aged from 19 to 64 years participated in the rhinitis morbidity survey, health behavior interview, and 24-h dietary recall test. Individuals who ate less than 500 kcal or more than 5000 kcal of daily total caloric intake were excluded. The study was approved by the institutional review board of Korea Centers for Disease Control and Prevention (2011-02CON-06-C, 2012-01EXP-01-2C).
General characteristics
General characteristics of subjects were grouped according to gender (male and female), age (19–29, 30–49, and 50–64), household income (high, middle high, middle low, and low), residential area (city and rural area), marital status (married, unmarried), occupation status (employed, unemployed), and educational level (less than graduate of a high school, graduate of a high school, and college degree or more) based on the guidelines of the 2011 and 2012 KNHANES.
Health-related behaviors
Smoking status (current smoker, ex-smoker, and nonsmoker), drinking status (≥4 times/week, 2–3 times/week, 1–4 times/month, and <1 time/month), stress status (feel it very much, feel somewhat, feel a little, and rarely), and exercise status (<1 day/week, 1–2 days/week, 3–4 days/week, and ≥5 days/week) were examined for analysis of health-related behaviors. Weight status based on the body mass index (kg/m2) was divided according to four groups: underweight, <18.5; normal, 18.5–23.0; overweight, 23.0–25.0; and obese, ≥25.0.
Dietary behaviors of subjects
Meal occasion (breakfast, lunch, and dinner), snack (yes or no), frequency of meals per day, eating out frequency (≥2 times/day, once per day, 5–6 times/week, 3–4 times/week, 1–2 times/week, 1–3 times/month, rarely), and food security. Food security status was assessed using a self-reported hunger measure on the dietary situation of subjects' households in the previous year based on the KNHANES data and regarded as household food security status of subject. 30 Four groups of food security status were classified, including the enough food secure group, defined as enough and various foods to eat for all family members; mildly food insecure group, defined as a sufficient amount of food, but insufficient variety of food; the moderately food insecure group, defined as sometimes unable to acquire enough food to eat because of insufficient money; and the severely food insecure group, defined as often not enough food to eat because of insufficient money, based on the previous studies. 30,31
Criteria for the definition of rhinitis
The prevalence of rhinitis was defined with self-reported physician diagnosis of rhinitis (variable name: T_Q_ARDG, Questionnaire diagnosed with rhinitis by a doctor) in the health interview surveys (a survey question regarding sinusitis was excluded). Subjects who responded yes were classified as having rhinitis. Subjects with a response of no were classified as normal subjects without rhinitis, and subjects who did not respond were excluded.
Intake of food and nutrient
In this study, food and nutrient intakes except plant foods were analyzed using the variables of food code (variable name: n_kindg1, n_kindg2) and food intake (variable name: nf_intk) on the data of the 24-h recall test. Items of food group intake were categorized based on the variables of classification for 18 food group intakes (total food, cereals and grain products, potatoes and starches, sugars and sweets, legumes and their products, seeds and nuts, vegetables, mushrooms, fruits, meat, poultry, and their products, eggs, fish and shellfish, seaweeds, milk and dairy products, oils and fats, beverages, seasonings, and other foods). Intakes of macronutrient and micronutrient and the percentage of carbohydrates, fat, and proteins contributing to energy at the individual level were also calculated.
Intake of plant food (kimchi, nonsalted vegetables, and fruits)
The total nonsalted vegetable and fruit intakes per day were calculated using the variables of the food code name (variable name: n_fname2) and food intake (variable name: nf_intk) on the 24-h recall test of the KNHANES. For analysis of intake of nonsalted vegetables and fruits, salted vegetables (salted and pickled vegetables), starch vegetables (potato, sweet potato, corn, etc.), dried vegetables, jams, canned fruits with sugar, and fruit juice were excluded based on the study by Kwon et al. 32 Kimchi intake was analyzed using variables related to dish name (variable name: n_dname), food code (variable name: n_fcode2), food name (variable name: n_fname2), and food intake (variable name: nf_intk) based on the 24-h recall test. In this study, kimchi included baechu (Chinese cabbage) kimchi, godulbaegi (lxeris sonchifolia H.) kimchi, gat (mustard leaf) kimchi, ggakdugi (diced radish kimchi), buchu (Korean leek) kimchi, pa (scallion) kimchi, oisobaki (stuffed cucumber kimchi), seokbakji (radish and various vegetables kimchi), nabak kimchi (radish watery kimchi), dongchimi (water-based radish kimchi), yeolmu (young summer radish) kimchi, altarimu (young radish) kimchi, bossam (wrapped kimchi) kimchi, sunmu (turnip) kimchi, yuchae (canola) kimchi, baek (white kimchi), geotjeoli (fresh kimchi), ggaennip (perilla leaf) kimchi, and earlgari baechu (winter-grown cabbage) kimchi.
Statistical analyses
Statistical analyses were performed using SAS software, version 9.4 (SAS Institute, Cary, NC, USA). Due to the complex sampling design of the KNHANES study, the relevant primary sampling units, stratification, and sample weights were considered in our analysis. The results of general characteristics and dietary factors were in the form of frequency and weighted% between the group without rhinitis and the group with rhinitis using frequency analysis. Food and nutrient intakes according to the prevalence of rhinitis are in forms of mean and standard error through the survey mean procedure. The difference in food and nutrient intake according to the prevalence of rhinitis was tested by t-test without adjustment and tested using the generalized linear model procedure with adjustment through the surveyreg procedure of SAS. The adjustment variables were gender, age, and energy intakes. Plant intakes were classified according to four categories (nonsalted vegetables+fruits, kimchi, kimchi+nonsalted vegetables, kimchi+nonsalted vegetables+fruits) and the intakes were divided according to quintiles (quintile 1, quintile 2, quintile 3, quintile 4, and quintile 5). Regarding the association with the five groups and rhinitis prevalence, the odds ratio (OR) and 95% confidence interval (CI) were obtained using the surveylogistic procedure. Multivariate logistic regression was performed and adjustments were gradually performed for all independent variables, including demographic, dietary, and lifestyle factors. All analyses were two-tailed and a P-value = .05 was considered statistically significant.
Results
General characteristics according to the prevalence of rhinitis
Table 1 shows the general characteristics of subjects. The prevalence of rhinitis in Korean adults aged 19 to 64 years was 16.3%. Among the study sample of 7494 subjects, the proportion of males was 3.4% higher than that of females for subjects without rhinitis and the proportion of females was inversely 13.4% higher than that of males for subjects with rhinitis (P < .0001). The 30–49 age group had the largest number of subjects (with and without rhinitis) among the three age groups, and average age was 41.8 for subjects without rhinitis and 37.1 for those with rhinitis (P < .0001). The majority of subjects with and without rhinitis had an education level of college or higher. Regarding household income, subjects in the high group without rhinitis and middle-high group with rhinitis showed the highest proportions among four groups of subjects (P < .001).
Subjects without rhinitis.
Weighted%.
Subjects with rhinitis.
P-value by chi-square.
P-value by t-test.
Health-related behaviors of subjects according to the prevalence of rhinitis
Health-related behaviors of subjects according to the prevalence of rhinitis are shown in Table 2. Among the 7494 subjects, rhinitis (28.1%) was 8.9% higher in the smoker group than in those without rhinitis (19.2%). Regarding alcohol consumption status, the proportion of 1–4 times per month group with rhinitis (3.9%) was 3.1% lower than those without rhinitis (7.0%). No differences in stress status and exercise were observed between subjects with and without rhinitis. Regarding the weight status, subjects with and without rhinitis showed the highest rate of normal, followed by obesity groups (P = .0025).
Subjects without rhinitis.
Weighted%.
Subjects with rhinitis.
P-value by chi-square.
BMI, body mass index.
Dietary behaviors of subjects according to the prevalence of rhinitis
Table 3 shows dietary behaviors of subjects according to the prevalence of rhinitis. No differences in daily meals, snack intake, or food security status were observed between subjects with and without rhinitis. Eating out frequency data revealed a higher proportion in the groups of 1–2 times per week, 3–4 times per week, 5–6 times per week, one time per day, and ≥2 times per day for subjects with rhinitis than those without rhinitis. Inversely, groups with 1–3 times per month and rarely for subjects with rhinitis showed a lower proportion than those without rhinitis (P = .0008).
Subjects without rhinitis.
Weighted%.
Subjects with rhinitis.
P-value by chi-square.
Nutrient intake of subjects according to the prevalence of rhinitis
Nutrient intakes of subjects according to the prevalence of rhinitis are shown in Table 4. When the adjustment was performed, differences in the contribution rate of protein for energy were observed between subjects with and without rhinitis (crude P-value <.05); however, no differences were observed when the adjustments for gender, age, and energy intake were performed. The ratios of protein to fat energy contribution were higher in subjects with rhinitis than in those without rhinitis; however, the ratio contributed by carbohydrate energy and fiber intake was higher in subjects without rhinitis than in those with rhinitis. The intake of vitamin C for the subjects with rhinitis was higher than those without rhinitis in both adjusted and unadjusted instances. A significant difference was observed after adjustments for gender, age, and energy intake (adjusted P-value = .0093). Regarding the contribution rate of carbohydrates and fat for energy, there were significant differences in both adjusted (gender, age, and energy intake) and unadjusted instances (crude P-value <.0001, adjusted P-value <.05). In particular, the percent of energy from carbohydrates was higher in subjects without rhinitis than in those with rhinitis and the percentage of energy from fat was higher in subjects with rhinitis than in those without rhinitis.
Subjects without rhinitis.
Subjects with rhinitis.
P-value by t-test.
Adjusted for gender, age, and energy intake using the procedure surveyreg of SAS.
Food group intakes of subjects according to the prevalence of rhinitis
Food intakes of subjects according to the prevalence of rhinitis are shown in Table 5. Significant differences in the intake of vegetables and milk and dairy products were observed between subjects with and without rhinitis when the adjustment was not performed (crude P-value <.05). However, no differences were observed when data were adjusted for gender, age, and energy intake. In addition, significant differences in the intake of oils and fats were observed between subjects with and without rhinitis when the adjustment was not performed, but a significant difference was observed when the adjustments for gender, age, and energy intake were performed (adjusted P-value <.05). Especially, the intakes of fruit between subjects without and with rhinitis were not significantly different when there were no adjustments. However, when adjusted for gender, age, and energy intake, the intakes of fruit were significantly different (adjusted P-value <.05). No significant differences in the intakes of the other foods were observed between subjects with and without rhinitis.
Subjects without rhinitis.
Subjects with rhinitis.
P-value by t-test.
Adjusted for gender, age, and energy intake.
Including salted vegetable, kimchi, and vegetable juice.
Including fruits preserved in sugar, jam, and fruit juice.
Intake of plant food (nonsalted vegetables, fruits, and kimchi) of subjects according to the prevalence of rhinitis
Intakes of plant food (nonsalted vegetables, fruits, and kimchi) of subjects according to the prevalence of rhinitis are shown in Table 6. Intake of nonsalted vegetables, fruits, and kimchi was analyzed using the variables of food name, food code, dish name, dish code, and food intake. Intakes of all plant foods for subjects with rhinitis were lower than in those without rhinitis for both adjusted and unadjusted data.
Subjects without rhinitis.
Subjects with rhinitis.
p-value by t-test.
p-value by GLM (Generalized Linear Model).
Adjusted for gender, age and energy intake.
Excluding fruits preserved in sugar, jam and fruits juice.
Excluding salted vegetable and vegetable juice.
Ratio of prevalence of rhinitis by their quintiles and intake range of plant food
Ratios of prevalence of rhinitis according to quintiles and intake range of plant food (nonsalted vegetables, fruits, and kimchi) are shown in Table 7. The quintiles of plant food intake were divided based on the classification of plant food (nonsalted vegetables+fruits, kimchi, nonsalted vegetables+kimchi, nonsalted vegetables+kimchi+fruits) as shown in Table 6. According to the quintile of plant food intake, the prevalence of rhinitis was 15.1–18.0% for nonsalted vegetables+fruits, 14.8–19.7% for kimchi, 15.2–18.3% for nonsalted vegetables+kimchi, and 15.7–17.4% for nonsalted vegetables+kimchi+fruits.
Without: Subjects without rhinitis, With: Subjects with rhinitis.
Weighted%.
Relationship between prevalence of rhinitis and plant food intake
Logistic regression analysis of the relationship between prevalence of rhinitis and plant food intake is shown in Table 8. Logistic regression analysis was performed to determine the relationship between prevalence of rhinitis and plant food intake (nonsalted vegetable+fruit intake, kimchi intake, nonsalted vegetable+kimchi intake, nonsalted vegetable+kimchi+fruit intake). The results showed that only kimchi intake was inversely associated with the prevalence of rhinitis. In results for decreased prevalence of rhinitis, the quintile 3 (range of kimchi intake: 60.53–108.0 g), quintile 4 (108.0–180.0 g), and quintile 5 (180.03–600.7 g) groups, compared with the reference of quintile 1 (0–23.7 g), showed 28% (OR = 0.720), 25.5% (OR = 0.745), and 29.8% (OR = 0.702) (P for trend = .0086) with no adjustment (Model 1). With the Model 2 adjusted for gender, age, and energy intake, the quintile 4 and quintile 5 groups showed a decrease in the prevalence of rhinitis of 17.4% (OR = 0.826) and 17.3% (OR = 0.827), respectively. Regarding the general characteristics of Model 3 and Model 4 with gradual adjustment (household income, educational level, marital status, and weight status) and dietary life (smoking, drinking, stress, breakfast intake status, food security, and energy intake), the quintile 4 groups of Model 3 and Model 4 showed decreased prevalence of rhinitis of 18.3% (OR = 0.817) and 18.9% (OR = 0.811), respectively.
Model 1: Crude.
Model 2: Adjusted for gender, age, and energy intake.
Model 3: Adjusted for gender, age, energy intake, smoking, drinking, stress, and weight status.
Model 4: Adjusted for gender, age, energy intake, smoking, drinking, stress status, weight status, food security, snack, eating out frequency and breakfast, education level, household income, and marital status.
Odds ratio (95% CI: confidence interval).
P-trends were obtained by surveylogistic procedure of SAS.
P < .05.
Discussion
To the best of our knowledge, this is the first study to examine the relationship between plant food (fruits, vegetables, and kimchi) consumption and the prevalence of rhinitis among Korean adults based on the data of KNHANES. Lower intakes of all plant foods were observed in subjects with rhinitis than in those without rhinitis. Especially, the prevalence of rhinitis decreased with increasing kimchi consumption. According to the results in Table 1, the second highest rate among four classified groups was observed in the obese group with rhinitis. Han et al., 33 who examined a cross-sectional study of obesity indicators and rhinitis based on the data of 8165 subjects in the 2005–2006 National Health and Nutrition Examination Survey (NHANES) conducted in the United States, reported an association of obesity with increased odds of rhinitis in male adults. Most previous studies reported a relationship between obesity and AR in adolescents. Some found no relationship between overweight/obesity and AR in children. 34 Others reported a positive relationship between obesity and AR in children and young adults. 35 –37 Therefore, further longitudinal studies on the relationship between obesity and rhinitis should be conducted in the future.
Regarding food group intake according to the prevalence of rhinitis, a significant difference in the intake of oils and fats was observed between subjects with and without rhinitis with adjustments for gender, age, and energy intake (adjusted P-value <.05). Fish, polyunsaturated fatty acid (PUFA), and vitamin D intake have been suggested to affect the prevalence of rhinitis. 38 –41 Our results showed no difference in fish consumption between the two groups according to the prevalence, while significantly higher consumption of oils and fats was observed in subjects with rhinitis than in those without rhinitis. Similar to our results, some studies of PUFA from fish showed no relationship or increased prevalence of rhinitis. 42,43 Other studies reported that fish consumption in infancy decreased the prevalence of rhinitis in children aged 5 to 12 years. 44,45 Most studies have been conducted in infants or children up to age 12 years, thus the previous findings may not compare with our results based on data from adults. The relationship between fish and oils, including PUFA consumption and rhinitis, is still controversial, and more cross-sectional studies for children and adults are required in the future.
According to the World Health Organization (WHO) and World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR), daily intake of at least 400 g of vegetables and fruits is recommended. 46,47 This study showed that all subjects consumed insufficient amounts of vegetables and fruits with an average of 368.2 g per day compared with the recommended intake. Moreover, with the intakes of fruits and vitamin C, those of the group with rhinitis were significantly higher than the other (adjusted P value <.05). This result suggests that the group with rhinitis might consume high amount of fruits with high vitamin C consciously because allergic disease, including rhinitis, is known to be associated with dysfunction of immune system. It is necessary to analyze additional research about the relationship between this result and prevalence of rhinitis in the future. The nonsalted vegetable, fruit, and kimchi intake (482.5 g) of total subjects surpassed the recommended guidelines as in the previous study by Kim et al. 6,42 However, those of subjects with rhinitis were lower than those of subjects without rhinitis, although there was no significant difference. In the 2008 KNHANES data, only 5.3% of subjects consumed the recommended intake of fruits and vegetables and consumption rates of adolescents aged 13 to 18 years and adults aged 19 to 39 years showed a decrease compared with other age groups. All of these results indicated that kimchi consumption among the Korean population is essential for obtaining adequate fruit and vegetable intakes.
In this study, kimchi consumption was inversely associated with the prevalence of rhinitis. Kim et al. 28 examined the relationship between kimchi consumption and asthma among Korean adults on the fourth and fifth KNHANES and reported a significant inverse association between kimchi consumption and the prevalence of asthma in adults. They found that subjects with asthma consumed lower amounts of kimchi and fish than those without asthma. Kimchi is a fermented vegetable food, rich in vitamins, minerals, dietary fibers, and other functional components, including gingerol, chlorophyll, and phenols. Many studies have reported on the health effects of kimchi, including antimutagenic and anticancer, 8,9 antioxidative, 48,49 antiobesity, 50 –52 and cholesterol-lowering 53 effects, and LAB from the fermentation process of kimchi also contribute several functional properties, including antimutagenic, antimicrobial, antiallergic, and increased immune function effects. 54 –59
Kimchi contains ∼107–108 LAB per gram and the major bacteria include a variety of Leuconostoc and Lactobacillus species, including Leuconostoc mesenteroides, Leuconostoc citreum, Leuconostoc gasicomitatum, Lactobacillus plantarum, Lb. sakei, and Lb. brevi s. 7,60 Many researchers have reported that intestinal bacteria containing LAB are helpful in development and maintenance of the immune system by enhancing intestinal mucosa immune cells. 60 –62 Okada et al. 63 reported that allergic diseases induced by overactive Th2 cells and excessive immunoglobulin E (IgE) synthesis might be closely related to insufficient microbial stimulation. Despite the necessity of IgE for proper function of the immune system, inadequate IgE synthesis could cause the release of inflammatory mediators from mast cells, resulting in allergic diseases, including atopic dermatitis, rhinitis, asthma, and food allergy. 64 Lee et al., 29 who studied the effects of LAB strains (L. plantarum, L. rhamnosus, Bifidobacterium lactis) isolated from kimchi on immune parameters in NC/Nga mice, found some positive effects of lowering production of IgE level and IL-4 and IL-5, which are regulatory factors of allergic diseases. In a similar study, Lee et al., 65 who studied the antiallergic effects of Lactobacillus strains isolated from kimchi used as yogurt starters, reported that two strains of L. plantarum from kimchi exerted regulatory effects on Th2 cells.
This study has some limitations. First, general plant food, including kimchi consumption, was not measured due to the use of the convenience sampling survey based on the one-day 24-h recall method and within-person variation. Second, time trends regarding the prevalence of rhinitis could not be examined due to the inconsistent questionnaire items regarding rhinitis from the KNHANES. (The questionnaire items regarding rhinitis were excluded on the 2010 KNHANES.) Finally, because no previous studies have been reported, the relationship between dietary factors and rhinitis in Korea could not be determined.
In conclusion, results of our study show that kimchi consumption among Korean adults was inversely associated with the prevalence of rhinitis. Therefore, kimchi consumption is important as a source of vegetable intake and provides an effect on allergic disease. Consumption of kimchi should be increased among the Korean population through providing publicized promotion and education on the excellence of kimchi. Further studies such as epidemiological and clinical trials are required in the future to more accurately determine the relationship between kimchi consumption and prevalence of rhinitis.
Footnotes
Acknowledgment
This study was supported by the World Institute of Kimchi.
Author Disclosure Statement
No competing financial interests exist.