Atopic dermatitis is associated with active and passive cigarette smoking in adolescents

So Young Kim; Songyong Sim; Hyo Geun Choi

doi:10.1371/journal.pone.0187453

Abstract

Objective

The relationship between passive smoking and atopic dermatitis has previously been reported, but few studies have simultaneously evaluated the association of atopic dermatitis with active and passive smoking.

Methods

The relationships between atopic dermatitis and active and passive smoking were evaluated in Korean adolescents. We used a large, representative, population-based survey (The Korea Youth Risk Behavior Web-based Survey) conducted in 2011 and 2012. Active smoking was classified into 3 groups (0 days, 1–19 days, and ≥ 20 days/month). Passive smoking was categorized into 3 groups (0 days, 1–4 days, and ≥ 5 days/week). Atopic dermatitis diagnosed by a medical doctor either during the past 1 month or during the participant’s lifetime was surveyed. Age, sex, obesity status, region of residence, economic level, and parental educational level of the participants were adjusted as confounders. Adjusted odds ratios (AORs) and 95% confidence intervals (CI) were calculated using multiple logistic regression analysis with complex sampling.

Results

A total of 6.8% (10,020/135,682) of the participants reported atopic dermatitis during the last 12 months. Active smoking was significantly associated with atopic dermatitis (previous 12 months) (AOR [95% CI] of smoking ≥ 20 days/month = 1.18 [1.07–1.29]; 1–19 days/month = 1.11 [0.99–1.23], P = 0.002). Passive smoking was also related to atopic dermatitis (previous 12 months) (AOR [95% CI] of smoking ≥ 5 days/week = 1.12 [1.05–1.20]; 1–4 days/week = 1.08 [1.03–1.13], P < 0.001).

Conclusion

Atopic dermatitis was significantly associated with active and passive smoking in Korean adolescents.

Citation: Kim SY, Sim S, Choi HG (2017) Atopic dermatitis is associated with active and passive cigarette smoking in adolescents. PLoS ONE 12(11): e0187453. https://doi.org/10.1371/journal.pone.0187453

Editor: Bernard Le Foll, Centre for Addiction and Mental Health, CANADA

Received: March 8, 2017; Accepted: October 19, 2017; Published: November 1, 2017

Copyright: © 2017 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The data underlying this study are third party data that are available to qualified researchers from Korean Youth Risk Behaviour Web-based Survey (KYRBWS). Interested researchers may apply for access to these data by contacting KYRBWS directly (https://yhs.cdc.go.kr/new/, tel: +82-43-719-7474,7471). The authors do not have any special access to these data and confirm that interested researchers may apply for access to these data in the manner described.

Funding: This work was supported in part by a research grant (NRF-2015-R1D1A1A01060860) from the National Research Foundation (NRF) of Korea, a Research Grant funded by Hallym University Sacred Heart Hospital (HURF-2016-38), and a Korea Ministry of Environment (MOE) as "The Environmental Health Action Program"(2016001360009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Atopic dermatitis is a common occurrence worldwide, with a prevalence of 20% in young Americans and 29% in young Koreans [1,2]. Numerous studies have explored the modifiable factors of atopic dermatitis including smoking. Although the adverse effects of smoking on asthma have been well documented in adolescents, the implications of smoking on atopic dermatitis are controversial. Several studies have demonstrated that atopic dermatitis was highly correlated with passive smoking, especially when infants were exposed to passive smoking during prenatal or early neonatal periods by their mother [2,3]. Children who were exposed to passive smoking during prenatal or neonatal periods showed a higher odds ratio (OR) (2.06) of atopic dermatitis in a cross-sectional study [2]. In another cross-sectional study, atopic dermatitis was estimated to be 1.97 times more likely to occur per 100 ng/mg increase in the urine cotinine level in children exposed to passive smoking [3]. Prospective birth cohort studies demonstrated no significant correlation between prenatal smoking and atopic dermatitis [4,5]. Several cross-sectional studies have shown a lower prevalence of allergic sensitization in smokers [6,7].

These contradictory findings may be the result of disparities in study design and covariables adjusted for in the analysis. For instance, the results of a few prospective cohort studies, which reported negative or non-significant correlations between atopic dermatitis and passive smoking, may have involved a small study population or exhibited selection bias due to the inclusion of restricted residential regions and a lack of compliance to the survey [4,5,8]. Additionally, because atopic dermatitis generally develops in young individuals and it is rare of children to smoke, the majority of studies have focused on the effects of passive smoking on atopic dermatitis in children.

The purpose of this study was to explore the associations of active and passive smoking with atopic dermatitis in a large, representative Korean adolescent population. Few studies have simultaneously considered passive smoking and active smoking. The present study is one of the largest population-based surveys using numerous adjusted variables. We considered numerous potential confounders including age, sex, obesity, region of residence, economic levels, and education levels of the participants’ parents using multiple logistic regression analysis.

Materials and methods

Study population and data collection

The Institutional Review Board (IRB) of the Centers for Disease Control and Prevention of Korea (KCDC) approved this study (2014-06EXP-02-P-A). Written informed consent was obtained from each participant prior to the survey. Because this web-based survey was performed at a school with many participants, informed consent from their parents was exempted. This consent procedure was approved by the IRB of the KCDC.

This cross-sectional study used the data from the Korea Youth Risk Behavior Web-based Survey (KYRBWS). This study covers the entire nation using statistical methods based on designed sampling and adjusted weighted values. The surveys evaluated data from South Korean adolescents using a stratified, two-stage (schools and classes) clustered sampling based on data from the Education Ministry. Sampling was weighted by statisticians, who performed post-stratification and considered the non-response rates and the extreme values. The results of the KYRBWS, conducted in 2011 and 2012, were analyzed. In 2011, 800 middle schools and 800 high schools were selected (participation rate = 95.5% [75,643/79,202]). In 2012, 797 middle schools and 800 high schools were selected (participation rate = 96.4% [74,186/76,980]). The detailed sampling methods are described on the KYRBWS website [9]. The data were collected by the KCDC. Korean adolescents from the 7^th through 12^th grades completed the self-administered questionnaire voluntarily and anonymously. The validity and reliability of the KYRBWS have been documented by other studies [10,11].

Of a total of 149,829 participants, those who did not record their height or weight (4,127 participants) were excluded from this study. Finally, 145,702 participants (73,984 males; 71,718 females), ranging in age from 12 through 18 years, were included in this study (Fig 1).

Download:

Fig 1. A schematic illustration of participant selection in the present study.

Among a total of 149,829 participants, participants without height or weight (n = 4,127) were excluded. The data for the 145,702 participants were analyzed.

https://doi.org/10.1371/journal.pone.0187453.g001

Survey

The understanding, reliability and validity of each question were evaluated by the KCDC to determine whether the questions met the criteria of the surveys [12]. The days of physical activity included the number of days of exercise, consisting of more than 60 minutes in which the heart beat or respiration were sufficiently increased, during the past 7 days. Obesity was categorized into 4 groups according to the Centers for Disease Control and Prevention guidelines for the body mass index (BMI, kg/m²) for children and teens [13]: obese ≥ 95^th percentile; overweight ≥ 85^th percentile and < 95^th percentile; healthy weight ≥ 5^th percentile and < 85^th percentile; and underweight < 5^th percentile. The region of residence was divided by administrative district into 3 groups: large city; small city; and rural area. The economic level was divided into 5 levels from the highest to the lowest level. The parent education level was divided into 4 groups: graduated college or higher; graduated high school; graduated middle school or less; and unknown or no parent. Participants who did not know the educational levels of their parents or who had no parents were not excluded because this could increase the missing values among participants with relatively low economic levels.

To measure active smoking, the participants were asked the following question: “In the last 30 days, how many days did you smoke at least one cigarette?” Active smoking was divided into 3 groups: 0 days per month; 1–9 days per month; and ≥ 20 days per month. To measure passive smoking, the participants were asked the following question: “In the last 7 days, how many days have you been together with another person (family member or guest) who smoked in your house?” Passive smoking was divided into 3 groups: 0 days per week; 1–4 days per week; and ≥ 5 days per week. To measure E-smoking, the participants were asked the following question: “In the last 30 days, have you smoked an E-cigarette?” E-smoking was divided into two categories: yes or no.

The participants were asked about their history of atopic dermatitis diagnosed by physician as previous studies [14]. The participants were asked the following questions about their history of atopic dermatitis in the past 12 months and during their lifetime: “Have you ever been diagnosed with atopic dermatitis by a doctor?” “In the past 12 months, have you been diagnosed with atopic dermatitis by a doctor?” Participants who had a history of diagnosis by a medical doctor were recorded as positive.

Statistical analysis

The differences in general characteristics according to the atopic dermatitis history (previous 12 months) were calculated using a linear regression analysis with complex sampling for age and days of physical activity; a chi-squared test with Rao-Scott correction for sex, obesity, region of residence, economic level of the household, education level of the father, education level of the mother, active smoking, passive smoking, and E-smoking was conducted.

Passive smoking rates according to active and E-smoking were compared using a chi-squared test with Rao-Scott correction.

The ORs and adjusted ORs (AORs) of active, passive and E-smoking for an atopic dermatitis history (previous 12 months) were calculated using (i) simple logistic regression analysis with complex sampling (unadjusted); (ii) multiple logistic regression analysis with complex sampling adjusted for age and sex (model 1); (iii) model 1 adjusted for physical exercise, obesity, region of residence, economic level, education level of the father, and education level of the mother (model 2); and (iv) model 2 adjusted for active smoking, passive smoking, and E-smoking (model 3). The ORs and AORs of active, passive and E-smoking for atopic dermatitis history (entire lifetime) were also calculated using the same methods.

Two-tailed analyses were conducted; a value of P < 0.05 was considered to be statistically significant, and 95% confidence intervals (CI) were calculated. The weighted values recommended by the KYRBWS were applied, and all results are presented as weighted values. The results were statistically analyzed using SPSS version 21.0 (IBM, Armonk, NY, USA).

Results

A total of 6.8% (10,020/135,682) of the participants reported atopic dermatitis in the past 12 months (Table 1). The average age of the atopic dermatitis group was 15.0 years, which was not significantly different from that of normal participants (15.0 years) (P = 0.968). The prevalence of active smoking (P = 0.003) and passive smoking (P < 0.001) were significantly different between the normal and atopic dermatitis groups. However, the prevalence of E-smoking was not significantly different between the groups. Other variables including sex, obesity, economic level, and parental education levels were significantly different between the normal and atopic dermatitis groups (all P < 0.001). Days of physical exercise and region of residence were not significantly different between the normal and atopic dermatitis groups.

Download:

Table 1. General characteristics of participants.

https://doi.org/10.1371/journal.pone.0187453.t001

Active smoking and E-smoking were significantly related to passive smoking (both P < 0.001) (Table 2). Thus, we adjusted for active smoking, E-smoking, and passive smoking in addition to other variables (model 3). Active smoking was significantly associated with atopic dermatitis (previous 12 months) and exhibited a dose-response relationship when adjusted for age and sex (model 1) and other variables (model 2), although no significant relationship was observed in the unadjusted model (Table 3). These significant relationships between active smoking and atopic dermatitis were maintained even after adjustments for passive smoking and E-smoking (AORs of model 3 [95% CI] for ≥ 20 days per month = 1.18 [1.07–1.29] and for 1–19 days a month = 1.11 [0.99–1.23], P = 0.002). Passive smoking demonstrated consistently significant relationships with atopic dermatitis (previous 12 months) in unadjusted model 1, model 2, and model 3 (AORs of model 3 [95% CI] for ≥ 5 days per week = 1.12 [1.05–1.20] and for 1–4 days a week = 1.08 [1.03–1.13], P < 0.001). E-smoking showed a significant association with atopic dermatitis only in model 1 and model 2 (AORs of model 2 = 1.14, 95% CI = 1.06–1.23, P < 0.001). After adjusting for active and passive smoking (model 3), E-smoking did not show a statistically significant relationship with atopic dermatitis.

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Table 2. Passive smoking rates according to active and electronic cigarette smoking.

https://doi.org/10.1371/journal.pone.0187453.t002

Download:

Table 3. Odd ratios of active, passive and electronic cigarette smoking for atopic dermatitis (recent 12 months) using multiple logistic regression analysis with complex sampling (Reference = no smoking).

https://doi.org/10.1371/journal.pone.0187453.t003

The effects of active, passive, and E-smoking on atopic dermatitis over the participant’s entire lifetime showed comparable results with those of atopic dermatitis for the past 12 months (S1 Table). Passive smoking demonstrated positive relationships with atopic dermatitis over the participant’s entire lifetime. E-smoking was not significantly related to atopic dermatitis over the participant’s entire lifetime.

Discussion

The prevalence of atopic dermatitis (previous 12 months) was significantly associated with active and passive smoking.

Consistent with previous studies [2,3], passive smoking was significantly related to atopic dermatitis in the present study. Passive smoking primarily (85%) consists of the hazardous sidestream, which arises from the unfiltered burning of the raw cigarette [15]. The adverse health effects of sidestream smoke are comparable or greater than those of mainstream smoke. After sidestream smoke exposure, allergic responses to inhaled allergens may be rapidly provoked and prolonged through the elevations of IgE, IgG1, and eosinophils [16]. Moreover, macrophage functions are impaired by sidestream smoke [17].

The present study showed higher ORs of active smoking than passive smoking for the prevalence of atopic dermatitis. In accordance with the present results, a recent large-scale, cross-sectional study demonstrated higher ORs for atopic dermatitis for active smoking than for passive smoking [18]. Because an active smoker is expected to encounter higher concentrations and larger amounts of smoke fumes, the adverse effects of smoking may be more remarkable than in passive smokers. Additionally, active smokers were more likely to be exposed to prior passive smoking, which could affect the prevalence of atopic dermatitis. Indeed, a previous study demonstrated a 3.62 times higher prevalence of later-onset atopic dermatitis in previously active smoking-exposed children [19]. Although evidence for the pathophysiologic mechanisms is still lacking, smoking may have several plausible effects on atopic dermatitis. Approximately 4,500 chemical components of cigarettes may modulate the immune system [20]. Smokers have demonstrated low serum concentrations and shortened lifespans of pathogen-specific immunoglobulins [21]. Smoking increases the autoantibody levels [22]. These combined effects of smoking could be predicted to affect allergic sensitization. The inflammatory reaction is another plausible mechanism of the effect of smoking on atopic dermatitis. Strong correlations have been found between smoking and various inflammatory markers, such as the white blood cell count, fibrinogen level, plasma viscosity, and high-sensitivity C-reactive protein level [23]. The skin-barrier function can be damaged by toxic substances produced by smoking, such as nicotine and carbon monoxide, which disturb the blood flow and oxygenation of the skin [24]. These disturbances of the skin and associated subcutaneous structures allow allergens to permeate into the skin, which results in atopic dermatitis [2].

In the present study, E-smoking was also quantified, but could not provide clear information on the relationship between E-smoking use and atopic dermatitis. The insignificant association may have originated from a small proportion of the population of E-smoking, which weakens the statistical power. Many of E-smokers were also the active or passive smokers (S2 Table). Thus, the influence of combined smoking status could not be excluded, although these factors were adjusted in this study. In addition, the binary classification without consideration of the amounts of E-smoking exposure may also have contributed to the lack of relationship between E-smoking and atopic dermatitis. Larger populations who practice E-smoking should be explored to determine the effect of E-smoking on atopic dermatitis.

In the present study, 6.8% of the participants had atopic dermatitis. This calculation is lower than the previously reported value of 20% in a prospective cohort study [2]. In that study, the prevalence of atopic dermatitis could be exaggerated due to selection bias and long-term follow-up loss. The KYRBWS showed a high response rate with a small number of excluded participants due to incomplete data (2.8%). Furthermore, our participants were strategically selected among the entire Korean adolescent population. This representativeness combined with the large survey population increased the validity of our results. However, generalizing the present results should be approached with caution due to likely ethnic, sex, and age effects. Due to the cross-sectional study design, the causality could not be elucidated, and the participants could be affected by the healthy smoker bias. Participants with atopic dermatitis may be more prone to respiratory allergic symptoms, which led them to avoid smoking to manage their respiratory symptoms. Although parental atopy could not be accessed in this study, further analyses adjusted asthma and rhinitis (model 4) also demonstrated significant relation between active or passive smoking and atopic dermatitis (S3 Table). The number of cigarette smoked per day had some variations among participants (S4 Table). The prevalence and the frequency of passive smoking could be underestimated in this study due to the self-reported nature of the study. However, the passive smoking exposure in adolescents has been reported to be well represented by the questionnaire survey and the correlation with urinary cotinine levels [25]. Due to the limitation of survey from large cohort population, detailed questionnaires could not be investigated on AD in this study. Additionally, the present study could not assess objective parameters, such as serum IgE levels or urinary cotinine levels. However, the reliability and validity of the smoking survey of the KYRBWS have been estimated to exhibit 78.0% sensitivity, 97.7% specificity, and a kappa value of 0.80 [9].

Conclusion

Atopic dermatitis in the past 12 months is significantly associated with active and passive smoking in Korean adolescents. These relationships demonstrated positive associations in accordance with the frequency and dose of active and passive smoking.

Supporting information

S1 Table. Odd ratios of active, passive and electronic cigarette smoking for atopic dermatitis (entire life) using multiple logistic regression analysis with complex sampling (Reference = no smoking).

https://doi.org/10.1371/journal.pone.0187453.s001

(DOCX)

S2 Table. Electronic cigarette smoking rates according to active and passive smoking.

https://doi.org/10.1371/journal.pone.0187453.s002

(DOCX)

S3 Table. Odd ratios of active, passive and electronic cigarette smoking for atopic dermatitis (recent 12 months) using multiple logistic regression analysis with complex sampling (Reference = no smoking).

https://doi.org/10.1371/journal.pone.0187453.s003

(DOCX)

S4 Table. General characteristics of participants.

https://doi.org/10.1371/journal.pone.0187453.s004

(DOCX)

References

1. Deckers IA, McLean S, Linssen S, Mommers M, van Schayck CP, Sheikh A. Investigating international time trends in the incidence and prevalence of atopic eczema 1990–2010: a systematic review of epidemiological studies. PLoS One 2012; 7: e39803. pmid:22808063
- View Article
- PubMed/NCBI
- Google Scholar
2. Yi O, Kwon HJ, Kim H, Ha M, Hong SJ, Hong YC, et al. Effect of environmental tobacco smoke on atopic dermatitis among children in Korea. Environ Res 2012; 113: 40–45. pmid:22264877
- View Article
- PubMed/NCBI
- Google Scholar
3. Kramer U, Lemmen CH, Behrendt H, Link E, Schafer T, Gostomzyk J, et al. The effect of environmental tobacco smoke on eczema and allergic sensitization in children. Br J Dermatol 2004; 150: 111–118. pmid:14746624
- View Article
- PubMed/NCBI
- Google Scholar
4. Linneberg A, Simonsen JB, Petersen J, Stensballe LG, Benn CS Differential effects of risk factors on infant wheeze and atopic dermatitis emphasize a different etiology. J Allergy Clin Immunol 2006; 117: 184–189. pmid:16387604
- View Article
- PubMed/NCBI
- Google Scholar
5. Tanaka K, Miyake Y, Sasaki S, Ohya Y, Hirota Y, Osaka Maternal and Child Health Study Group. Maternal smoking and environmental tobacco smoke exposure and the risk of allergic diseases in Japanese infants: the Osaka Maternal and Child Health Study. J Asthma 2008; 45: 833–838. pmid:18972305
- View Article
- PubMed/NCBI
- Google Scholar
6. Jarvis D, Chinn S, Luczynska C, Burney P The association of smoking with sensitization to common environmental allergens: results from the European Community Respiratory Health Survey. J Allergy Clin Immunol 1999; 104: 934–940. pmid:10550735
- View Article
- PubMed/NCBI
- Google Scholar
7. Wuthrich B, Schindler C, Medici TC, Zellweger JP, Leuenberger P IgE levels, atopy markers and hay fever in relation to age, sex and smoking status in a normal adult Swiss population. SAPALDIA (Swiss Study on Air Pollution and Lung Diseases in Adults) Team. Int Arch Allergy Immunol 1996; 111: 396–402. pmid:8957114
- View Article
- PubMed/NCBI
- Google Scholar
8. Hancox RJ, Welch D, Poulton R, Taylor DR, McLachlan CR, Greene JM, et al. Cigarette smoking and allergic sensitization: a 32-year population-based cohort study. J Allergy Clin Immunol 2008; 121: 38–42 e33. pmid:18061657
- View Article
- PubMed/NCBI
- Google Scholar
9. the Korea Youth Risk Behavior Web-based Survey. http://yhs.cdc.go.kr.
10. Bae J, Joung H, Kim JY, Kwon KN, Kim Y, Park SW, et al. Validity of self-reported height, weight, and body mass index of the Korea Youth Risk Behavior Web-based Survey questionnaire. J Prev Med Public Health 2010; 43: 396–402. pmid:20959710
- View Article
- PubMed/NCBI
- Google Scholar
11. Bae J, Joung H, Kim JY, Kwon KN, Kim YT, Park SW Test-retest reliability of a questionnaire for the Korea Youth Risk Behavior Web-based Survey. J Prev Med Public Health 2010; 43: 403–410. pmid:20959711
- View Article
- PubMed/NCBI
- Google Scholar
12. Reliability and validity of the Korea Youth Risk Behavior Web-based Survey Questionnaire 2009. http://yhs.cdc.go.kr/
13. Centers for Disease Control and Prevention. About BMI for Children and Teens. http://www.cdc.gov/healthyweight/assessing/bmi/childrens_bmi/about_childrens_bmi.html.
14. Kim SY, Sim S, Kim SG, Choi HG. Sleep Deprivation Is Associated with Bicycle Accidents and Slip and Fall Injuries in Korean Adolescents. PLoS One 2015:10: e0135753. pmid:26280345
- View Article
- PubMed/NCBI
- Google Scholar
15. Tae B, Oliveira KC, Conceicao RR, Valenti VE, de Souza JS, Laureano-Melo R, et al. Evaluation of globins expression in brain, heart, and lung in rats exposed to side stream cigarette smoke. Environ Toxicol. 2016
- View Article
- Google Scholar
16. Seymour BW, Pinkerton KE, Friebertshauser KE, Coffman RL, Gershwin LJ. Second-hand smoke is an adjuvant for T helper-2 responses in a murine model of allergy. J Immunol 1997; 159: 6169–6175. pmid:9550419
- View Article
- PubMed/NCBI
- Google Scholar
17. Edwards K, Braun KM, Evans G, Sureka AO, Fan S. Mainstream and sidestream cigarette smoke condensates suppress macrophage responsiveness to interferon gamma. Hum Exp Toxicol 1999;18: 233–240. pmid:10333308
- View Article
- PubMed/NCBI
- Google Scholar
18. Graif Y, German L, Ifrah A, Livne I, Shohat T. Dose-response association between smoking and atopic eczema: results from a large cross-sectional study in adolescents. Dermatology 2013; 226: 195–199. pmid:23711459
- View Article
- PubMed/NCBI
- Google Scholar
19. Lee CH, Chuang HY, Hong CH, Huang SK, Chang YC, Ko YC, et al. Lifetime exposure to cigarette smoking and the development of adult-onset atopic dermatitis. Br J Dermatol 2011; 164: 483–489. pmid:21054333
- View Article
- PubMed/NCBI
- Google Scholar
20. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2: 372–377. pmid:12033743
- View Article
- PubMed/NCBI
- Google Scholar
21. Ferson M, Edwards A, Lind A, Milton GW, Hersey P. Low natural killer-cell activity and immunoglobulin levels associated with smoking in human subjects. Int J Cancer 1979; 23: 603–609. pmid:457307
- View Article
- PubMed/NCBI
- Google Scholar
22. Mathews JD, Whittingham S, Hooper BM, Mackay IR, Stenhouse NS. Association of autoantibodies with smoking, cardiovascular morbidity, and death in the Busselton population. Lancet 1973; 2: 754–758. pmid:4126476
- View Article
- PubMed/NCBI
- Google Scholar
23. Frohlich M, Sund M, Lowel H, Imhof A, Hoffmeister A, Koenig W, et al. Independent association of various smoking characteristics with markers of systemic inflammation in men. Results from a representative sample of the general population (MONICA Augsburg Survey 1994/95). Eur Heart J 2003; 24: 1365–1372. pmid:12871694
- View Article
- PubMed/NCBI
- Google Scholar
24. Leow YH, Maibach HI. Cigarette smoking, cutaneous vasculature, and tissue oxygen. Clin Dermatol 1998; 16: 579–584. pmid:9787969
- View Article
- PubMed/NCBI
- Google Scholar
25. Forastiere F, Agabiti N, Dell'Orco V, Pistelli R, Corbo GM, Brancato G, et al. Questionnaire data as predictors of urinary cotinine levels among nonsmoking adolescents. Arch Environ Health 1993; 48: 230–234. pmid:8357271
- View Article
- PubMed/NCBI
- Google Scholar

[ref1] 1. Deckers IA, McLean S, Linssen S, Mommers M, van Schayck CP, Sheikh A. Investigating international time trends in the incidence and prevalence of atopic eczema 1990–2010: a systematic review of epidemiological studies. PLoS One 2012; 7: e39803. pmid:22808063
View Article
PubMed/NCBI
Google Scholar

[2] View Article

[3] PubMed/NCBI

[4] Google Scholar

[ref2] 2. Yi O, Kwon HJ, Kim H, Ha M, Hong SJ, Hong YC, et al. Effect of environmental tobacco smoke on atopic dermatitis among children in Korea. Environ Res 2012; 113: 40–45. pmid:22264877
View Article
PubMed/NCBI
Google Scholar

[6] View Article

[7] PubMed/NCBI

[8] Google Scholar

[ref3] 3. Kramer U, Lemmen CH, Behrendt H, Link E, Schafer T, Gostomzyk J, et al. The effect of environmental tobacco smoke on eczema and allergic sensitization in children. Br J Dermatol 2004; 150: 111–118. pmid:14746624
View Article
PubMed/NCBI
Google Scholar

[10] View Article

[11] PubMed/NCBI

[12] Google Scholar

[ref4] 4. Linneberg A, Simonsen JB, Petersen J, Stensballe LG, Benn CS Differential effects of risk factors on infant wheeze and atopic dermatitis emphasize a different etiology. J Allergy Clin Immunol 2006; 117: 184–189. pmid:16387604
View Article
PubMed/NCBI
Google Scholar

[14] View Article

[15] PubMed/NCBI

[16] Google Scholar

[ref5] 5. Tanaka K, Miyake Y, Sasaki S, Ohya Y, Hirota Y, Osaka Maternal and Child Health Study Group. Maternal smoking and environmental tobacco smoke exposure and the risk of allergic diseases in Japanese infants: the Osaka Maternal and Child Health Study. J Asthma 2008; 45: 833–838. pmid:18972305
View Article
PubMed/NCBI
Google Scholar

[18] View Article

[19] PubMed/NCBI

[20] Google Scholar

[ref6] 6. Jarvis D, Chinn S, Luczynska C, Burney P The association of smoking with sensitization to common environmental allergens: results from the European Community Respiratory Health Survey. J Allergy Clin Immunol 1999; 104: 934–940. pmid:10550735
View Article
PubMed/NCBI
Google Scholar

[22] View Article

[23] PubMed/NCBI

[24] Google Scholar

[ref7] 7. Wuthrich B, Schindler C, Medici TC, Zellweger JP, Leuenberger P IgE levels, atopy markers and hay fever in relation to age, sex and smoking status in a normal adult Swiss population. SAPALDIA (Swiss Study on Air Pollution and Lung Diseases in Adults) Team. Int Arch Allergy Immunol 1996; 111: 396–402. pmid:8957114
View Article
PubMed/NCBI
Google Scholar

[26] View Article

[27] PubMed/NCBI

[28] Google Scholar

[ref8] 8. Hancox RJ, Welch D, Poulton R, Taylor DR, McLachlan CR, Greene JM, et al. Cigarette smoking and allergic sensitization: a 32-year population-based cohort study. J Allergy Clin Immunol 2008; 121: 38–42 e33. pmid:18061657
View Article
PubMed/NCBI
Google Scholar

[30] View Article

[31] PubMed/NCBI

[32] Google Scholar

[ref9] 9. the Korea Youth Risk Behavior Web-based Survey. http://yhs.cdc.go.kr.

[ref10] 10. Bae J, Joung H, Kim JY, Kwon KN, Kim Y, Park SW, et al. Validity of self-reported height, weight, and body mass index of the Korea Youth Risk Behavior Web-based Survey questionnaire. J Prev Med Public Health 2010; 43: 396–402. pmid:20959710
View Article
PubMed/NCBI
Google Scholar

[35] View Article

[36] PubMed/NCBI

[37] Google Scholar

[ref11] 11. Bae J, Joung H, Kim JY, Kwon KN, Kim YT, Park SW Test-retest reliability of a questionnaire for the Korea Youth Risk Behavior Web-based Survey. J Prev Med Public Health 2010; 43: 403–410. pmid:20959711
View Article
PubMed/NCBI
Google Scholar

[39] View Article

[40] PubMed/NCBI

[41] Google Scholar

[ref12] 12. Reliability and validity of the Korea Youth Risk Behavior Web-based Survey Questionnaire 2009. http://yhs.cdc.go.kr/

[ref13] 13. Centers for Disease Control and Prevention. About BMI for Children and Teens. http://www.cdc.gov/healthyweight/assessing/bmi/childrens_bmi/about_childrens_bmi.html.

[ref14] 14. Kim SY, Sim S, Kim SG, Choi HG. Sleep Deprivation Is Associated with Bicycle Accidents and Slip and Fall Injuries in Korean Adolescents. PLoS One 2015:10: e0135753. pmid:26280345
View Article
PubMed/NCBI
Google Scholar

[45] View Article

[46] PubMed/NCBI

[47] Google Scholar

[ref15] 15. Tae B, Oliveira KC, Conceicao RR, Valenti VE, de Souza JS, Laureano-Melo R, et al. Evaluation of globins expression in brain, heart, and lung in rats exposed to side stream cigarette smoke. Environ Toxicol. 2016
View Article
Google Scholar

[49] View Article

[50] Google Scholar

[ref16] 16. Seymour BW, Pinkerton KE, Friebertshauser KE, Coffman RL, Gershwin LJ. Second-hand smoke is an adjuvant for T helper-2 responses in a murine model of allergy. J Immunol 1997; 159: 6169–6175. pmid:9550419
View Article
PubMed/NCBI
Google Scholar

[52] View Article

[53] PubMed/NCBI

[54] Google Scholar

[ref17] 17. Edwards K, Braun KM, Evans G, Sureka AO, Fan S. Mainstream and sidestream cigarette smoke condensates suppress macrophage responsiveness to interferon gamma. Hum Exp Toxicol 1999;18: 233–240. pmid:10333308
View Article
PubMed/NCBI
Google Scholar

[56] View Article

[57] PubMed/NCBI

[58] Google Scholar

[ref18] 18. Graif Y, German L, Ifrah A, Livne I, Shohat T. Dose-response association between smoking and atopic eczema: results from a large cross-sectional study in adolescents. Dermatology 2013; 226: 195–199. pmid:23711459
View Article
PubMed/NCBI
Google Scholar

[60] View Article

[61] PubMed/NCBI

[62] Google Scholar

[ref19] 19. Lee CH, Chuang HY, Hong CH, Huang SK, Chang YC, Ko YC, et al. Lifetime exposure to cigarette smoking and the development of adult-onset atopic dermatitis. Br J Dermatol 2011; 164: 483–489. pmid:21054333
View Article
PubMed/NCBI
Google Scholar

[64] View Article

[65] PubMed/NCBI

[66] Google Scholar

[ref20] 20. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2: 372–377. pmid:12033743
View Article
PubMed/NCBI
Google Scholar

[68] View Article

[69] PubMed/NCBI

[70] Google Scholar

[ref21] 21. Ferson M, Edwards A, Lind A, Milton GW, Hersey P. Low natural killer-cell activity and immunoglobulin levels associated with smoking in human subjects. Int J Cancer 1979; 23: 603–609. pmid:457307
View Article
PubMed/NCBI
Google Scholar

[72] View Article

[73] PubMed/NCBI

[74] Google Scholar

[ref22] 22. Mathews JD, Whittingham S, Hooper BM, Mackay IR, Stenhouse NS. Association of autoantibodies with smoking, cardiovascular morbidity, and death in the Busselton population. Lancet 1973; 2: 754–758. pmid:4126476
View Article
PubMed/NCBI
Google Scholar

[76] View Article

[77] PubMed/NCBI

[78] Google Scholar

[ref23] 23. Frohlich M, Sund M, Lowel H, Imhof A, Hoffmeister A, Koenig W, et al. Independent association of various smoking characteristics with markers of systemic inflammation in men. Results from a representative sample of the general population (MONICA Augsburg Survey 1994/95). Eur Heart J 2003; 24: 1365–1372. pmid:12871694
View Article
PubMed/NCBI
Google Scholar

[80] View Article

[81] PubMed/NCBI

[82] Google Scholar

[ref24] 24. Leow YH, Maibach HI. Cigarette smoking, cutaneous vasculature, and tissue oxygen. Clin Dermatol 1998; 16: 579–584. pmid:9787969
View Article
PubMed/NCBI
Google Scholar

[84] View Article

[85] PubMed/NCBI

[86] Google Scholar

[ref25] 25. Forastiere F, Agabiti N, Dell'Orco V, Pistelli R, Corbo GM, Brancato G, et al. Questionnaire data as predictors of urinary cotinine levels among nonsmoking adolescents. Arch Environ Health 1993; 48: 230–234. pmid:8357271
View Article
PubMed/NCBI
Google Scholar

[88] View Article

[89] PubMed/NCBI

[90] Google Scholar

Figures

Abstract

Objective

Methods

Results

Conclusion

Introduction

Materials and methods

Study population and data collection

Survey

Statistical analysis

Results

Discussion

Conclusion

Supporting information

S1 Table. Odd ratios of active, passive and electronic cigarette smoking for atopic dermatitis (entire life) using multiple logistic regression analysis with complex sampling (Reference = no smoking).

S2 Table. Electronic cigarette smoking rates according to active and passive smoking.

S3 Table. Odd ratios of active, passive and electronic cigarette smoking for atopic dermatitis (recent 12 months) using multiple logistic regression analysis with complex sampling (Reference = no smoking).

S4 Table. General characteristics of participants.

References