Active Smoking, Environmental Tobacco Smoke and
Bronchitic Symptoms among Adolescents in Taiwan: a
prospective cohort study
Jer-Min Chena,b, Bing-Fang Hwangc, Yang-Ching Chena,b, Yungling Leo Leea,d
a Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan
b Department of Family Medicine, Taipei City Hospital, Taipei, Taiwan
c Department of Occupational Safety and Health, College of Public Health, China Medical University, Taichung, Taiwan
d Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan
Jer-Min Chen, MD; e-mail: [email protected]
Bing-Fang Hwang, PhD; e-mail: [email protected] Yang-Ching Chen, MD; e-mail: [email protected]
Correspondence to:
Yungling Leo Lee, MD, PhD
Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, No.17, Xuzhou Road, 516R, Taipei 100, Taiwan; Tel: +886-2-3366-8016
Fax: +886-2-2392-0456 E-mail: [email protected]
Key words: adolescents, smoking, tobacco smoke pollution, asthma, bronchitis
ABSTRACT
Objective
The study investigates the association between active smoking, exposure to
environmental tobacco smoke (ETS) and the development of bronchitis and bronchitic symptoms among adolescents.
Methods
A prospective cohort study was conducted with 4,134 adolescents aged 12-14 from the Taiwan Children Health Study in 14 communities in Taiwan since 2007. Parents or guardians completed written questionnaires regarding demographic information, household ETS and respiratory symptoms at baseline. The adolescents themselves completed identical questionnaires on respiratory outcomes in the 2009 survey. Associations between active smoking, exposure to ETS and the 2-year incidence of respiratory outcomes were analyzed by multiple Poisson regression models, taking overdispersion into account.
Results
Active smoking was associated with an increased risk of developing chronic cough and chronic phlegm. We found significant dose-response associations between the duration of smoking, the numbers of cigarettes and the onset of bronchitic symptoms. Exposure to ETS was a significant risk factor for the development of chronic cough. Among asthmatic adolescents, exposure to ETS was associated with an additional risk for the onset of chronic phlegm.
Conclusion
This study demonstrates that active smoking and exposure to ETS are associated with higher risks for developing bronchitic symptoms among adolescents.
Introduction
Smoking and exposure to environmental tobacco smoke (ETS) are serious and growing public health problems worldwide (CDC, 2006). The increasing prevalence of regular smoking up to 10% among youths was found in some countries (Warren et al., 2009), and more than 50% of children in Taiwan live with smokers (Wen et al., 2005). Both active smoking and exposure to ETS are linked to a multitude of respiratory diseases and symptoms (Strachan and Cook, 1998; Withers et al., 1998). These illnesses include chronic bronchitis and associated symptoms can have a marked influence on the performance of children in school (Liberty et al., 2010) and are associated with poorer exercise capacity, incident airflow limitation and increased mortality risk later in life (Martinez et al., 2014; Guerra et al., 2009).
Most previous studies designed to determine the effects of smoking on asthma and other bronchitic symptoms have been conducted among older participants with a long history of smoking (Forey et al., 2011). The evidence for an association between smoking and bronchitis among adolescents has been limited, and most of these studies are cross-sectional in design (Forey et al., 2011); thus, causal inferences have been difficult to establish. Some studies have concluded that active smoking increases the risk of developing bronchitis and bronchitic symptoms (Karunanayake et al., 2011; Withers et al., 1998), while others have found weak associations (Eagan et al., 2002; Frank et al., 2007). Previous studies have also suggested that ETS is a substantial risk factor for the incidence of respiratory diseases. However, Stoddard and Miller reported that younger children may be more affected by ETS than older children (Stoddard and Miller, 1995) and longitudinal data on adolescents has remained scarce. Many adolescents with a history of asthma or wheezing disorders have taken up smoking and have a continued exposure to ETS. Numerous studies have shown that tobacco smoke can cause
decrements in lung function and can increase the frequency of asthma attacks (Cook and Strachan, 1999). Trédaniel et al. has reported that there was no sufficient evidence to infer a causal relationship between ETS exposure and respiratory symptoms among adults with asthma (Trédaniel et al., 1994).
In the present study, we used a longitudinal study with a nationally representative sample to investigate the relationship between cigarette smoking and ETS exposure and
the incidence of bronchitis and bronchitic symptoms. We also assessed the risk of
developing respiratory symptoms associated with ETS exposure in asthmatic participants.
Study design
The Taiwan Children Health Study (TCHS) is a prospective study of the
determinants of children’s respiratory health. The details of the design and methods of this study have been described in previous publications (Tsai et al., 2010). In brief, a total 4,134 seventh-grade children were enrolled into the study from public schools in 14 communities covering different parts of Taiwan in 2007. Parents or guardians of each participant completed a self-administered questionnaire that provided demographic information, respiratory health conditions, tobacco smoke exposure and household environmental characteristics at cohort entry. The cohort participants were followed up on during the school visit in 2009 with an updated questionnaire that contained identical questions concerning respiratory outcomes. The study was approved by the Institutional Review Board at the National Taiwan University Hospital and complied with the principles outlined in the Declaration of Helsinki.
Definition of respiratory health outcomes
Questions regarding respiratory diseases were modified from the questionnaire used in the Children’s Health Study in Southern California (McConnell et al., 1999). The
respiratory health outcomes of interest were bronchitis and bronchitic symptoms. Participants who were disease-free at baseline and who reported a “yes” answer to the question: “Has a physician ever diagnosed you as having bronchitis?” on the follow-up questionnaire were classified as having new-onset bronchitis. Chronic cough was defined on the follow-up questionnaire by the questions: “During the past 12 months, have you had a cough first thing in the morning that lasted for as much as 3 months in a row?” or “During the past 12 months, have you had a cough at other times lasting at least 3 months in a row?”. The presence of new-onset chronic phlegm was determined by a “yes” answer to the following question: “Other than with colds, did you usually seem congested in the chest or bring up phlegm?”.
We also assessed the association between active smoking, ETS and new-onset
bronchitic symptoms among asthmatic adolescents. An asthmatic participant was defined as someone who reported a positive answer to the questions: “Has a physician ever diagnosed your child as having asthma?” or “During the past 12 months, has this child had a wheezing or whistling sound in the chest?” on the baseline questionnaire.
Personal smoking history and environmental tobacco smoke exposures
Information on the personal smoking behavior of each adolescent was obtained by a confidential interview that was conducted by experienced field staff during the baseline school visits. Personal smoking was defined as a history of smoking more than 100 cigarettes during the participant’s lifetime. The report of weekly smoking amount was classified as nonsmokers, infrequent (1 to 6 cigarettes) and regular smokers (7 or more cigarettes). The amount of yearly smoking was also categorized into 3 groups: none, 1-299 cigarettes and 300 or more cigarettes.
We obtained information about the smoking status of each participant’s parents, adult household members and regular visitors. Current ETS exposure was defined as someone who was exposed to smoke continuously prior to the date of baseline interview. We categorized the intensity of ETS exposure into 2 groups: the amount of daily smoking exposure and the percentage of lifetime exposed to ETS. The amount of daily ETS exposure was categorized as none, 1-10 cigarettes and 11 or more cigarettes and the percentage of ETS exposure was determined by 20% of a person’s lifetime.
Statistical analysis
The incidence of new cases of respiratory outcomes was calculated using the number of new cases divided by the person-years at risk over a 2-year period of follow-up. The relationships between active smoking and ETS and the incidence of respiratory diseases were analyzed by Poisson regression models. To account for overdispersion of incidence rates in Poisson models, the scale parameter was adjusted using Pearson chi-square statistics (Le, 2003). Based on the study design and our a priori considerations of potential confounders, we introduced age, gender, parental history of asthma, parental history of atopy, maternal smoking during pregnancy and community into all of our models. If the estimates of smoking effects changed by more than 10% when a covariate was introduced into the base models, then the covariate was included in the final models. Participants with missing covariate information were included in the models using missing indicators. To investigate the effects on the relationship between active smoking and ETS and new-onset respiratory diseases among asthmatic adolescents, we conducted a stratified analysis using likelihood ratio tests to examine the interactive effects between
tobacco smoke and personal history with or without asthma/wheeze. All analyses were carried out using SAS software version 9.1 (SAS institute, Cary, NC, USA).
Results
A total of 3,909 participants completed the up questionnaire, with a follow-up rate of 94.6%. The loss to follow-follow-up of participants was mostly due to families moving out of the school district area based on interviews with the school staff and on telephone interviews with the families of participants. Because of baseline respiratory conditions
and missing or “not known” answers to questions on three bronchitic outcomes, 3664 bronchitis-free, 3680 chronic cough-free and 3704 chronic phlegm-free participants were recruited at cohort entry. Table 1 shows the distribution of selected characteristics among participants in the separate respiratory health outcomes. At cohort entry, the proportion of gender was almost equal (51.1% female and 48.9% male) and the majority of children were 12 years of age. Exposure to maternal smoking in pregnancy was reported for 3.7% of the cohort. More than 40% of the children were exposed to ETS and 5.6% of the children had an active smoking habit.
The number of new cases of bronchitis, chronic cough and chronic phlegm were 59, 278 and 363 after a 2-year follow-up.The incidence of bronchitis was 8.1/1000 person-years, the incidence of chronic cough was 37.9/1000 person-years and the incidence of chronic phlegm was 49.2/1000 person-years for chronic phlegm.
The rate ratio (RR) and the 95% confidence interval (CI) for bronchitis and
bronchitic symptoms in relation to active smoking are shown in Table 2. We found that active smoking was positively associated with new-onset chronic cough (RR = 1.72; 95% CI: 1.11 to 2.64) and chronic phlegm (RR = 1.64; 95% CI: 1.11 to 2.43). We observed a dose-response relationship between duration, weekly and yearly amounts of smoking and the incidence of bronchitic symptoms. Children who smoked cigarettes for more than one year had an increased risk for developing chronic cough (RR = 2.07, 95%: CI: 1.12 to 3.82) and chronic phlegm (RR = 2.23, 95% CI: 1.32 to 3.79) when compared with nonsmokers. Consistent with the risk associated with active smoking assessed on a duration basis, adolescents who reported active smoking on a weekly basis (more than 7 cigarettes per week) and yearly basis (more than 300 cigarettes) were at a 2.21-fold and 2.10-fold increased risk for the incidence of chronic cough.
Table 3 shows the association between ETS and the onset of bronchitic symptoms. In our cohort, exposure to ETS was significantly related to chronic cough (RR = 1.31, 95% CI: 1.03 to 1.67). The percentage of current ETS exposure also showed a trend toward increased risk of developing chronic cough. Restricting the analysis to participants without a history of asthma did not substantially alter the above findings (Appendix Table 1 and 2).
We also analyzed our data for the incidence of asthma and wheezing disorders in the TCHS cohort. Similar risks were observed between active smoking and ETS and
wheezing disorders; however it is difficult to make this conclusion firmly because of small numbers of cases over the 2-year period of follow-up (Appendix Table 3).
In further analyses, we observed the increased risk for new-onset chronic phlegm among asthmatic adolescents who had been exposed to ETS (Table 4). Children who had a history of asthma or wheeze and who were exposed to current ETS had an increased risk (RR = 1.98; 95% CI: 1.09 to 3.60) when they were compared with unexposed non-asthmatic adolescents (p for interaction = 0.02).
Discussion
Our population-based prospective study demonstrates that active smoking and exposure to ETS significantly increase the risk of new-onset bronchitic symptoms among adolescents. Active smoking was associated with the development of chronic cough and chronic phlegm. The increased duration and the weekly and yearly amount of active smoking showed significant trends in the risk of developing bronchitic symptoms. The exposure to ETS increased the risk of new-onset chronic phlegm in participants with a
personal history of asthma or wheeze. To the best of our knowledge, this is the first longitudinal study that has identified an association between active smoking and ETS and bronchitis/bronchitic symptoms among adolescents.
In the current study, we enrolled a large nationally representative population cohort and had a very high follow-up rate (94.6%). Some individual and environmental factors, such as maternal smoking during pregnancy (Gilliland et al., 2001), family history of asthma or atopy (Lee et al., 2003; Sears et al., 1996), body mass index (Nystad et al., 2004) and socio-economic status (Ellison-Loschmann et al., 2007), may have affected the development of respiratory diseases, and we adjusted the above covariates in our Poisson regression models to minimize these potentially confounding effects.
Cigarette smoke has complex effects on the proinflammatory and immune responses in the pulmonary system. Chronic inflammation, consisting of the enlargement of the mucous glands and the remodeling of the bronchi, reflects a deregulated healing process in the tissue that is damaged by the inhalation of tobacco smoke (Hogg et al., 2004). This process causes the development of a chronic cough, mucus hypersecretion and phlegm production in the airways. Previous research suggested that chronic cough and phlegm are not only an important cause of school absence and medical use in childhood (Spee-van der Wekke et al., 1998), but also associated with poorer exercise capacity, the higher incidence of chronic obstructive pulmonary disease and increased mortality risk later in life (Martinez et al., 2014; de Marco et al., 2007; Guerra et al., 2009).
Our finding that there is an increased risk of the incidence of bronchitic symptoms after the onset of active smoking is consistent with previous evidence showing that tobacco smoke causes adverse effects on respiratory health. Karunanayake et al. (2011) found an increased risk of developing cough and phlegm with a risk of 2.04 and 2.02 in individuals in the 20-70-year-old age group in rural Canada. Withers et al. (1998) noted that regular smoking was positively associated with late-onset cough, but was not
significantly associated with persistent cough in children aged 6-8 years. However, Eagan et al. (2002) observed a weak association between smoking and the development of chronic cough among Norwegian participants aged 15 to 70. Previous research suggested that being 50 years of age or older was an independent risk factor of the incidence of bronchitic symptoms (Eagan et al., 2002). The majority of evidence regarding the cigarette smoking effects came from the studies of elderly cohorts, and longitudinal data
on adolescents or children has remained scarce. In our study, active smoking showed significant trends in the risks of developing chronic cough and chronic phlegm in adolescents. There was no significant association observed between the incidence of bronchitis and active smoking in our study; however, the small numbers of bronchitis cases may explain this observation. Yeatts et al. (2003) reported that current smoking and exposure to ETS were positively associated with undiagnosed wheezing among
adolescents. Therefore, underreporting, possibly due to the underdiagnosis of respiratory diseases is a possible reason for the observed lack of an association.
We also assessed the effect of exposure to household ETS on the risk of developing respiratory diseases. In Taiwan, children are not typically exposed to ETS in school due to the legislative ban on public smoking; therefore, household exposure is likely the predominant source of ETS. A previous meta-analysis has suggested that maternal smoking is a stronger risk factor for the incidence of respiratory illness in early childhood than it is for the incidence of respiratory illness at school age (Strachan and Cook, 1998). We found a significant association between ETS and the onset of chronic cough in our study. These smaller effects may reflect the decreasing level of exposure to ETS from household sources as children age.
We found that exposure to ETS was associated with an additional risk for the onset of bronchitic symptoms among asthmatic adolescents. Exposure to ETS and active smoking can aggravate the severity of respiratory diseases and can increase
hospitalization rates. However, asthmatic status in childhood does not prevent smoking initiation in adulthood (Vignoud et al., 2011), and many asthmatic children are still exposed to high levels of tobacco smoke at home (Irvine et al., 1997). Previous research has suggested that it remains controversial whether ETS exposure is associated with chronic respiratory symptoms and decrements in lung function among asthmatic adults (Trédaniel et al., 1994). In our study, adolescents with a history of asthma or wheeze and who were exposed to ETS had the greatest risk of developing chronic phlegm when they were compared with un-exposed non-asthmatic adolescents. Similarly, Schwartz et al. (2000) reported that exposure to ETS was associated with increases in respiratory
symptoms including cough and phlegm production among younger asthmatic children in Finland. We observed a protective effect against developing bronchitic symptoms between an asthmatic history and a regular smoking habit in adolescents. The possible
explanation for this is that a reduced severity of asthma was observed among asthmatic smokers at baseline when they were compared with asthmatic non-smokers; thus, the “healthy smoker” effect might account for this inverse association.
Our study has some limitations. The measurement of active smoking and ETS exposure by questionnaire may be relatively imprecise. However, the validity of exposure estimates based on questionnaire responses has been found to provide reasonably valid data and Spanier et al. (2011) observed that the parental reporting of ETS may
underestimate the risk of respiratory diseases in children. Another limitation to this study is the potential misclassification of respiratory diseases that may lead to underestimation of the effect estimates. A self-reported respiratory outcome questionnaire has been demonstrated to be valid and repeatable and has been widely used in epidemiologic studies (Burney et al., 1989). It is possible that bronchitic symptoms, including cough and phlegm may mimic the symptoms of an asthmatic attack and may, therefore, lead to an overestimation of the risk. However, this seems unlikely because the effect estimates did not change substantially when we restricted the analyses to adolescents without a history of asthma at baseline (Appendix table 1 and 2).
In conclusion, we performed a large, high follow-up rate longitudinal study to discover that active smoking and exposure to ETS are important risk factors for the incidence of bronchitic symptoms in adolescents. Moreover, asthmatic adolescents who are exposed to ETS have an additional risk of developing bronchitic symptoms. Effective tobacco control efforts focusing on the prevention of smoking initiation and the reduction of ETS exposure are urgently needed to reduce the adverse impact on respiratory health in adolescents.
Conflict of interest statement
The authors declare that there are no conflicts of interests.
Acknowledgment
This work was partially supported by grants #98-2314-B-002-138-MY3 and #96-2314-B-006-053 from the Taiwan National Science Council. The sponsors had no role in the design of the study, the collection and analysis of the data, or in the preparation of the manuscript.
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Table 1
Baseline characteristics of the study population, Taiwan Children Health Study, 2007.
Selected characteristics at study entrya
Bronchitis-free Chronic cough- Chronic
phlegm-cohort free cohort free cohort
(N=3,664) (N=3,680) (N=3,704) n % n % n % Gender Boys 1768 48.2 1791 48.7 1803 48.7 Girls 1896 51.8 1889 51.3 1901 51.3 Age, years 12 2914 80.0 2948 80.1 2956 79.9 13 729 19.9 711 19.3 725 19.6 14 8 0.2 8 0.2 8 0.2 Parental incomeb ≦400,000 1205 35.6 1199 35.2 1198 35.0 400,000～800,000 1372 40.5 1382 40.6 1395 40.7 ＞800,000 811 23.9 826 24.2 833 24.3
Parental history of asthma
Yes 94 2.6 102 2.8 104 2.8
No 3570 97.4 3578 97.2 3600 97.2
Parental history of atopyc
Yes 863 23.6 916 24.9 919 24.8
No 2801 76.4 2764 75.1 2785 75.2
Maternal smoking during pregnancy
Yes 140 3.8 137 3.7 135 3.6 No 3524 96.2 3543 96.3 3569 96.4 BMI classification Underweight 1465 40.2 1464 40.0 1478 40.1 Normal 1054 28.9 1061 29.0 1062 28.8 Overweight 497 13.6 495 13.5 503 13.6 Obese 629 17.3 641 17.5 640 17.4 Current ETS Yes 1564 43.0 1568 42.9 1595 43.3 No 2075 57.0 2090 57.1 2086 56.7 Active smoking Yes 202 5.5 199 5.4 201 5.5 No 3446 94.5 3464 94.6 3486 94.5
Abbreviation: ETS, environmental tobacco smoke.
a Number of subjects does not add up to total N because of missing data. b New Taiwan dollars per year ($1 US = $ 30 New Taiwan).
Table 2
Effects of active smoking on bronchitis and bronchitic symptoms, Taiwan Children Health Study, 2007-2009.
A b b r e v i a t i o n s : I R , i n
cidence rate per 1000 person-years; RR, rate ratio; and CI, confidence interval.
a Models are adjusted for age, sex, parental history of asthma, parental history of atopy, maternal smoking during pregnancy, body mass index, ETS exposure and community.
Bronchitis Chronic cough Chronic phlegm
IR RR 95% CI IR RR 95% CI IR RR 95% CI Active smokinga No 8.0 1 36.4 1 47.9 1 Yes 10.0 1.26 (0.44, 3.60) 60.9 1.72 (1.11, 2.64) 72.5 1.64 (1.11, 2.43) Duration None 8.0 1 36.4 1 47.9 1 ≦1 year 9.4 1.22 (0.29, 5.17) 61.9 1.70 (0.96, 3.00) 65.4 1.49 (0.87, 2.57) ＞1 year 6.7 0.91 (0.12, 6.75) 73.3 2.07 (1.12, 3.82) 96.7 2.23 (1.32, 3.79) p for trend 0.97 0.003 0.001
Amount smoked weekly
None 8.0 1 36.4 1 47.9 1
＜7 4.8 0.62 (0.08, 4.57) 58.8 1.60 (0.88, 2.88) 66.0 1.52 (0.88, 2.63)
≧7 13.2 1.80 (0.43, 7.59) 77.9 2.21 (1.23, 3.99) 92.1 2.05 (1.19, 3.53)
p for trend 0.72 0.002 0.003
Amount smoked yearly
None 8.0 1 36.4 1 47.9 1
＜300 8.0 1.02 (0.24, 4.35) 67.5 1.80 (1.09, 2.98) 73.6 1.65 (1.03, 2.66)
≧300 9.6 1.33 (0.18, 9.86) 68.6 2.10 (0.98, 4.50) 90.0 2.15 (1.10, 4.20)
Table 3
Effects of environmental tobacco smoke (ETS) on bronchitis and bronchitic symptoms, Taiwan Children Health Study, 2007-2009.
Bronchitis Chronic cough Chronic phlegm
IR RR 95% CI IR RR 95% CI IR RR 95% CI
Current ETS
No 8.9 1 33.9 1 47.2 1
Yes 7.0 0.72 (0.42, 1.25) 43.8 1.31 (1.03, 1.67) 51.5 1.14 (0.92, 1.41)
Daily amount of ETS
None 8.9 1 33.9 1 47.2 1 ≦10 8.6 0.90 (0.48, 1.65) 44.9 1.36 (1.06, 1.76) 52.5 1.16 (0.93, 1.45) ＞10 1.6 0.14 (0.01, 1.35) 41.7 1.22 (0.79, 1.88) 50.2 1.09 (0.74, 1.59) p for trend 0.08 0.04 0.24 Percent of ETSa None 8.9 1 33.9 1 47.2 1 ≦20% 6.1 0.68 (0.35, 1.32) 43.3 1.06 (0.70, 1.62) 50.4 1.12 (0.88, 1.43) ＞20% 9.2 0.84 (0.40, 1.75) 45.3 1.24 (0.90, 1.70) 55.2 1.20 (0.89, 1.61) p for trend 0.44 0.02 0.13
Abbreviations: IR, incidence rate per 1000 person-years; RR, rate ratio; and CI, confidence interval.
Models are adjusted for age, sex, parental history of asthma, parental history of atopy, maternal smoking during pregnancy, body mass index, smoking habit and community.
Table 4
Joint effects of exposure to environmental smoke (ETS), active smoking and personal history of asthma or wheeze at baseline on the incidence on bronchitic symptoms, Taiwan Children Health Study, 2007-2009.
Current ETSa Active smokingb
Unexposed Exposed No Yes
RR 95% CI RR 95% CI RR 95% CI RR 95% CI Chronic cough Asthma/wheeze No 1 1.23 (0.94, 1.60) 1 2.01 (1.27, 3.16) Yes 1.4 3 (0.91, 2.26) 1.40 (0.76, 2.57) 1.8 5 (1.34, 2.53) 0.32 (0.07, 1.40) p for interaction 0.28 0.03 Chronic phlegm Asthma/wheeze No 1 1.03 (0.81, 1.29) 1 1.91 (1.29, 2.87) Yes 0.8 6 (0.54, 1.36) 1.98 (1.09, 3.60) 1.3 4 (0.99, 1.81) 0.17 (0.02, 1.31) p for interaction 0.02 0.03
Abbreviations: RR, rate ratio; and CI, confidence interval.
a Models are adjusted for age, sex, parental history of asthma, parental history of atopy, maternal smoking during pregnancy, smoking habit, body mass index and community.
b Models are adjusted for age, sex, parental history of asthma, parental history of atopy, maternal smoking during pregnancy, ETS exposure, body mass index and community.
