YPMED-03947; No. of pages: 6; 4C: Preventive Medicine xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Preventive Medicine journal homepage: www.elsevier.com/locate/ypmed
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Jer-Min Chen a,b, Bing-Fang Hwang c, Yang-Ching Chen a,b, Yungling Leo Lee a,d,⁎ a
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Available online xxxx
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Keywords: Adolescents Smoking Tobacco smoke pollution Asthma Bronchitis
Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan Department of Family Medicine, Taipei City Hospital, Taipei, Taiwan Departiment of Occupational Safety and Health, College of Public Health, China Medical University, Taichung, Taiwan d Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan b
a b s t r a c t
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Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study
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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 4134 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. © 2014 Published by Elsevier Inc.
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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 (Guerra et al., 2009; Martinez et al., 2014). Most previous studies designed to determine the effects of smoking on asthma and other bronchitic symptoms have been conducted among
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Introduction
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⁎ Corresponding author at: Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, No. 17, Xuzhou Road, 516R, Taipei 100, Taiwan. Fax: +886 2 2392 0456. E-mail addresses: [email protected] (J.-M. Chen), [email protected] (B.-F. Hwang), [email protected] (Y.-C. Chen), [email protected] (Y.L. Lee).
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34
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
http://dx.doi.org/10.1016/j.ypmed.2014.05.007 0091-7435/© 2014 Published by Elsevier Inc.
Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
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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 4134 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.
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Definition of respiratory health outcomes
94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112
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 newonset 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.
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Personal smoking history and environmental tobacco smoke exposures
114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129
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.
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Statistical analysis
131 132 133 134 135 136 137
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
Results
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Study design
A total of 3909 participants completed the follow-up questionnaire, with a follow-up rate of 94.6%. The loss to 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: 1.02 to 1.84). 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 Tables 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;
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Materials and methods
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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).
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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.
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J.-M. Chen et al. / Preventive Medicine xxx (2014) xxx–xxx
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Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
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J.-M. Chen et al. / Preventive Medicine xxx (2014) xxx–xxx Table 1 Baseline characteristics of the study population, Taiwan Children Health Study, 2007.
N
%
N
%
1768 1896
48.2 51.8
1791 1889
48.7 51.3
1803 1901
48.7 51.3
2914 729 8
80.0 19.9 0.2
2948 711 8
80.1 19.3 0.2
2956 725 8
79.9 19.6 0.2
1205 1372 811
35.6 40.5 23.9
1199 1382 826
35.2 40.6 24.2
1198 1395 833
35.0 40.7 24.3
94 3570
2.6 97.4
102 3578
2.8 97.2
104 3600
2.8 97.2
863 2801
23.6 76.4
916 2764
24.9 75.1
919 2785
24.8 75.2
140 3524
3.8 96.2
137 3543
3.7 96.3
135 3569
3.6 96.4
1465 1054 497 629
40.2 28.9 13.6 17.3
1464 1061 495 641
40.0 29.0 13.5 17.5
1478 1062 503 640
40.1 28.8 13.6 17.4
1564 2075
43.0 57.0
1568 2090
42.9 57.1
1595 2086
43.3 56.7
202 3446
5.5 94.5
199 3464
5.4 94.6
201 3486
5.5 94.5
F
%
O
N Gender Boys Girls Age, years 12 13 14 Parental incomeb ≦400,000 400,000–800,000 N800,000 Parental history of asthma Yes No Parental history of atopyc Yes No Maternal smoking during pregnancy Yes No BMI classification Underweight Normal Overweight Obese Current ETS Yes No Active smoking Yes No
Chronic phlegm-free cohort (N = 3704)
R O
t1:4 t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19 t1:20 t1:21 t1:22 t1:23 t1:24 t1:25 t1:26 t1:27 t1:28 t1:29 t1:30 t1:31 t1:32 t1:33 t1:34 t1:35
Chronic cough-free cohort (N = 3680)
P
Bronchitis-free cohort (N = 3664)
D
Selected characteristics at study entrya t1:3
E
t1:1
Q2 t1:2
3
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). c Atopy is defined as allergic rhinitis or atopic dermatitis.
202 203
95% CI: 1.09 to 3.60) when they were compared with unexposed nonasthmatic adolescents (p for interaction = 0.02).
204
Discussion
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Our population-based prospective study demonstrates that active smoking and exposure to ETS significantly increase the risk of new-
t2:1 t2:2 t2:3
Table 2 Effects of active smoking on bronchitis and bronchitic symptoms, Taiwan Children Health Study, 2007–2009. Abbreviations: IR, incidence rate per 1000 person-years; RR, rate ratio; and CI, confidence interval.
t2:4
N C O
R
R
E
C
T
t1:36 t1:37 t1:38 t1:39
Bronchitis
t2:5
Active smokinga No Yes Duration None ≦1 year N1 year p for trend Amount smoked weekly None b7 ≧7 p for trend Amount smoked yearly None b300 ≧300 p for trend
t2:24
a
U
t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23
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 amounts 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
Chronic cough
Chronic phlegm
IR
RR
95% CI
IR
RR
95% CI
IR
RR
95% CI
8.0 10.0
1 1.26
(0.44, 3.60)
36.4 60.9
1 1.72
(1.11, 2.64)
47.9 72.5
1 1.64
(1.11, 2.43)
8.0 9.4 6.7
1 1.22 0.91 0.97
(0.29, 5.17) (0.12, 6.75)
36.4 61.9 73.3
1 1.70 2.07 0.003
(0.96, 3.00) (1.12, 3.82)
47.9 65.4 96.7
1 1.49 2.23 0.001
(0.87, 2.57) (1.32, 3.79)
8.0 4.8 13.2
1 0.62 1.80 0.72
(0.08, 4.57) (0.43, 7.59)
36.4 58.8 77.9
1 1.60 2.21 0.002
(0.88, 2.88) (1.23, 3.99)
47.9 66.0 92.1
1 1.52 2.05 0.003
(0.88, 2.63) (1.19, 3.53)
8.0 8.0 9.6
1 1.02 1.33 0.88
(0.24, 4.35) (0.18, 9.86)
36.4 67.5 68.6
1 1.80 2.10 0.003
(1.09, 2.98) (0.98, 4.50)
47.9 73.6 90.0
1 1.65 2.15 0.003
(1.03, 2.66) (1.10, 4.20)
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.
Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
207 208 209 210 211 212 213
4 t3:1 t3:2
J.-M. Chen et al. / Preventive Medicine xxx (2014) xxx–xxx
Table 3 Effects of environmental tobacco smoke (ETS) on bronchitis and bronchitic symptoms, Taiwan Children Health Study, 2007–2009.
t3:3
Bronchitis
t3:4
IR
RR
95% CI
IR
RR
95% CI
IR
RR
95% CI
8.9 7.0
1 0.72
(0.42, 1.25)
33.9 43.8
1 1.31
(1.03, 1.67)
47.2 51.5
1 1.14
(0.92, 1.41)
8.9 8.6 1.6
1 0.90 0.14 0.08
(0.48, 1.65) (0.01, 1.35)
33.9 44.9 41.7
1 1.36 1.22 0.04
(1.06, 1.76) (0.79, 1.88)
47.2 52.5 50.2
1 1.16 1.09 0.24
(0.93, 1.45) (0.74, 1.59)
8.9 6.1 9.2
1 0.68 0.84 0.44
(0.35, 1.32) (0.40, 1.75)
33.9 43.3 45.3
1 1.06 1.24 0.02
(0.70, 1.62) (0.90, 1.70)
47.2 50.4 55.2
1 1.12 1.20 0.13
(0.88, 1.43) (0.89, 1.61)
F
Current ETS No Yes Daily amount of ETS None ≦10 N10 p for trend Percent of ETSa None ≦20% N20% p for trend
Chronic phlegm
O
t3:5 t3:6 t3:7 t3:8 t3:9 t3:10 t3:11 t3:12 t3:13 t3:14 t3:15 t3:16 t3:17
Chronic cough
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. a Average percent of ETS in lifetime.
214
240
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 (de Marco et al., 2007; Guerra et al., 2009; Martinez et al., 2014). 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
t4:1 t4:2 t4:3
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.
231 232 233 234 235 236 237 238 239
t4:4 t4:5 t4:6 t4:7 t4:8 t4:9 t4:10 t4:11 t4:12 t4:13 t4:14 t4:15 t4:16 t4:17 t4:18
P
D
E
T
C
229 230
E
227 228
R
225 226
R
223 224
O
221 222
C
219 220
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.
N
217 218
U
215 216
R O
t3:18 t3:19 t3:20
Chronic cough Asthma/wheeze
p for interaction
Active smokingb
Unexposed
Exposed
No
Yes
RR
95% CI
RR
95% CI
RR
95% CI
RR
95% CI
No Yes
1 1.43 0.28
(0.91, 2.26)
1.23 1.40
(0.94, 1.60) (0.76, 2.57)
1 1.85 0.03
(1.34, 2.53)
2.01 0.32
(1.27, 3.16) (0.07, 1.40)
No Yes
1 0.86 0.02
(0.54, 1.36)
1.03 1.98
(0.81, 1.29) (1.09, 3.60)
1 1.34 0.03
(0.99, 1.81)
1.91 0.17
(1.29, 2.87) (0.02, 1.31)
p for interaction Chronic phlegm Asthma/wheeze
Current ETSa
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.
Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
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Conflict of interest statement
324
Acknowledgment
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This work was partially supported by grants #98-2314-B-002138-MY3 and #96-2314-B-006-053 from the Taiwan National Science Council. The sponsors had no role in the design of the study, in the collection and analysis of the data, or in the preparation of the manuscript.
327 328 329
The authors declare that there are no conflicts of interests.
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Burney, P.G., Laitinen, L.A., Perdrizet, S., et al., 1989. Validity and repeatability of the IUATLD (1984) Bronchial Symptoms Questionnaire: an international comparison. Eur. Respir. J. 2, 940–945. CDC, 2006. The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General. , US Department of Health and Human Services, CDC, Atlanta, GA (Available at http://www.ncbi.nlm.nih.gov/books/NBK44324/pdf/TOC. pdf [Accessed April 2014]). Cook, D.G., Strachan, D.P., 1999. Health effects of passive smoking-10: summary of effects of parental smoking on the respiratory health of children and implications for research. Thorax 54, 357–366. de Marco, R., Accordini, S., Cerveri, I., et al., 2007. Incidence of chronic obstructive pulmonary disease in a cohort of young adults according to the presence of chronic cough and phlegm. Am. J. Respir. Crit. Care Med. 175, 32–39. Eagan, T.M., Bakke, P.S., Eide, G.E., Gulsvik, A., 2002. Incidence of asthma and respiratory symptoms by sex, age and smoking in a community study. Eur. Respir. J. 19, 599–605. Ellison-Loschmann, L., Sunyer, J., Plana, E., et al., 2007. Socioeconomic status, asthma and chronic bronchitis in a large community-based study. Eur. Respir. J. 29, 897–905. Forey, B.A., Thornton, A.J., Lee, P.N., 2011. Systematic review with meta-analysis of the epidemiological evidence relating to COPD, chronic bronchitis and emphysema. BMC Pulm. Med. 11, 36. Frank, P.I., Hazell, M.L., Morris, J.A., Linehan, M.F., Frank, T.L., 2007. A longitudinal study of changes in respiratory status in young adults, 1993–2001. Int. J. Tuber. Lung Dis. 11, 338–343. Gilliland, F.D., Li, Y.F., Peters, J.M., 2001. Effects of maternal smoking during pregnancy and environmental tobacco smoke on asthma and wheezing in children. Am. J. Respir. Crit. Care Med. 163, 429–436. Guerra, S., Sherrill, D.L., Venker, C., Ceccato, C.M., Halonen, M., Martinez, F.D., 2009. Chronic bronchitis before age 50 years predicts incident airflow limitation and mortality risk. Thorax 64, 894–900. Hogg, J.C., Chu, F., Utokaparch, S., et al., 2004. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N. Engl. J. Med. 350, 2645–2653. Irvine, L., Crombie, I.K., Clark, R.A., et al., 1997. What determines levels of passive smoking in children with asthma? Thorax 52, 766–769. Karunanayake, C.P., Rennie, D.C., Pahwa, P., Chen, Y., Dosman, J.A., 2011. Predictors of respiratory symptoms in a rural Canadian population: a longitudinal study of respiratory health. Can. Respir. J. 18, 149–153. Le, C.T., 2003. Introductory Biostatistics. , John Wiley & Sons, Hoboken, NJ. Lee, Y.L., Lin, Y.C., Hsiue, T.R., Hwang, B.F., Guo, Y.L., 2003. Indoor and outdoor environmental exposures, parental atopy, and physician-diagnosed asthma in Taiwanese schoolchildren. Pediatrics 112, e389. Liberty, K.A., Pattemore, P., Reid, J., Tarren-Sweeney, M., 2010. Beginning school with asthma independently predicts low achievement in a prospective cohort of children. Chest 138, 1349–1355. Martinez, C.H., Kim, V., Chen, Y., et al., 2014. The clinical impact of non-obstructive chronic bronchitis in current and former smokers. Respir. Med. 108, 491–499. McConnell, R., Berhane, K., Gilliland, F., et al., 1999. Air pollution and bronchitic symptoms in Southern California children with asthma. Environ. Health Perspect. 107, 757–760. Nystad, W., Meyer, H.E., Nafstad, P., Tverdal, A., Engeland, A., 2004. Body mass index in relation to adult asthma among 135,000 Norwegian men and women. Am. J. Epidemiol. 160, 969–976. Schwartz, J., Timonen, K.L., Pekkanen, J., 2000. Respiratory effects of environmental tobacco smoke in a panel study of asthmatic and symptomatic children. Am. J. Respir. Crit. Care Med. 161, 802–806. Sears, M.R., Holdaway, M.D., Flannery, E.M., Herbison, G.P., Silva, P.A., 1996. Parental and neonatal risk factors for atopy, airway hyper-responsiveness, and asthma. Arch. Dis. Child. 75, 392–398. Spanier, A.J., Kahn, R.S., Xu, Y., Hornung, R., Lanphear, B.P., 2011. Comparison of biomarkers and parent report of tobacco exposure to predict wheeze. J. Pediatr. 159, 776–782. Spee-van der Wekke, J., Meulmeester, J.F., Radder, J.J., Verloove-Vanhorick, S.P., 1998. School absence and treatment in school children with respiratory symptoms in the Netherlands: data from the Children Health Monitoring System. J. Epidemiol. Community Health 52, 359–363. Stoddard, J.J., Miller, T., 1995. Impact of parental smoking on the prevalence of wheezing respiratory illness in children. Am. J. Epidemiol. 141, 96–102. Strachan, D.P., Cook, D.G., 1998. Health effects of passive smoking. 6. Parental smoking and childhood asthma: longitudinal and case–control studies. Thorax 53, 204–212. Trédaniel, J., Boffetta, P., Saracci, R., Hirsch, A., 1994. Exposure to environmental tobacco smoke and adult non-neoplastic respiratory diseases. Eur. Respir. J. 7, 173–185. Tsai, C.H., Huang, J.H., Hwang, B.F., Lee, Y.L., 2010. Household environmental tobacco smoke and risks of asthma, wheeze and bronchitic symptoms among children in Taiwan. Respir. Res. 11, 11. Vignoud, L., Pin, I., Boudier, A., et al., 2011. Smoking and asthma: disentangling their mutual influences using a longitudinal approach. Respir. Med. 105, 1805–1814.
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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 selfreported 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 Tables 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 on the reduction of ETS exposure are urgently needed to reduce the adverse impact on respiratory health in adolescents.
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Warren, C.W., Lea, V., Lee, J., Jones, N.R., Asma, S., McKenna, M., 2009. Change in tobacco use among 13–15 year olds between 1999 and 2008: findings from the Global Youth Tobacco Survey. Glob. Health Promot. 16 (2 Suppl.), 38–90. Wen, C.P., Levy, D.T., Cheng, T.Y., Hsu, C.C., Tsai, S.P., 2005. Smoking behaviour in Taiwan, 2001. Tob. Control. 14 (Suppl. 1), i51–i55.
Withers, N.J., Low, L., Holgate, S.T., Clough, J.B., 1998. The natural history of respiratory symptoms in a cohort of adolescents. Am. J. Respir. Crit. Care Med. 158, 352–357. Yeatts, K., Davis, K.J., Sotir, M., Herget, C., Shy, C., 2003. Who gets diagnosed with asthma? Frequent wheeze among adolescents with and without a diagnosis of asthma. Pediatrics 111, 1046–1054.
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Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
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Contents lists available at ScienceDirect
Preventive Medicine journal homepage: www.elsevier.com/locate/ypmed
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Jer-Min Chen a,b, Bing-Fang Hwang c, Yang-Ching Chen a,b, Yungling Leo Lee a,d,⁎ a
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Keywords: Adolescents Smoking Tobacco smoke pollution Asthma Bronchitis
Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan Department of Family Medicine, Taipei City Hospital, Taipei, Taiwan Departiment of Occupational Safety and Health, College of Public Health, China Medical University, Taichung, Taiwan d Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan b
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Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study
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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 4134 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. © 2014 Published by Elsevier Inc.
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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 (Guerra et al., 2009; Martinez et al., 2014). Most previous studies designed to determine the effects of smoking on asthma and other bronchitic symptoms have been conducted among
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Introduction
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⁎ Corresponding author at: Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, No. 17, Xuzhou Road, 516R, Taipei 100, Taiwan. Fax: +886 2 2392 0456. E-mail addresses: [email protected] (J.-M. Chen), [email protected] (B.-F. Hwang), [email protected] (Y.-C. Chen), [email protected] (Y.L. Lee).
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34
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
http://dx.doi.org/10.1016/j.ypmed.2014.05.007 0091-7435/© 2014 Published by Elsevier Inc.
Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
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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 4134 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.
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Definition of respiratory health outcomes
94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112
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 newonset 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.
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Personal smoking history and environmental tobacco smoke exposures
114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129
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.
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Statistical analysis
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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
Results
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Study design
A total of 3909 participants completed the follow-up questionnaire, with a follow-up rate of 94.6%. The loss to 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: 1.02 to 1.84). 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 Tables 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;
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Materials and methods
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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).
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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.
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J.-M. Chen et al. / Preventive Medicine xxx (2014) xxx–xxx Table 1 Baseline characteristics of the study population, Taiwan Children Health Study, 2007.
N
%
N
%
1768 1896
48.2 51.8
1791 1889
48.7 51.3
1803 1901
48.7 51.3
2914 729 8
80.0 19.9 0.2
2948 711 8
80.1 19.3 0.2
2956 725 8
79.9 19.6 0.2
1205 1372 811
35.6 40.5 23.9
1199 1382 826
35.2 40.6 24.2
1198 1395 833
35.0 40.7 24.3
94 3570
2.6 97.4
102 3578
2.8 97.2
104 3600
2.8 97.2
863 2801
23.6 76.4
916 2764
24.9 75.1
919 2785
24.8 75.2
140 3524
3.8 96.2
137 3543
3.7 96.3
135 3569
3.6 96.4
1465 1054 497 629
40.2 28.9 13.6 17.3
1464 1061 495 641
40.0 29.0 13.5 17.5
1478 1062 503 640
40.1 28.8 13.6 17.4
1564 2075
43.0 57.0
1568 2090
42.9 57.1
1595 2086
43.3 56.7
202 3446
5.5 94.5
199 3464
5.4 94.6
201 3486
5.5 94.5
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%
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N Gender Boys Girls Age, years 12 13 14 Parental incomeb ≦400,000 400,000–800,000 N800,000 Parental history of asthma Yes No Parental history of atopyc Yes No Maternal smoking during pregnancy Yes No BMI classification Underweight Normal Overweight Obese Current ETS Yes No Active smoking Yes No
Chronic phlegm-free cohort (N = 3704)
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t1:4 t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19 t1:20 t1:21 t1:22 t1:23 t1:24 t1:25 t1:26 t1:27 t1:28 t1:29 t1:30 t1:31 t1:32 t1:33 t1:34 t1:35
Chronic cough-free cohort (N = 3680)
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Bronchitis-free cohort (N = 3664)
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Selected characteristics at study entrya t1:3
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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). c Atopy is defined as allergic rhinitis or atopic dermatitis.
202 203
95% CI: 1.09 to 3.60) when they were compared with unexposed nonasthmatic adolescents (p for interaction = 0.02).
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Discussion
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Our population-based prospective study demonstrates that active smoking and exposure to ETS significantly increase the risk of new-
t2:1 t2:2 t2:3
Table 2 Effects of active smoking on bronchitis and bronchitic symptoms, Taiwan Children Health Study, 2007–2009. Abbreviations: IR, incidence rate per 1000 person-years; RR, rate ratio; and CI, confidence interval.
t2:4
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t1:36 t1:37 t1:38 t1:39
Bronchitis
t2:5
Active smokinga No Yes Duration None ≦1 year N1 year p for trend Amount smoked weekly None b7 ≧7 p for trend Amount smoked yearly None b300 ≧300 p for trend
t2:24
a
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t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23
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 amounts 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
Chronic cough
Chronic phlegm
IR
RR
95% CI
IR
RR
95% CI
IR
RR
95% CI
8.0 10.0
1 1.26
(0.44, 3.60)
36.4 60.9
1 1.72
(1.11, 2.64)
47.9 72.5
1 1.64
(1.11, 2.43)
8.0 9.4 6.7
1 1.22 0.91 0.97
(0.29, 5.17) (0.12, 6.75)
36.4 61.9 73.3
1 1.70 2.07 0.003
(0.96, 3.00) (1.12, 3.82)
47.9 65.4 96.7
1 1.49 2.23 0.001
(0.87, 2.57) (1.32, 3.79)
8.0 4.8 13.2
1 0.62 1.80 0.72
(0.08, 4.57) (0.43, 7.59)
36.4 58.8 77.9
1 1.60 2.21 0.002
(0.88, 2.88) (1.23, 3.99)
47.9 66.0 92.1
1 1.52 2.05 0.003
(0.88, 2.63) (1.19, 3.53)
8.0 8.0 9.6
1 1.02 1.33 0.88
(0.24, 4.35) (0.18, 9.86)
36.4 67.5 68.6
1 1.80 2.10 0.003
(1.09, 2.98) (0.98, 4.50)
47.9 73.6 90.0
1 1.65 2.15 0.003
(1.03, 2.66) (1.10, 4.20)
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.
Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
207 208 209 210 211 212 213
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Table 3 Effects of environmental tobacco smoke (ETS) on bronchitis and bronchitic symptoms, Taiwan Children Health Study, 2007–2009.
t3:3
Bronchitis
t3:4
IR
RR
95% CI
IR
RR
95% CI
IR
RR
95% CI
8.9 7.0
1 0.72
(0.42, 1.25)
33.9 43.8
1 1.31
(1.03, 1.67)
47.2 51.5
1 1.14
(0.92, 1.41)
8.9 8.6 1.6
1 0.90 0.14 0.08
(0.48, 1.65) (0.01, 1.35)
33.9 44.9 41.7
1 1.36 1.22 0.04
(1.06, 1.76) (0.79, 1.88)
47.2 52.5 50.2
1 1.16 1.09 0.24
(0.93, 1.45) (0.74, 1.59)
8.9 6.1 9.2
1 0.68 0.84 0.44
(0.35, 1.32) (0.40, 1.75)
33.9 43.3 45.3
1 1.06 1.24 0.02
(0.70, 1.62) (0.90, 1.70)
47.2 50.4 55.2
1 1.12 1.20 0.13
(0.88, 1.43) (0.89, 1.61)
F
Current ETS No Yes Daily amount of ETS None ≦10 N10 p for trend Percent of ETSa None ≦20% N20% p for trend
Chronic phlegm
O
t3:5 t3:6 t3:7 t3:8 t3:9 t3:10 t3:11 t3:12 t3:13 t3:14 t3:15 t3:16 t3:17
Chronic cough
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. a Average percent of ETS in lifetime.
214
240
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 (de Marco et al., 2007; Guerra et al., 2009; Martinez et al., 2014). 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
t4:1 t4:2 t4:3
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.
231 232 233 234 235 236 237 238 239
t4:4 t4:5 t4:6 t4:7 t4:8 t4:9 t4:10 t4:11 t4:12 t4:13 t4:14 t4:15 t4:16 t4:17 t4:18
P
D
E
T
C
229 230
E
227 228
R
225 226
R
223 224
O
221 222
C
219 220
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.
N
217 218
U
215 216
R O
t3:18 t3:19 t3:20
Chronic cough Asthma/wheeze
p for interaction
Active smokingb
Unexposed
Exposed
No
Yes
RR
95% CI
RR
95% CI
RR
95% CI
RR
95% CI
No Yes
1 1.43 0.28
(0.91, 2.26)
1.23 1.40
(0.94, 1.60) (0.76, 2.57)
1 1.85 0.03
(1.34, 2.53)
2.01 0.32
(1.27, 3.16) (0.07, 1.40)
No Yes
1 0.86 0.02
(0.54, 1.36)
1.03 1.98
(0.81, 1.29) (1.09, 3.60)
1 1.34 0.03
(0.99, 1.81)
1.91 0.17
(1.29, 2.87) (0.02, 1.31)
p for interaction Chronic phlegm Asthma/wheeze
Current ETSa
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.
Please cite this article as: Chen, J.-M., et al., Active smoking, environmental tobacco smoke and bronchitic symptoms among adolescents in Taiwan: A prospective cohort study, Prev. Med. (2014), http://dx.doi.org/10.1016/j.ypmed.2014.05.007
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Conflict of interest statement
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Acknowledgment
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This work was partially supported by grants #98-2314-B-002138-MY3 and #96-2314-B-006-053 from the Taiwan National Science Council. The sponsors had no role in the design of the study, in the collection and analysis of the data, or in the preparation of the manuscript.
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The authors declare that there are no conflicts of interests.
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Incidence of asthma and respiratory symptoms by sex, age and smoking in a community study. Eur. Respir. J. 19, 599–605. Ellison-Loschmann, L., Sunyer, J., Plana, E., et al., 2007. Socioeconomic status, asthma and chronic bronchitis in a large community-based study. Eur. Respir. J. 29, 897–905. Forey, B.A., Thornton, A.J., Lee, P.N., 2011. Systematic review with meta-analysis of the epidemiological evidence relating to COPD, chronic bronchitis and emphysema. BMC Pulm. Med. 11, 36. Frank, P.I., Hazell, M.L., Morris, J.A., Linehan, M.F., Frank, T.L., 2007. A longitudinal study of changes in respiratory status in young adults, 1993–2001. Int. J. Tuber. Lung Dis. 11, 338–343. Gilliland, F.D., Li, Y.F., Peters, J.M., 2001. Effects of maternal smoking during pregnancy and environmental tobacco smoke on asthma and wheezing in children. Am. J. Respir. Crit. Care Med. 163, 429–436. Guerra, S., Sherrill, D.L., Venker, C., Ceccato, C.M., Halonen, M., Martinez, F.D., 2009. 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Parental and neonatal risk factors for atopy, airway hyper-responsiveness, and asthma. Arch. Dis. Child. 75, 392–398. Spanier, A.J., Kahn, R.S., Xu, Y., Hornung, R., Lanphear, B.P., 2011. Comparison of biomarkers and parent report of tobacco exposure to predict wheeze. J. Pediatr. 159, 776–782. Spee-van der Wekke, J., Meulmeester, J.F., Radder, J.J., Verloove-Vanhorick, S.P., 1998. School absence and treatment in school children with respiratory symptoms in the Netherlands: data from the Children Health Monitoring System. J. Epidemiol. Community Health 52, 359–363. Stoddard, J.J., Miller, T., 1995. Impact of parental smoking on the prevalence of wheezing respiratory illness in children. Am. J. Epidemiol. 141, 96–102. Strachan, D.P., Cook, D.G., 1998. Health effects of passive smoking. 6. Parental smoking and childhood asthma: longitudinal and case–control studies. Thorax 53, 204–212. Trédaniel, J., Boffetta, P., Saracci, R., Hirsch, A., 1994. 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References
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Supplementary data to this article can be found online at http://dx. 331 doi.org/10.1016/j.ypmed.2014.05.007. 332
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Appendix A. Supplementary data
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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 selfreported 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 Tables 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 on the reduction of ETS exposure are urgently needed to reduce the adverse impact on respiratory health in adolescents.
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Withers, N.J., Low, L., Holgate, S.T., Clough, J.B., 1998. The natural history of respiratory symptoms in a cohort of adolescents. Am. J. Respir. Crit. Care Med. 158, 352–357. Yeatts, K., Davis, K.J., Sotir, M., Herget, C., Shy, C., 2003. Who gets diagnosed with asthma? Frequent wheeze among adolescents with and without a diagnosis of asthma. Pediatrics 111, 1046–1054.
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