Abstract Objective We aimed to evaluate the association between environmental tobacco smoke (ETS) exposure and urinary cotinine levels in current adolescent smokers and nonsmokers. The secondary objective was to explore the association between ETS exposure and nicotine dependence in adolescent smokers. Methods Using the results from a validation study for the 2012 Global Youth Tobacco Survey in Mexico, we quantified urinary cotinine levels in adolescent smokers and nonsmokers. We fitted a multivariate regression model to assess the association between household exposure to ETS and cotinine levels in adolescent smokers and nonsmokers. In addition, using the questionnaire’s answers for morning cravings, we fitted a multivariate Poisson regression model to explore the association between household ETS exposure and nicotine dependence in adolescent smokers. Results For each day of household ETS exposure, cotinine levels increase by 5% in adolescent smokers compared to a 2% increase in nonsmokers, adjusting for the number of cigarettes smoked per week, age and sex (exp(β) 1.05; 95% confidence interval [CI] [1.00, 1.10]; p = .041). Morning cravings increase 11% for each day of household ETS exposure adjusting for the number of cigarettes smoked per week, age and sex (prevalence ratio [PR] 1.11; 95% CI [0.99, 1.25]; p = .064). Conclusions There is an association between ETS exposure and cotinine levels, and ETS may contribute to nicotine dependence in adolescent smokers. If confirmed, avoiding ETS exposure could prove helpful for addiction control and quitting in adolescents. Implications Evidence suggests that ETS increases cotinine levels in nonsmokers and adult smokers. However, no study has explored the association between ETS exposure and cotinine levels and addiction in adolescent smokers. This paper provides evidence of an association between ETS exposure and cotinine levels in adolescent smokers: each day of environmental tobacco smoke exposure at home increased cotinine levels by 5% among smokers. In addition, morning cravings in adolescent smokers increased 11% for every day of ETS exposure. ETS exposure is a significant source of nicotine for adolescent smokers and could play an important role in addiction. Introduction The addictive effects of smoking and ETS exposure in the smoking population remain understudied and controversial.1 Increasing ETS exposure seems to increase the nicotine intake of smokers; adult smokers living in homes where others smoke had significantly higher cotinine levels than smokers who did not report ETS exposure.2 Inhaled nicotine from ETS occupies nicotinic acetylcholine receptors, facilitating nicotine dependence among smokers in a similar way as active smoking.3 Evidence suggests that ETS exposure during adolescence could play an important role in smoking initiation, active smoking, and cessation4,5; however, the specific pathway for such association remains unknown.1 Adolescence is the most critical period of life for the development of nicotine addiction.6,7 Adolescents have the lowest rate of cessation attempts and success across the lifespan.8 Every year, two-thirds of adolescent smokers try to quit, but only 2% succeed.8,9 While previous research has shown that nonsmoking children and adolescents exposed to environmental tobacco smoke (ETS) present craving and withdrawal symptoms, no study has explored the association between ETS exposure and cotinine levels and addiction in adolescent smokers.10 Understanding the contribution of ETS exposure to cotinine levels and addiction in smokers is paramount to increase the odds for quitting in this population. We aimed to evaluate the association between ETS exposure and urinary cotinine levels in current adolescent smokers and nonsmokers. The secondary aim was to explore the association between ETS exposure and nicotine dependence in adolescent smokers. Methods A total of 1257 students between 11 and 17 years old participating in a validation study for the 2012 Global Youth Tobacco Survey in Mexico provided both a questionnaire and a urine sample. The questionnaire evaluated tobacco-related attitudes, knowledge, and behaviors; the sample design and survey methods have been previously described.11 Parental informed consent and student verbal assent was received in accordance to the Ethics Committee from the National Institute of Public Health in Mexico (920–955). Cotinine Concentrations of urinary cotinine were quantified using gas chromatography.11 The detection limit was 16.09 ng/mL. All participants with undetectable cotinine levels were imputed with half the limit of detection (8.04 ng/mL). Nicotine Dependence Nicotine dependence was characterized by the urge to smoke in the morning, using the question “Do you ever have a cigarette or feel like having a cigarette first thing in the morning?” with predefined answers: “I have never smoked cigarettes,” “I no longer smoke cigarettes” “No, I do not feel like having a cigarette first thing in the morning”; “Yes, I sometimes feel like having a cigarette first thing in the mornings”; and “Yes, I always feel like having a cigarette first thing in the mornings.” Answers were dichotomized into “yes” if the answers were sometimes or always, and “no” if the answer was otherwise. ETS Exposure ETS exposure was assessed using the question: “During the past 7 days, on how many days have people smoked in your home, in your presence?” with potential answers: “0 days”, “1–2 days”, “3–4 days”, “5–6 days”, and “7 days.” For the inferential analysis, the mid value of each range was used. Smoking Status To determine current smoking status, we used the question: “During the past 30 days (1 month), on how many days did you smoke cigarettes?”, with potential answers: “0 days”, “1 to 2 days”, “3 to 5 days”, “6 to 9 days”, “10 to 19 days”, “20 to 29 days”, and “All 30 days”. Participants who did not smoke during the past 30 days were classified as nonsmokers, while the rest were considered smokers. Since the number of cigarettes smoked increases both the cotinine levels and ETS exposure through mainstream smoke and self-produced ETS exposure, for those classified as smokers, we considered the number of cigarettes per week. To estimate the number of cigarettes per week we used two questions: (1) “During the past 30 days, on how many days did you smoke? (with the above-mentioned answer categories), and (2) “During the past 30 days, on the days you smoked, how many cigarettes did you smoke?” with the following predefined answer categories: “I did not some cigarettes during the past 30 days”, “less than 1 cigarette”, “one cigarette”, “2 to 5 cigarettes”, “6 to 10 cigarettes”, and “11 to 20 cigarettes”. We used the mid-value of the specified range in each answer category and multiplied the number of days they smoked times the number of cigarettes to obtain the number of cigarettes per day; this result was further multiplied times 30 and divided by seven to obtain the number of cigarettes per week. Covariates Self-reported age in years and sex were considered potential confounders. Statistical Analysis Frequencies and percentages for the categorical variables and median and interquartile range for the continuous variables were used to describe the data. Bivariate associations were assessed using Chi-square or Fisher’s exact test for categorical variables, and Wilcoxon test for continuous variables. Participants with missing data (n = 97) were excluded from the analysis. To evaluate the association between ETS and cotinine levels, in both smokers and nonsmokers, we fitted a robust linear regression model stratified by smoking status. The log-transformed cotinine concentration was used as the outcome variable, and cigarettes per week (in smokers) and ETS exposure as predictor variables, controlling for age and sex. Coefficients were back transformed to facilitate interpretation. To explore the association between ETS and nicotine dependence in smokers, we fitted a multivariate Poisson regression with urge to smoke in the mornings as the outcome; cigarettes per week and ETS were the main predictors, controlling for age and sex. We established a significance level of p < .05 for all tests. All analyses were performed in Stata 13.0 (StataCorp LP, College Station, TX). Results Sample characteristics stratified by smoking status are presented in Supplementary Table 1. Out of 1160 participants, 20% were smokers. Among smokers, 45.7% reported no ETS exposure at home, compared to 60.3% among nonsmokers. Median cotinine levels by smoking status and days of ETS exposure at home are displayed in Supplementary Table 2. For smokers, cotinine levels increased as the days of ETS exposure at home increased (p for trend .011). For nonsmokers, cotinine concentrations did not increase in a linear fashion, with the highest median concentration being observed in those exposed 5–6 days per week (p for trend .001). The associations between ETS at home and cotinine levels stratifying by smoking status are described in Table 1. Among smokers, cotinine levels increased 5% for each day of exposure to ETS (exp(β) 1.05; 95% CI [1.00, 1.10]; p = .041) and for every cigarette per week (exp(β) 1.05; 95% CI [1.02, 1.08]; p ≤ .001), adjusting for age and sex. In nonsmokers, cotinine levels increased 2% for each day of exposure to ETS, adjusting for age and sex (exp(β) 1.02; 95% CI [1.01, 1.03]; p = .001). Table 1. Robust Multiple Linear Regression for the Association Between Cotinine Levels, Smoking, and ETS Exposure Exp(β)a (95% CI) p value Smokers Days of ETS exposure at home 1.05 (1.00, 1.10) .041 Cigarettes per week 1.05 (1.02, 1.08) <.001 Age (years) 1.21 (1.11, 1.32) <.001 Sex (female) 1.14 (0.87, 1.48) .340 Nonsmokers Days of ETS exposure at home 1.02 (1.01,1.03) .001 Age (years) 1.00 (0.97,1.02) .689 Sex (female) 0.99 (0.93,1.04) .636 Exp(β)a (95% CI) p value Smokers Days of ETS exposure at home 1.05 (1.00, 1.10) .041 Cigarettes per week 1.05 (1.02, 1.08) <.001 Age (years) 1.21 (1.11, 1.32) <.001 Sex (female) 1.14 (0.87, 1.48) .340 Nonsmokers Days of ETS exposure at home 1.02 (1.01,1.03) .001 Age (years) 1.00 (0.97,1.02) .689 Sex (female) 0.99 (0.93,1.04) .636 CI = Confidence interval; ETS = Environmental tobacco smoke. aThe log-transformed cotinine concentration was used as the outcome variable. Coefficients were back transformed to facilitate interpretation. View Large Table 2 presents the association between ETS exposure and morning cravings among smokers. Adjusting for age and sex, each day of ETS exposure at home is associated with an 11% increase in the prevalence of nicotine dependence (PR 1.11; 95% CI [0.99, 1.25]; p = .064). In the same model, each cigarette per week is associated with a 5% increase in the prevalence of nicotine dependence (PR 1.05; 95% CI (1.02, 1.07); p < .001). Table 2. Multivariate Poisson Regression to Evaluate the Association Between Nicotine Dependence, Smoking, and ETS in Smokers PR (95% CI) p value Days of ETS exposure at home 1.11 (0.99, 1.25) .064 Cigarettes per week 1.05 (1.02, 1.07) <.001 Age (years) 0.89 (0.69, 1.16) .390 Sex (female) 1.30 (0.61, 7.76) .492 PR (95% CI) p value Days of ETS exposure at home 1.11 (0.99, 1.25) .064 Cigarettes per week 1.05 (1.02, 1.07) <.001 Age (years) 0.89 (0.69, 1.16) .390 Sex (female) 1.30 (0.61, 7.76) .492 CI = Confidence interval; ETS = Environmental tobacco smoke. View Large Discussion The effects of ETS exposure among smokers have been poorly studied. Recent evidence showed that adult smokers exposed to ETS at home have higher cotinine levels than those living in smoke-free homes.2 Among smoking adolescents, we found a positive association between cotinine levels and frequency of ETS exposure at home after adjustment for number of cigarettes smoked per day. The magnitude of one day of exposure to ETS at home was similar to that observed for one cigarette smoked per week, both increasing cotinine levels by 5%. Urinary cotinine levels correlate with several smoking behaviors, including number of cigarettes per day, time since last cigarette, and having a family member who smokes at home.12 Previous studies have shown that smokers are more likely to be exposed to ETS than nonsmokers,1 ETS must be considered as an important source of nicotine in adolescent smokers, and a potential target for cessation programs. A 2015 systematic review of observational studies found mixed evidence of an association between ETS exposure and nicotine dependence.1 Three studies included in this review were conducted in adolescents: two found an association and one did not.5,13,14 We found that the more days per week adolescents are exposed to ETS, the prevalence of nicotine dependence is more likely to increase, independently of the number of cigarettes they smoke per week. Even though our results were marginally significant, we believe our findings help to elucidate the biological pathway for this association since we also found an association of ETS and cotinine independent of active smoking. Some limitations must be mentioned. The question used to assess nicotine dependence is not a full questionnaire, such as the Fagerström. Time to first cigarette after waking up in the morning has become increasingly recognized as an indicator of nicotine dependence and is highly correlated with cotinine concentrations.15 The question used in the GYTS survey was derived from the Fagerström test and was validated and used in other studies to assess nicotine dependence.5,16 Another limitation is that the true contribution of ETS to cotinine is likely underestimated, since we only considered household exposure, lacking information on other sites such as public places. However, the smoke-free law in Mexico has decreased ETS exposure levels in public places, reducing the contribution to individual exposure.17 Another concern is that the half-life of cotinine is 19 hours, providing a short window for detection. This could pose a risk for misclassification bias for those who are occasionally exposed to nicotine; cotinine levels are more likely to decay after no nicotine exposure for 18–20 hours.18 Still, given that cotinine levels only decay and there is no increase, we would be underestimating the association. Previous studies have shown that ETS contributes to smoking initiation, dependence, and cessation in adolescents.5,14,19,20 The findings of this paper provide evidence of an important association between ETS exposure and cotinine levels, and of the potential role of ETS exposure in nicotine dependence. Understanding the contribution of ETS exposure to adolescent addiction could open a new front for smoking prevention; encouraging smokers to stop smoking indoors and promoting 100% smoke-free households and environments could become a useful tool to reduce nicotine dependence and increase the odds of quitting. Future studies are needed to confirm these associations and explore the impact of ETS exposure reduction in the cessation process. Supplementary Material Supplementary data are available at Nicotine & Tobacco Research online. Funding This work was supported by the Health Ministry of Mexico (Mexico City, Mexico) grant number 448–6617. Declaration of Interests The authors have no conflicts of interest or financial relationships relevant to this article to disclose. Acknowledgments Technical support for this study was provided by the Health Ministry of Mexico (Mexico City, Mexico). The authors would like to thank the Pan-American Health Organization (Mexico City, Mexico), the Centers for Disease Control (Atlanta, MA), the Health Ministry of the State of Hidalgo (Pachuca, Mexico), the Education Ministry of Mexico, the National Commission Against Addiction, the National Center for the Prevention and Control of Addictions, the National Office for Tobacco Control and the State Councils Against Addictions for their continued support in the development of this project. The authors are grateful to all research assistants, lab technicians, and participants involved in this project. References 1. Okoli CTC, Kodet J. A systematic review of secondhand tobacco smoke exposure and smoking behaviors: smoking status, susceptibility, initiation, dependence, and cessation. Addict Behav . 2015; 47: 22– 32. Google Scholar CrossRef Search ADS PubMed 2. Lindsay RP, Tsoh JY, Sung HY, Max W. Secondhand smoke exposure and serum cotinine levels among current smokers in the USA. Tob Control . 2016; 25( 2): 224– 231. doi: 10.1136/tobaccocontrol-2014-051782 Google Scholar CrossRef Search ADS PubMed 3. Brody AL, Mandelkern MA, London EDet al. . Effect of secondhand smoke on occupancy of nicotinic acetylcholine receptors in brain. Arch Gen Psychiatry . 2011; 68( 9): 953– 960. Google Scholar CrossRef Search ADS PubMed 4. Okoli CT, Browning S, Rayens MK, Hahn EJ. Secondhand tobacco smoke exposure, nicotine dependence, and smoking cessation. Public Health Nurs . 2008; 25( 1): 46– 56. Google Scholar CrossRef Search ADS PubMed 5. Wang MP, Ho SY, Lo WS, Lam TH. Smoking family, secondhand smoke exposure at home, and nicotine addiction among adolescent smokers. Addict Behav . 2012; 37( 6): 743– 746. Google Scholar CrossRef Search ADS PubMed 6. Riggs NR, Chou CP, Li C, Pentz MA. Adolescent to emerging adulthood smoking trajectories: when do smoking trajectories diverge, and do they predict early adulthood nicotine dependence? Nicotine Tob Res . 2007; 9( 11): 1147– 1154. Google Scholar CrossRef Search ADS PubMed 7. Heinz AJ, Kassel JD, Berbaum M, Mermelstein R. Adolescents’ expectancies for smoking to regulate affect predict smoking behavior and nicotine dependence over time. Drug Alcohol Depend . 2010; 111( 1–2): 128– 135. Google Scholar CrossRef Search ADS PubMed 8. Bancej C, O’Loughlin J, Platt RW, Paradis G, Gervais A. Smoking cessation attempts among adolescent smokers: a systematic review of prevalence studies. Tob Control . 2007; 16( 6): e8. Google Scholar CrossRef Search ADS PubMed 9. The Global Youth Tobacco Survey Collaborative Group. Tobacco use among youth: a cross country comparison. Tob Control . 2002; 11( 3): 252– 270. CrossRef Search ADS PubMed 10. Branstetter SA, Muscat JE. Time to first cigarette and serum cotinine levels in adolescent smokers: National health and nutrition examination survey, 2007–2010. Nicotine Tob Res . 2013; 15( 3): 701– 707. Google Scholar CrossRef Search ADS PubMed 11. del Carmen Valladolid-López M, Barrientos-Gutiérrez T, Reynales-Shigematsu LMet al. . Evaluating the validity of self-reported smoking in Mexican adolescents. BMJ Open . 2015; 5( 10): e007485. Google Scholar CrossRef Search ADS PubMed 12. Lonergan BJ, Meaney S, Perry IJet al. . Smokers still underestimate the risks posed by secondhand smoke: a repeated cross-sectional study. Nicotine Tob Res . 2014; 16( 8): 1121– 1128. Google Scholar CrossRef Search ADS PubMed 13. Grana RA, Ramo DE, Fromont SC, Hall SM, Prochaska JJ. Correlates of tobacco dependence and motivation to quit among young people receiving mental health treatment. Drug Alcohol Depend . 2012; 125( 1-2): 127– 131. Google Scholar CrossRef Search ADS PubMed 14. Vançelik S, Beyhun NE, Acemoğlu H. Interactions between exhaled CO, smoking status and nicotine dependency in a sample of Turkish adolescents. Turk J Pediatr . 2009; 51( 1): 56– 64. Google Scholar PubMed 15. Heatherton TF, Kozlowski LT, Frecker RC, Fagerström KO. The Fagerström Test for Nicotine Dependence: a revision of the Fagerström Tolerance Questionnaire. Br J Addict . 1991; 86( 9): 1119– 1127. Google Scholar CrossRef Search ADS PubMed 16. Lam E, Giovino GA, Shin M, Lee K, Rolle I, Asma S. Relationship between frequency and intensity of cigarette smoking and TTFC/C among students of the GYTS in select countries, 2007–2009. J Sch Heal . 2014; 84( 9): 549– 558. Google Scholar CrossRef Search ADS 17. Barrientos-Gutierrez T, Amick BC3rd, Gimeno Det al. . Mechanical systems versus smoking bans for secondhand smoke control. Nicotine Tob Res . 2012; 14( 3): 282– 289. Google Scholar CrossRef Search ADS PubMed 18. Caraballo RS, Giovino GA, Pechacek TF, Mowery PD. Factors associated with discrepancies between self-reports on cigarette smoking and measured serum cotinine levels among persons aged 17 years or older: Third National Health and Nutrition Examination Survey, 1988-1994. Am J Epidemiol . 2001; 153( 8): 807– 814. Google Scholar CrossRef Search ADS PubMed 19. Wang MP, Ho SY, Lo WS, Lam TH. Smoking family, secondhand smoke exposure at home, and quitting in adolescent smokers. Nicotine Tob Res . 2013; 15( 1): 185– 191. Google Scholar CrossRef Search ADS PubMed 20. Wang MP, Ho SY, Lam TH. Parental smoking, exposure to secondhand smoke at home, and smoking initiation among young children. Nicotine Tob Res . 2011; 13( 9): 827– 832. Google Scholar CrossRef Search ADS PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Research on Nicotine and Tobacco. All rights reserved. For permissions, please e-mail: email@example.com.
Nicotine and Tobacco Research – Oxford University Press
Published: Apr 1, 2018
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