Parental smoke exposure and the development of nicotine craving in adolescent novice smokers: the roles of DRD2, DRD4, and OPRM1 genotypes

BMC Pulmonary Medicine

Joseph R. DiFranza³  Rutger C.M.E. Engels²  Marloes Kleinjan¹ 

[1] Trimbos Institute (Netherlands Institute of Mental Health and Addiction), Da Costakade 45, Utrecht, 3521 VS, The Netherlands;Behavioural Science Institute, Radboud University Nijmegen, Montessorilaan 3, Nijmegen, 6525 HR, The Netherlands;University of Massachusetts Medical School, 55 N Lake Ave, Worcester 01655, MA, USA

关键词: Parental smoke exposure;    Genes;    Novice smokers;    Early adolescents;    Craving;   

Others  :  1228326
DOI  :  10.1186/s12890-015-0114-z

 received in 2014-07-25, accepted in 2015-09-28,  发布年份 2015

【 摘 要 】

Background

Among adolescent novice smokers, craving is often the first, and is the most reported, symptom of nicotine dependence. Until now, little has been known about the development of craving symptoms in novice smokers. The aim of this study was to identify specific genetic (i.e., DRD2 Taq1A, DRD4 48 bp VNTR, and OPRM1 A118G polymorphisms) and environmental mechanisms that underlie the emergence of both cue-induced and cognitive craving among adolescent novice smokers.

Method

A five-wave longitudinal, genetically-informed survey study was conducted with intervals of four months. The sample included 376 early adolescent smokers (12–13 years of age at baseline). Self-report questionnaires were completed regarding smoking behavior, observed parental smoking behavior, and both cue-induced and cognitive craving.

Results

Data were analyzed with a latent growth curve approach. For both cue-induced and cognitive craving, significant interaction effects were found for DRD2 Taq1A with parental smoke exposure. A1-allele carriers did not seem to be influenced by the environment with regard to craving development. Adolescents who are homozygous for the A2-allele and who are more exposed to parental smoking experience the highest levels of both types of craving over time. No significant interaction effects were found between parental smoke exposure and DRD4 48 bp VNTR or OPRM1 A118G.

Conclusions

Previous studies identified DRD2 Taq1A A1-allele carriers as vulnerable to developing nicotine dependence. However, this study showed that parental smoking increased the chances of developing dependence more rapidly for early adolescents who are considered to be less sensitive to the rewarding effects of nicotine according to their DRD2 Taq1A genotype. It is thus especially important that these young people not be exposed to smoking in their social environment.

【 授权许可】

   
2015 Kleinjan et al.

【 图 表 】

Fig. 1.

Fig. 2.

【 参考文献 】

• [1]Kassel JD. Smoking and stress: correlation, causation, and context. Am Psychol. 2000; 55:1155-1156.
• [2]DiFranza JR. Initial symptoms of nicotine dependence in adolescents. Tob Control. 2000; 9:313-319.
• [3]DiFranza JR, Savageau JA, Fletcher K, Pbert L, O’Loughlin J, McNeill AD et al.. Susceptibility to nicotine dependence: the Development and Assessment of Nicotine Dependence in Youth 2 study. Pediatrics. 2007; 120:e974-83.
• [4]Riedel BW, Robinson LA, Klesges RC, McLain-Allen B. Ethnic differences in smoking withdrawal effects among adolescents. Addict Behav. 2003; 28:129-40.
• [5]Bagot KS, Heishman SJ, Moolchan ET. Tobacco craving predicts lapse to smoking among adolescent smokers in cessation treatment. Nicotine Tob Res. 2007; 9:647-52.
• [6]Rojas NL, Killen JD, Haydel KF, Robinson TN. Nicotine dependence among adolescent smokers. Arch Pediatr Adolesc Med. 1998; 152:151-156.
• [7]DiFranza JR, Wellman RJ. A sensitization-homeostasis model of nicotine craving, withdrawal, and tolerance: integrating the clinical and basic science literature. Nicotine Tob Res. 2005; 7:9-26.
• [8]DiFranza JR, Wellman RJ, Mermelstein R, Pbert L, KleinJ D, Sargent JD et al.. The Natural History and Diagnosis of Nicotine Addiction. Curr Pediatr Rev. 2011; 7:88-96.
• [9]Erblich J, Lerman C, Self DW, Diaz GA, Bovbjerg DH. Effects of dopamine D2 receptor (DRD2) and transporter (SLC6A3) polymorphisms on smoking cue-induced cigarette craving among African-American smokers. Mol Psychiatry. 2005; 10:407-414.
• [10]Hutchison KE, LaChance H, Niaura R, Bryan A, Smolen A. The DRD4 VNTR polymorphism influences reactivity to smoking cues. J Abnorm Psychol. 2002; 111:134-143.
• [11]Vandenbergh DJ, O’Connor RJ, Grant MD, Jefferson AL, Vogler GP, Strasser A a et al.. Dopamine receptor genes (DRD2, DRD3 and DRD4) and gene-gene interactions associated with smoking-related behaviors. Addict Biol. 2007; 12:106-116.
• [12]Brody AL, Mandelkern MA, Olmstead RE, Scheibal D, Hahn E, Shiraga S et al.. Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. Arch Gen Psychiatry. 2006; 63:808-816.
• [13]Laucht M, Becker K, Frank J. Genetic Variation in Dopamine Pathways Differentially Associated With Smoking Progression in Adolescence. J Am Acad Child Adolesc Psychiatry. 2008; 47:673-681.
• [14]Laucht M, Becker K, El-Faddagh M, Hohm E, Schmidt MH. Association of the DRD4 exon III polymorphism with smoking in fifteen-year-olds: a mediating role for novelty seeking? J Am Acad Child Adolesc Psychiatry. 2005; 44:477-484.
• [15]Shields PG, Lerman C, Audrain J, Bowman ED, Main D, Boyd NR et al.. Dopamine D4 receptors and the risk of cigarette smoking in African- Americans and Caucasians. Cancer Epidemiol Biomarkers Prev. 1998; 7:453-458.
• [16]Munafò MR, Timpson NJ, David SP, Ebrahim S, Lawlor DA. Association of the DRD2 gene Taq1A polymorphism and smoking behavior: a meta-analysis and new data. Nicotine Tob Res. 2009; 11:64-76.
• [17]Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom K-O. Fagerstrom test for nicotine dependence Br J Addiction 1991.pdf. Br J Addict. 1991; 86:1119-1127.
• [18]Robinson TE, Berridge KC. Addiction. Annu Rev Psychol. 2003; 54:25-53.
• [19]Berridge KC. Pleasures of the brain. Brain Cogn. 2003; 52:106-128.
• [20]Verhagen M, Kleinjan M, Engels RCME. A systematic review of the A118G (Asn40Asp) variant of OPRM1 in relation to smoking initiation, nicotine dependence and smoking cessation. Pharmacogenomics. 2012; 13:917-933.
• [21]Ray R, Jepson C, Patterson F, Strasser A, Rukstalis M, Perkins K et al.. Association of OPRM1 A118G variant with the relative reinforcing value of nicotine. Psychopharmacology (Berl). 2006; 188:355-363.
• [22]Kleinjan M, Poelen EA, Engels RCME, Verhagen M. Dual growth of adolescent smoking and drinking: evidence for an interaction between the mu-opioid receptor (OPRM1) A118G polymorphism and sex. Addict Biol. 2012.
• [23]Carter BL, Tiffany SENT. A Meta-analysis of cue-reactivity in addiction research. Addiction. 1999; 94:327-340.
• [24]Droungas A, Ehrman RN. Childress a R, O’Brien CP: Effect of smoking cues and cigarette availability on craving and smoking behavior. Addict Behav. 1995; 20:657-673.
• [25]Field M, Cox WM. Attentional bias in addictive behaviors: A review of its development, causes, and consequences. Drug Alcohol Depend. 2008; 97:1-20.
• [26]Payne TJ, Schare ML, Levis DJ, Colletti G. Exposure to Smoking-Relevant Cues: Effects on Desire to Smoke and Topographical Components of Smoking Behavior. Addict Behav;. 1991; 16:467-479.
• [27]Steinberg L. A Social Neuroscience Perspective on Adolescent Risk-Taking. Dev Rev. 2008; 28:78-106.
• [28]Wiers RW, Bartholow BD, van den Wildenberg E, Thush C, Engels RCME, Sher KJ et al.. Automatic and controlled processes and the development of addictive behaviors in adolescents: A review and a model. Pharmacol Biochem Behav. 2007; 86:263-283.
• [29]Kleinjan M, Engels RCME, van Leeuwe J, Brug J, van Zundert RMP, van den Eijnden RJJM. Mechanisms of adolescent smoking cessation: roles of readiness to quit, nicotine dependence, and smoking of parents and peers. Drug Alcohol Depend. 2009; 99:204-214.
• [30]Okoli CTC, Richardson CG, Johnson JL. An examination of the relationship between adolescents’ initial smoking experience and their exposure to peer and family member smoking. Addict Behav. 2008; 33:1183-1191.
• [31]Al-Delaimy WK, Crane J, Woodward A. Passive smoking in children: effect of avoidance strategies, at home as measured by hair nicotine levels. Arch Environ Health. 2001; 56:117-122.
• [32]Dimich-Ward H, Gee H, Brauer M, Leung V. Analysis of nicotine and cotinine in the hair of hospitality workers exposed to environmental tobacco smoke. J Occup Environ Med Am Coll Occup Environ Med. 1997; 39:946-948.
• [33]Jarvis MJ, Russell MA, Feyerabend C. Absorption of nicotine and carbon monoxide from passive smoking under natural conditions of exposure. Thorax. 1983; 38:829-833.
• [34]Brody AL, Mandelkern MA, London ED, Khan A, Kozman D, Costello MR et al.. Effect of secondhand smoke on occupancy of nicotinic acetylcholine receptors in brain. Arch Gen Psychiatry. 2011; 68:953-960.
• [35]Small E, Shah HP, Davenport JJ, Geier JE, Yavarovich KR, Yamada H et al.. Tobacco smoke exposure induces nicotine dependence in rats. Psychopharmacology (Berl). 2010; 208:143-158.
• [36]Yamada H, Bishnoi M, Keijzers KFM, Van Tuijl IA, Small E, Shah HP et al.. Preadolescent tobacco smoke exposure leads to acute nicotine dependence but does not affect the rewarding effects of nicotine or nicotine withdrawal in adulthood in rats. Pharmacol Biochem Behav. 2010; 95:401-409.
• [37]Otten R, Engels RCME, Prinstein MJ. A prospective study of perception in adolescent smoking. J Adolesc Health. 2009; 44:478-484.
• [38]Racicot S, McGrath JJ, O’Loughlin J. An investigation of social and pharmacological exposure to secondhand tobacco smoke as possible predictors of perceived nicotine dependence, smoking susceptibility, and smoking expectancies among never-smoking youth. Nicotine Tob Res. 2011; 13:926-933.
• [39]Schuck K, Otten R, Engels RCME, Kleinjan M. The relative role of nicotine dependence and smoking-related cognitions in adolescents’ process of smoking cessation. Psychol Heal. 2011; 26:1310-1326.
• [40]Leonardi-Bee J, Jere ML, Britton J. Exposure to parental and sibling smoking and the risk of smoking uptake in childhood and adolescence: a systematic review and meta-analysis. Thorax. 2011; 66:847-855.
• [41]Hu M-C, Davies M, Kandel DB. Epidemiology and correlates of daily smoking and nicotine dependence among young adults in the United States. Am J Public Health. 2006; 96:299-308.
• [42]De Leeuw RNH, Engels RCME, Vermulst AA, Scholte RHJ. Relative risks of exposure to different smoking models on the development of nicotine dependence during adolescence: a five-wave longitudinal study. J Adolesc Health. 2009; 45:171-178.
• [43]Rutter M. Genes and Behavior; Nature-Nurture Interplay Explained. Blackwell Publishing, Malden, MA; 2006.
• [44]Rutter M, Silberg J. Gene-environment interplay in relation to emotional and behavioral disturbance. Annu Rev Psychol. 2002; 53:463-490.
• [45]Hiemstra M, Kleinjan M, van Schayck OCP, Engels RCME, Otten R. Environmental smoking and smoking onset in adolescence: the role of dopamine-related genes. Findings from two longitudinal studies. PLoS One. 2014; 9: Article ID e86497
• [46]Koopmans JR, Slutske WS. The genetics of smoking initiation and quantity smoked in Dutch adolescent and young adult twins. Behav Genet. 1999; 29:383-393.
• [47]Vink JM, Willemsen G, Boomsma DI. Heritability of smoking initiation and nicotine dependence. Behav Genet. 2005; 35:397-406.
• [48]Nilsson KW, Oreland L, Kronstrand R, Leppert J. Smoking as a product of gene-environment interaction. Ups J Med Sci. 2009; 114:100-107.
• [49]Singleton EG, Gorelick DA. Mechanisms of alcohol craving and their clinical implications. Recent Dev Alcohol. 1998; 14:177-195.
• [50]Gauderman W, Morrison J: Quanto 1.2.3. A computer program for power and sample size calculations for genetic-epidemiology studies. 2007.
• [51]Kleinjan M, Wanner B, Vitaro F, Van den Eijnden RJJM, Brug J, Engels RCME. Nicotine dependence subtypes among adolescent smokers: examining the occurrence, development and validity of distinct symptom profiles. Psychol Addict Behav. 2010; 24:61-74.
• [52]Kleinjan M, Vitaro F, Wanner B, Brug J, Van den Eijnden RJJM, Engels RCME. Predicting nicotine dependence profiles among adolescent smokers: the roles of personal and social-environmental factors in a longitudinal framework. BMC Public Health. 2012; 12:196. BioMed Central Full Text
• [53]Stivoro: Smoking: The Hard Facts (Roken, de Harde Feiten). Den Haag; 2012.
• [54]Audrain-McGovern J, Rodriguez D, Wileyto EP, Schmitz KH, Shields PG. Effect of team sport participation on genetic predisposition to adolescent smoking progression. Arch Gen Psychiatry. 2006; 63:433-441.
• [55]Bau CHD, Almeida S, Hutz MH. The Taq1 A1 allele of the dopamine D2 receptor gene and alcoholism in Brazil. Am J Med Genet. 2000; 96:302-306.
• [56]Larsen H, Van der Zwaluw CS, Overbeek G, Granic I, Franke B, Engels RCME. The DRD4 genotype and social adaptation of alcohol use: a geneenvironment interaction. Psych Science. 2010; 21:1064-1068.
• [57]Harakeh Z, Scholte RHJ, de Vries H, Engels RCME. Parental rules and communication: their association with adolescent smoking. Addiction. 2005; 100:862-70.
• [58]Kleinjan M, Brug J, van den Eijnden RJJM, Vermulst AA, van Zundert RMP, Engels RCME. Associations between the transtheoretical processes of change, nicotine dependence and adolescent smokers’ transition through the stages of change. Addiction. 2008; 103:331-338.
• [59]Kremers SP, Mudde AN, de Vries H. Subtypes within the precontemplation stage of adolescent smoking acquisition. Addict Behav. 2001; 26:237-251.
• [60]DiFranza JR, Wellman RJ, Ursprung WWSA, Sabiston C. The Autonomy Over Smoking Scale. Psychol Addict Behav J Soc Psychol Addict Behav. 2009; 23:656-665.
• [61]DiFranza JR, Sweet M, Savageau JA, Ursprung WWS. The assessment of tobacco dependence in young users of smokeless tobacco. Tob Control. 2012;471–476.
• [62]Dijkstra A, Borland R. Residual outcome expectations and relapse in ex-smokers. Heal Psychol. 2003; 22:340-346.
• [63]Muthén BO, Muthén LK. Mplus User’s Guide (sixth edition). Muthén & Muthén, Los Angeles; 2007.
• [64]Hu L, Bentler PM. Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Struct Equ Model A Multidiscip J. 1999;1–55.
• [65]Zhu SH, Pulvers K. Beyond withdrawal symptoms: response to DiFranza. Addiction. 2008; 103:512-513.
• [66]Becklake MR, Ghezzo H, Ernst P. Childhood predictors of smoking in adolescence: a follow-up study of Montreal schoolchildren. Can Med Assoc J. 2005; 173:377-379.
• [67]Bernat DH, Erickson DJ, Widome R, Perry CL, Forster JL. Adolescent smoking trajectories: results from a population-based cohort study. J Adolesc Heal. 2008; 43:334-340.
• [68]Kleinjan M, Van den Eijnden RJJM, Van Leeuwe J, Brug J, Van de Ven, MOM, Engels, RCME. Adolescents’ movement towards cessation of smoking: Role and relative value of the processes of change and nicotine dependence. Psychol Health. 2008;23:729-743.
• [69]Wiebe SA, Espy KA, Stopp C, Respass J, Stewart P, Jameson TR et al.. Gene-environment interactions across development: Exploring DRD2 genotype and prenatal smoking effects on self-regulation. Dev Psychol. 2009; 45:31-44.
• [70]Van der Zwaluw CS, Engels RCME, Vermulst AA, Franke B, Buitelaar J, Verkes RJ et al.. Interaction between dopamine D2 receptor genotype and parental rule-setting in adolescent alcohol use: evidence for a gene-parenting interaction. Mol Psychiatry. 2010; 15:727-735.
• [71]Noble EP, Blum K, Ritchie T, Montgomery A, Sheridan PJ. Allelic association of the D2 dopamine receptor gene with receptor-binding characteristics in alcoholism. Arch Gen Psychiatry. 1991; 48:648-654.
• [72]DiFranza JR, Savageau JA, Rigotti NA, Ockene JK, McNeill AD, Coleman M et al.. Trait anxiety and nicotine dependence in adolescents: a report from the DANDY study. Addict Behav. 2004; 29:911-919.
• [73]Kandel DB, Hu M-C, Griesler PC, Schaffran C. On the development of nicotine dependence in adolescence. Drug Alcohol Depend. 2007; 91:26-39.
• [74]Sartor CE, Lessov-Schlaggar CN, Scherrer JF, Bucholz KK, Madden PAF, Pergadia ML et al.. Initial response to cigarettes predicts rate of progression to regular smoking: findings from an offspring-of-twins design. Addict Behav. 2010; 35:771-778.
• [75]Difranza JR, Savageau JA, Fletcher K, Pbert L, Loughlin O, Mcneill AD et al.. Susceptibility to Nicotine Dependence : The Development and Assessment of Nicotine Dependence in Youth 2 Study. Arch Pediatr Adolesc Med. 2007; 161:704-710.
• [76]Schuck K, Otten R, Engels RCME, Kleinjan M. Initial responses to the first dose of nicotine in novel smokers: The role of exposure to environmental smoking and genetic predisposition. Psychol Health. 2014; 29:698-716.
• [77]Cloninger CR, Svrakic DM, Przybeck TR. A psychobiological model of temperament and character. Arch Gen Psychiatry. 1993; 50:975-990.
• [78]Lochbuehler K, Verhagen M, Munafò MR, Engels RCME. Lack of association of DRD4 exon 3 VNTR genotype with reactivity to dynamic smoking cues in movies. Drug Alcohol Depend. 2013; 132:324-328.
• [79]Field M, Munafò MR, Franken IHA. A meta-analytic investigation of the relationship between attentional bias and subjective craving in substance abuse. Psychol Bull. 2009; 135:589-607.
• [80]Singleton E, Moolchan E, Heishman S. Tobacco Craving Questionnaire: Reliability and validity of a new multifactorial instrument. Nicotine Tob Res. 2003; 5:645-654.
• [81]Rutter M. Biological implications of gene-environment interaction. J Abnorm Child Psychol. 2008; 36:969-75.
• [82]Marchini J, Cardon LR, Phillips MS, Donnelly P. The effects of human population structure on large genetic association studies. Nat Genet. 2004; 36:512-7.