Behavior Genetics

, Volume 42, Issue 4, pp 614–625 | Cite as

Genetic and Environmental Influences Underlying Externalizing Behaviors, Cigarette Smoking and Illicit Drug Use Across Adolescence

  • Tellervo Korhonen
  • Antti Latvala
  • Danielle M. Dick
  • Lea Pulkkinen
  • Richard J. Rose
  • Jaakko Kaprio
  • Anja C. Huizink
Original Paper

Abstract

We investigated genetic and environmental influences common to adolescent externalizing behavior (at age 12), smoking (at age 14) and initiation of drug use (at age 17) using the FinnTwin12 cohort data. Multivariate Cholesky models were fit to data from 737 monozygotic and 722 dizygotic twin pairs. Heritability of externalizing behavior was 56%, that of smoking initiation/amount 20/32%, and initiation of drug use 27%. In the best-fitting model common environmental influences explained most of the covariance between externalizing behavior and smoking initiation (69%) and amount (77%). Covariance between smoking initiation/amount and drug use was due to additive genetic (42/22%) and common environmental (58/78%) influences. Half of the covariance between externalizing behavior and drug use was due to shared genetic and half due to the environments shared by co-twins. Using a longitudinal, prospective design, our results indicate that early observed externalizing behavior provides significant underlying genetic and environmental influences common to later substance use, here manifested as initiation of drug use in late adolescence.

Keywords

Externalizing behavior Smoking Drugs Genetic modeling 

References

  1. Achenbach TM (1991) Manual for the child behavior checklist 4–18 and 1991 profile. University of Vermont, BurlingtonGoogle Scholar
  2. Agrawal A, Lynskey MT (2006) The genetic epidemiology of cannabis use, abuse and dependence. Addiction 101(6):801–812PubMedCrossRefGoogle Scholar
  3. Agrawal A, Lynskey MT (2008) Are there genetic influences on addiction: evidence from family, adoption and twin studies. Addiction 103(7):1069–1081PubMedCrossRefGoogle Scholar
  4. Agrawal A, Silberg JL, Lynskey MT, Maes HH, Eaves LJ (2010) Mechanisms underlying the lifetime co-occurrence of tobacco and cannabis use in adolescent and young adult twins. Drug Alcohol Depend 108(1–2):49–55PubMedCrossRefGoogle Scholar
  5. Barman SK, Pulkkinen L, Kaprio J, Rose RJ (2004) Inattentiveness, parental smoking and adolescent smoking initiation. Addiction 99(8):1049–1061PubMedCrossRefGoogle Scholar
  6. Boomsma D, Busjahn A, Peltonen L (2002) Classical twin studies and beyond. Nat Rev Genet 3(11):872–882PubMedCrossRefGoogle Scholar
  7. Crews F, HE J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86(2):189–199PubMedCrossRefGoogle Scholar
  8. Dick DM, Meyers JL, Rose RJ, Kaprio J, Kendler KS (2011) Measures of current alcohol consumption and problems: two independent twin studies suggest a complex genetic architecture. Alcohol Clin Exp Res 35(12):2152–2161PubMedCrossRefGoogle Scholar
  9. Fergusson DM, Horwood LJ, Ridder EM (2007) Conduct and attentional problems in childhood and adolescence and later substance use, abuse and dependence: results of a 25-year longitudinal study. Drug Alcohol Depend 88(Suppl 1):S14–S26PubMedCrossRefGoogle Scholar
  10. Fowler T, Lifford K, Shelton K, Rice F, Thapar A, Neale MC, McBride A, Van Den Bree MB (2007) Exploring the relationship between genetic and environmental influences on initiation and progression of substance use. Addiction 102(3):413–422PubMedCrossRefGoogle Scholar
  11. Hamilton AS, Lessov-Schlaggar CN, Cockburn MG, Unger JB, Cozen W, Mack TM (2006) Gender differences in determinants of smoking initiation and persistence in California twins. Cancer Epidemiol Biomarkers Prev 15(6):1189–1197PubMedCrossRefGoogle Scholar
  12. Han C, McGue MK, Iacono WG (1999) Lifetime tobacco, alcohol and other substance use in adolescent Minnesota twins: univariate and multivariate behavioral genetic analyses. Addiction 94(7):981–993PubMedCrossRefGoogle Scholar
  13. Happonen M, Pulkkinen L, Kaprio J, Van der Meere J, Viken RJ, Rose RJ (2002) The heritability of depressive symptoms: multiple informants and multiple measures. J Child Psychol Psychiatry 43(4):471–479PubMedCrossRefGoogle Scholar
  14. Hayatbakhsh MR, Najman JM, Jamrozik K, Al Mamun A, Bor W, Alati R (2008) Adolescent problem behaviours predicting DSM-IV diagnoses of multiple substance use disorder. Findings of a prospective birth cohort study. Soc Psychiatry Psychiatr Epidemiol 43(5):356–363PubMedCrossRefGoogle Scholar
  15. Hazen E, Schlozman S, Berensin E (2008) Adolescent psychological development: a review. Pediatr Rev 29(5):161–167PubMedCrossRefGoogle Scholar
  16. Hicks BM, Krueger RF, Iacono WG, McGue M, Patrick CJ (2004) Family transmission and heritability of externalizing disorders: a twin-family study. Arch Gen Psychiatry 61(9):922–928PubMedCrossRefGoogle Scholar
  17. Huizink AC, Levälahti E, Korhonen T, Dick DM, Pulkkinen L, Rose RJ, Kaprio J (2010) Tobacco, cannabis, and other illicit drug use among Finnish adolescent twins: causal relationship or correlated liabilities? J Stud Alcohol Drugs 71(1):5–14PubMedGoogle Scholar
  18. Kaprio J (2006) Twin studies in Finland 2006. Twin Res Hum Genet 9(6):772–777PubMedCrossRefGoogle Scholar
  19. Kaprio J, Pulkkinen L, Rose RJ (2002) Genetic and environmental factors in health-related behaviors: studies on Finnish twins and twin families. Twin Res Hum Genet 5(5):366–371Google Scholar
  20. Kendler KS, Jacobson KC, Prescott CA, Neale MC (2003) Specificity of genetic and environmental risk factors for use and abuse/dependence of cannabis, cocaine, hallucinogens, sedatives, stimulants, and opiates in male twins. Am J Psychiatry 160(4):687–695PubMedCrossRefGoogle Scholar
  21. Kendler KS, Myers J, Prescott CA (2007) Specificity of genetic and environmental risk factors for symptoms of cannabis, cocaine, alcohol, caffeine, and nicotine dependence. Arch Gen Psychiatry 64(11):1313–1320PubMedCrossRefGoogle Scholar
  22. King SM, Iacono WG, McGue M (2004) Childhood externalizing and internalizing psychopathology in the prediction of early substance use. Addiction 99(12):1548–1559PubMedCrossRefGoogle Scholar
  23. Kirisci L, Mezzich AC, Reynolds M, Tarter RE, Aytaclar S (2009) Prospective study of the association between neurobehavior disinhibition and peer environment on illegal drug use in boys and girls. Am J Drug Alcohol Abuse 35(3):145–150PubMedCrossRefGoogle Scholar
  24. Koopmans JR, van Doornen LJ, Boomsma DI (1997) Association between alcohol use and smoking in adolescent and young adult twins: a bivariate genetic analysis. Alcohol Clin Exp Res 21(3):537–546PubMedGoogle Scholar
  25. Korhonen T, Huizink AC, Dick DM, Pulkkinen L, Rose RJ, Kaprio J (2008) Role of individual, peer and family factors in the use of cannabis and other illicit drugs: a longitudinal analysis among Finnish adolescent twins. Drug Alcohol Depend 97:33–43PubMedCrossRefGoogle Scholar
  26. Korhonen T, Levalahti E, Dick DM, Pulkkinen L, Rose RJ, Kaprio J, Huizink AC (2010a) Externalizing behaviors and cigarette smoking as predictors for use of illicit drugs: a longitudinal study among Finnish adolescent twins. Twin Res Hum Genet 13(6):550–558PubMedCrossRefGoogle Scholar
  27. Korhonen T, Van Leeuwen AP, Reijneveld SA, Ormel J, Verhulst FC, Huizink AC (2010b) Externalizing behavior problems and cigarette smoking as predictors of cannabis use: the TRAILS study. J Am Acad Adolesc Psychiatry 49(1):61–69Google Scholar
  28. Krueger RF, Hicks BM, Patrick CJ, Carlson SR, Iacono WG, McGue M (2002) Etiologic connections among substance dependence, antisocial behavior, and personality: modeling the externalizing spectrum. J Abnorm Psychol 111(3):411–424PubMedCrossRefGoogle Scholar
  29. Li MD, Cheng R, Ma JZ, Swan GE (2003) A meta-analysis of estimated genetic and environmental effects on smoking behavior in male and female adult twins. Addiction 98:23–31PubMedCrossRefGoogle Scholar
  30. Maes HH, Woodard CE, Murrelle L, Meyer JM, Silberg JL, Hewitt JK, Rutter M, Simonoff E, Pickles A, Carbonneau R, Neale MC, Eaves LJ (1999) Tobacco, alcohol and drug use in eight- to sixteen-year-old twins: the Virginia twin study of adolescent behavioral development. J Stud Alcohol 60(3):293–305PubMedGoogle Scholar
  31. Miles DR, Carey G (1997) Genetic and environmental architecture of human aggression. J Pers Soc Psychol 72(1):207–217PubMedCrossRefGoogle Scholar
  32. Miles DR, van den Bree MBM, Pickens RW (2002) Sex differences in shared genetic and environmental influences between conduct disorder symptoms and marijuana use in adolescents. Am J Med Genet 114(2):159–168PubMedCrossRefGoogle Scholar
  33. Neale MC, Maes HH (2006) Methodology for genetic studies of twins and families. Kluwer Academic Publishers B.V., DordrechtGoogle Scholar
  34. Neale MC, Boker SM, Xie G, Maes HH (2006a) Mx: statistical modeling, 6th edn. Virginia Commonwealth University, RichmondGoogle Scholar
  35. Neale MC, Harvey E, Maes HH, Sullivan PF, Kendler KS (2006b) Extensions to the modeling of initiation and progression: applications to substance use and abuse. Behav Genet 36(4):507–524PubMedCrossRefGoogle Scholar
  36. Neale MC, Roysamb E, Jacobson K (2006c) Multivariate genetic analysis of sex limitation and G × E interaction. Twin Res Hum Genet 9(4):481–489PubMedGoogle Scholar
  37. Pulkkinen L, Kaprio J, Rose RJ (1999) Peers, teachers and parents as assessors of the behavioural and emotional problems of twins and their adjustment: the Multidimensional Peer Nomination Inventory. Twin Res Hum Genet 2(4):274–285Google Scholar
  38. Pulkkinen L, Vaalamo I, Hietala R, Kaprio J, Rose RJ (2003) Peer reports of adaptive behavior in twins and singletons: is twinship a risk or an advantage? Twin Res Hum Genet 6(2):106–118Google Scholar
  39. Rhee SH, Hewitt JK, Young SE, Corley RP, Crowley TJ, Stallings MC (2003) Genetic and environmental influences on substance initiation, use, and problem use in adolescents. Arch Gen Psychiatry 60(12):1256–1264PubMedCrossRefGoogle Scholar
  40. Rimpelä A, Rainio S, Pere L, Lintonen TP (2006) Use of tobacco products, alcohol use and exposure to drugs in 1977–2005. Ministry of Social Affairs and Health, HelsinkiGoogle Scholar
  41. Rose RJ, Broms U, Korhonen T, Dick DM, Kaprio J (2009) Genetics of smoking behavior. In: Kim YK (ed) Handbook of behavior genetics. Springer, New YorkGoogle Scholar
  42. Shelton K, Lifford K, Fowler T, Rice F, Neale M, Harold G, Thapar A, Van Den Bree M (2007) The association between conduct problems and the initiation and progression of marijuana use during adolescence: a genetic analysis across time. Behav Genet 37(2):314–325PubMedCrossRefGoogle Scholar
  43. Spear SP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417–463PubMedCrossRefGoogle Scholar
  44. StataCorp (2005) Stata statistical software. StataCorp, College StationGoogle Scholar
  45. United Nations International Drug Control Programme (1997) World drug report. United Nations Office for Drugs Control and Crime Prevention, New YorkGoogle Scholar
  46. Vaalamo I, Pulkkinen L, Kinnunen T, Kaprio J, Rose RJ (2002) Interactive effects of internalizing and externalizing problem behaviors on recurrent pain in children. J Pediatr Psychol 27(3):245–257PubMedCrossRefGoogle Scholar
  47. Vega WA, Gil AG (2005) Revisiting drug progression: long-range effects of early tobacco use. Addiction 100(9):1358–1369PubMedCrossRefGoogle Scholar
  48. Verweij KJH, Zietsch BP, Lynskey MT, Medland SE, Neale MC, Martin NG et al (2010) Genetic and environmental influences on cannabis use initiation and problematic use: a meta-analysis of twin studies. Addiction 105(3):417–430PubMedCrossRefGoogle Scholar
  49. Vierikko E, Pulkkinen L, Kaprio J, Viken R, Rose RJ (2003) Sex differences in genetic and environmental effects on aggression. Aggress Behav 29:55–68CrossRefGoogle Scholar
  50. Vierikko E, Pulkkinen L, Kaprio J, Rose RJ (2004) Genetic and environmental influences on the relationship between aggression and hyperactivity–impulsivity as rated by teachers and parents. Twin Res Hum Genet 7(3):261–274Google Scholar
  51. Virtanen R, Aromaa M, Koskenvuo M, Sillanpaa M, Pulkkinen L, Metsahonkala L, Suominen S, Rose RJ, Helenius H, Kaprio J (2004) Externalizing problem behaviors and headache: a follow-up study of adolescent Finnish twins. Pediatrics 114(4):981–987PubMedCrossRefGoogle Scholar
  52. White VM, Hopper JL, Wearing AJ, Hill DJ (2003) The role of genes in tobacco smoking during adolescence and young adulthood: a multivariate behaviour genetic investigation. Addiction 98(8):1087–1100PubMedCrossRefGoogle Scholar
  53. Young SE, Rhee SH, Stallings MC, Corley RP, Hewitt JK (2006) Genetic and environmental vulnerabilities underlying adolescent substance use and problem use: general or specific? Behav Genet 36:603–615PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Tellervo Korhonen
    • 1
    • 7
    • 8
  • Antti Latvala
    • 1
    • 7
  • Danielle M. Dick
    • 2
  • Lea Pulkkinen
    • 3
  • Richard J. Rose
    • 4
  • Jaakko Kaprio
    • 1
    • 5
    • 7
  • Anja C. Huizink
    • 6
    • 9
  1. 1.Department of Mental Health and Substance Abuse ServicesNational Institute for Health and WelfareHelsinkiFinland
  2. 2.Department of Psychiatry, Virginia Institute for Psychiatric and Behavioral GeneticsVirginia Commonwealth UniversityRichmondUSA
  3. 3.Department of PsychologyUniversity of JyväskyläJyväskyläFinland
  4. 4.Department of Psychological and Brain SciencesIndiana UniversityBloomingtonUSA
  5. 5.Institute for Molecular MedicineUniversity of HelsinkiHelsinkiFinland
  6. 6.Department of Developmental PsychologyVU University AmsterdamAmsterdamThe Netherlands
  7. 7.Department of Public HealthUniversity of HelsinkiHelsinkiFinland
  8. 8.HelsinkiFinland
  9. 9.Behavioral Science InstituteNijmegenThe Netherlands

Personalised recommendations