Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T08:49:47.697Z Has data issue: false hasContentIssue false

Alcohol consumption in men is influenced by qualitatively different genetic factors in adolescence and adulthood

Published online by Cambridge University Press:  02 January 2013

A. C. Edwards*
Affiliation:
Virginia Institute for Psychiatric and Behavioral Genetics, Department of Psychiatry, Virginia Commonwealth University, Richmond, VA, USA
K. S. Kendler
Affiliation:
Virginia Institute for Psychiatric and Behavioral Genetics, Department of Psychiatry, Virginia Commonwealth University, Richmond, VA, USA
*
*Address for correspondence: A. C. Edwards, Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Department of Psychiatry, PO Box 980126, Richmond, VA 23298-0126, USA. (Email: [email protected])

Abstract

Background

Alcohol consumption is influenced by genetic factors. Previous studies have examined the heritability of alcohol consumption, or related phenotypes, from adolescence into adulthood, frequently finding that total heritability changes over time. However, it remains unclear whether the same genes underlie liability to alcohol consumption across development versus whether novel risk genes become important over time.

Method

A population-based study of adult male twins (n=1790) born in Virginia, USA, retrospectively reported on their average monthly alcohol consumption from early adolescence through adulthood. We used twin modeling methods to explore genetic and environmental influences on alcohol consumption over time.

Results

One latent genetic factor accounted for the majority of the heritability in alcohol consumption during mid- to late adolescence, but its influence declined thereafter; from young adulthood forward, heritability was largely attributable to a second genetic factor. The total heritability of alcohol consumption increased from 0 at ages 12–14 years to 0.40 by ages 18–21 years. Shared environmental factors declined in influence over time.

Conclusions

The heritability of alcohol consumption over time is dynamic both quantitatively and qualitatively. These results have important implications for gene identification endeavors. Furthermore, these findings could inform efforts to elucidate developmentally dynamic behaviors, such as antisocial behavior.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agrawal, A, Wetherill, L, Bucholz, KK, Kramer, J, Kuperman, S, Lynskey, MT, Nurnberger, JI Jr., Schuckit, M, Tischfield, JA, Edenberg, HJ, Foroud, T, Bierut, LJ (2012). Genetic influences on craving for alcohol. Addictive Behavior. Published online 19 March 2012. doi:10.1016/j.addbeh.2012.03.021.Google ScholarPubMed
Akaike, H (1987). Factor analysis and AIC. Psychometrika 52, 317332.CrossRefGoogle Scholar
Baik, I, Cho, NH, Kim, SH, Han, BG, Shin, C (2011). Genome-wide association studies identify genetic loci related to alcohol consumption in Korean men. American Journal of Clinical Nutrition 93, 809816.CrossRefGoogle ScholarPubMed
Bergen, SE, Gardner, CO, Kendler, KS (2007). Age-related changes in heritability of behavioral phenotypes over adolescence and young adulthood: a meta-analysis. Twin Research and Human Genetics 10, 423433.CrossRefGoogle Scholar
Bierut, LJ, Agrawal, A, Bucholz, KK, Doheny, KF, Laurie, C, Pugh, E, Fisher, S, Fox, L, Howells, W, Bertelsen, S, Hinrichs, AL, Almasy, L, Breslau, N, Culverhouse, RC, Dick, DM, Edenberg, HJ, Foroud, T, Grucza, RA, Hatsukami, D, Hesselbrock, V, Johnson, EO, Kramer, J, Krueger, RF, Kuperman, S, Lynskey, M, Mann, K, Neuman, RJ, Nothen, MM, Nurnberger, JI Jr., Porjesz, B, Ridinger, M, Saccone, NL, Saccone, SF, Schuckit, MA, Tischfield, JA, Wang, JC, Rietschel, M, Goate, AM, Rice, JP (2010). A genome-wide association study of alcohol dependence. Proceedings of the National Academy of Sciences of the United States of America 107, 50825087.CrossRefGoogle ScholarPubMed
Boekeloo, BO, Novik, MG (2011). Clinical approaches to improving alcohol education and counseling in adolescents and young adults. Adolescent Medicine: State of the Art Reviews 22, 631648, xiv.Google ScholarPubMed
Boker, S, Neale, M, Maes, H, Wilde, M, Spiegel, M, Brick, T, Spies, J, Estabrook, R, Kenny, S, Bates, T, Mehta, P, Fox, J (2011). OpenMx: an open source extended structural equation modeling framework. Psychometrika 76, 306317.CrossRefGoogle ScholarPubMed
Bouchery, EE, Harwood, HJ, Sacks, JJ, Simon, CJ, Brewer, RD (2011). Economic costs of excessive alcohol consumption in the U.S., 2006. American Journal of Preventative Medicine 41, 516524.CrossRefGoogle ScholarPubMed
Button, TM, Rhee, SH, Hewitt, JK, Young, SE, Corley, RP, Stallings, MC (2007). The role of conduct disorder in explaining the comorbidity between alcohol and illicit drug dependence in adolescence. Drug and Alcohol Dependence 87, 4653.CrossRefGoogle ScholarPubMed
Chen, CM, Dufour, MC, Yi, H (2004). Alcohol consumption among young adults ages 18–24 in the United States: results from the 2001–2002 NESARC survey. Alcohol Research and Health 28, 269280.Google Scholar
Dawson, DA (1994). Consumption indicators of alcohol dependence. Addiction 89, 345350.CrossRefGoogle ScholarPubMed
Dawson, DA, Grant, BF, Li, TK (2005). Quantifying the risks associated with exceeding recommended drinking limits. Alcoholism, Clinical and Experimental Research 29, 902908.CrossRefGoogle ScholarPubMed
Dhalla, S, Kopec, JA (2007). The CAGE questionnaire for alcohol misuse: a review of reliability and validity studies. Clinical and Investigative Medicine 30, 3341.CrossRefGoogle ScholarPubMed
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. Alcoholism, Clinical and Experimental Research 35, 21522161.CrossRefGoogle ScholarPubMed
Edenberg, HJ, Koller, DL, Xuei, X, Wetherill, L, McClintick, JN, Almasy, L, Bierut, LJ, Bucholz, KK, Goate, A, Aliev, F, Dick, D, Hesselbrock, V, Hinrichs, A, Kramer, J, Kuperman, S, Nurnberger, JI Jr., Rice, JP, Schuckit, MA, Taylor, R, Todd Webb, B, Tischfield, JA, Porjesz, B, Foroud, T (2010). Genome-wide association study of alcohol dependence implicates a region on chromosome 11. Alcoholism, Clinical and Experimental Research 34, 840852.CrossRefGoogle ScholarPubMed
Edwards, AC, Larsson, H, Lichtenstein, P, Kendler, KS (2011 a). Early environmental influences contribute to covariation between internalizing symptoms and alcohol intoxication frequency across adolescence. Addictive Behaviors 36, 175182.CrossRefGoogle ScholarPubMed
Edwards, AC, Sihvola, E, Korhonen, T, Pulkkinen, L, Moilanen, I, Kaprio, J, Rose, RJ, Dick, DM (2011 b). Depressive symptoms and alcohol use are genetically and environmentally correlated across adolescence. Behavior Genetics 41, 476487.CrossRefGoogle ScholarPubMed
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, 413422.CrossRefGoogle ScholarPubMed
Frank, J, Cichon, S, Treutlein, J, Ridinger, M, Mattheisen, M, Hoffmann, P, Herms, S, Wodarz, N, Soyka, M, Zill, P, Maier, W, Mossner, R, Gaebel, W, Dahmen, N, Scherbaum, N, Schmal, C, Steffens, M, Lucae, S, Ising, M, Muller-Myhsok, B, Nothen, MM, Mann, K, Kiefer, F, Rietschel, M (2012). Genome-wide significant association between alcohol dependence and a variant in the ADH gene cluster. Addiction Biology 17, 171180.CrossRefGoogle Scholar
Freedman, D, Thornton, A, Camburn, D, Alwin, D, Young-demarco, L (1988). The life history calendar: a technique for collecting retrospective data. Sociological Methodology 18, 3768.CrossRefGoogle Scholar
Geels, LM, Bartels, M, van Beijsterveldt, TC, Willemsen, G, van der Aa, N, Boomsma, DI, Vink, JM (2012). Trends in adolescent alcohol use: effects of age, sex and cohort on prevalence and heritability. Addiction 107, 518527.CrossRefGoogle ScholarPubMed
Giacosa, A, Adam-Blondon, AF, Baer-Sinnott, S, Barale, R, Bavaresco, L, Di Gaspero, G, Dugo, L, Ellison, RC, Gerbi, V, Gifford, D, Janssens, J, La Vecchia, C, Negri, E, Pezzotti, M, Santi, L, Santi, L, Rondanelli, M (2012). Alcohol and wine in relation to cancer and other diseases. European Journal of Cancer Prevention 21, 103108.CrossRefGoogle ScholarPubMed
Grant, JD, Agrawal, A, Bucholz, KK, Madden, PA, Pergadia, ML, Nelson, EC, Lynskey, MT, Todd, RD, Todorov, AA, Hansell, NK, Whitfield, JB, Martin, NG, Heath, AC (2009). Alcohol consumption indices of genetic risk for alcohol dependence. Biological Psychiatry 66, 795800.CrossRefGoogle ScholarPubMed
Hansell, NK, Agrawal, A, Whitfield, JB, Morley, KI, Gordon, SD, Lind, PA, Pergadia, ML, Montgomery, GW, Madden, PA, Todd, RD, Heath, AC, Martin, NG (2009). Can we identify genes for alcohol consumption in samples ascertained for heterogeneous purposes? Alcoholism, Clinical and Experimental Research 33, 729739.CrossRefGoogle ScholarPubMed
Heath, AC, Whitfield, JB, Martin, NG, Pergadia, ML, Goate, AM, Lind, PA, McEvoy, BP, Schrage, AJ, Grant, JD, Chou, YL, Zhu, R, Henders, AK, Medland, SE, Gordon, SD, Nelson, EC, Agrawal, A, Nyholt, DR, Bucholz, KK, Madden, PA, Montgomery, GW (2011). A quantitative-trait genome-wide association study of alcoholism risk in the community: findings and implications. Biological Psychiatry 70, 513518.CrossRefGoogle ScholarPubMed
Hicks, BM, Blonigen, DM, Kramer, MD, Krueger, RF, Patrick, CJ, Iacono, WG, McGue, M (2007). Gender differences and developmental change in externalizing disorders from late adolescence to early adulthood: a longitudinal twin study. Journal of Abnormal Psychology 116, 433447.CrossRefGoogle ScholarPubMed
Johnston, LD, O'Malley, PM, Bachman, JG, Schulenberg, JE (2011). Marijuana use continues to rise among U.S. teens, while alcohol use hits historic lows. University of Michigan News Service: Ann Arbor, MI.Google Scholar
Kendler, KS, Gardner, C, Dick, DM (2011 a). Predicting alcohol consumption in adolescence from alcohol-specific and general externalizing genetic risk factors, key environmental exposures and their interaction. Psychological Medicine 41, 15071516.CrossRefGoogle ScholarPubMed
Kendler, KS, Jacobson, K, Myers, JM, Eaves, LJ (2008 a). A genetically informative developmental study of the relationship between conduct disorder and peer deviance in males. Psychological Medicine 38, 10011011.CrossRefGoogle ScholarPubMed
Kendler, KS, Kalsi, G, Holmans, PA, Sanders, AR, Aggen, SH, Dick, DM, Aliev, F, Shi, J, Levinson, DF, Gejman, PV (2011 b). Genomewide association analysis of symptoms of alcohol dependence in the molecular genetics of schizophrenia (MGS2) control sample. Alcoholism, Clinical and Experimental Research 35, 963975.CrossRefGoogle ScholarPubMed
Kendler, KS, Myers, J, Dick, D, Prescott, CA (2010). The relationship between genetic influences on alcohol dependence and on patterns of alcohol consumption. Alcoholism, Clinical and Experimental Research 34, 10581065.CrossRefGoogle ScholarPubMed
Kendler, KS, Prescott, CA (2006). Genes, Environment, and Psychopathology. The Guilford Press: Boston, MA.Google Scholar
Kendler, KS, Schmitt, E, Aggen, SH, Prescott, CA (2008 b). Genetic and environmental influences on alcohol, caffeine, cannabis, and nicotine use from early adolescence to middle adulthood. Archives of General Psychiatry 65, 674682.CrossRefGoogle ScholarPubMed
Knopik, VS, Heath, AC, Bucholz, KK, Madden, PA, Waldron, M (2009). Genetic and environmental influences on externalizing behavior and alcohol problems in adolescence: a female twin study. Pharmacology, Biochemistry and Behavior 93, 313321.CrossRefGoogle ScholarPubMed
Legrand, LN, Keyes, M, McGue, M, Iacono, WG, Krueger, RF (2008). Rural environments reduce the genetic influence on adolescent substance use and rule-breaking behavior. Psychological Medicine 38, 13411350.CrossRefGoogle ScholarPubMed
Lind, PA, Macgregor, S, Vink, JM, Pergadia, ML, Hansell, NK, de Moor, MH, Smit, AB, Hottenga, JJ, Richter, MM, Heath, AC, Martin, NG, Willemsen, G, de Geus, EJ, Vogelzangs, N, Penninx, BW, Whitfield, JB, Montgomery, GW, Boomsma, DI, Madden, PA (2010). A genomewide association study of nicotine and alcohol dependence in Australian and Dutch populations. Twin Research and Human Genetics 13, 1029.CrossRefGoogle ScholarPubMed
Malone, SM, Taylor, J, Marmorstein, NR, McGue, M, Iacono, WG (2004). Genetic and environmental influences on antisocial behavior and alcohol dependence from adolescence to early adulthood. Developmental Psychopathology 16, 943966.CrossRefGoogle ScholarPubMed
McCambridge, J, McAlaney, J, Rowe, R (2011). Adult consequences of late adolescent alcohol consumption: a systematic review of cohort studies. PLoS Medicine 8, e1000413.CrossRefGoogle ScholarPubMed
Moffitt, TE (1993). Adolescence-limited and life-course-persistent antisocial behavior: a developmental taxonomy. Psychological Review 100, 674701.CrossRefGoogle ScholarPubMed
Nigg, JT, Glass, JM, Wong, MM, Poon, E, Jester, JM, Fitzgerald, HE, Puttler, LI, Adams, KM, Zucker, RA (2004). Neuropsychological executive functioning in children at elevated risk for alcoholism: findings in early adolescence. Journal of Abnormal Psychology 113, 302314.CrossRefGoogle ScholarPubMed
Nigg, JT, Wong, MM, Martel, MM, Jester, JM, Puttler, LI, Glass, JM, Adams, KM, Fitzgerald, HE, Zucker, RA (2006). Poor response inhibition as a predictor of problem drinking and illicit drug use in adolescents at risk for alcoholism and other substance use disorders. Journal of the American Academy of Child and Adolescent Psychiatry 45, 468475.CrossRefGoogle ScholarPubMed
Pagan, JL, Rose, RJ, Viken, RJ, Pulkkinen, L, Kaprio, J, Dick, DM (2006). Genetic and environmental influences on stages of alcohol use across adolescence and into young adulthood. Behavior Genetics 36, 483497.CrossRefGoogle ScholarPubMed
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. Archives of General Psychiatry 60, 12561264.CrossRefGoogle ScholarPubMed
Rose, RJ, Dick, DM, Viken, RJ, Pulkkinen, L, Kaprio, J (2004). Genetic and environmental effects on conduct disorder and alcohol dependence symptoms and their covariation at age 14. Alcoholism, Clinical and Experimental Research 28, 15411548.CrossRefGoogle ScholarPubMed
Sartor, CE, Xian, H, Scherrer, JF, Lynskey, MT, Duncan, AE, Haber, JR, Grant, JD, Bucholz, KK, Jacob, T (2008). Psychiatric and familial predictors of transition times between smoking stages: results from an offspring-of-twins study. Addictive Behaviors 33, 235251.CrossRefGoogle ScholarPubMed
Schumann, G, Coin, LJ, Lourdusamy, A, Charoen, P, Berger, KH, Stacey, D, Desrivieres, S, Aliev, FA, Khan, AA, Amin, N, Aulchenko, YS, Bakalkin, G, Bakker, SJ, Balkau, B, Beulens, JW, Bilbao, A, de Boer, RA, Beury, D, Bots, ML, Breetvelt, EJ, Cauchi, S, Cavalcanti-Proenca, C, Chambers, JC, Clarke, TK, Dahmen, N, de Geus, EJ, Dick, D, Ducci, F, Easton, A, Edenberg, HJ, Esko, T, Fernandez-Medarde, A, Foroud, T, Freimer, NB, Girault, JA, Grobbee, DE, Guarrera, S, Gudbjartsson, DF, Hartikainen, AL, Heath, AC, Hesselbrock, V, Hofman, A, Hottenga, JJ, Isohanni, MK, Kaprio, J, Khaw, KT, Kuehnel, B, Laitinen, J, Lobbens, S, Luan, J, Mangino, M, Maroteaux, M, Matullo, G, McCarthy, MI, Mueller, C, Navis, G, Numans, ME, Nunez, A, Nyholt, DR, Onland-Moret, CN, Oostra, BA, O'Reilly, PF, Palkovits, M, Penninx, BW, Polidoro, S, Pouta, A, Prokopenko, I, Ricceri, F, Santos, E, Smit, JH, Soranzo, N, Song, K, Sovio, U, Stumvoll, M, Surakk, I, Thorgeirsson, TE, Thorsteinsdottir, U, Troakes, C, Tyrfingsson, T, Tonjes, A, Uiterwaal, CS, Uitterlinden, AG, van der Harst, P, van der Schouw, YT, Staehlin, O, Vogelzangs, N, Vollenweider, P, Waeber, G, Wareham, NJ, Waterworth, DM, Whitfield, JB, Wichmann, EH, Willemsen, G, Witteman, JC, Yuan, X, Zhai, G, Zhao, JH, Zhang, W, Martin, NG, Metspalu, A, Doering, A, Scott, J, Spector, TD, Loos, RJ, Boomsma, DI, Mooser, V, Peltonen, L, Stefansson, K, van Duijn, CM, Vineis, P, Sommer, WH, Kooner, JS, Spanagel, R, Heberlein, UA, Jarvelin, MR, Elliott, P (2011). Genome-wide association and genetic functional studies identify autism susceptibility candidate 2 gene (AUTS2) in the regulation of alcohol consumption. Proceedings of the National Academy of Sciences of the United States of America 108, 71197124.CrossRefGoogle ScholarPubMed
Treutlein, J, Cichon, S, Ridinger, M, Wodarz, N, Soyka, M, Zill, P, Maier, W, Moessner, R, Gaebel, W, Dahmen, N, Fehr, C, Scherbaum, N, Steffens, M, Ludwig, KU, Frank, J, Wichmann, HE, Schreiber, S, Dragano, N, Sommer, WH, Leonardi-Essmann, F, Lourdusamy, A, Gebicke-Haerter, P, Wienker, TF, Sullivan, PF, Nothen, MM, Kiefer, F, Spanagel, R, Mann, K, Rietschel, M (2009). Genome-wide association study of alcohol dependence. Archives of General Psychiatry 66, 773784.CrossRefGoogle ScholarPubMed
Tuvblad, C, Narusyte, J, Grann, M, Sarnecki, J, Lichtenstein, P (2011). The genetic and environmental etiology of antisocial behavior from childhood to emerging adulthood. Behavior Genetics 41, 629640.CrossRefGoogle ScholarPubMed
van Beek, JH, Kendler, KS, de Moor, MH, Geels, LM, Bartels, M, Vink, JM, van den Berg, SM, Willemsen, G, Boomsma, DI (2012). Stable genetic effects on symptoms of alcohol abuse and dependence from adolescence into early adulthood. Behavior Genetics 42, 4056.CrossRefGoogle ScholarPubMed
Viken, RJ, Kaprio, J, Koskenvuo, M, Rose, RJ (1999). Longitudinal analyses of the determinants of drinking and of drinking to intoxication in adolescent twins. Behavior Genetics 29, 455461.CrossRefGoogle ScholarPubMed
Wang, KS, Liu, X, Zhang, Q, Wu, LY, Zeng, M (2012). Genome-wide association study identifies 5q21 and 9p24.1 (KDM4C) loci associated with alcohol withdrawal symptoms. Journal of Neural Transmission 119, 425433.CrossRefGoogle ScholarPubMed
Whitfield, JB, Zhu, G, Madden, PA, Neale, MC, Heath, AC, Martin, NG (2004). The genetics of alcohol intake and of alcohol dependence. Alcoholism, Clinical and Experimental Research 28, 11531160.CrossRefGoogle ScholarPubMed
Zuo, L, Gelernter, J, Zhang, CK, Zhao, H, Lu, L, Kranzler, HR, Malison, RT, Li, CS, Wang, F, Zhang, XY, Deng, HW, Krystal, JH, Zhang, F, Luo, X (2012). Genome-wide association study of alcohol dependence implicates KIAA0040 on chromosome 1q. Neuropsychopharmacology 37, 557566.CrossRefGoogle ScholarPubMed
Zuo, L, Zhang, CK, Wang, F, Li, CS, Zhao, H, Lu, L, Zhang, XY, Lu, L, Zhang, H, Zhang, F, Krystal, JH, Luo, X (2011). A novel, functional and replicable risk gene region for alcohol dependence identified by genome-wide association study. PLoS One 6, e26726.CrossRefGoogle ScholarPubMed