Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T06:23:15.799Z Has data issue: false hasContentIssue false
  • English
  • Français

Monoamine oxidase A and childhood adversity as risk factors for conduct disorder in females

Published online by Cambridge University Press:  28 August 2008

E. C. Prom-Wormley ,
L. J. Eaves ,
D. L. Foley ,
C. O. Gardner ,
K. J. Archer ,
B. K. Wormley ,
H. H. Maes ,
B. P. Riley  and
J. L. Silberg
E. C. Prom-Wormley*
Affiliation:
Department of Integrative Life Sciences, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA
L. J. Eaves
Affiliation:
Department of Human Genetics, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA
D. L. Foley
Affiliation:
Orygen Youth Health Research Centre, University of Melbourne, Australia Department of Psychiatry, University of Melbourne, Australia
C. O. Gardner
Affiliation:
Department of Psychiatry, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA
K. J. Archer
Affiliation:
Virginia Institute for Biostatistics, Virginia Commonwealth University, USA
B. K. Wormley
Affiliation:
Department of Psychiatry, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA
H. H. Maes
Affiliation:
Department of Human Genetics, Virginia Commonwealth University, USA Department of Psychiatry, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA Massey Cancer Center of Virginia Commonwealth University, USA
B. P. Riley
Affiliation:
Department of Human Genetics, Virginia Commonwealth University, USA Department of Psychiatry, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA
J. L. Silberg
Affiliation:
Department of Human Genetics, Virginia Commonwealth University, USA Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, USA
*
*Address for correspondence: Dr E. C. Prom-Wormley, Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, PO Box 980126, Richmond, VA 23298-0126, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Recent studies among males have reported a genotype–environment interaction (G×E) in which low-activity alleles at the monoamine oxidase A (MAOA) locus conferred greater sensitivity to the effects of childhood adversity on risk for conduct disorder (CD). So far, few studies of females have controlled for gene–environment correlation or used females heterozygous for this X-linked gene.

Method

Logistic regression analysis of a sample of 721 females ages 8–17 years from the longitudinal Virginia Twin Study of Adolescent Behavioral Development (VTSABD) assessed the additive effects of MAOA genotypes on risk for CD, together with the main effect of childhood adversity and parental antisocial personality disorder (ASP), as well as the interaction of MAOA with childhood adversity on risk for CD.

Results

A significant main effect of genotype on risk for CD was detected, where low-activity MAOA imparted the greatest risk to CD in girls while controlling for the significant effects of maternal ASP and childhood adversity. Significant G×E with weak effect was detected when environmental exposure was untransformed, indicating a higher sensitivity to childhood adversity in the presence of the high-activity MAOA allele. The interaction was no longer statistically significant after applying a ridit transformation to reflect the sample sizes exposed at each level of childhood adversity.

Conclusions

The main effect of MAOA on risk for CD in females, its absence in males and directional difference of interaction is suggestive of genotype–sex interaction. As the effect of G×E on risk for CD was weak, its inclusion is not justified.

Keywords

Childhood adversityconduct disordergender differencesgene–environment interactionMAOA
Type
Original Articles
Information
Psychological Medicine , Volume 39 , Issue 4 , April 2009 , pp. 579 - 590
Copyright
Copyright © 2008 Cambridge University Press

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

Angold, A, Costello, EJ (2000). The Child and Adolescent Psychiatric Assessment (CAPA). Journal of the American Academy of Child and Adolescent Psychiatry 39, 39–48.CrossRefGoogle ScholarPubMed
APA (1987). Diagnostic and Statistical Manual of Mental Disorders, 3rd edn. American Psychiatric Association: Washington, DC.Google Scholar
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association: Washington, DC.Google Scholar
Bassarath, L (2001). Conduct disorder: a biopsychosocial review. Canadian Journal of Psychiatry 46, 609–616.CrossRefGoogle ScholarPubMed
Becker, KB, McCloskey, LA (2002). Attention and conduct problems in children exposed to family violence. American Journal of Orthopsychiatry 72, 83–91.CrossRefGoogle ScholarPubMed
Benjamin, D, Van Bakel, I, Craig, IW (2000). A novel expression based approach for assessing the inactivation status of human X-linked genes. European Journal of Human Genetics 8, 103–108.CrossRefGoogle ScholarPubMed
Bross, IDJ (1958). How to use ridit analysis. Biometrics 14, 18–38.CrossRefGoogle Scholar
Brunner, HG, Nelen, M, Breakefield, XO, Ropers, HH, van Oost, BA (1993). Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262, 578–580.CrossRefGoogle ScholarPubMed
Burgess, DL, Conger, RD (1978). Family interaction in abusive, neglectful and normal families. Child Development 49, 1163–1173.CrossRefGoogle ScholarPubMed
Button, TMM, Scourfield, J, Martin, N, Purcell, S, McGuffin, P (2005). Family dysfunction interacts with genes in the causation of antisocial symptoms. Behavior Genetics 35, 115–120.CrossRefGoogle ScholarPubMed
Cadoret, RJ, Cain, C (1980). Sex differences in predictors of antisocial behavior in adoptees. Archives of General Psychiatry 37, 1171–1175.CrossRefGoogle ScholarPubMed
Cadoret, RJ, Yates, WR, Troughton, E, Woodworth, G, Stewart, MA (1995). Genetic–environmental interaction in the genesis of aggressivity and conduct disorders. Archives of General Psychiatry 52, 916–924.CrossRefGoogle ScholarPubMed
Carrel, L, Willard, HF (2005). X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434, 400–404.CrossRefGoogle ScholarPubMed
Cases, O, Seif, I, Grimsby, J, Gaspar, P, Chen, K, Puournin, S, Müeller, U, Aguet, M, Babinet, C, Chen Shih, J, De Maeyer, E (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268, 1763–1766.CrossRefGoogle ScholarPubMed
Caspi, A, McClay, J, Moffitt, TE, Mill, J, Martin, J, Craig, IW, Taylor, A, Poulton, R (2002). Role of genotype in the cycle of violence in maltreated children. Science 297, 851–854.CrossRefGoogle ScholarPubMed
Craig, IW (2005). The role of monoamine oxidase A, MAOA, in the aetiology of antisocial behaviour: the importance of gene–environment interactions. Novartis Foundation Symposium 268, 227–237; discussion 237–253.CrossRefGoogle ScholarPubMed
Dodge, KA (1986). A social-information processing model of social competence in children. In Minnesota Symposium in Child Psychology, vol. 18 (ed. Perlmutter, M.), pp. 77–125. Erlbaum: Hillsdale, NJ.Google Scholar
Eaves, L, Erkanli, A, Silberg, J, Angold, A, Maes, H, Foley, DL (2005). Application of Baysian inference using Gibbs sampling to item-response theory modeling of multi-symptom genetic data. Behavior Genetics 35, 765–780.CrossRefGoogle Scholar
Eaves, LJ (2006). Genotype×environment interaction in psychopathology: fact or artifact? Twin Research and Human Genetics 9, 1–8.CrossRefGoogle ScholarPubMed
Eaves, LJ, Silberg, JL, Meyer, JM, Maes, HH, Simonoff, E, Pickles, A, Rutter, M, Neale, MC, Reynolds, CA, Erikson, MT, Heath, AC, Loeber, R, Truett, KR, Hewitt, JK (1997). Genetics and developmental psychopathology: 2. The main effects of genes and environment on behavioral problems in the Virginia Twin Study of Adolescent Behavioral Development. Journal of Child Psychology and Psychiatry 38, 965–980.CrossRefGoogle ScholarPubMed
Ehrensaft, MK (2005). Interpersonal relationships and sex differences in the development of conduct problems. Clinical Child and Family Psychology Review 8, 39–63.CrossRefGoogle ScholarPubMed
Eley, TC, Lichtenstein, P, Stevenson, J (1999). Sex differences in the etiology of aggressive and non-aggressive antisocial behavior: results from two twin studies. Child Development 70, 155–168.CrossRefGoogle Scholar
Falconer, DS, Mackay, TFC (1996). Introduction to Quantitative Genetics, 4th edn. Longan: New York.Google Scholar
Farrington, DP, Loeber, R (2000). Epidemiology of juvenile violence. Child and Adolescent Psychiatric Clinics of North America 9, 733–748.CrossRefGoogle ScholarPubMed
Fergusson, DM, Horwood, LJ (1998). Exposure to interparental violence in childhood and psychosocial adjustment in young adulthood. Child Abuse and Neglect 22, 339–357.CrossRefGoogle ScholarPubMed
Fisher, RA (1918). The correlation between relatives on the supposition of Mendelian inheritance. Transactions of the Royal Society of Edinburgh 52, 399–433.CrossRefGoogle Scholar
Fisher, RA, Immer, FR, Tedin, O (1932). The genetical interpretation of statistics of the third degree in the study of quantitative inheritance. Genetics 17, 107–124.CrossRefGoogle Scholar
Foley, DL, Eaves, LJ, Wormley, B, Silberg, JL, Maes, HH, Kuhn, J, Riley, B (2004). Childhood adversity, monoamine oxidase A genotype, and risk for conduct disorder. Archives of General Psychiatry 61, 738–744.CrossRefGoogle ScholarPubMed
Fraga, MF, Ballestar, E, Paz, MF, Ropero, S, Setien, F, Ballestar, ML, Heine-Suner, D, Cigudosa, JC, Urioste, M, Benitez, J, Boix-Chornet, M, Sanchez-Aguilera, A, Ling, C, Carlsson, E, Poulsen, P, Vaag, A, Stephan, Z, Spector, TD, Wu, YZ, Plass, C, Esteller, M (2005). Epigenetic differences arise during the lifetime of monozygotic twins. Proceedings of the National Academy of Sciences USA 102, 10604–10609.CrossRefGoogle ScholarPubMed
Ge, X, Conger, RD, Cadoret, RJ, Neiderhiser, JM, Yates, WR, Troughton, E, Stewart, MA (1996). The developmental interface between nature and nurture: a mutual influence model of child antisocial behavior and parent behaviors. Developmental Psychology 32, 574–589.CrossRefGoogle Scholar
Gelhorn, HL, Stallings, MC, Young, SE, Corley, RP, Rhee, SH, Hewitt, JK (2005). Genetic and environmental influences on conduct disorder: symptom, domain and full-scale analyses. Journal of Child Psychology and Psychiatry 46, 580–591.CrossRefGoogle ScholarPubMed
Gottfredson, M, Hirschi, T (1990). A General Theory of Crime. Stanford University Press: Stanford, CA.CrossRefGoogle Scholar
Graham, P, Stevenson, J (1985). A twin study of genetic influences on behavioral deviance. Journal of the American Academy of Child Psychiatry 24, 33–41.CrossRefGoogle ScholarPubMed
Haberstick, BC, Lessem, JM, Hopfer, CJ, Smolen, A, Ehringer, MA, Timberlake, D, Hewitt, J (2005). Monoamine oxidase A (MAOA) and antisocial behaviors in the presence of childhood and adolescent maltreatment. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 135, 59–64.CrossRefGoogle Scholar
Herrera, VM, McCloskey, LA (2001). Gender differences in the risk for delinquency among youth exposed to family violence. Child Abuse and Neglect 25, 1037–1051.CrossRefGoogle ScholarPubMed
Hewitt, JK, Silberg, JL, Rutter, M, Simonoff, E, Meyer, JM, Maes, H, Pickles, A, Neale, MC, Loeber, R, Erickson, MT, Kendler, KS, Heath, AC, Truett, KR, Reynolds, CA, Eaves, LJ (1997). Genetics and developmental psychopathology: 1. Phenotypic assessment in the Virginia Twin Study of Adolescent Behavioral Development. Journal of Child Psychology and Psychiatry 38, 943–963.CrossRefGoogle ScholarPubMed
Hudziak, JJ, van Beijsterveldt, CE, Bartels, M, Rietveld, MJ, Rettew, DC, Derks, EM, Boomsma, DI (2003). Individual differences in aggression: genetic analyses by age, gender, and informant in 3-, 7-, and 10-year-old Dutch twins. Behavior Genetics 33, 575–589.CrossRefGoogle ScholarPubMed
Ilomaki, E, Viilo, K, Hakko, H, Marttunen, M, Makikyro, T, Rasanen, P (2006). Familial risks, conduct disorder and violence: a Finnish study of 278 adolescent boys and girls. European Journal of Child and Adolescent Psychiatry 15, 46–51.CrossRefGoogle ScholarPubMed
Jacobson, KC, Prescott, CA, Kendler, KS (2002). Sex differences in the genetic and environmental influences on the development of antisocial behavior. Development and Psychopathology 14, 395–416.CrossRefGoogle ScholarPubMed
Jaffee, SR, Caspi, A, Moffitt, TE, Dodge, KA, Rutter, M, Taylor, A, Tully, LA (2005). Nature×nurture: genetic vulnerabilities interact with physical maltreatment to promote conduct problems. Development and Psychopathology 17, 67–84.CrossRefGoogle Scholar
Kim-Cohen, J, Caspi, A, Taylor, A, Williams, B, Newcombe, R, Craig, IW, Moffitt, TE (2006). MAOA, maltreatment, and gene–environment interaction predicting children's mental health: new evidence and a meta-analysis. Molecular Psychiatry 11, 903–913.CrossRefGoogle ScholarPubMed
Kinsfogel, KM, Grych, JH (2004). Interparental conflict and adolescent dating relationships: integrating cognitive, emotional, and peer influences. Journal of Family Psychology 18, 505–515.CrossRefGoogle ScholarPubMed
Langbehn, DR, Cadoret, RJ, Yates, WR, Troughton, EP, Stewart, MA (1998). Distinct contributions of conduct and oppositional defiant symptoms to adult antisocial behavior: evidence from an adoption study. Archives of General Psychiatry 55, 821–829.CrossRefGoogle ScholarPubMed
Loeber, R, Burke, JD, Lahey, BB, Winters, A, Zera, M (2000). Oppositional defiant and conduct disorder: a review of the past 10 years, part I. Journal of the American Academy of Child and Adolescent Psychiatry 39, 1468–1484.CrossRefGoogle ScholarPubMed
Lyons, MJ, True, WR, Eisen, SA, Goldberg, J, Meyer, J, Faraone, SV, Eaves, LJ, Tsuang, MT (1995). Differential heritability of adult and juvenile antisocial traits. Archives of General Psychiatry 52, 906–915.CrossRefGoogle ScholarPubMed
Maes, H, Silberg, J, Neale, MC, Eaves, LJ (2007). Genetic and cultural transmission of antisocial behavior: an extended twin parent model. Twin Research and Human Genetics 10, 136–150.CrossRefGoogle ScholarPubMed
Mather, K, Jinks, JL (1982). Biometrical Genetics. Chapman & Hall: London.CrossRefGoogle Scholar
Maughan, B, Rowe, R, Messer, J, Goodman, R, Meltzer, H (2004). Conduct disorder and oppositional defiant disorder in a national sample: developmental epidemiology. Journal of Child Psychology and Psychiatry 45, 609–621.CrossRefGoogle Scholar
McCabe, KM, Lansing, AE, Garland, A, Hough, R (2002). Gender differences in psychopathology, functional impairment, and familial risk factors among adjudicated delinquents. Journal of the American Academy of Child and Adolescent Psychiatry 41, 860–867.CrossRefGoogle ScholarPubMed
Meyer, JM, Rutter, M, Silberg, JL, Maes, HH, Simonoff, E, Shillady, LL, Pickles, A, Hewitt, JK, Eaves, LJ (2000). Familial aggregation for conduct disorder symptomatology: the role of genes, marital discord and family adaptability. Psychological Medicine 30, 759–774.CrossRefGoogle ScholarPubMed
Meyer, JM, Silberg, JL, Simonoff, E, Kendler, KS, Hewitt, JK (1996). The Virginia Twin-Family Study of Adolescent Behavioral Development: assessing sample biases in demographic correlates of psychopathology. Psychological Medicine 26, 1119–1133.CrossRefGoogle ScholarPubMed
Meyer-Lindenberg, A, Buckholtz, JW, Kolachana, B, Hariri, AR, Pezawas, L, Blasi, G, Wabnitz, A, Honea, R, Verchiniski, B, Callicott, JH, Egan, M, Mattay, V, Weinberger, DR (2006). Neural mechanisms of genetic risk for impulsivity and violence in humans. Proceedings of the National Academy of Sciences USA 103, 6269–6274.CrossRefGoogle ScholarPubMed
Moffitt, TE, Caspi, A, Rutter, M, Silva, PA (2001 a). Sex Differences in Antisocial Behavior. Cambridge University Press: Cambridge, UK.CrossRefGoogle Scholar
Moffitt, TE, Caspi, A, Rutter, M, Silva, PA (2001 b). Sex effects in risk predictors for antisocial behavior: are males exposed to more risk factors for antisocial behavior? In Sex Differences in Antisocial Behavior: Conduct Disorder, Delinquency, and Violence in the Dunedin Longitudinal Study, pp. 109–122. Cambridge University Press: Cambridge, UK.CrossRefGoogle Scholar
Neale, MC, Maes, HM (2002). Methodology for Genetic Studies of Twins and Families. Kluwer: Dordrecht, The Netherlands.Google Scholar
Nilsson, KW, Sjöberg, RL, Damberg, M, Leppert, J, Öhrvik, J, Alm, PO, Lindstrom, L, Oreland, L (2005). Role of monoamine oxidase A genotype and psychosocial factors in male adolescent criminal activity. Biological Psychiatry 59, 121–127.CrossRefGoogle ScholarPubMed
Nordquist, N, Oreland, L (2006). Monoallelic expression of MAOA in skin fibroblasts. Biochemical and Biophysical Research Communications 348, 763–767.CrossRefGoogle ScholarPubMed
O'Connor, TG, Deater-Deckard, K, Fulker, D, Rutter, M, Plomin, R (1998). Genotype–environment correlations in late childhood and early adolescence: antisocial behavioral problems and coercive parenting. Developmental Psychology 34, 970–981.CrossRefGoogle ScholarPubMed
Osofsky, JD (1995). Children who witness domestic violence: the invisible victims. SRCD Social Policy Report 9, 1–16.CrossRefGoogle Scholar
Pinsonneault, JK, Papp, AC, Sadee, W (2006). Allelic mRNA expression of X-linked monoamine oxidase A (MAOA) in human brain: dissection of epigenetic and genetic factors. Human Molecular Genetics 15, 2636–2649.CrossRefGoogle ScholarPubMed
Plomin, R, DeFries, JC, Loehlin, JC (1977). Genotype–environment interaction and correlation in the analysis of human behavior. Psychological Bulletin 84, 309–322.CrossRefGoogle ScholarPubMed
Rhee, SH, Waldman, ID (2002). Genetic and environmental influences on antisocial behavior: a meta-analysis of twin and adoption studies. Psychological Bulletin 128, 490–529.CrossRefGoogle ScholarPubMed
Riggins-Caspers, KM, Cadoret, RJ, Knutson, JF, Langbehn, D (2003). Biology–environment interaction and evocative biology–environment correlation: contributions of harsh discipline and parental psychopathology to problem adolescent behaviors. Behavior Genetics 33, 205–220.CrossRefGoogle ScholarPubMed
Sabol, SZ, Hu, S, Hamer, D (1998). A functional polymorphism in the monoamine oxidase A gene promoter. Human Genetics 103, 273–279.CrossRefGoogle ScholarPubMed
Scaramella, LV, Conger, RD, Spoth, R, Simons, RL (2002). Evaluation of a social contextual model of delinquency: a cross-study replication. Child Development 73, 175–195.CrossRefGoogle ScholarPubMed
Scarr, S, McCartney, K (1983). How people make their own environments: a theory of genotype–environment effects. Child Development 54, 424–435.Google Scholar
Simonoff, E, Pickles, A, Meyer, JM, Silberg, JL, Maes, HH, Loeber, R, Rutter, M, Hewitt, JK, Eaves, LJ (1997). The Virginia Twin Study of Adolescent Behavioral Development. Influences of age, sex, and impairment on rates of disorder. Archives of General Psychiatry 54, 801–808.CrossRefGoogle ScholarPubMed
Sjöberg, RL, Nilsson, KW, Wargelius, HL, Leppert, J, Lindstrom, L, Oreland, L (2007). Adolescent girls and criminal activity: role of MAOA-LPR genotype and psychosocial factors. American Journal of Medical Genetics, Part B. Neuropsychiatric Genetics 144, 159–164.CrossRefGoogle Scholar
Slutske, WS, Heath, AC, Dinwiddie, SH, Madden, PA, Bucholz, KK, Dunne, MP, Statham, DJ, Martin, NG (1997). Modeling genetic and environmental influences in the etiology of conduct disorder: a study of 2,682 adult twin pairs. Journal of Abnormal Psychology 106, 266–279.CrossRefGoogle ScholarPubMed
Steiner, H (1997). Practice parameters for the assessment and treatment of children and adolescents with conduct disorder. Journal of the American Academy of Child and Adolescent Psychiatry 36, S122–S139.CrossRefGoogle ScholarPubMed
Young, SE, Smolen, A, Hewitt, JK, Haberstick, BC, Stallings, MC, Corley, RP, Crowley, TJ (2006). Interaction between MAO-A genotype and maltreatment in the risk for conduct disorder: failure to confirm in adolescent patients. American Journal of Psychiatry 163, 1019–1025.CrossRefGoogle ScholarPubMed