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Combined Influences of Genes, Prenatal Environment, Cortisol, and Parenting on the Development of Children’s Internalizing Versus Externalizing Problems

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Abstract

Research suggests that genetic, prenatal, endocrine, and parenting influences across development individually contribute to internalizing and externalizing problems in children. The present study tests the combined contributions of genetic risk for psychopathology, prenatal environments (maternal drug use and internalizing symptoms), child cortisol at age 4.5 years, and overreactive parenting influences across childhood on 6-year-old children’s internalizing and externalizing problems. We used data from an adoption design that included 361 domestically adopted children and their biological and adopted parents prospectively followed from birth. Only parenting influences contributed (independently) to externalizing problems. However, genetic influences were indirectly associated with internalizing problems (through increased prenatal risk and subsequent morning cortisol), and parenting factors were both directly and indirectly associated with internalizing problems (through morning cortisol). Results suggest that prenatal maternal drug use/symptoms and children’s morning cortisol levels are mechanisms of genetic and environmental influences on internalizing problems, but not externalizing problems, in childhood.

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References

  • Achenbach TM (1991) Manual for the child behavior checklist/4-18 and 1991 profile. University of Vermont, Burlington

    Google Scholar 

  • Alink LRA, van Ijzendoorn MH, Bakermans-Kranenburg MJ, Mesman J, Juffer F, Koot HM (2008) Cortisol and externalizing behavior in children and adolescents: mixed meta-analytic evidence for the inverse relation of basal cortisol and cortisol reactivity with externalizing behavior. Dev Psychobiol 50(5):427–450. doi:10.1002/dev.20300

    PubMed  Google Scholar 

  • Allen NB, Lewinsohn PM, Seeley JR (1998) Prenatal and perinatal influences on risk for psychopathology in childhood and adolescence. Dev Psychopathol 10(03):513–529

    PubMed  Google Scholar 

  • Andrews G, Stewart G, Allen R, Henderson AS (1990) The genetics of six neurotic disorders: a twin study. J Affect Disord 19(1):23–29

    PubMed  Google Scholar 

  • Archer J (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 30(3):319–345. doi:10.1016/j.neubiorev.2004.12.007

    PubMed  Google Scholar 

  • Arnold DS, O’Leary SG, Wolf LS, Acker MM (1993) The Parenting Scale: a measure of dysfunctional parenting in discipline situations. Psychol Assess 9(2):137–144

    Google Scholar 

  • Azar R, Paquette D, Zoccolillo M, Baltzer F, Tremblay RE (2007) The association of major depression, conduct disorder, and maternal overcontrol with a failure to show a cortisol buffered response in 4-month-old infants of teenage mothers. Biol Psychiatry 62(6):573–579. doi:10.1016/j.biopsych.2006.11.009

    PubMed  Google Scholar 

  • Bailey JA, Hill KG, Oesterle S, Hawkins JD (2009) Parenting practices and problem behavior across three generations: monitoring, harsh discipline, and drug use in the intergenerational transmission of externalizing behavior. Dev Psychol 45(5):1214–1226. doi:10.1037/a0016129

    PubMed  PubMed Central  Google Scholar 

  • Bale TL (2011) Sex differences in prenatal epigenetic programing of stress pathways. Stress 14(4):348–356

    PubMed  Google Scholar 

  • Bartels M, Van den Berg M, Sluyter F, Boomsma DI, de Geus EJC (2003) Heritability of cortisol levels: review and simultaneous analysis of twin studies. Psychoneuroendocrinology 28(2):121–137. doi:10.1016/s0306-4530(02)00003-3

    PubMed  Google Scholar 

  • Beck A, Steer R (1993) Beck anxiety invetory manual. The Psychological Corporation, San Antonio

    Google Scholar 

  • Beck AT, Steer RA, Brown GK (1996) Manual for beck depression inventory-II. Psychological Corporation, San Antonio

    Google Scholar 

  • Belsky J, Pluess M (2009) The nature (and nurture?) of plasticity in early human development. Perspect Psychol Sci 4(4):345–351

    Google Scholar 

  • Ben Amor L, Grizenko N, Schwartz G, Lageix P, Baron C, Ter-Stepanian M et al (2005) Perinatal complications in children with attention-deficit hyperactivity disorder and their unaffected siblings. J Psychiatr Neurosci 30:120–126

    Google Scholar 

  • Burghy CA, Stodola DE, Ruttle PL, Molloy EK, Armstrong JM, Oler JA et al (2012) Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nat Neurosci 15(12):1736–1741. doi:10.1038/nn.3257

    PubMed  PubMed Central  Google Scholar 

  • Burt SA (2009) Rethinking environmental contributions to child and adolescent psychopathology: a meta-analysis of shared environmental influences. Psychol Bull 135(4):6

    Google Scholar 

  • Cadoret RJ, Woolson R, Winokur G (1977) The relationship of age of onset in unipolar affective disorder to risk of alcoholism and depression in parents. Journal of Psychiatric Research 13(3):137–142. doi:10.1016/0022-3956(77)90002-4

    PubMed  Google Scholar 

  • Caspi A, Moffitt TE, Thornton A, Freedman D, Arnell JW, Harrington H et al (1996) The life history calendar: a research and clinical assessment method for collecting retrospective event-history data. Int J Methods Psychiatric Res 6(2):101–114

    Google Scholar 

  • Coussons-Read ME (2012) The psychoneuroimmunology of stress in pregnancy. Curr Dir Psychol Sci 21(5):323–328. doi:10.1177/0963721412453720

    Google Scholar 

  • De Bellis MD, Dahl RE, Perel JM, Birmaher B, Al-Shabbout M, Williamson DE et al (1996) Nocturnal ACTH, cortisol, growth hormone, and prolactin secretion in prepubertal depression. J Am Acad Ch Adol Psychiatr 35(9):1130–1138. doi:10.1097/00004583-199609000-00010

    Google Scholar 

  • Del Giudice M (2012) Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology 37(10):1614–1629. doi:10.1016/j.psyneuen.2012.05.014

    PubMed  Google Scholar 

  • Del Giudice M, Ellis BJ, Shirtcliff EA (2011) The adaptive calibration model of stress responsivity. Neurosci Biobehav Rev 35(7):1562–1592. doi:10.1016/j.neubiorev.2010.11.007

    PubMed  PubMed Central  Google Scholar 

  • D’Onofrio BM, Slutske WS, Turkheimer E, Emery RE, Harden KP, Heath AC et al (2007) Intergenerational transmission of childhood conduct problems: a children of twins study. Arch Gen Psychiatr 64(7):820–829

    PubMed  PubMed Central  Google Scholar 

  • Dozier M, Manni M, Gordon MK, Peloso E, Gunnar MR et al (2006) Foster children’s diurnal production of cortisol: an exploratory study. Child Maltreatment 11:189–197

    PubMed  Google Scholar 

  • Dressendorfer RA, Kirschbaum C, Rohde W, Stahl F, Strasburger CJ (1992) Synthesis of a cortisol-biotin conjugate and evaluation as a tracer in an immunoassay for salivary cortisol measurement. J Steroid Biochem Mol Biol 43:683–692

    PubMed  Google Scholar 

  • Eley TC (1997) Depressive symptoms in children and adolescents: etiological links between normality and abnormality: A research note. J Child Psychol Psychiatry 38(7):861–865. doi:10.1111/j.1469-7610.1997.tb01604.x

    PubMed  Google Scholar 

  • Ellingson JM, Rickert ME, Lichtenstein P, Langstrom N, D’Onofrio BM (2012) Disentangling the relationships between maternal smoking during pregnancy and co-occurring risk factors. Psychol Med 42(7):1547–1557

    PubMed  PubMed Central  Google Scholar 

  • Ellis BJ, Boyce WT, Belsky J, Bakermans-Kranenburg MJ, van Ijzendoorn MH (2011) Differential susceptibility to the environment: an evolutionary–neurodevelopmental theory. Dev Psychopathol 23(01):7–28. doi:10.1017/S0954579410000611

    PubMed  Google Scholar 

  • Essex MJ, Klein MH, Cho E, Kalin NH (2002) Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biol Psychiatr 52(8):776–784. doi:10.1016/s0006-3223(02)01553-6

    Google Scholar 

  • Fairchild G, van Goozen SHM, Stollery SJ, Brown J, Gardiner J, Herbert J et al (2008) Cortisol diurnal rhythm and stress reactivity in male adolescents with early-onset or adolescence-onset conduct disorder. Biol Psychiatr 64(7):599–606

    Google Scholar 

  • Feder A, Coplan JD, Goetz RR, Mathew SJ, Pine DS, Dahl RE et al (2004) Twenty-four-hour cortisol secretion patterns in prepubertal children with anxiety or depressive disorders. Biol Psychiatr 56(3):198–204. doi:10.1016/j.biopsych.2004.05.005

    Google Scholar 

  • Flinn MV, England BG (1997) Social economics of childhood glucocorticoid stress response and health. Am J Physical Anthropol 102(1):33–53

    Google Scholar 

  • Fries E, Hesse J, Hellhammer J, Hellhammer DH (2005) A new view on hypocortisolism. Psychoneuroendocrinology 30:1010–1016

    Google Scholar 

  • Ge X, Natsuaki MN, Martin DM, Leve LD, Neiderhiser JM, Shaw DS et al (2008) Bridging the divide: openness in adoption and postadoption psychosocial adjustment among birth and adoptive parents. J Fam Psychol 22(3):529–540

    PubMed  PubMed Central  Google Scholar 

  • Giesbrecht GF, Campbell T, Letourneau N, Kooistra L, Kaplan B (2012) Psychological distress and salivary cortisol covary within persons during pregnancy. Psychoneuroendocrinology 37(2):270–279

    PubMed  Google Scholar 

  • Glover V, O’Connor TG, O’Donnell K (2010) Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 35(1):17–22. doi:10.1016/j.neubiorev.2009.11.008

    PubMed  Google Scholar 

  • Goldschmidt L, Day NL, Richardson GA (2000) Effects of prenatal marijuana exposure on child behavior problems at age 10. Neurotoxicol Teratol 22(3):325–336

    PubMed  Google Scholar 

  • Graham J, Olchowski A, Gilreath T (2007) How many imputations are really needed? Some practical clarifications of multiple imputation theory. Prev Sci 8(3):206–213. doi:10.1007/s11121-007-0070-9

    PubMed  Google Scholar 

  • Granger DA, Serbin LA, Schwartzman A, Lehoux P, Cooperman J, Ikeda S (1998) Children’s salivary cortisol, internalising behaviour problems, and family environment: results from the concordia longitudinal risk project. Int J Behav Dev 22(4):707–728. doi:10.1080/016502598384135

    Google Scholar 

  • Gunnar MR, Donzella B (2002) Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27(1–2):199–220. doi:10.1016/s0306-4530(01)00045-2

    PubMed  Google Scholar 

  • Gunnar MR, Fisher PA (2006) Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Dev Psychopathol 18(3):651–677

    PubMed  Google Scholar 

  • Gunnar M, Quevedo K (2007) The neurobiology of stress and development. Ann Rev Psychol 58:145–173. doi:10.1146/annurev.psych.58.110405.085605

    Google Scholar 

  • Gunnar MR, Morison SJ, Chisholm K, Schuder M (2001) Salivary cortisol levels in children adopted from romanian orphanages. Dev Psychopathol 13(3):611–628

    PubMed  Google Scholar 

  • Gutteling BM, de Weerth C, Willemsen-Swinkels SHN, Huizink AC, Mulder EJH, Visser GHA et al (2005) The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Euro Ch Adol Psychiatr 14:41–51

    Google Scholar 

  • Halligan SL, Herbert J, Goodyer IM, Murray L (2004) Exposure to postnatal depression predicts elevated cortisol in adolescent offspring. Biol Psychiatr 55(4):376–381. doi:10.1016/j.biopsych.2003.09.013

    Google Scholar 

  • Hastings PD, Ruttle PL, Serbin LA, Mills RSL, Stack DM, Schwartzman AE (2011) Adrenocortical responses to strangers in preschoolers: relations with parenting, temperament, and psychopathology. Dev Psychobiol 53(7):694–710. doi:10.1002/dev.20545

    PubMed  Google Scholar 

  • Heim C, Newport DJ, Wagner D, Wilcox MM, Miller AH, Nemeroff CB (2002) The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis. Depress Anxiety 15(3):117–125. doi:10.1002/da.10015

    PubMed  Google Scholar 

  • Hettema JM, Neale MC, Kendler KS (2001) A review and meta-analysis of the genetic epidemiology of anxiety disorders. Am J Psychiatry 158(10):1568–1578

    PubMed  Google Scholar 

  • Hirschi T (1969) Causes of delinquency. University of California Press, Berkeley and Los Angeles

    Google Scholar 

  • Huizink AC, de Robles Medina PG, Mulder EJH, Visser GHA, Buitelaar JK (2003) Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry 44(6):810–818

    PubMed  Google Scholar 

  • Hunter AL, Minnis H, Wilson P (2011) Altered stress responses in children exposed to early adversity: a systematic review of salivary cortisol studies. Stress 14(6):614–626. doi:10.3109/10253890.2011.577848

    PubMed  Google Scholar 

  • Jabbi M, Korf J, Kema IP, Hartman C, van der Pompe G, Minderaa RB et al (2007) Convergent genetic modulation of the endocrine stress response involves polymorphic variations of 5-HTT, COMT and MAOA. Mol Psychiatry 12(5):483–490

    PubMed  Google Scholar 

  • Kagan J, Reznick S, Snidman N (1988) Biological bases of childhood shyness. Science 240:167

    PubMed  Google Scholar 

  • Kerr DR, Leve L, Harold G, Natsuaki M, Neiderhiser J, Shaw D, Reiss D (2013) Influences of biological and adoptive mothers’ depression and antisocial behavior on adoptees’ early behavior trajectories. J Abnorm Child Psychol 41(5):723–734. doi:10.1007/s10802-013-9711-6

    PubMed  PubMed Central  Google Scholar 

  • Kessler RC, Üstün TB (2004) The World Mental Health (WMH) Survey initiative version of the World Health Organization (WHO) Composite International Diagnostic Interview (CIDI). Int J Methods Psychiatr Res 13(2):93–121

    PubMed  Google Scholar 

  • Knopik VS (2009) Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol 34(1):462593

    Google Scholar 

  • Knopik VS, Maccani MA, Francazio S, McGeary JE (2012) The epigenetics of maternal cigarette smoking during pregnancy and effects on child development. Dev Psychopathol 24(4):1377–1390. doi:10.1017/s0954579412000776

    PubMed  PubMed Central  Google Scholar 

  • Kotelchuck M (1994) An evaluation of the Kessner adequacy of prenatal care index and a proposed adequacy of prenatal care utilization index. Am J Pub Health 84:1414–1420

    Google Scholar 

  • Kreek MJ, Nielsen DA, Butelman ER, LaForge KS (2005) Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction. Nat Neurosci 8(11):1450–1457

    PubMed  Google Scholar 

  • Laurent HK, Leve LD, Neiderhiser JM, Natsuaki MN, Shaw DS, Harold GT, Reiss D (2012) Effects of prenatal and postnatal parent depressive symptoms on adopted child hpa regulation: independent and moderated influences. Dev Psychol. doi:10.1037/a0028800

    PubMed Central  Google Scholar 

  • Laurent HK, Leve LD, Neiderhiser JM, Natsuaki MN, Shaw DS, Fisher PA, Marceau K, Harold G, Reiss D (2013) Effects of parental depressive symptoms on child adjustment moderated by hypothalamic pituitary adrenal activity: within- and between-family risk. Child Dev 84(2):528–542. doi:10.1111/j.1467-8624.2012.01859.x

    PubMed  PubMed Central  Google Scholar 

  • Leve LD, Neiderhiser JM, Shaw DS, Ganiban J, Natsuaki MN, Reiss D (2013) The Early Growth and Development Study: a prospective adoption study from birth through middle childhood. Twin Res Hum Genet 16(1):412–423. doi:10.1017/thg.2012.126

    PubMed  PubMed Central  Google Scholar 

  • Levinson DF (2006) The genetics of depression: a review. Biol Psychiatr 60(2):84–92

    Google Scholar 

  • Levy F, Hay DA, McStephen M, Wood C, Waldman I (1997) Attention-deficit hyperactivity disorder: a category or a continuum? Genetic analysis of a large-scale twin study. J Am Acad Ch Adol Psychiatr 36(6):737–744. doi:10.1097/00004583-199706000-00009

    Google Scholar 

  • Lipscomb ST, Leve LD, Harold GT, Neiderhiser JM, Shaw DS, Ge X, Reiss D (2011) Trajectories of parenting and child negative emotionality during infancy and toddlerhood: a longitudinal analysis. Child Dev 82(5):1661–1675. doi:10.1111/j.1467-8624.2011.01639.x

    PubMed  PubMed Central  Google Scholar 

  • Little RJA (1988) A test of missing completely at random for multivariate data with missing values. J Amer Statist Assoc 83:1198–1202. doi:10.2307/2290157

    Google Scholar 

  • Marceau K, Hajal N, Leve LD, Reiss D, Shaw DS, Ganiban JM et al (2013a) Measurement and associations of pregnancy risk factors with genetic influences, postnatal environmental influences, and toddler behavior. Int J Behav Dev 37(4):366–375. doi:10.1177/0165025413489378

    PubMed  PubMed Central  Google Scholar 

  • Marceau K, Ram N, Neiderhiser JM, Laurent HK, Shaw DS, Fisher P et al (2013b) Disentangling the effects of genetic, prenatal and parenting influences on children’s cortisol variability. Stress 16(6):607–615. doi:10.3109/10253890.2013.825766

    PubMed  PubMed Central  Google Scholar 

  • Marchand-Reilly J (2012) The role of fathers’ depressive symptoms and lax and overreactive discipline in children’s externalizing and internalizing behaviors. J Adult Dev 19(4):181–189. doi:10.1007/s10804-012-9145-3

    Google Scholar 

  • Marsman R, Rosmalen JG, Oldehinkel AJ, Ormel J, Buitelaar JK (2009) Does HPA-axis activity mediate the relationship between obstetric complications and externalizing behavior problems? The TRAILS study. Euro Child Adol Psychiatr 18:565–573. doi:10.1007/s00787-009-0014-y

    Google Scholar 

  • Mattson SN, Riley EP (2000) Parent ratings of behavior in children with heavy prenatal alcohol exposure and IQ-matched controls. Alcohol Clin Exper Res 24(2):226–231

    Google Scholar 

  • Maughan B, Taylor A, Caspi A, Moffit TE (2004) Prenatal smoking and early childhood conduct problems: testing genetic and environmental explanations of the association. Arch Gen Psychiatry, 61:836–843

    PubMed  Google Scholar 

  • McCarthy AM, Hanrahan K, Kleiber C, Zimmerman MB, Lutgendorf S, Tsalikian E (2009) Normative salivary cortisol values and responsivity in children. Applied Nurs Res 22(1):54–62. doi:10.1016/j.apnr.2007.04.009

    Google Scholar 

  • McKee L, Roland E, Coffelt N, Olson A, Forehand R, Massari C et al (2007) Harsh discipline and child problem behaviors: the roles of positive parenting and gender. J Fam Violence 22(4):187–196. doi:10.1007/s10896-007-9070-6

    Google Scholar 

  • McNeil T (1995) Perinatal risk factors and schizophrenia: selective review and methodological concerns. Epidemiol Rev 17:107–112

    PubMed  Google Scholar 

  • McNeil TF, Cantor-Graee E, Sjostrom K (1994) Obstetric complications as antecendents of schizophredia: empirical effects of using different obstetric complication scales. J Psychiatric Res 28:519–530

    Google Scholar 

  • Mill J, Petronis A (2008) Pre- and peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): the potential role of epigenetic processes in mediating susceptibility. J Child Psychol Psychiatr 49:1020–1030

    Google Scholar 

  • Muthen LK, Muthen BO (2004) Mplus user’s guide, 3rd edn. Muthén and Muthén, Los Angeles

    Google Scholar 

  • O’Conner TG, Ben-Shlomo Y, Heron J, Golding J, Adams D, Glover V (2005) Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Soc Biol Psychiatr 58:211–217

    Google Scholar 

  • Pemberton C, Neiderhiser JM, Leve LD, Natsuaki M, Shaw DS, Reiss D (2010) Influence of parental depressive symptoms on adopted toddler behaviors: an emerging developmental cascade of genetic and environmental effects. Dev Psychopathol 22:803–818

    PubMed  PubMed Central  Google Scholar 

  • Pettit JW, Olino TM, Roberts RE, Seeley JR, Lewinsohn PM (2008) Intergenerational transmission of internalizing problems: effects of parental and grandparental major depressive disorder on child behavior. J Clin Child Adol Psychol 37(3):640–650. doi:10.1080/15374410802148129

    Google Scholar 

  • Phillips DIW, Jones A (2006) Fetal programming of autonomic and HPA function: do people who were small babies have enhanced stress responses? J Physiol 572(1):45–50. doi:10.1113/jphysiol.2005.104695

    PubMed  PubMed Central  Google Scholar 

  • Pluess M, Belsky J (2011) Prenatal programming of postnatal plasticity? Dev Psychopathol 23:29–38

    PubMed  Google Scholar 

  • Raine A (1996) Autonomic nervous system factors underlying disinhibited, antisocial, and violent behavior biosocial perspectives and treatment implications. Annals NY Acad Sci 794(1):46–59. doi:10.1111/j.1749-6632.1996.tb32508.x

    Google Scholar 

  • Raine A (2002) Biosocial studies of antisocial and violent behavior in children and adults: a Review. J Abnorm Child Psychol 30(4):311–326

    PubMed  Google Scholar 

  • Repetti RL, Taylor SE, Seeman TE (2002) Risky families: family social environments and the mental and physical health of offspring. Psychol Bull 128(2):330–366

    PubMed  Google Scholar 

  • Rhee SH, Waldman ID (2002) Genetic and environmental influences on antisocial behavior: a meta-analysis of twin and adoption studies. Psychol Bull 128(3):490–529

    PubMed  Google Scholar 

  • Rice F, Thapar A (2009) Handbook of behavior genetics., Depression and anxiety in childhood and adolescence: Developmental pathways, genes and environmentSpringer, New York, pp 379–396

    Google Scholar 

  • Robins LN, Helzer JE, Croughan J, Ratcliff KS (1981) National Institute of Mental Health diagnostic interview schedule: its history, characteristics, and validity. Arch Gen Psychiatr 38(4):381

    PubMed  Google Scholar 

  • Robinson M, Mattes E, Oddy WH, de Klerk N, Li J, McLean NJ et al (2009) Hypertensive diseases of pregnancy and the development of behavioral problems in childhood and adolescence: the Western Australian Pregnancy Cohort Study. J Pediatrics 154:218–224

    Google Scholar 

  • Ruttle PL, Shirtcliff EA, Serbin LA, Ben-Dat Fisher D, Stack DM, Schwartzman AE (2011) Disentangling psychobiological mechanisms underlying internalizing and externalizing behaviors in youth: longitudinal and concurrent associations with cortisol. Horm Behav 59(1):123–132. doi:10.1016/j.yhbeh.2010.10.015

    PubMed  PubMed Central  Google Scholar 

  • Ryan S, Schechter J, Brennan P (2012) Perinatal factors, parenting behavior, and reactive aggression: does cortisol reactivity mediate this developmental risk process? J Abnorm Child Psychol 40(8):1211–1222. doi:10.1007/s10802-012-9649-0

    PubMed  Google Scholar 

  • Scerbo AS, Kolko DJ (1994) Salivary testosterone and cortisol in disruptive children: relationship to aggressive, hyperactive, and internalizing behaviors. J Am Acad Child Adol Psychiatr 33(8):1174–1184. doi:10.1097/00004583-199410000-00013

    Google Scholar 

  • Smider NA, Essex MJ, Kalin NH, Buss KA, Klein MH, Davidson RJ, Goldsmith HH (2002) Salivary cortisol as a predictor of socioemotional adjustment during kindergarten: a prospective study. Child Dev 73(1):75–92. doi:10.1111/1467-8624.00393

    PubMed  Google Scholar 

  • Sullivan PF, Neale MC, Kendler KS (2000) Genetic epidemiology of major depression: review and meta-analysis. Am J Psychiatry 157(10):1552–1562

    PubMed  Google Scholar 

  • Tarullo AR, Gunnar MR (2006) Child maltreatment and the developing HPA axis. Horm Behav 50(4):632–639. doi:10.1016/j.yhbeh.2006.06.010

    PubMed  Google Scholar 

  • Turner WM, Cutter HS, Worobec TG, O’Farrell TJ, Bayog RD, Tsuang MT (1993) Family history models of alcoholism: age of onset, consequences and dependence. J Stud Alcohol 54(2):164–171

    PubMed  Google Scholar 

  • Van den Bergh BRH, Mulder EJH, Mennes M, Glover V (2005) Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neurosci Biobehav Rev 29:237–258

    PubMed  Google Scholar 

  • van Goozen SH, Fairchild G, Snoek H, Harold GT (2007) The evidence for a neurobiological model of childhood antisocial behavior. Psychol Bull 133(1):149–182

    PubMed  Google Scholar 

  • Van Hulle CA, Shirtcliff EA, Lemery-Chalfant K, Goldsmith HH (2012) Genetic and environmental influences on individual differences in cortisol level and circadian rhythm in middle childhood. Horm Behav 62(1):36–42. doi:10.1016/j.yhbeh.2012.04.014

    PubMed  PubMed Central  Google Scholar 

  • Williams JHG, Ross L (2007) Consequences of prenatal toxin exposure for mental health in children and adolescents: a systematic review. Euro Child Adol Psychiatr 16:243–253

    Google Scholar 

  • Wüst S, Van Rossum EF, Federenko IS, Koper JW, Kumsta R, Hellhammer DH (2004) Common polymorphisms in the glucocorticoid receptor gene are associated with adrenocortical responses to psychosocial stress. J Clin Endocrinol Metab 89(2):565–573

    PubMed  Google Scholar 

  • Zahn-Waxler C, Shirtcliff EA, Marceau K (2008) Disorders of childhood and adolescence: gender and psychopathology. Ann Rev Clin Psychol 4(1):275–303. doi:10.1146/annurev.clinpsy.3.022806.091358

    Google Scholar 

  • Zuckerman M (1979) Sensation seeking: beyond the optimum level of arousal. Erlbaum, Hillsdale

    Google Scholar 

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Acknowledgments

We thank our participants and research staff for their extensive time and effort which made the present study possible. Data used in the current report was supported by NICHD, R01 HD042608 (Reiss, Leve), NIDA, R01 DA020585 (Neiderhiser), and OBSSR (the Office of the Director), NIH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Eunice Kennedy Shriver National Institute of Child Health & Human Development or the National Institutes of Health. The Early Growth and Development Study was also supported by NIMH, R01 MH092118 (Leve, Neiderhiser). Data analysis and manuscript preparation was supported in part by NIDA, F31 DA033737 and T32 DA016184 (Marceau).

Conflict of Interest

Kristine Marceau, Heidemarie K Laurent, Jenae M Neiderhiser, David Reiss, Daniel S Shaw, Misaki N Natsuaki, Phillip A Fisher and Leslie D Leve declare that they have no conflict of interest

Human and Animal Rights and Informed Consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 (5). Informed consent was obtained from all patients for being included in the study.

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Marceau, K., Laurent, H.K., Neiderhiser, J.M. et al. Combined Influences of Genes, Prenatal Environment, Cortisol, and Parenting on the Development of Children’s Internalizing Versus Externalizing Problems. Behav Genet 45, 268–282 (2015). https://doi.org/10.1007/s10519-014-9689-z

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