Effect of Prenatal Exposure to Tobacco Smoke on Inhibitory Control Neuroimaging Results from a 25-Year Prospective Study

JAMA Psychiatry

Volumn 71, Issue 7, 2014, Pages 786-796

  Holz, Nathalie E ^a   Boecker, Regina ^a   Baumeister, Sarah ^a   Hohm, Erika ^a   Zohsel, Katrin ^a   Buchmann, Arlette F ^a   Blomeyer, Dorothea ^a   Jennen Steinmetz, Christine ^a   Hohmann, Sarah ^a   Wolf, Isabella ^a   Plichta, Michael M ^a   Meyer Lindenberg, Andreas ^a   Banaschewski, Tobias ^a   Brandeis, Daniel ^a,b   Laucht, Manfred ^a,c  

^a CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF POTSDAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINE; TOBACCO SMOKE;

ADULT; ANTERIOR CINGULATE; ARTICLE; ATTENTION DEFICIT DISORDER; BRAIN FUNCTION; BRAIN SIZE; COHORT ANALYSIS; COMMUNITY SAMPLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; INFERIOR FRONTAL GYRUS; MAJOR CLINICAL STUDY; MALE; MATERNAL SMOKING; MATERNAL STRESS; NOVELTY SEEKING; PRENATAL EXPOSURE; PRENATAL STRESS; PROGENY; PROSPECTIVE STUDY; SCHEDULE FOR AFFECTIVE DISORDERS AND SCHIZOPHRENIA; SUBSTANCE ABUSE; SUPRAMARGINAL GYRUS; TASK PERFORMANCE; TEMPERAMENT; TOBACCO DEPENDENCE; VOXEL BASED MORPHOMETRY; YOUNG ADULT; ADOLESCENT; CHILD; EXPLORATORY BEHAVIOR; FRONTAL LOBE; INFANT; INHIBITION (PSYCHOLOGY); NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRESCHOOL CHILD; PROCEDURES; PSYCHOLOGY; SMOKING;

ADOLESCENT; ADULT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CHILD; CHILD, PRESCHOOL; EXPLORATORY BEHAVIOR; FEMALE; FRONTAL LOBE; FUNCTIONAL NEUROIMAGING; HUMANS; INFANT; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; NICOTINE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSPECTIVE STUDIES; SMOKING; YOUNG ADULT;

EID: 84903978019     PISSN: 2168622X     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamapsychiatry.2014.343     Document Type: Article

References (102)

1. World Health Organization (WHO). WHO Report on the Global Tobacco Epidemic, 2011:Warning About the Dangers of Tobacco. Geneva, Switzerland: WHO; 2011.
2. Ebrahim SH, Floyd RL, Merritt RK II, Decoufle P, Holtzman D. Trends in pregnancy-related smoking rates in the United States, 1987-1996. JAMA. 2000; 283(3):361-366.
3. Martin JA, Kochanek KD, Strobino DM, Guyer B, MacDorman MF. Annual summary of vital statistics - 2003. Pediatrics. 2005;115(3):619-634.
4. Hackshaw A, Rodeck C, Boniface S. Maternal smoking in pregnancy and birth defects: a systematic review based on 173 687 malformed cases and 11.7 million controls. Hum Reprod Update. 2011;17(5):589-604.
5. Ekblad M, GisslerM, Lehtonen L, Korkeila J. Prenatal smoking exposure and the risk of psychiatric morbidity into young adulthood. Arch Gen Psychiatry. 2010;67(8):841-849.
6. Button TM, Maughan B, McGuffin P. The relationship of maternal smoking to psychological problems in the offspring. Early Hum Dev. 2007;83 (11):727-732.
7. Laucht M, Schmidt MH. Maternal smoking during pregnancy: risk factor for ADHD in the offspring? [in German]. Z Kinder Jugendpsychiatr Psychother. 2004;32(3):177-185.
8. Milberger S, Biederman J, Faraone SV, Chen L, Jones J. Is maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children? Am J Psychiatry. 1996;153(9): 1138-1142.
9. Weissman MM,Warner V, Wickramaratne PJ, Kandel DB. Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J AmAcad Child Adolesc Psychiatry. 1999;38(7):892-899.
10. Langley K, Rice F, van den Bree MB, Thapar A. Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour: a review. Minerva Pediatr. 2005;57(6):359-371.
11. Galera C, Cote SM, BouvardMP, et al. Early risk factors for hyperactivity-impulsivity and inattention trajectories from age 17 months to 8 years. Arch Gen Psychiatry. 2011;68(12):1267-1275.
12. Biederman J, Monuteaux MC, Faraone SV,Mick E. Parsing the associations between prenatal exposure to nicotine and offspring psychopathology in a nonreferred sample. J Adolesc Health. 2009;45(2):142-148.
13. Langley K, Heron J, Smith GD, Thapar A. Maternal and paternal smoking during pregnancy and risk of ADHD symptoms in offspring: testing for intrauterine effects. Am J Epidemiol. 2012;176(3): 261-268.
14. Thapar A, Rice F, Hay D, et al. Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry. 2009;66(8):722-727.
15. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed, text revision.Washington, DC: American Psychiatric Association; 2000.
16. Boonstra AM, Kooij JJ, Oosterlaan J, Sergeant JA, Buitelaar JK. To act or not to act, that's the problem: primarily inhibition difficulties in adult ADHD. Neuropsychology. 2010;24(2):209-221.
17. Rubia K. "Cool" inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus "hot" ventromedial orbitofrontal-limbic dysfunction in conduct disorder: a review. Biol Psychiatry. 2011;69(12): e69-e87.
18. Rubia K, Overmeyer S, Taylor E, et al. Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. Am J Psychiatry. 1999;156(6): 891-896.
19. Rubia K, Taylor E, Smith AB, Oksanen H, Overmeyer S, Newman S. Neuropsychological analyses of impulsiveness in childhood hyperactivity [published correction appears in Br J Psychiatry 2001;179:272]. Br J Psychiatry. 2001; 179:138-143.
20. Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E. Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am J Psychiatry. 2005;162 (6):1067-1075.
21. El Marroun H, Schmidt MN, Franken IH, et al. Prenatal tobacco exposure and brain morphology: a prospective study in young children. Neuropsychopharmacology. 2014;39(4):792-800.
22. RivkinMJ, Davis PE, Lemaster JL, et al. Volumetric MRI study of brain in children with intrauterine exposure to cocaine, alcohol, tobacco, and marijuana. Pediatrics. 2008;121(4):741-750.
23. Derauf C, Lester BM, Neyzi N, et al. Subcortical and cortical structural central nervous system changes and attention processing deficits in preschool-aged children with prenatal methamphetamine and tobacco exposure. Dev Neurosci. 2012;34(4):327-341.
24. Ekblad M, Korkeila J, Parkkola R, Lapinleimu H, Haataja L, Lehtonen L; PIPARI Study Group. Maternal smoking during pregnancy and regional brain volumes in preterm infants. J Pediatr. 2010; 156(2):185-190.e1.
25. Toro R, Leonard G, Lerner JV, et al. Prenatal exposure to maternal cigarette smoking and the adolescent cerebral cortex. Neuropsychopharmacology. 2008;33(5):1019-1027.
26. Paus T, Nawazkhan I, Leonard G, et al. Corpus callosum in adolescent offspring exposed prenatally to maternal cigarette smoking. Neuroimage. 2008; 40(2):435-441.
27. Haghighi A, Schwartz DH, Abrahamowicz M, et al. Prenatal exposure to maternal cigarette smoking, amygdala volume, and fat intake in adolescence. JAMA Psychiatry. 2013;70(1):98-105.
28. Jacobsen LK, Picciotto MR, Heath CJ, et al. Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. J Neurosci. 2007;27(49):13491-13498.
29. Bennett DS, Mohamed FB, Carmody DP, et al. Response inhibition among early adolescents prenatally exposed to tobacco: an fMRI study. Neurotoxicol Teratol. 2009;31(5):283-290.
30. Longo CA, Fried PA, Cameron I, Smith AM. The long-term effects of prenatal nicotine exposure on response inhibition: an fMRI study of young adults. Neurotoxicol Teratol. 2013;39:9-18.
31. Jacobsen LK, Slotkin TA,Westerveld M, Mencl WE, Pugh KR. Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology. 2006;31(7):1550-1561.
32. Jacobsen LK, Slotkin TA, Mencl WE, Frost SJ, Pugh KR. Gender-specific effects of prenatal and adolescent exposure to tobacco smoke on auditory and visual attention. Neuropsychopharmacology. 2007;32(12):2453-2464.
33. Muller KU, Mennigen E, Ripke S, et al; IMAGEN Consortium. Altered reward processing in adolescents with prenatal exposure to maternal cigarette smoking. JAMA Psychiatry. 2013;70(8): 847-856.
34. Strohle A, Stoy M,Wrase J, et al. Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. Neuroimage. 2008;39(3):966-972.
35. Robinson M, Oddy WH, Li J, et al. Pre- and postnatal influences on preschool mental health: a large-scale cohort study. J Child Psychol Psychiatry. 2008;49(10):1118-1128.
36. Schneider S, Maul H, Freerksen N, Potschke-Langer M. Who smokes during pregnancy? an analysis of the German Perinatal Quality Survey 2005. Public Health. 2008;122(11): 1210-1216.
37. Weaver K, Campbell R, Mermelstein R, Wakschlag L. Pregnancy smoking in context: the influence of multiple levels of stress. Nicotine Tob Res. 2008;10(6):1065-1073.
38. Roza SJ, Verhulst FC, Jaddoe VW, et al. Maternal smoking during pregnancy and child behaviour problems: the Generation R Study. Int J Epidemiol. 2009;38(3):680-689.
39. Maughan B, Taylor A, Caspi A, Moffitt TE. Prenatal smoking and early childhood conduct problems: testing genetic and environmental explanations of the association. Arch Gen Psychiatry. 2004;61(8):836-843.
40. Griesler PC, Kandel DB, Davies M. Maternal smoking in pregnancy, child behavior problems, and adolescent smoking. J Res Adolesc. 1998;8: 159-185. doi:10.1207/s15327795jra0802-1.
41. Kandel DB,Wu P, Davies M. Maternal smoking during pregnancy and smoking by adolescent daughters.Am J Public Health. 1994;84(9):1407-1413.
42. Brennan PA, Grekin ER, Mortensen EL, Mednick SA. Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring. Am J Psychiatry. 2002;159 (1):48-54.
43. Buka SL, Shenassa ED, Niaura R. Elevated risk of tobacco dependence among offspring of mothers who smoked during pregnancy: a 30-year prospective study. Am J Psychiatry. 2003;160(11): 1978-1984.
44. Blasi G, Goldberg TE,Weickert T, et al. Brain regions underlying response inhibition and interference monitoring and suppression. Eur J Neurosci. 2006;23(6):1658-1664.
45. Bunge SA, Hazeltine E, Scanlon MD, Rosen AC, Gabrieli JD. Dissociable contributions of prefrontal and parietal cortices to response selection. Neuroimage. 2002;17(3):1562-1571.
46. Meyer-Lindenberg A, Buckholtz JW, Kolachana B, et al. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci U S A. 2006;103(16):6269-6274.
47. Anckarsater H, Stahlberg O, Larson T, et al. The impact of ADHD and autism spectrum disorders on temperament, character, and personality development. Am J Psychiatry. 2006; 163(7):1239-1244.
48. Lynn DE, Lubke G, YangM, et al. Temperament and character profiles and the dopamine D4 receptor gene in ADHD. Am J Psychiatry. 2005;162 (5):906-913.
49. Laucht M, Esser G, Schmidt MH. Developmental outcome of infants born with biological and psychosocial risks. J Child Psychol Psychiatry. 1997;38(7):843-853.
50. Laucht M, Esser G, Baving L, et al. Behavioral sequelae of perinatal insults and early family adversity at 8 years of age. J AmAcad Child Adolesc Psychiatry. 2000;39(10):1229-1237.
51. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO. The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict. 1991;86(9): 1119-1127.
52. Babor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG. AUDIT: The Alcohol Use Disorders Identification Test: Guidelines for Use in Primary Care. Geneva, Switzerland:World Health Organization; 2001.
53. Esser G, Blanz B, Geisel B, Laucht M. Mannheim Parent Interview-Structured Interview for Child Psychiatric Disorders [in German].Weinheim, Germany: Beltz; 1989.
54. Delmo C,Weiffenbach O, GabrielM, Poustka F. Kiddie-Sads-Present and Lifetime Version (K-SADS-PL): Auflage der Deutsche Forschungsversion. 3rd ed. Frankfurt, Germany: Klinik fur Psychiatrie und Psychotherapie des Kindes, Jugendalters der Universitat Frankfurt; 2000. http: //www.adhs-essen.com/PDF/K- SADS-Fragebogen .pdf. Accessed April 11, 2014.
55. Kaufman J, Birmaher B, Brent D, Rao U, Ryan N. Kiddie Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL). Version 1.0 of October 1996. Department of Psychiatry, University of Pittsburghwebsite. http://www.psychiatry.pitt.edu /node/8233. Accessed April 9, 2014.
56. Cloninger CR, Przybeck TR, Svrakic DM,Wetzel RD. The Temperament and Character Inventory (TCI): A Guide to Its Development and Use. St Louis, MO:Washington University Center for Psychobiology of Personality; 1994.
57. Swick D, Ashley V, Turken U. Are the neural correlates of stopping and not going identical? quantitativemeta-analysis of two response inhibition tasks. Neuroimage. 2011;56(3):1655-1665.
58. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15(1): 273-289.
59. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19(3):1233-1239.
60. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage. 2007;38(1): 95-113.
61. Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P. The anterior cingulate cortex: the evolution of an interface between emotion and cognition. Ann N Y Acad Sci. 2001;935:107-117.
62. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain. 1995;118(Pt 1):279-306.
63. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 2000;4(6):215-222.
64. Cortese S, Kelly C, Chabernaud C, et al. Toward systems neuroscience of ADHD: ameta-analysis of 55 fMRI studies. Am J Psychiatry. 2012;169(10): 1038-1055.
65. Batty MJ, Liddle EB, Pitiot A, et al. Cortical gray matter in attention-deficit/hyperactivity disorder: a structural magnetic resonance imaging study. J AmAcad Child Adolesc Psychiatry. 2010;49(3): 229-238.
66. Cloninger CR, Svrakic DM, Przybeck TR. A psychobiological model of temperament and character. Arch Gen Psychiatry. 1993;50(12):975-990.
67. Nieoullon A. Dopamine and the regulation of cognition and attention. Prog Neurobiol. 2002;67 (1):53-83.
68. Gusnard DA, RaichleME, RaichleME. Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci. 2001;2(10): 685-694.
69. Spreng RN, Mar RA, Kim AS. The common neural basis of autobiographical memory, prospection, navigation, theory ofmind, and the default mode: a quantitativemeta-analysis. J Cogn Neurosci. 2009;21(3):489-510.
70. Berkman ET, Falk EB, Lieberman MD. Interactive effects of three core goal pursuit processes on brain control systems: goal maintenance, performance monitoring, and response inhibition. PLoS One. 2012;7(6):e40334.
71. Brieber S, Neufang S, Bruning N, et al. Structural brain abnormalities in adolescents with autism spectrum disorder and patients with attention deficit/hyperactivity disorder. J Child Psychol Psychiatry. 2007;48(12):1251- 1258.
72. McLaughlin KA, Sheridan MA, Winter W, Fox NA, Zeanah CH, Nelson CA.Widespread reductions in cortical thickness following severe early-life deprivation: a neurodevelopmental pathway to attention-deficit/hyperactivity disorder [published online September 20, 2013]. Biol Psychiatry. doi:10.1016/j.biopsych.2013.08.016.
73. Gaysina D, Fergusson DM, Leve LD, et al. Maternal smoking during pregnancy and offspring conduct problems: evidence from 3 independent genetically sensitive research designs. JAMA Psychiatry. 2013;70(9):956-963.
74. Frick PJ, Morris AS. Temperament and developmental pathways to conduct problems. J Clin Child Adolesc Psychol. 2004;33(1):54-68.
75. Sterzer P, Stadler C, Krebs A, Kleinschmidt A, Poustka F. Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biol Psychiatry. 2005;57(1):7-15.
76. Passamonti L, Fairchild G, Goodyer IM, et al. Neural abnormalities in early-onset and adolescence-onset conduct disorder. Arch Gen Psychiatry. 2010;67(7):729-738.
77. Rubia K, Halari R, Cubillo A, Mohammad AM, Scott S, Brammer M. Disorder-specific inferior prefrontal hypofunction in boys with pure attention-deficit/hyperactivity disorder compared to boys with pure conduct disorder during cognitive flexibility. Hum Brain Mapp. 2010;31(12):1823-1833.
78. Slotkin TA, Orband-Miller L, Queen KL, WhitmoreWL, Seidler FJ. Effects of prenatal nicotine exposure on biochemical development of rat brain regions: maternal drug infusions via osmotic minipumps. J Pharmacol Exp Ther. 1987; 240(2):602-611.
79. Slotkin TA, Southard MC, Adam SJ, Cousins MM, Seidler FJ. Alpha7 nicotinic acetylcholine receptors targeted by cholinergic developmental neurotoxicants: nicotine and chlorpyrifos. Brain Res Bull. 2004;64(3):227-235.
80. Ernst M, Moolchan ET, Robinson ML. Behavioral and neural consequences of prenatal exposure to nicotine. J AmAcad Child Adolesc Psychiatry. 2001;40(6):630-641.
81. Seidler FJ, Levin ED, Lappi SE, Slotkin TA. Fetal nicotine exposure ablates the ability of postnatal nicotine challenge to release norepinephrine from rat brain regions. Brain Res Dev Brain Res. 1992;69 (2):288-291.
82. Wickstrom R. Effects of nicotine during pregnancy: human and experimental evidence. Curr Neuropharmacol. 2007;5(3):213-222.
83. Slotkin TA, Pinkerton KE, Auman JT, Qiao D, Seidler FJ. Perinatal exposure to environmental tobacco smoke upregulates nicotinic cholinergic receptors in monkey brain. Brain Res Dev Brain Res. 2002;133(2):175-179.
84. Abreu-Villaca Y, Seidler FJ, Tate CA, Cousins MM, Slotkin TA. Prenatal nicotine exposure alters the response to nicotine administration in adolescence: effects on cholinergic systems during exposure and withdrawal. Neuropsychopharmacology. 2004;29(5):879-890.
85. Picard F, Sadaghiani S, Leroy C, Courvoisier DS, Maroy R, Bottlaender M. High density of nicotinic receptors in the cingulo-insular network. Neuroimage. 2013;79:42-51.
86. Dwyer JB, McQuown SC, Leslie FM. The dynamic effects of nicotine on the developing brain. Pharmacol Ther. 2009;122(2):125-139.
87. Galvan A, Poldrack RA, Baker CM, McGlennen KM, London ED. Neural correlates of response inhibition and cigarette smoking in late adolescence. Neuropsychopharmacology. 2011;36 (5):970-978.
88. Barker DJ, Clark PM. Fetal undernutrition and disease in later life. Rev Reprod. 1997;2(2):105-112.
89. de Rooij SR,Wouters H, Yonker JE, Painter RC, Roseboom TJ. Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci U S A. 2010;107(39):16881-16886.
90. Knopik VS, Maccani MA, Francazio S,McGeary JE. The epigenetics of maternal cigarette smoking during pregnancy and effects on child development. Dev Psychopathol. 2012;24(4): 1377-1390.
91. Suter M, Ma J, Harris A, et al. Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics. 2011;6(11):1284-1294.
92. Wilhelm-Benartzi CS, Houseman EA, Maccani MA, et al. In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta. Environ Health Perspect. 2012;120(2):296-302.
93. Suter M, Abramovici A, Showalter L, et al. In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism. 2010;59 (10):1481-1490.
94. Kahn RS, Khoury J, NicholsWC, Lanphear BP. Role of dopamine transporter genotype and maternal prenatal smoking in childhood hyperactive-impulsive, inattentive, and oppositional behaviors. J Pediatr. 2003;143(1): 104-110.
95. Sun H, Yuan F, Shen X, Xiong G,Wu J. Role of COMT in ADHD: a systematic meta-analysis. Mol Neurobiol. 2014;49(1):251-261.
96. XuQ, Ma JZ, Payne TJ, Li MD.Determination of methylated CpG sites in the promoter region of catechol-O-methyltransferase (COMT) and their involvement in the etiology of tobacco smoking. Front Psychiatry. 2010;1:16.
97. Lindqvist R, Lendahls L, Tollbom O, Aberg H, Hakansson A. Smoking during pregnancy: comparison of self-reports and cotinine levels in 496 women. Acta Obstet Gynecol Scand. 2002;81 (3):240-244.
98. Rebagliato M. Validation of self reported smoking. J Epidemiol Community Health. 2002;56 (3):163-164.
99. AltinkME, Slaats-Willemse DI, Rommelse NN, et al. Effects of maternal and paternal smoking on attentional control in children with and without ADHD. Eur Child Adolesc Psychiatry. 2009;18(8): 465-475.
100. Xu H,Wen LM, Rissel C, Baur LA. Smoking status and factors associated with smoking of first-time mothers during pregnancy and postpartum: findings from the Healthy Beginnings Trial. Matern Child Health J. 2013;17(6):1151-1157.
101. Jylha P, Ketokivi M, Mantere O, et al. Temperament, character and personality disorders. Eur Psychiatry. 2013;28(8):483-491.
102. Banaschewski T, Hollis C, Oosterlaan J, et al. Towards an understanding of unique and shared pathways in the psychopathophysiology of ADHD. Dev Sci. 2005;8(2):132-140.