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The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers

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Abstract

Aim

To examine, in a prospective study, the influence of prenatal stress on infant temperament and problem behavior.

Method

Self-report data on stress and anxiety, and levels of cortisol in saliva were collected from nulli-parous women during pregnancy. Temperament of the child was measured at 27 months by parent report on the Infant Characteristics Questionnaire. Behavior of the child was assessed by direct observation during the administration of the Bayley Scales of Development 2–30, and by parent report on the Child Behavior Checklist 2–3.

Results

Complete data were available for 103 healthy toddlers. Logistic regression analyses were performed and results were adjusted for possible prenatal, perinatal and postnatal confounders. Perceived stress during pregnancy was a predictor of lower levels of restless/disruptive temperament (OR=0.77), more total behavioral problems (OR=1.17), and more externalizing behavioral problems (OR=1.12) in 2-year-olds. Fear of bearing a handicapped child was a predictor of higher levels of restless/disruptive temperament (OR=1.39) and more attention regulation problems in toddlers (OR=1.46).

Conclusions

Increased levels of maternal prenatal stress appear to be associated with temperamental and behavioral problems in toddlers.

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References

  1. Achenbach TM (1991) Manual for the Child Behavior Checklist 2–3 and 1992 Profile. Burlington: University of Vermont

  2. Achenbach TM, Edelbrock C, Howell CT (1987) Empirically based assessment of the behavioral/emotional problems of 2- and 3-year-old children. J Abn Child Psychol 15:629–650

    Google Scholar 

  3. Alonso SJ, Arevalo R, Afonso D, Rodriguez M (1991) Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring. Physiol Behav 50:511–517

    Google Scholar 

  4. Alonso SJ, Navarro E, Rodriguez M (1994) Permanent dopaminergic alterations in the nucleus accumbens after prenatal stress. Pharmacol Biochem Behav 49:353–358

    Google Scholar 

  5. Barbazanges A, Piazza PV, Le Moal M, Maccari S (1996) Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943–3949

    Google Scholar 

  6. Barker DJP (1994a) Mothers, babies, and disease in later life. BMJ Publishing Group, London

  7. Barker DJP (1994b) Mothers, babies and health in later life. Churchill Livingstone, Edinburgh

  8. Bates JE, Freeland CA, Lounsbury ML (1979) Measurement of infant difficultness. Child Development 50:794–803

    Google Scholar 

  9. Bayley N (1969) Bayley Scales of Infant Development. Psychological Corp, New York

  10. Burks N, Martin B (1985) Everyday problems and life change events: ongoing versus acute sources of stress. J Hum Stress spring 11:27–35

    Google Scholar 

  11. Clarke AS, Schneider ML (1993) Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev Psychobiol 26:293–304

    Google Scholar 

  12. Cohen S, Williamson GM (1987) Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S (eds) The social psychology of health. Newbury Park, California: SAGE Publications, pp 31–49

  13. Cratty MS, Ward HE, Johnson EA, Azzaro AJ,Birkle DL (1995) Prenatal stress increases corticotrophin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res 675:297–302

    Google Scholar 

  14. Dahlof LG, Hard E, Larsson K (1978) Influence of maternal stress on the development of the fetal genital system. Physiol Behav 20:193–195

    Google Scholar 

  15. Fride E, Weinstock M (1984) The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat. Dev Psychobiol 17:651–660

    Google Scholar 

  16. Gitau R, Fisk NM, Glover V (2001) Maternal stress in pregnancy and its effect on the human foetus: An overview of research finding. Stress 4:195–203

    Google Scholar 

  17. Glynn LM, Wadhwa PD, Dunkel-Schetter C, Chicz-Demet A, Sandman CA (2001) When stress happens matters: effects of earthquake timing on stress responsivity in pregnancy. Am J Obstet Gynecol 184:637–642

    Google Scholar 

  18. Goldberg DP (1972) The detection of psychiatric illness by questionnaire. Oxford University Press, London

  19. Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N (1998) Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Devel Neurosci 16:209–216

    Google Scholar 

  20. Huizink AC (2000) Prenatal stress and its effect on infant development. PhD. Thesis, Utrecht University, the Netherlands

  21. Huizink AC, Mulder EJH, Buitelaar JK (2004) Prenatal stress and risk for psychopathology. Specific effects or induction of general susceptibility. Psychol Bull 130:115–142

    Google Scholar 

  22. Huizink AC, Mulder EJH, Robles de Medina PG, Visser GHA, Buitelaar JK (2004) Is pregnancy anxiety a distinctive syndrome? Early Hum Dev 79:81–91

    Google Scholar 

  23. Huizink AC, Robles De Medina PG, Mulder EJH, Visser GHA, Buitelaar JK (2002) Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry 41:1078–1085

    Google Scholar 

  24. Kalff AC, Kroes M, Vles JS, Bosma H, Feron FJ, Hendriksen JG, Steyaert J, van Zeben TM, Crolla IF, Jolles J (2001) Factors affecting the relation between parental education as well as occupation and problem behaviour in Dutch 5-to 6-year-old children. Soc Psychiatry Psychiatr Epidemiol 36:324–331

    Google Scholar 

  25. Kanner AD, Coyne JC, Schaefer C, Lazarus RS (1981) Comparison of two models of stress measurement: daily hassles and uplifts versus major life events. J Behav Med 4:1–39

    Google Scholar 

  26. Koeter MWJ, Ormel J (1991) General Health Questionnaire. Nederlandse bewerking. Swets test services, The Netherlands

  27. Kohnstamm GA (1984) Bates’ Infant Characteristics Questionnaire (ICQ) in the Netherlands. Eric Reports 251:179

    Google Scholar 

  28. Kuvacic I, Skrablin S, Hodzic D, Milkovic G (1996) Possible influence of expatriation on perinatal outcome. Acta Obstet Gynecol Scand 75:367–371

    Google Scholar 

  29. Lazarus RS, Folkman S (1984) Stress, Appraisal, and Coping. Springer, New York

  30. Lordi B, Protais P, Mellier D, Caston J (1997) Acute stress in pregnant rats: effects on growth rate, learning, and memory capabilities of the offspring. Physiol Behav 62:1087–1092

    Google Scholar 

  31. Mesman J, Koot HM (2001) Early preschool predictors of preadolescent internalizing and externalizing DSMIV diagnoses. J Am Acad Child Adolesc Psychiatry 40:1029–1036

    Google Scholar 

  32. Mesman J, Bongers IL, Koot HM (2001) Preschool developmental pathways to preadolescent internalizing and externalizing problems. J Child Psychol Psychiatry Allied Disciplines 42:679–689

    Google Scholar 

  33. Mulder EJH, Robles de Medina PG, Huizink AC, Van den Bergh BRH, Buitelaar JK, Visser GHA (2002) Prenatal maternal stress: effects on pregnancy and the (unborn) child. Early Hum Dev 70:3–14

    Google Scholar 

  34. Nejtek VA (2002) High and low emotion events influence emotional stress perceptions and are associated with salivary cortisol response changes in a consecutive stress paradigm. Psychoneuroendocrinology 27:337–352

    Google Scholar 

  35. O’Connor TG, Heron J, Golding J, Beveridge M, Glover V (2002) Maternal antenatal anxiety and children’s behavioral/emotional problems at 4 years. Br J Psychiatry 180:502–508

    Google Scholar 

  36. Orlebeke JC, Knol DL, Verhulst FC (1999) Child behavior problems increased by maternal smoking during pregnancy. Arch Environ Health 54:15–19

    Google Scholar 

  37. Orlebeke JF, Knol DL, Boomsma DI, Verhulst FC (1998) Frequency of parental report of problem behavior in children decreases with increasing maternal age at delivery. Psychol Rep 82:395–404

    Google Scholar 

  38. Paarlberg KM, Vingerhoets AJ, Passchier J, Dekker GA, Heinen AG, van Geijn HP (1999) Psychosocial predictors of low birthweight: a prospective study. Br J Obstet Gynaecol 106:834–841

    Google Scholar 

  39. Peters DA (1982) Prenatal stress: effects on brain biogenic amine and plasma corticosterone levels. Pharmacol Biochem Behav 31:839–943

    Google Scholar 

  40. Rhees RW, Fleming DE (1981) Effects of malnutrition, maternal stress or ACTH injections during pregnancy on sexual behavior of male offspring. Physiol Behav 27:879–882

    Google Scholar 

  41. Rini CK, Dunkel-Schetter C, Wadhwa PD, Sandman CA (1999) Psychological adaptation and birth outcomes: The role of personal resources, stress, and sociocultural context in pregnancy. Health Psychol 18:333–345

    Google Scholar 

  42. Saylor CF, Boyce GC, Price C (2003) Early predictors of school-age behavior problems and social skills in children with intraventricular hemorrhage (IVH) and/or extremely low birth-weight (ELBW). Child Psychiatry Hum Dev 33:175–192

    Google Scholar 

  43. Schneider ML (1992a) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Devel Psychobiol 25:529–540

    Google Scholar 

  44. Schneider ML (1992b) Delayed object permanence development in prenatally stressed rhesus monkey infants (Macaca mulatta). Occup Ther J Res 12:96–110

    Google Scholar 

  45. Schneider ML, Coe CL (1993) Repeated social stress during pregnancy impairs neuromotor development of the primate infant. J Devel Behav Pediatr 14:81–87

    Google Scholar 

  46. Schneider ML, Clarke S, Kraemer GW, Roughton EC, Lubach GR, Rimm-Kaufman S, Schmidt D, Ebert M (1998) Prenatal stress alters brain biogenic amine levels in primates. Dev Psychopathol 10:27–440

    Google Scholar 

  47. Secco ML, Moffatt ME (2003) Situational, maternal, and infant influences on parenting stress among adolescent mothers. Issues Compr Pediatr Nurs 26:103–122

    Google Scholar 

  48. Selten JP, van der Graaf Y, van Duursen R, Gispen-de Wied CC, Kahn RS (1999) Psychotic illness after prenatal exposure to the 1953 Dutch Flood Disaster. Schizophr Res 35:243–245

    Google Scholar 

  49. Sobrian SK, Vaughn VT, Ashe WK, Markovic B, Djuric V, Jankovic BD (1997) Gestational exposure to loud noise alters the development and postnatal responsiveness of humoral and cellular components of the immune system in offspring. Environ Res 73:227–241

    Google Scholar 

  50. Stone AA, Neale IM (1982) Development of a methodology for assessing daily experiences. In: Blaum A, Singer EF (eds.) Advances in Environmental Psychology. Vol. 4. Environment and health. Hillsdale, Erlbaum, New York, pp 49–83

  51. Takahashi LK (1994) Stimulus control of behavioral inhibition in the preweanling rat. Physiol Behav 55:717–721

    Google Scholar 

  52. Takahashi LK, Kalin NH (1991) Early development and temporal characteristics of stress induced secretion of pituitary-adrenal hormones in prenatally-stressed rat pups. Brain Res 574:131–137

    Google Scholar 

  53. Takahashi LK, Baker EW, Kalin NH (1990) Ontogeny of behavioral and hormonal responses to stress in prenatally stressed male rat pups. Physiol Behav 47:357–364

    Google Scholar 

  54. Takahashi LK, Baker, EW, Kalin NH (1992) Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol Behav 51:319–323

    Google Scholar 

  55. Van den Bergh B (1990) The influence of maternal emotions during pregnancy on fetal and neonatal behavior. Pre Peri Natal Psychol J 5:119–130

    Google Scholar 

  56. Van den Bergh B, Marcoen A (2004) High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev 75:1085–1097

    Google Scholar 

  57. Van der Meulen BF, Smrkovsky M (1983) BOS 2–30. Bayley ontwikkelingsschalen: handleiding. Swets and Zeitlinger BV, Lisse, The Netherlands

    Google Scholar 

  58. Vingerhoets AJJM, Jeninga AJ, Menges LJ (1989) Het meten van chronische en alledaagse stressoren: Eerste onderzoekservaringen met de Alledaagse Problemen Lijst (APL)II [The measurement of daily hassles and chronic stressors: the development of the Everyday Problem Checklist (EPCL, Dutch: APL)]. Gedrag Gezond 17:10–17

    Google Scholar 

  59. Wadhwa PD, Dunkel-Schetter C, Chicz-Demet A, Porto M, Sandman CA (1996) Prenatal psychosocial factors and the neuroendocrine axis in human pregnancy. Psychosom Med 58:432–446

    CAS  PubMed  Google Scholar 

  60. Wadhwa PD, Sandman CA, Porto M, Dunkel-Schetter C, Garite TJ (1993) The association between prenatal stress and infant birth weight and gestational age at birth: a prospective investigation. Am J Obstetr Gynecol 169:858–865

    Google Scholar 

  61. Wakschlag LS, Pickett KE, Middlecamp MK, Walton LL, Tenzer P, Leventhal BL (2003) Pregnant smokers who quit, pregnant smokers who don’t: does history of problem behavior make a difference? Soc Sci Med 56:2449–246

    Google Scholar 

  62. Ward IL, Weisz J (1984) Differential effects of maternal stress on circulating levels of corticosterone, progesterone and testosterone in male and female rat foetuses and their mothers. Endocrinology 114:1635–16440

    Google Scholar 

  63. Weinstock M (1997) Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci Biobehav Rev 21:1–10

    Google Scholar 

  64. Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behavior of the offspring. Prog Neurobiol 65:427–451

    Google Scholar 

  65. Weinstock M, Fride E, Hertzberg R (1988) Prenatal stress effects on functional development of the offspring. Progressive Brain Res 73:319–331

    Google Scholar 

  66. Weinstock M, Matlina E, Maor GI, Rosen H, McEwen BS (1992) Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary-adrenal system in the female rat. Brain Res 595:195–200

    Google Scholar 

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Correspondence to Barbara M. Gutteling.

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Gutteling, B.M., de Weerth, C., Willemsen-Swinkels, S.H.N. et al. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Europ.Child & Adolescent Psych 14, 41–51 (2005). https://doi.org/10.1007/s00787-005-0435-1

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