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
Achenbach TM (1991) Manual for the Child Behavior Checklist 2–3 and 1992 Profile. Burlington: University of Vermont
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
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
Alonso SJ, Navarro E, Rodriguez M (1994) Permanent dopaminergic alterations in the nucleus accumbens after prenatal stress. Pharmacol Biochem Behav 49:353–358
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
Barker DJP (1994a) Mothers, babies, and disease in later life. BMJ Publishing Group, London
Barker DJP (1994b) Mothers, babies and health in later life. Churchill Livingstone, Edinburgh
Bates JE, Freeland CA, Lounsbury ML (1979) Measurement of infant difficultness. Child Development 50:794–803
Bayley N (1969) Bayley Scales of Infant Development. Psychological Corp, New York
Burks N, Martin B (1985) Everyday problems and life change events: ongoing versus acute sources of stress. J Hum Stress spring 11:27–35
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
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
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
Dahlof LG, Hard E, Larsson K (1978) Influence of maternal stress on the development of the fetal genital system. Physiol Behav 20:193–195
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
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
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
Goldberg DP (1972) The detection of psychiatric illness by questionnaire. Oxford University Press, London
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
Huizink AC (2000) Prenatal stress and its effect on infant development. PhD. Thesis, Utrecht University, the Netherlands
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
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
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
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
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
Koeter MWJ, Ormel J (1991) General Health Questionnaire. Nederlandse bewerking. Swets test services, The Netherlands
Kohnstamm GA (1984) Bates’ Infant Characteristics Questionnaire (ICQ) in the Netherlands. Eric Reports 251:179
Kuvacic I, Skrablin S, Hodzic D, Milkovic G (1996) Possible influence of expatriation on perinatal outcome. Acta Obstet Gynecol Scand 75:367–371
Lazarus RS, Folkman S (1984) Stress, Appraisal, and Coping. Springer, New York
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
Mesman J, Koot HM (2001) Early preschool predictors of preadolescent internalizing and externalizing DSMIV diagnoses. J Am Acad Child Adolesc Psychiatry 40:1029–1036
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
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
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
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
Orlebeke JC, Knol DL, Verhulst FC (1999) Child behavior problems increased by maternal smoking during pregnancy. Arch Environ Health 54:15–19
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
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
Peters DA (1982) Prenatal stress: effects on brain biogenic amine and plasma corticosterone levels. Pharmacol Biochem Behav 31:839–943
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
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
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
Schneider ML (1992a) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Devel Psychobiol 25:529–540
Schneider ML (1992b) Delayed object permanence development in prenatally stressed rhesus monkey infants (Macaca mulatta). Occup Ther J Res 12:96–110
Schneider ML, Coe CL (1993) Repeated social stress during pregnancy impairs neuromotor development of the primate infant. J Devel Behav Pediatr 14:81–87
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
Secco ML, Moffatt ME (2003) Situational, maternal, and infant influences on parenting stress among adolescent mothers. Issues Compr Pediatr Nurs 26:103–122
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
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
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
Takahashi LK (1994) Stimulus control of behavioral inhibition in the preweanling rat. Physiol Behav 55:717–721
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
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
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
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
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
Van der Meulen BF, Smrkovsky M (1983) BOS 2–30. Bayley ontwikkelingsschalen: handleiding. Swets and Zeitlinger BV, Lisse, The Netherlands
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
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
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
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
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
Weinstock M (1997) Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci Biobehav Rev 21:1–10
Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behavior of the offspring. Prog Neurobiol 65:427–451
Weinstock M, Fride E, Hertzberg R (1988) Prenatal stress effects on functional development of the offspring. Progressive Brain Res 73:319–331
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
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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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DOI: https://doi.org/10.1007/s00787-005-0435-1