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Evidence for sex differences in fetal programming of physiological stress reactivity in infancy

Published online by Cambridge University Press:  07 April 2014

Florin Tibu
Affiliation:
University of Manchester
Jonathan Hill*
Affiliation:
University of Manchester
Helen Sharp
Affiliation:
University of Liverpool
Kate Marshall
Affiliation:
University of Manchester
Vivette Glover
Affiliation:
Imperial College London
Andrew Pickles
Affiliation:
King's College London
*
Address correspondence and reprint requests to: Jonathan Hill, Centre for Developmental Science and Disorders, University of Manchester, Room 3.305, Third Floor, Jean McFarlane Building, University Place, Oxford Road, Manchester M13 9PL, UK; E-mail: jonathan.hill@manchester.ac.uk.

Abstract

Associations between low birth weight and prenatal anxiety and later psychopathology may arise from programming effects likely to be adaptive under some, but not other, environmental exposures and modified by sex differences. If physiological reactivity, which also confers vulnerability or resilience in an environment-dependent manner, is associated with birth weight and prenatal anxiety, it will be a candidate to mediate the links with psychopathology. From a general population sample of 1,233 first-time mothers recruited at 20 weeks gestation, a sample of 316 stratified by adversity was assessed at 32 weeks and when their infants were aged 29 weeks (N = 271). Prenatal anxiety was assessed by self-report, birth weight from medical records, and vagal reactivity from respiratory sinus arrhythmia during four nonstressful and one stressful (still-face) procedure. Lower birth weight for gestational age predicted higher vagal reactivity only in girls (interaction term, p = .016), and prenatal maternal anxiety predicted lower vagal reactivity only in boys (interaction term, p = .014). These findings are consistent with sex differences in fetal programming, whereby prenatal risks are associated with increased stress reactivity in females but decreased reactivity in males, with distinctive advantages and penalties for each sex.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2014 

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References

Abel, K. M., Wicks, S., Susser, E. S., Dalman, C., Pedersen, M. G., Mortensen, P. B., et al. (2010). Birth weight, schizophrenia, and adult mental disorder: Is risk confined to the smallest babies? Archives of General Psychiatry, 67, 923930.CrossRefGoogle Scholar
Bangasser, D. A., Curtis, A., Reyes, B. A., Bethea, T. T., Parastatidis, I., Ischiropoulos, H., et al. (2010). Sex differences in corticotropin-releasing factor receptor signaling and trafficking: Potential role in female vulnerability to stress-related psychopathology. Molecular Psychiatry, 15, 877, 896–877, 904.CrossRefGoogle ScholarPubMed
Barker, D. J. (2007). The origins of the developmental origins theory. Journal of Internal Medicine, 261, 412417.CrossRefGoogle ScholarPubMed
Barker, E. D., Jaffee, S. R., Uher, R., & Maughan, B. (2011). The contribution of prenatal and postnatal maternal anxiety and depression to child maladjustment. Depression and Anxiety, 28, 696702.Google Scholar
Beck, J. E., & Shaw, D. S. (2005). The influence of perinatal complications and environmental adversity on boys’ antisocial behavior. Journal of Child Psychology and Psychiatry, 46, 3546.Google Scholar
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271301.CrossRefGoogle ScholarPubMed
Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., & Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144150.Google Scholar
Brennan, P. A., & Raine, A. (1997). Biosocial bases of antisocial behavior: Psychophysiological, neurological, and cognitive factors. Clinical Psychology Review, 17, 589604.Google Scholar
Calkins, S. D., & Dedmon, S. E. (2000). Physiological and behavioral regulation in two-year-old children with aggressive/destructive behavior problems. Journal of Abnormal Child Psychology, 28, 103118.Google Scholar
Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74, 144153.Google Scholar
Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45, 101112.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783804.Google Scholar
Conradt, E., & Ablow, J. (2010). Infant physiological response to the still-face paradigm: Contributions of maternal sensitivity and infants’ early regulatory behavior. Infant Behavior and Development, 33, 251265.CrossRefGoogle Scholar
Costello, E. J., Worthman, C., Erkanli, A., & Angold, A. (2007). Prediction from low birth weight to female adolescent depression: A test of competing hypotheses. Archives of General Psychiatry, 64, 338344.Google Scholar
Curtis, W. J., & Cicchetti, D. (2007). Emotion and resilience: A multilevel investigation of hemispheric electroencephalogram asymmetry and emotion regulation in maltreated and nonmaltreated children. Development and Psychopathology, 19, 811840.CrossRefGoogle ScholarPubMed
de Bruijn, A. T., van Bakel, H. J., & van Baar, A. L. (2009). Sex differences in the relation between prenatal maternal emotional complaints and child outcome. Early Human Development, 85, 319324.CrossRefGoogle ScholarPubMed
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 728.CrossRefGoogle Scholar
Feldman, R., Singer, M., & Zagoory, O. (2010). Touch attenuates infants’ physiological reactivity to stress. Developmental Science, 13, 271278.Google Scholar
Frye, C. A., & Wawrzycki, J. (2003). Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Hormones and Behavior, 44, 319326.Google Scholar
Glover, V. (2011). Prenatal stress and the origins of psychopathology: An evolutionary perspective. Journal of Child Psychology and Psychiatry, 52, 356367.Google Scholar
Glover, V., & Hill, J. (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective. Physiology & Behavior, 106, 736740.Google Scholar
Graham, J. W. (2003). Adding missing-data-relevant variables to FIML-based structural equation models. Structural Equation Modeling, 10, 80100.Google Scholar
Hamlin, J. K., Wynn, K., & Bloom, P. (2007). Social evaluation by preverbal infants. Nature, 450, 557559.CrossRefGoogle ScholarPubMed
Kajantie, E., & Raikkonen, K. (2010). Early life predictors of the physiological stress response later in life. Neuroscience & Biobehavioral Reviews, 35, 2332.Google Scholar
Lehtonen, R., & Pahkinen, E. (2004). Practical methods for the design and analysis of complex surveys (2nd ed.). Chichester: Wiley.Google Scholar
Li, J., Olsen, J., Vestergaard, M., & Obel, C. (2010). Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: A nationwide follow-up study in Denmark. European Child and Adolescent Psychiatry, 19, 747753.Google Scholar
Meaney, M. J., Szyf, M., & Seckl, J. R. (2007). Epigenetic mechanisms of perinatal programming of hypothalamic–pituitary–adrenal function and health. Trends in Molecular Medicine, 13, 269277.Google Scholar
Moffitt, T. E., Caspi, A., Margolin, G., Krueger, R. F., Magdol, L., Silva, P. A., et al. (1997). Do partners agree about abuse in their relationship? A psychometric evaluation of interpartner agreement. Psychological Assessment, 9, 4756.CrossRefGoogle Scholar
Moore, G. A. (2009). Infants’ and mothers’ vagal reactivity in response to anger. Journal of Child Psychology and Psychiatry, 50(11), 13921400.Google Scholar
Moore, G. A. (2010). Parent conflict predicts infants’ vagal regulation in social interaction. Development and Psychopathology, 22, 2333.CrossRefGoogle ScholarPubMed
Moore, G. A., & Calkins, S. D. (2004). Infants’ vagal regulation in the still-face paradigm is related to dyadic coordination of mother–infant interaction. Developmental Psychology, 40, 10681080.Google Scholar
Moore, G. A., Hill-Soderlund, A. L., Propper, C. B., Calkins, S. D., Mills-Koonce, W. R., & Cox, M. J. (2009). Mother–infant vagal regulation in the face-to-face still-face paradigm is moderated by maternal sensitivity. Child Development, 80, 209223.Google Scholar
Muthén, L. K., & Muthén, B. O. (2009). Mplus user's guide (5th ed.). Los Angeles: Author.Google Scholar
Mychasiuk, R., Gibb, R., & Kolb, B. (2011). Prenatal stress produces sexually dimorphic and regionally specific changes in gene expression in hippocampus and frontal cortex of developing rat offspring. Developmental Neuroscience, 33, 531538.CrossRefGoogle ScholarPubMed
Noble, M., Wright, G., Dibben, C., Smith, G., McLennan, D., & Antila, C. (2004). The English Indices of Deprivation 2004 (rev.). Report to the Office of the Deputy Prime Minister. London: Neighbourhood Renewal Unit.Google Scholar
Obradovic, J. (2012). How can the study of physiological reactivity contribute to our understanding of adversity and resilience processes in development? Development and Psychopathology, 24, 371387.Google Scholar
Obradovic, J., Bush, N. R., Stamperdahl, J., Adler, N. E., & Boyce, W. T. (2010). Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Development, 81, 270289.Google Scholar
O'Connor, T. G., Heron, J., Golding, J., Beveridge, M., & Glover, V. (2002). Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. British Journal of Psychiatry, 180, 502508.Google Scholar
O'Connor, T. G., Heron, J., Golding, J., & Glover, V. (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. Journal of Child Psychology and Psychiatry, 44, 10251036.Google Scholar
Pickles, A., Dunn, G., & Vasquez-Barquero, J. L. (1995). Screening for stratification in two-phase epidemiological surveys. Statistical Methods in Medical Research, 4, 7389.Google Scholar
Porges, S. W. (1985). US Patent No. 4,510,944. Washington, DC: US Patent and Trademark Office.Google Scholar
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116143.Google Scholar
Porges, S. W., & Bohrer, R. E. (1990). Analyses of periodic processes in psychophysiological research. In Cacioppo, J. T. & Tassinary, L. G. (Eds.), Principles of psychophysiology: Physical, social, and inferential elements (pp. 708753). New York: Cambridge University Press.Google Scholar
Rodriguez, A., & Bohlin, G. (2005). Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? Journal of Child Psychology and Psychiatry, 46, 246254.CrossRefGoogle ScholarPubMed
Rutter, M., Caspi, A., & Moffitt, T. E. (2003). Using sex differences in psychopathology to study causal mechanisms: Unifying issues and research strategies. Journal of Child Psychology and Psychiatry, 44, 10921115.CrossRefGoogle ScholarPubMed
Schulz, K. M., Pearson, J. N., Neeley, E. W., Berger, R., Leonard, S., Adams, C. E., et al. (2011). Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiology & Behavior, 104, 340347.CrossRefGoogle ScholarPubMed
Seckl, J. R. (2008). Glucocorticoids, developmental “programming” and the risk of affective dysfunction. Progress in Brain Research, 167, 1734.CrossRefGoogle ScholarPubMed
Sharp, H., Pickles, A., Meaney, M., Abbott, K., Tibu, F., & Hill, J. (2012). Frequency of infant stroking reported by mothers moderates the effect of prenatal depression on infant behavioural and physiological outcomes. PLOS One, 7, e45446. doi:10.1371/journal.pone.0045446 Google Scholar
Spielberger, C. D. (1983). Manual for the State–Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Stanley, C., Murray, L., & Stein, A. (2004). The effect of postnatal depression on mother–infant interaction, infant response to the still-face perturbation, and performance on an instrumental learning task. Development and Psychopathology, 16, 118.Google Scholar
Talge, N. M., Neal, C., & Glover, V. (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: How and why? Journal of Child Psychology and Psychiatry, 48, 245261.Google Scholar
Tronick, E. (2006). The inherent stress of normal daily life and social interaction leads to the development of coping and resilience, and variation in resilience in infants and young children: Comments on the papers of Suomi and Klebanov & Brooks-Gunn. Annals of the New York Academy of Sciences, 1094, 83104.Google Scholar
Tronick, E., Als, H., Adamson, L., Wise, S., & Brazelton, T. B. (1978). The infant's response to entrapment between contradictory messages in face-to-face interaction. Journal of the American Academy of Child Psychiatry, 17, 113.Google Scholar
Van den Bergh, B. R., Mulder, E. J., Mennes, M., & Glover, V. (2005). Antenatal maternal anxiety and stress and the neurobehavioral development of the fetus and child: Links and possible mechanisms. Neuroscience & Biobehavioral Reviews, 29, 237258.Google Scholar
Van den Bergh, B. R., Van Calster, B., Smits, T., Van Huffel, S., & Lagae, L. (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology, 33, 536545.Google Scholar
Van Goozen, S. H., Fairchild, G., Snoek, H., & Harold, G. T. (2007). The evidence for a neurobiological model of childhood antisocial behavior. Psychological Bulletin, 133, 149182.Google Scholar
Van Lieshout, R. J., & Boylan, K. (2010). Increased depressive symptoms in female but not male adolescents born at low birth weight in the offspring of a national cohort. Canadian Journal of Psychiatry, 55, 422430.Google Scholar
Warren, S. L., & Simmens, S. J. (2005). Predicting toddler anxiety/depressive symptoms: Effects of caregiver sensitivity on temperamentally vulnerable children. Infant Mental Health Journal, 26, 4055.CrossRefGoogle ScholarPubMed
Weinberg, M. K., Tronick, E. Z., Cohn, J. F., & Olson, K. L. (1999). Gender differences in emotional expressivity and self-regulation during early infancy. Developmental Psychology, 35, 175188.Google Scholar
Weinstock, M. (2007). Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochemical Research, 32, 17301740.Google Scholar
Weinstock, M. (2011). Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: An update. Stress, 14, 604613.Google Scholar
Weisman, O., Zagoory-Sharon, O., & Feldman, R. (2012). Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement. Biological Psychiatry, 72, 982989.Google Scholar
Zagron, G., & Weinstock, M. (2006). Maternal adrenal hormone secretion mediates behavioral alterations induced by prenatal stress in male and female rats. Behavioral Brain Research, 175, 323328.Google Scholar
Zohar, I., & Weinstock, M. (2011). Differential effect of prenatal stress on the expression of cortiocotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats. Journal of Neuroendocrinology, 23, 320328.Google Scholar