Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-28T16:53:49.711Z Has data issue: false hasContentIssue false
  • English
  • Français

Sexually dimorphic and interactive effects of prenatal maternal cortisol and psychological distress on infant cortisol reactivity

Published online by Cambridge University Press:  18 July 2016

Gerald F. Giesbrecht ,
Nicole Letourneau ,
Tavis S. Campbell  and
The Alberta Pregnancy Outcomes and Nutrition Study Team
Gerald F. Giesbrecht*
Affiliation:
University of Calgary
Nicole Letourneau
Affiliation:
University of Calgary
Tavis S. Campbell
Affiliation:
University of Calgary
The Alberta Pregnancy Outcomes and Nutrition Study Team
Affiliation:
University of Calgary
*
Address correspondence and reprint requests to: Gerald F. Giesbrecht, Department of Paediatrics, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

In utero exposure to maternal psychological distress is a risk factor for developmental psychopathology, and these effects are believed to partially occur via dysregulation of the maternal and fetal hypothalamus–adrenal–pituitary axes. Nevertheless, only a few human studies have directly assessed the effects of prenatal cortisol exposure on infant cortisol reactivity, and none have investigated sex differences or potential interactions between prenatal cortisol and psychological distress. Here we report on a prospective longitudinal investigation (N = 236) of in utero exposure to maternal cortisol and distress in a relatively high socioeconomic status and low-risk population to determine whether these exposures interact in their effects on infant (M age = 3.0 months, range = 2.3–5.0 months, 51.9% male) cortisol reactivity and whether there are sex differences in these effects. Results revealed both sexually dimorphic and interactive effects of prenatal cortisol and distress, even after controlling for postnatal distress. In general, blunted reactivity in females was associated with exposure to high maternal distress and flattened patterns of diurnal maternal cortisol, whereas blunted reactivity in males was associated with exposure to steeper morning increases and daytime decreases in maternal cortisol. The findings suggest that sex differences in the effects of prenatal cortisol and distress on infant cortisol reactivity are a plausible mechanism by which maternal experiences during pregnancy contribute to sex differences in the development of psychopathology.

Type
Regular Articles
Information
Development and Psychopathology , Volume 29 , Issue 3 , August 2017 , pp. 805 - 818
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

The authors gratefully acknowledge the participants of the Alberta Pregnancy Outcomes and Nutrition (APrON) study and the support of the APrON Study Team, whose individual members are B. J. Kaplan, C. J. Field, D. Dewey, R. C. Bell, F. P. Bernier, M. Cantell, L. M. Casey, M. Eliasziw, A. Farmer, L. Gagnon, G. F. Giesbrecht, L. Goonewardene, D. W. Johnston, L. Kooistra, N. Letourneau, D. P. Manca, J. W. Martin, L. J. McCargar, M. O'Beirne, V. J. Pop, and N. Singhal. This research was supported by grants from Alberta Innovates Health Solutions; the Canadian Institutes of Health Research; the Alberta Center for Child, Family and Community Research; and generous donors of the Alberta Children's Hospital Foundation. The sources of funding had no role in the study design; in the collection, analysis, or interpretation of data; in writing the manuscript; or in the decision to submit the manuscript for publication.

References

Alexander, N., Rosenlocher, F., Stalder, T., Linke, J., Distler, W., Morgner, J., et al. (2012). Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children. Journal of Clinical Endocrinology and Metabolism, 97, 3538–3544.Google Scholar
Altemus, M., Sarvaiya, N., & Neill Epperson, C. (2014). Sex differences in anxiety and depression clinical perspectives. Frontiers in Neuroendocrinology, 35, 320–330.CrossRefGoogle ScholarPubMed
Azar, R., Paquette, D., Zoccolillo, M., Baltzer, F., & Tremblay, R. E. (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. Biological Psychiatry, 62, 573–579.Google Scholar
Bale, T. L. (2011). Sex differences in prenatal epigenetic programming of stress pathways. Stress, 14, 348–356.CrossRefGoogle ScholarPubMed
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., et al. (2010). Early life programming and neurodevelopmental disorders. Biological Psychiatry, 68, 314–319.CrossRefGoogle ScholarPubMed
Barker, D. J. (2004). Developmental origins of adult health and disease. Journal of Epidemiology and Community Health, 58, 114–115.CrossRefGoogle ScholarPubMed
Bateson, P., Barker, D., Clutton-Brock, T., Deb, D., D'Udine, B., Foley, R. A., et al. (2004). Developmental plasticity and human health. Nature, 430, 419–421.Google Scholar
Bayley, N. (1993). Bayley Scales of Infant Development (2nd ed.). San Antonio, TX: Psycholgical Corporation.Google Scholar
Bergman, K., Sarkar, P., Glover, V., & O'Connor, T. G. (2010). Maternal prenatal cortisol and infant cognitive development: Moderation by infant-mother attachment. Biological Psychiatry, 67, 1026–1032.CrossRefGoogle ScholarPubMed
Bonicatto, S., Dew, M. A., Soria, J. J., & Seghezzo, M. E. (1997). Validity and reliability of Symptom Checklist ‘90 (SCL90) in an Argentine population sample. Social Psychiatry and Psychiatric Epidemiology, 32, 332–338.Google Scholar
Bornstein, M. H. (1989). Sensitive periods in development: Structural characteristics and causal interpretations. Psychology Bulletin, 105, 179–197.Google Scholar
Bosch, N. M., Riese, H., Reijneveld, S. A., Bakker, M. P., Verhulst, F. C., Ormel, J., et al. (2012). Timing matters: Long term effects of adversities from prenatal period up to adolescence on adolescents’ cortisol stress response. The TRAILS study. Psychoneuroendocrinology, 37, 1439–1447.CrossRefGoogle ScholarPubMed
Brand, S. R., Brennan, P. A., Newport, D. J., Smith, A. K., Weiss, T., & Stowe, Z. N. (2010). The impact of maternal childhood abuse on maternal and infant HPA axis function in the postpartum period. Psychoneuroendocrinology, 35, 686–693.CrossRefGoogle ScholarPubMed
Brennan, P. A., Pargas, R., Walker, E. F., Green, P., Newport, D. J., & Stowe, Z. (2008). Maternal depression and infant cortisol: Influences of timing, comorbidity and treatment. Journal of Child Psychology and Psychiatry, 49, 1099–1107.Google Scholar
Burton, G., & Fowden, A. (2012). Review: The placenta and developmental programming: Balancing fetal nutrient demands with maternal resource allocation. Placenta, 33, S23–S27.CrossRefGoogle ScholarPubMed
Buss, C., Entringer, S., Davis, E. P., Hobel, C. J., Swanson, J. M., Wadhwa, P. D., et al. (2012). Impaired executive function mediates the association between maternal pre-pregnancy body mass index and child ADHD symptoms. PLOS ONE, 7, e37758.CrossRefGoogle ScholarPubMed
Clifton, V. L. (2010). Review: Sex and the human placenta: Mediating differential strategies of fetal growth and survival. Placenta, 31(Suppl.), S33–S39.Google Scholar
Coe, C. L., Kramer, M., Czeh, B., Gould, E., Reeves, A. J., Kirschbaum, C., et al. (2003). Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biological Psychiatry, 54, 1025–1034.CrossRefGoogle ScholarPubMed
Cottrell, E. C., & Seckl, J. R. (2009). Prenatal stress, glucocorticoids and the programming of adult disease. Frontiers in Behavioral Neuroscience, 3, 19.CrossRefGoogle ScholarPubMed
Cox, J. L., Holden, J., & Sagovsky, R. (1987). Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. British Journal of Psychiatry, 150, 782–786.CrossRefGoogle ScholarPubMed
Cranford, J. A., Shrout, P. E., Iida, M., Rafaeli, E., Yip, T., & Bolger, N. (2006). A procedure for evaluating sensitivity to within-person change: Can mood measures in diary studies detect change reliably? Personality and Social Psychology Bulletin, 32, 917–929.CrossRefGoogle ScholarPubMed
Davis, E., Glynn, L. M., Waffarn, F., & Sandman, C. A. (2011). Prenatal maternal stress programs infant stress regulation. Journal of Child Psychology and Psychiatry, 52, 119–129.Google Scholar
Davis, E., & Sandman, C. A. (2010). The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Development, 81, 131–148.Google Scholar
Davis, E. P., & Pfaff, D. (2014). Sexually dimorphic responses to early adversity: Implications for affective problems and autism spectrum disorder. Psychoneuroendocrinology, 49, 11–25.Google Scholar
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 1562–1592.CrossRefGoogle ScholarPubMed
Derogatis, L. R. (1994). Symptom Checklist-90—R: Administration, scoring, and procedures manual (Vol. 3). Minneapolis, MN: Pearson.Google Scholar
de Weerth, C., & Buitelaar, J. K. (2005). Physiological stress reactivity in human pregnancy—A review. Neuroscience & Biobehavioral Reviews, 29, 295–312.Google Scholar
de Weerth, C., Buitelaar, J. K., & Beijers, R. (2013). Infant cortisol and behavioral habituation to weekly maternal separations: Links with maternal prenatal cortisol and psychosocial stress. Psychoneuroendocrinology, 38, 2863–2874.Google Scholar
de Weerth, C., Jansen, J., Vos, M. H., Maitimu, I., & Lentjes, E. G. (2007). A new device for collecting saliva for cortisol determination. Psychoneuroendocrinology, 32, 1144–1148.Google Scholar
de Weerth, C., Wied, G. D., Jansen, L. M., & Buitelaar, J. K. (2007). Cardiovascular and cortisol responses to a psychological stressor during pregnancy. Acta Obstetricia et Gynecologica Scandinavica, 86, 1181–1192.CrossRefGoogle ScholarPubMed
DiPietro, J. A. (2012). Maternal stress in pregnancy: Considerations for fetal development. Journal of Adolescent Health, 51(Suppl. 2), S3–S8.CrossRefGoogle ScholarPubMed
DiPietro, J. A., Costigan, K. A., Kivlighan, K. T., Chen, P., & Laudenslager, M. L. (2011). Maternal salivary cortisol differs by fetal sex during the second half of pregnancy. Psychoneuroendocrinology, 36, 588–591.CrossRefGoogle ScholarPubMed
DiPietro, J. A., Kivlighan, K. T., Costigan, K. A., & Laudenslager, M. L. (2009). Fetal motor activity and maternal cortisol. Developmental Psychobiology, 51, 505–512.CrossRefGoogle ScholarPubMed
DiPietro, J. A., Novak, M. F., Costigan, K. A., Atella, L. D., & Reusing, S. P. (2006). Maternal psychological distress during pregnancy in relation to child development at age two. Child Development, 77, 573–587.Google Scholar
Doyle, C., Werner, E., Feng, T., Lee, S., Altemus, M., Isler, J. R., et al. (2015). Pregnancy distress gets under fetal skin: Maternal ambulatory assessment & sex differences in prenatal development. Developmental Psychobiology, 57, 607–625.CrossRefGoogle ScholarPubMed
Ellis, B. J., & Del Giudice, M. (2013). Beyond allostatic load: Rethinking the role of stress in regulating human development. Development and Psychopathology. Advance online pubilcation.Google ScholarPubMed
Emack, J., Kostaki, A., Walker, C. D., & Matthews, S. G. (2008). Chronic maternal stress affects growth, behaviour and hypothalamo-pituitary-adrenal function in juvenile offspring. Hormones and Behavior, 54, 514–520.CrossRefGoogle ScholarPubMed
Fekedulegn, D. B., Andrew, M. E., Burchfiel, C. M., Violanti, J. M., Hartley, T. A., Charles, L. E., et al. (2007). Area under the curve and other summary indicators of repeated waking cortisol measurements. Psychosomatic Medicine, 69, 651–659.CrossRefGoogle ScholarPubMed
Giesbrecht, G. F., Campbell, T., & Letourneau, N. (2015). Sexually dimorphic adaptations in basal maternal stress physiology during pregnancy and implications for fetal development. Psychoneuroendocrinology, 56, 168–178.CrossRefGoogle ScholarPubMed
Giesbrecht, G. F., Campbell, T., Letourneau, N., & Kaplan, B. J. (2013). Advancing gestation does not attenuate biobehavioural coherence between psychological distress and cortisol. Biological Psychology, 93, 45–51.CrossRefGoogle Scholar
Giesbrecht, G. F., Campbell, T., Letourneau, N., Kooistra, L., & Kaplan, B. J. (2012). Psychological distress and salivary cortisol covary within persons during pregnancy. Psychoneuroendocrinology, 37, 270–279.CrossRefGoogle ScholarPubMed
Gitau, R., Cameron, A., Fisk, N. M., & Glover, V. (1998). Fetal exposure to maternal cortisol. Lancet, 352, 707–708.Google Scholar
Gitau, R., Fisk, N. M., Teixeira, J. M., Cameron, A., & Glover, V. (2001). Fetal hypothalamic-pituitary-adrenal stress responses to invasive procedures are independent of maternal responses. Journal of Clinical Endocrinology and Metabolism, 86, 104–109.Google ScholarPubMed
Glover, V., Miles, R., Matta, S., Modi, N., & Stevenson, J. (2005). Glucocorticoid exposure in preterm babies predicts saliva cortisol response to immunization at 4 months. Pediatric Research, 58, 1233–1237.CrossRefGoogle ScholarPubMed
Gluckman, P. D., Hanson, M. A., Bateson, P., Beedle, A. S., Law, C. M., Bhutta, Z. A., et al. (2009). Towards a new developmental synthesis: Adaptive developmental plasticity and human disease. Lancet, 373, 1654–1657.Google Scholar
Granger, D. A., Hibel, L. C., Fortunato, C. K., & Kapelewski, C. H. (2009). Medication effects on salivary cortisol: Tactics and strategy to minimize impact in behavioral and developmental science. Psychoneuroendocrinology, 34, 1437–1448.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 13, 515–538.Google Scholar
Gutteling, B., de Weerth, C., & Buitelaar, J. (2005). Prenatal stress and children's cortisol reaction to the first day of school. Psychoneuroendocrinology, 30, 541–549.CrossRefGoogle Scholar
Gutteling, B. M., de Weerth, C., & Buitelaar, J. K. (2004). Maternal prenatal stress and 4- to 6-year-old children's salivary cortisol concentrations pre- and post-vaccination. Stress, 7, 257–260.Google Scholar
Harris, A., & Seckl, J. (2011). Glucocorticoids, prenatal stress and the programming of disease. Hormones and Behavior, 59, 279–289.Google Scholar
Hesketh, T., & Xing, Z. W. (2006). Abnormal sex ratios in human populations: Causes and consequences. Proceedings of the National Academy of Sciences, 103, 13271–13275.Google Scholar
Holi, M. M., Sammallahti, P. R., & Aalberg, V. A. (1998). A Finnish validation study of the SCL-90. Acta Psychiatrica Scandinavica, 97, 42–46.CrossRefGoogle ScholarPubMed
Jacobs, N., Myin-Germeys, I., Derom, C., Delespaul, P., van Os, J., & Nicolson, N. A. (2007). A momentary assessment study of the relationship between affective and adrenocortical stress responses in daily life. Biological Psychology, 74, 60–66.CrossRefGoogle ScholarPubMed
Jomeen, J., & Martin, C. (2007). Replicability and stability of the multidimensional model of the Edinburgh Postnatal Depression Scale in late pregnancy. Journal of Psychiatric and Mental Health Nursing, 14, 319–324.Google Scholar
Karlen, J., Frostell, A., Theodorsson, E., Faresjo, T., & Ludvigsson, J. (2013). Maternal influence on child HPA axis: A prospective study of cortisol levels in hair. Pediatrics, 132, e1333–e1340.Google Scholar
Khashan, A. S., McNamee, R., Henriksen, T. B., Pedersen, M. G., Kenny, L. C., Abel, K. M., et al. (2011). Risk of affective disorders following prenatal exposure to severe life events: A Danish population-based cohort study. Journal of Psychiatric Research, 45, 879–885.Google Scholar
Kristjansson, S. D., Kircher, J. C., & Webb, A. K. (2007). Multilevel models for repeated measures research designs in psychophysiology: An introduction to growth curve modeling. Psychophysiology, 44, 728–736.CrossRefGoogle ScholarPubMed
Laplante, D. P., Barr, R. G., Brunet, A., Galbaud du Fort, G., Meaney, M. L., Saucier, J. F., et al. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research, 56, 400–410.Google Scholar
Laurent, H. K., Leve, L. D., Neiderhiser, J. M., Natsuaki, M. N., Shaw, D. S., Harold, G. T., et al. (2013). Effects of prenatal and postnatal parent depressive symptoms on adopted child HPA regulation: Independent and moderated influences. Developmental Psychology, 49, 876–886.Google Scholar
Llabre, M. M., Spitzer, S., Siegel, S., Saab, P. G., & Schneiderman, N. (2004). Applying latent growth curve modeling to the investigation of individual differences in cardiovascular recovery from stress. Psychosomatic Medicine, 66, 29–41.CrossRefGoogle Scholar
McNair, D. M., & Heuchert, P. (2007). Profile of Mood States: POMS: Technical update. Toronto: Multi-Health Systems.Google Scholar
Mericq, V., Medina, P., Kakarieka, E., Marquez, L., Johnson, M. C., & Iniguez, G. (2009). Differences in expression and activity of 11beta-hydroxysteroid dehydrogenase type 1 and 2 in human placentas of term pregnancies according to birth weight and gender. European Journal of Endocrinology, 161, 419–425.Google Scholar
Mina, T. H., & Reynolds, R. M. (2014). Mechanisms linking in utero stress to altered offspring behavior. Current Topics in Behavioral Neuroscience, 18, 93–122.Google Scholar
Morgan, C. D., Wiederman, M. W., & Magnus, R. D. (1998). Discriminant validity of the SCL-90 dimensions of anxiety and depression. Assessment, 5, 197–201.Google Scholar
Nierop, A., Bratsikas, A., Klinkenberg, A., Nater, U. M., Zimmermann, R., & Ehlert, U. (2006). Prolonged salivary cortisol recovery in second-trimester pregnant women and attenuated salivary alpha-amylase responses to psychosocial stress in human pregnancy. Journal of Clinical Endocrinology and Metabolism, 91, 1329–1335.Google Scholar
Obel, C., Hedegaard, M., Henriksen, T. B., Secher, N. J., Olsen, J., & Levine, S. (2005). Stress and salivary cortisol during pregnancy. Psychoneuroendocrinology, 30, 647–656.Google Scholar
O'Connor, T. G., Ben-Shlomo, Y., Heron, J., Golding, J., Adams, D., & Glover, V. (2005). Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biological Psychiatry, 58, 211–217.Google Scholar
O'Connor, T. G., Bergman, K., Sarkar, P., & Glover, V. (2013). Prenatal cortisol exposure predicts infant cortisol response to acute stress. Developmental Psychobiology, 55, 145–155.CrossRefGoogle ScholarPubMed
O'Donnell, K. J., Bugge Jensen, A., Freeman, L., Khalife, N., O'Connor, T. G., & Glover, V. (2012). Maternal prenatal anxiety and downregulation of placental 11beta-HSD2. Psychoneuroendocrinology, 37, 818–826.CrossRefGoogle ScholarPubMed
Okun, M. L., Krafty, R. T., Buysse, D. J., Monk, T. H., Reynolds III, C. F., Begley, A., et al. (2010). What constitutes too long of a delay? Determining the cortisol awakening response (CAR) using self-report and PSG-assessed wake time. Psychoneuroendocrinology, 35, 460–468.CrossRefGoogle ScholarPubMed
Preacher, K. J., Curran, P. J., & Bauer, D. J. (2006). Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31, 437–448.CrossRefGoogle Scholar
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916–931.Google Scholar
Saif, Z., Hodyl, N. A., Stark, M. J., Fuller, P. J., Cole, T., Lu, N., et al. (2015). Expression of eight glucocorticoid receptor isoforms in the human preterm placenta vary with fetal sex and birthweight. Placenta, 36, 723–730.Google Scholar
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2013). Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. Journal of Psychosomatic Research, 75, 327–335.Google Scholar
Sandovici, I., Hoelle, K., Angiolini, E., & Constância, M. (2012). Placental adaptations to the maternal-fetal environment: Implications for fetal growth and developmental programming. Reproductive Biomedicine Online, 25, 68–89.Google Scholar
Scholtz, W., & Phillips, D. I. (2009). Fetal orgins of mental health: Evidence and mechanisms. Brain, Behavior, and Immunity, 23, 905–916.Google Scholar
Seckl, J. R. (2008). Glucocorticoids, developmental “programming” and the risk of affective dysfunction. Progress in Brain Research, 167, 17–34.Google Scholar
Stinson, L. J., Stroud, L. R., Buka, S. L., Eaton, C. B., Lu, B., Niaura, R., et al. (2015). Prospective evaluation of associations between prenatal cortisol and adulthood coronary heart disease risk: The New England family study. Psychosomatic Medicine, 77, 237–245.Google Scholar
Szuran, T. F., Pliska, V., Pokorny, J., & Welzl, H. (2000). Prenatal stress in rats: Effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiology & Behavior, 71, 353–362.Google Scholar
Tabachnick, B., & Fidell, L. (2012). Using multivariate statistics: International edition. Needham Heights, MA: Pearson.Google Scholar
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639.Google Scholar
Tollenaar, M. S., Beijers, R., Jansen, J., Riksen-Walraven, J. M., & de Weerth, C. (2011). Maternal prenatal stress and cortisol reactivity to stressors in human infants. Stress, 14, 53–65.CrossRefGoogle ScholarPubMed
Van den Bergh, B. R., Van Calster, B., Pinna Puissant, S., & Van Huffel, S. (2008). Self-reported symptoms of depressed mood, trait anxiety and aggressive behavior in post-pubertal adolescents: Associations with diurnal cortisol profiles. Hormones and Behavior, 54, 253–257.Google Scholar
Vedhara, K., Metcalfe, C., Brant, H., Crown, A., Northstone, K., Dawe, K., et al. (2012). Maternal mood and neuroendocrine programming: Effects of time of exposure and sex. Journal of Neuroendocrinology, 24, 999–1011.Google Scholar
Weaver, I. C. (2009). Shaping adult phenotypes through early life environments. Birth Defects Research, 87C, 314–326.CrossRefGoogle Scholar
Weinstock, M. (2001). Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Progress in Neurobiology, 65, 427–451.Google Scholar
Welberg, L. A., & Seckl, J. R. (2001). Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology, 13, 113–128.Google Scholar
Wust, S., Wolf, J., Hellhammer, D. H., Federenko, I., Schommer, N., & Kirschbaum, C. (2000). The cortisol awakening response-normal values and confounds. Noise and Health, 2, 79.Google Scholar
Yehuda, R., Engel, S. M., Brand, S. R., Seckl, J., Marcus, S. M., & Berkowitz, G. S. (2005). Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. Journal of Clinical Endocrinology and Metabolism, 90, 4115–4118.CrossRefGoogle Scholar
Yong Ping, E., Laplante, D. P., Elgbeili, G., Hillerer, K. M., Brunet, A., O'Hara, M. W., et al. (2015). Prenatal maternal stress predicts stress reactivity at 2(1/2) years of age: The Iowa Flood Study. Psychoneuroendocrinology, 56, 62–78.Google Scholar
Zijlmans, M. A., Riksen-Walraven, J. M., & de Weerth, C. (2015). Associations between maternal prenatal cortisol concentrations and child outcomes: A systematic review. Neuroscience & Biobehavioral Reviews, 53, 1–24.Google Scholar