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The role of HPA-axis function during pregnancy in the intergenerational transmission of maternal adverse childhood experiences to child behavior problems

Published online by Cambridge University Press:  03 March 2020

Jenna C. Thomas-Argyriou
Department of Psychology, University of Calgary, Calgary, AB, Canada Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada
Nicole Letourneau
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada Faculty of Nursing & Cumming School of Medicine (Pediatrics, Psychiatry & Community Health Sciences), University of Calgary, Calgary, AB, Canada
Deborah Dewey
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada Department of Pediatrics, University of Calgary, Calgary, AB, Canada Department of Community Health Sciences, University of Calgary, Calgary, AB, Canada
Tavis S. Campbell
Department of Psychology, University of Calgary, Calgary, AB, Canada
Gerald F. Giesbrecht*
Department of Psychology, University of Calgary, Calgary, AB, Canada Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada Department of Pediatrics, University of Calgary, Calgary, AB, Canada Department of Community Health Sciences, University of Calgary, Calgary, AB, Canada
Author for Correspondence: Gerald F. Giesbrecht, PhD, Department of Pediatrics, University of Calgary Child Development Center, #355, 3820–24 Ave, NW, Calgary, AB, Canada, T3B 2X9; E-mail:


The current study aimed to understand the mediating and/or moderating role of prenatal hypothalamic–pituitary–adrenal (HPA) axis function in the association between maternal adverse childhood experiences (ACEs) and child internalizing and externalizing behavior problems at age 4. The influence of timing and child sex were also explored. Participants were 248 mother–child dyads enrolled in a prospective longitudinal cohort study (the Alberta Pregnancy Outcomes and Nutrition Study). Maternal ACEs were retrospectively assessed while maternal self-reported depression and diurnal salivary cortisol were assessed prospectively at 6–26 weeks gestation (T1) and 27–37 weeks gestation (T2). Maternal report of child internalizing and externalizing problems was assessed at 4 years (T3). Results revealed that there was a negative indirect association between maternal ACEs and child internalizing behavior via a higher maternal cortisol awakening response (CAR). Maternal diurnal cortisol slope moderated the association between maternal ACEs and child behavior problems. Some of these effects were dependent on child sex, such that higher ACEs and a flatter diurnal slope at T1 was associated with more internalizing behavior in female children and more externalizing behavior in male children. There were timing effects such that the mediating and moderating effects were strongest at T1.

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Adam, E. K., Quinn, M. E., Tavernier, R., McQuillan, M. T., Dahlke, K. A., & Gilbert, K. E. (2017). Diurnal cortisol slopes and mental and physical health outcomes: A systematic review and meta-analysis. Psychoneuroendocrinology, 83, 2541. ScholarPubMed
Ahnert, L., Gunnar, M. R., Lamb, M. E., Barthel, M., Anhert, L., Gunnar, M. R., … Barthel, M. (2004). Transition to child care: Associations with infant-mother attachment, infant negative emotion, and cortisol elevations. Child Development, 75, 639650. ScholarPubMed
Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage Publications.Google Scholar
Altemus, M., Sarvaiya, N., & Neill Epperson, C. (2014). Sex differences in anxiety and depression clinical perspectives. Frontiers in Neuroendocrinology, 35, 320330. ScholarPubMed
Anda, R. F., Croft, J. B., Felitti, V. J., Nordenberg, D., Giles, W. H., Williamson, D. F., & Giovano, G. A. (1999). Adverse childhood experiences and smoking during adolescence and adulthood. Journal of the American Medical Association, 282, 16521658. ScholarPubMed
Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, C., Perry, B. D., … Giles, W. H. (2006). The enduring effects of abuse and related adverse experiences in childhood: A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience, 256, 174186. ScholarPubMed
Arpi, E., & Ferrari, F. (2013). Preterm birth and behavior problems in infants and preschool-age children: A review of the recent literature. Developmental Medicine and Child Neurology, 55, 788796. ScholarPubMed
Bale, T. L. (2011). Sex differences in prenatal epigenetic programming of stress pathways. Stress, 14, 348356. ScholarPubMed
Barker, D. J. (1995). Fetal origins of coronary heart disease. BMJ, 311, 171174. ScholarPubMed
Barker, D. J. (1998). In utero programming of chronic disease. Clinical Science, 95, 115128. ScholarPubMed
Barker, D. J., Osmond, C., Kajantie, E., & Eriksson, J. G. (2009). Growth and chronic disease: Findings in the Helsinki Birth Cohort. Annals of Human Biology, 36, 445458. ScholarPubMed
Barnett, B. E., Hanna, B., & Parker, G. (1983). Life event scales for obstetric groups. Journal of Psychosomatic Research, 27, 313320. ScholarPubMed
Beijers, R., Buitelaar, J. K., & de Weerth, C. (2014). Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: Beyond the HPA axis. European Journal of Child and Adolescent Psychiatry, 23, 943956. ScholarPubMed
Bergink, V., Kooistra, L., Lambregste-van den Berg, M. P., Wijnen, H., Bunevicius, R., van Baar, A., & Pop, V. (2011). Validation of the Edinburgh Depression Scale during pregnancy. Journal of Psychosomatic Research, 70, 385389. ScholarPubMed
Bergman, K., Sarkar, P., O'Connor, T. G., Modi, N., & Glover, V. (2007). Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. Journal of the American Academy of Child and Adolescent Psychiatry, 46, 14541463. ScholarPubMed
Bhagwagar, Z., Hafizi, S., & Cowen, P. J. (2005). Increased salivary cortisol after waking in depression. Psychopharmacology, 182, 5457. ScholarPubMed
Bøe, T., Sivertsen, B., Heiervang, E., Goodman, R., Lundervold, A. J., & Hysing, M. (2014). Socioeconomic status and child mental health: The role of parental emotional well-being and parenting practices. Journal of Abnormal Child Psychology, 42, 705715. ScholarPubMed
Böhmelt, A. H., Nater, U. M., Franke, S., Hellhammer, D. H., & Ehlert, U. (2005). Basal and stimulated hypothalamic–pituitary–adrenal axis activity in patients with functional gastrointestinal disorders and healthy controls. Psychosomatic Medicine, 67, 288294. ScholarPubMed
Bolten, M. I., Wurmser, H., Buske-Kirschbaum, A., Papousek, M., Pirke, K. M., & Hellhammer, D. (2011). Cortisol levels in pregnancy as a psychobiological predictor for birth weight. Archives of Women's Mental Health, 14, 3341. 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, 332338. Scholar
Braithwaite, E. C., Pickles, A., Sharp, H., Glover, V., O'Donnell, K. J., Tibu, F., & Hill, J. (2017). Maternal prenatal cortisol predicts infant negative emotionality in a sex-dependent manner. Physiology & Behavior, 175, 3136. Scholar
Bruskas, D., & Tessin, D. H. (2013). Adverse childhood experiences and psychosocial well-being of women who were in foster care as children. The Permanente Journal, 17, e131e141. Scholar
Bublitz, M. H., Parade, S., & Stroud, L. R. (2014). The effects of childhood sexual abuse on cortisol trajectories in pregnancy are moderated by current family functioning. Biological Psychology, 103, 152157. ScholarPubMed
Bublitz, M. H., & Stroud, L. R. (2012). Childhood sexual abuse is associated with cortisol awakening response over pregnancy: Preliminary findings. Psychoneuroendocrinology, 37, 14251430. ScholarPubMed
Bublitz, M. H., & Stroud, L. R. (2013). Maternal history of child abuse moderates the association between daily stress and diurnal cortisol in pregnancy: A pilot study. Stress, 16, 706710. ScholarPubMed
Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012). Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences of the United States of America, 109, E1312E1319. ScholarPubMed
Buss, C., Entringer, S., Reyes, J. F., Chicz-DeMet, A., Sandman, C. A., Waffarn, F., & Wadhwa, P. D. (2009). The maternal cortisol awakening response in human pregnancy is associated with the length of gestation. American Journal of Obstetrics and Gynecology, 20, 398.e1398.e8. Scholar
Cassidy, J. (1994). Emotion regulation: Influences of attachment relationships. Monographs of the Society for Research in Child Development, 59, 228249. ScholarPubMed
Chen, P. J., Chou, C. C., Yang, L., Tsai, Y. L., Chang, Y. C., & Liaw, J. J. (2017). Effects of aromatherapy massage on pregnant women's stress and immune function: A longitudinal, prospective, randomized controlled trial. Journal of Alternative and Complementary Medicine, 23, 778786. Scholar
Christiaens, I., Hegadoren, K., & Olson, D. M. (2015). Adverse childhood experiences are associated with spontaneous preterm birth: A case–control study. BMC Medicine, 13, 124. ScholarPubMed
Cohen, S., Doyle, W. J., & Baum, A. (2006). Socioeconomic status is associated with stress hormones. Psychosomatic Medicine, 68, 414420. ScholarPubMed
Cowen, P. J. (2010). Not fade away: The HPA axis and depression. Psychological Medicine, 40, 14. ScholarPubMed
Cox, J. L., Holden, J. M., & Sagovsky, R. (1987). Detection of postnatal depression. Development of the 10-item Edinburgh postnatal depression scale. The British Journal of Psychiatry, 150, 782786. ScholarPubMed
Crick, N. R., & Zahn-Waxler, C. (2003). The development of psychopathology in females and males: Current progress and future challenges. Development and Psychopathology, 15, 719742. ScholarPubMed
Davis, E. P., Glynn, L. M., Dunkel Schetter, C., Hobel, C., Chicz-DeMet, A., & Sandman, C. A. (2007). Prenatal exposure to maternal depression and cortisol influences infant temperament. Journal of the American Academy of Child and Adolescent Psychiatry, 46, 737746. ScholarPubMed
Davis, E. P., & 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, 131–48. ScholarPubMed
Davis, E. P., & Sandman, C. A. (2012). Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology, 37, 12241233. ScholarPubMed
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 15621592. ScholarPubMed
Derogatis, L. R. (1992). SCL-90-R Administration, Scoring, and Procedures Manual-II. Towson, MD: Clinical Psychometric Research.Google Scholar
Deuschle, M., Hendlmeier, F., Witt, S., Rietschel, M., Gilles, M., Sánchez-Guijo, A., … Hellweg, R. (2018). Cortisol, cortisone, and BDNF in amniotic fluid in the second trimester of pregnancy: Effect of early life and current maternal stress and socioeconomic status. Development and Psychopathology, 30, 971980. ScholarPubMed
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, 28632874. ScholarPubMed
de Weerth, C., van Hees, Y., & Buitelaar, J. K. (2003). Prenatal maternal cortisol levels and infant behavior during the first 5 months. Early Human Development, 74, 139151. 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, 573587. ScholarPubMed
Dong, M., Giles, W. H., Felitti, V. J., Dube, S. R., Williams, J. E., Chapman, D. P., & Anda, R. F. (2004). Insights into causal pathways for ischemic heart disease: Adverse childhood experiences study. Circulation, 110, 17611766. ScholarPubMed
Dozier, M., Peloso, E., Lewis, E., Laurenceau, J. P., & Levine, S. (2008). Effects of an attachment-based intervention on the cortisol production of infants and toddlers in foster care. Development and Psychopathology, 20, 845859. ScholarPubMed
Dube, S. R., Anda, R. F., Felitti, V. J., Edwards, V. J., & Croft, J. B. (2002). Adverse childhood experiences and personal alcohol abuse as an adult. Addictive Behaviors, 27, 713725. ScholarPubMed
Dube, S. R., Felitti, V., Dong, M., Chapman, D. P., Giles, W. H., & Anda, R. F. (2003). Childhood abuse, neglect and household dysfunction and the risk of illicit drug use: The adverse childhood experiences study. Pediatrics, 111, 564572. ScholarPubMed
Dube, S. R., Williamson, D. F., Thompson, T., Felitti, V. J., & Anda, R. F. (2004). Assessing the reliability of retrospective reports of adverse childhood experiences among adult HMO members attending a primary care clinic. Child Abuse & Neglect, 28, 729737. ScholarPubMed
Ehlert, U., Gaab, J., & Heinrichs, M. (2001). Psychoneuroendocrinological contributions to the etiology of depression, posttraumatic stress disorder, and stress-related bodily disorders: The role of the hypothalamus–pituitary–adrenal axis. Biological Psychology, 57, 141152. ScholarPubMed
Ellman, L. M., Schetter, C. D., Hobel, C. J., Chicz-Demet, A., Glynn, L. M., & Sandman, C. A. (2008). Timing of fetal exposure to stress hormones: Effects on newborn physical and neuromuscular maturation. Developmental Psychobiology, 50, 232241.; 10.1002/dev.20293CrossRefGoogle ScholarPubMed
Fekedulegn, D. B., Andrew, M. E., Burchfiel, C. M., Violanti, J. M., Hartley, T. A., Charles, L. E., & Miller, D. B. (2007). Area under the curve and other summary indicators of repeated waking cortisol measurements. Psychosomatic Medicine, 69, 651659. ScholarPubMed
Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., … Marks, J. S. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. American Journal of Preventive Medicine, 14, 245258. ScholarPubMed
Fisher, P. A., Stoolmiller, M., Gunnar, M. R., & Burraston, B. O. (2007). Effects of a therapeutic intervention for foster preschoolers on diurnal cortisol activity. Psychoneuroendocrinology, 32, 892905. ScholarPubMed
Fisher, P. A., Van Ryzin, M. J., & Gunnar, M. R. (2011). Mitigating HPA axis dysregulation associated with placement changes in foster care. Psychoneuroendocrinology, 36, 531539. ScholarPubMed
Fries, E., Dettenborn, L., & Kirschbaum, C. (2009). The cortisol awakening response (CAR): Facts and future directions. International Journal of Psychophysiology, 72, 6773. ScholarPubMed
Geiss, A., Varadi, E., Steinbach, K., Bauer, H. W., & Anton, F. (1997). Psychoneuroimmunological correlates of persisting sciatic pain in patients who underwent discectomy. Neuroscience Letters, 237, 6568.CrossRefGoogle ScholarPubMed
Gelaye, B., & Koenen, K. C. (2018). The intergenerational impact of prenatal stress: Time to focus on prevention? Biological Psychiatry, 83, 9293. ScholarPubMed
Giesbrecht, G. F., Letourneau, N., & Campbell, T. S. (2017). Sexually dimorphic and interactive effects of prenatal maternal cortisol and psychological distress on infant cortisol reactivity. Development and Psychopathology, 29, 805818. ScholarPubMed
Glynn, L. M., & Baram, T. Z. (2019). The influence of unpredictable, fragmented parental signals on the developing brain. Frontiers in Neuroendocrinology, 53, 100736. doi:10.1016/j.yfrne.2019.01.002CrossRefGoogle ScholarPubMed
Glynn, L. M., & Sandman, C. A. (2012). Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Developmental Science, 15, 601610. ScholarPubMed
Gonzalez, A., Jenkins, J. M., Steiner, M., & Fleming, A. S. (2009). The relation between early life adversity, cortisol awakening response and diurnal salivary cortisol levels in postpartum women. Psychoneuroendocrinology, 34, 7686. ScholarPubMed
Grabow, A. P., Khurana, A., Natsuaki, M. N., Neiderhiser, J. M., Harold, G. T., Shaw, D. S., … Leve, L. D. (2017). Using an adoption-biological family design to examine associations between maternal trauma, maternal depressive symptoms, and child internalizing and externalizing behaviors. Development and Psychopathology, 29, 17071720. ScholarPubMed
Graham, A. M., Rasmussen, J. M., Entringer, S., Ward, E. B., Rudolph, M. D., Gilmore, J. H., … Buss, C. (2019). Maternal cortisol concentrations during pregnancy and sex-specific associations with neonatal amygdala connectivity and emerging internalizing behaviors. Biological Psychiatry, 85, 172181. ScholarPubMed
Gustafsson, H., Doyle, C., Gilchrist, M., Werner, E., & Monk, C. (2017). Maternal abuse history and reduced fetal heart rate variability: Abuse-related sleep disturbance is a mediator. Development and Psychopathology, 29, 10231034. ScholarPubMed
Hales, C. N., & Barker, D. J. P. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia, 35, 595601.CrossRefGoogle ScholarPubMed
Hayes, A. F. (2012). PROCESS: A versatile computational tool for observed variable mediation, moderation, and conditional process modeling. Retrieved from Scholar
Hayes, A. F., & Preacher, K. J. (2013). Conditional process modeling: Using structural equation modeling to examine contingent causal processes. In Hancock, G. R. & Mueller, R. O. (Eds.), Structural equation modeling: A second course (2nd ed., pp. 219266). Charlotte, NC: Information Age Publishing.Google Scholar
Holi, M. M., Sammallahti, P. R., & Aalberg, V. A. (1998). A Finnish validation study of the SCL-90. Acta Psychiatrica Scandinavica, 97, 4246. ScholarPubMed
Huizink, A. C., Mulder, E. J. H., & Buitelaar, J. K. (2004). Prenatal stress and risk for psychopathology: Specific effects or induction of general susceptibility? Psychological Bulletin, 130, 115142. ScholarPubMed
Johnson, P. O., & Neyman, J. (1936). Tests of certain linear hypotheses and their application to some educational problems. Statistical Research Memoirs, 1, 5793.Google Scholar
Jomeen, J., & Martin, C. R. (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, 319324. ScholarPubMed
Kaplan, B. J., Giesbrecht, G. F., Leung, B. M. L., Field, C. J., Dewey, D., Bell, R. C., … APrON Study Team. (2014). The Alberta Pregnancy Outcomes and Nutrition (APrON) cohort study: Rationale and methods. Maternal & Child Nutrition, 10, 4460. ScholarPubMed
Kessler, R. C., McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., … Williams, D. R. (2010). Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. The British Journal of Psychiatry, 197, 378385. ScholarPubMed
King, S. M., Iacono, W. G., & McGue, M. (2004). Childhood externalizing and internalizing psychopathology in the prediction of early substance use. Addiction, 99, 15481559. ScholarPubMed
Kwon, E. J., & Kim, Y. J. (2017). What is fetal programming?: A lifetime health is under the control of in utero health. Obstetric and Gynecological Science, 60, 506519. ScholarPubMed
Laurent, H. K., Ablow, J. C., & Measelle, J. (2011). Risky shifts: How the timing and course of mothers’ depressive symptoms across the perinatal period shape their own and infant's stress response profiles. Development and Psychopathology, 23, 521538. ScholarPubMed
Lebel, C., Walton, M., Letourneau, N., Giesbrecht, G. F., Kaplan, B. J., & Dewey, D. (2016). Prepartum and postpartum maternal depressive symptoms are related to children's brain structure in preschool. Biological Psychiatry, 80, 859868. ScholarPubMed
Letourneau, N., Dewey, D., Kaplan, B. J., Ntanda, H., Novick, J., Thomas, J. C., … APrON Study Team. (2018). Intergenerational transmission of adverse childhood experiences via maternal depression and anxiety and moderation by child sex. Journal of Developmental Origins of Health and Disease, 3, 112. Scholar
Leung, B. M. Y., McDonald, S. W., Kaplan, B. J., Giesbrecht, G. F., & Tough, S. C. (2013). Comparison of sample characteristics in two pregnancy cohorts: Community-based versus population-based recruitment methods. BMC Medical Research Methodology, 6, Article 149. Retrieved from Scholar
Li, M., D'Arcy, C., & Meng, X. (2016). Maltreatment in childhood substantially increases the risk of adult depression and anxiety in prospective cohort studies: Systematic review, meta-analysis, and proportional attributable fractions. Psychological Medicine, 46, 717730. ScholarPubMed
Lindert, J., von Ehrenstein, O. S., Grashow, R., Gal, G., Braehler, E., & Weisskopf, M. G. (2014). Sexual and physical abuse in childhood is associated with depression and anxiety over the life course: Systematic review and meta-analysis. International Journal of Public Health, 59, 359372. ScholarPubMed
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behavior and cognition. Nature Reviews Neuroscience, 10, 434445. Scholar
Lyons, D. M., Parker, K. J., Katz, M., & Schatzberg, A. F. (2009). Developmental cascades linking stress inoculation, arousal regulation, and resilience. Frontiers in Behavioral Neuroscience, 3, Article 32. Retrieved from ScholarPubMed
MacKinnon, D. P., Krull, J. L., & Lockwood, C. M. (2000). Equivalence of the mediation, confounding and suppression effect. Prevention Science, 1, Article 173. Retrieved from ScholarPubMed
Madigan, S., Wade, M., Plamondon, A., Maguire, J. L., & Jenkins, J. M. (2017). Maternal adverse childhood experience and infant health: Biomedical and psychosocial risks as intermediary mechanisms. The Journal of Pediatrics, 187, 282289. ScholarPubMed
Madigan, S., Wade, M., Tarabulsy, G., Jenkins, J. M., & Shouldice, M. (2014). Association between abuse history and adolescent pregnancy: A meta-analysis. Journal of Adolescent Health, 55, 151159. ScholarPubMed
Marceau, K., Laurent, H. K., Neiderhiser, J. M., Reiss, D., Shaw, D. S., Natsuaki, M. N., … Leve, L. D. (2015). Combined influences of genes, prenatal environment, cortisol, and parenting on the development of children's internalizing versus externalizing problems. Behavior Genetics, 45, 268282. ScholarPubMed
Matvienko-Sikar, K., & Dockray, S. (2017). Effects of a novel positive psychological intervention on prenatal stress and well-being: A pilot randomised controlled trial. Women and Birth, 30, e111e118. ScholarPubMed
Maxwell, S. D., Fineberg, A. M., Drabick, D. A., Murphy, S. K., & Ellman, L. M. (2018). Maternal prenatal stress and other developmental risk factors for adolescent depression: Spotlight on sex differences. Journal of Abnormal Child Psychology, 46, 381397. ScholarPubMed
Mesman, J., & Koot, H. M. (2001). Early preschool predictors of preadolescent internalizing and externalizing DSM-IV diagnoses. Journal of the American Academy of Child and Adolescent Psychiatry, 40, 10291036. ScholarPubMed
Metzler, M., Merrick, M. T., Klevens, J., Ports, K. A., & Ford, D. C. (2017). Adverse childhood experiences and life opportunities: Shifting the narrative. Children and Youth Services Review, 72, 141149. Scholar
Miller, G. E., Culhane, J., Grobman, W., Simhan, H., Williamson, D. E., Adam, E. K., … Borders, A. (2017). Mothers’ childhood hardship forecasts adverse pregnancy outcomes: Role of inflammatory, lifestyle, and psychosocial pathways. Brain, Behavior, and Immunity, 65, 1119. ScholarPubMed
Min, M. O., Singer, L. T., Minnes, S., Kim, H., & Short, E. (2012). Mediating links between maternal childhood trauma and preadolescent behavioral adjustment. Journal of Interpersonal Violence, 28, 831851. ScholarPubMed
Miranda, J. K., Granero, R., & Ezpeleta, L. (2013). Maternal childhood abuse, intimate partner violence, and child psychopathology: The mediator role of mothers’ mental health. Violence Against Women, 19, 5068. ScholarPubMed
Moisiadis, V. G., & Matthews, S. G. (2014). Glucocorticoids and fetal programming part 2: Mechanisms. Nature Reviews Endocrinology, 10, 403411. ScholarPubMed
Moog, N. K., Buss, C., Entringer, S., Shahbaba, B., Gillen, D. L., Hobel, C. J., & Wadhwa, P. D. (2016). Maternal exposure to childhood trauma is associated during pregnancy with placental-fetal stress physiology. Biological Psychiatry, 79, 831839. ScholarPubMed
Moog, N. K., Entringer, S., Rasmussen, J. M., Styner, M., Gilmore, J. H., Kathmann, N., … Buss, C. (2018). Intergenerational effect of maternal exposure to childhood maltreatment on newborn brain anatomy. Biological Psychiatry, 83, 120127. ScholarPubMed
Morgan, C. D., Wiederman, M. W., & Magnus, R. D. (1998). Discriminant validity of the SCL-90 dimensions of anxiety and depression. Assessment, 5, 197201. ScholarPubMed
Najman, J. M., Williams, G. M., Nikles, J., Spence, S., Bor, W., O'Callaghan, M., … Andersen, M. J. (2000). Mothers’ mental illness and child behavior problems: Cause-effect association or observation bias? Journal of the American Academy of Child and Adolescent Psychiatry, 39, 592602. ScholarPubMed
Narusyte, J., Ropponen, A., Alexanderson, K., & Svedberg, P. (2017). Internalizing and externalizing problems in childhood and adolescence as predictors of work incapacity in young adulthood. Social Psychiatry and Psychiatric Epidemiology, 52, 11591168. ScholarPubMed
Okun, M. L., Krafty, R. T., Buysse, D. J., Monk, T. H., Reynolds, C. F., Begley, A., & Hall, M. (2010). What constitutes too long of a delay? Determining the cortisol awakening response (CAR) using self-report and PSG-assessed wake time. Psychoneuroendocrinology, 35, 460468. ScholarPubMed
Oxford, M., & Finlay, D. (2013). NCAST Caregiver/Parent Child Interaction Teaching Manual (2nd ed.). Seattle, WA: NCAST Programs.Google Scholar
Pawlby, S., Hay, D., Sharp, D., Waters, C. S., & Pariante, C. M. (2011). Antenatal depression and offspring psychopathology: The influence of childhood maltreatment. The British Journal of Psychiatry, 199, 106112. ScholarPubMed
Plant, D. T., Barker, E. D., Waters, C. S., Pawlby, S., & Pariante, C. M. (2013). Intergenerational transmission of maltreatment and psychopathology: The role of antenatal depression. Psychological Medicine, 43, 519528. ScholarPubMed
Plant, D. T., Jones, F. W., Pariante, C. M., & Pawlby, S. (2017). Association between maternal childhood trauma and offspring childhood psychopathology: Mediation analysis from the ALSPAC cohort. The British Journal of Psychiatry, 211, 144150. ScholarPubMed
Plant, D. T., Pariante, C. M., Sharp, D., & Pawlby, S. (2015). Maternal depression during pregnancy and offspring depression in adulthood: Role of child maltreatment. The British Journal of Psychiatry, 207, 213220. ScholarPubMed
Preacher, K. J., Rucker, D. D., & Hayes, A. F. (2007). Addressing moderated mediation hypotheses: Theory, methods, and prescriptions. Multivariate Behavioral Research, 42, 185227. ScholarPubMed
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, 916931. ScholarPubMed
Public Health Agency of Canada Team. (2009). What mothers say: The Canadian Maternity Experiences Survey. Ottawa: Government of Canada.Google Scholar
Reynolds, C. R., & Kamphaus, R. W. (2004). Behavior Assessment System for Children-Second Edition (BASC-2). Bloomington, MN: Pearson.Google Scholar
Richter, J., Bittner, A., Petrowski, K., Junge-Hoffmeister, J., Bergmann, S., Joraschky, P., & Weidner, K. (2012). Effects of an early intervention on perceived stress and diurnal cortisol in pregnant women with elevated stress, anxiety, and depressive symptomatology. Journal of Psychosomatic Obstetrics and Gynaecology, 33, 162170. ScholarPubMed
Rijlaarsdam, J., Stevens, G. W., Jansen, P. W., Ringoot, A. P., Jaddoe, V. W., Hofman, A., & Tiemeier, H. (2014). Maternal childhood maltreatment and offspring emotional and behavioral problems maternal and paternal mechanisms of risk transmission. Child Maltreatment, 19, 6778. ScholarPubMed
Roberts, R., O'Connor, T., Dunn, J., & Golding, J. (2004). The effects of child sexual abuse in later family life: Mental health, parenting and adjustment of offspring. Child Abuse & Neglect, 28, 525545. ScholarPubMed
Sancho-Rossignol, A., Schilliger, Z., Cordero, M. I., Serpa, S. R., Epiney, M., Hüppi, P., … Schechter, D. S. (2018). The association of maternal exposure to domestic violence during childhood with prenatal attachment, maternal-fetal heart rate, and infant behavioral regulation. Frontiers in Psychiatry, 9, Article 358. Retrieved from ScholarPubMed
Sandman, C. A. (2018). Prenatal CRH: An integrating signal of fetal distress. Development and Psychopathology, 30, 941952. ScholarPubMed
Sandman, C. A., Davis, E. P., Buss, C., & Glynn, L. M. (2011). Prenatal programming of human neurological function. International Journal of Peptides, 2011, Article 837596. Retrieved from ScholarPubMed
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, 327335. Scholar
Schlotz, W., Hellhammer, J., Schulz, P., & Stone, A. A. (2004). Perceived work overload and chronic worrying predict weekend-weekday differences in the cortisol awakening response. Psychosomatic Medicine, 66, 207214. ScholarPubMed
Shea, A. K., Streiner, D. L., Fleming, A., Kamath, M. V., Broad, K., & Steiner, M. (2007). The effect of depression, anxiety and early life trauma on the cortisol awakening response during pregnancy: Preliminary results. Psychoneuroendocrinology, 32, 10131020. ScholarPubMed
Smith, M. V, Gotman, N., & Yonkers, K. A. (2016). Early childhood adversity and pregnancy outcomes. Maternal and Child Health Journal, 20, 790798. ScholarPubMed
SPSS Inc. (2013). SPSS for Windows. Armnok, NY, NY: IBM.Google Scholar
Sroufe, L. A. (2000). Early relationships and the development of children. Infant Mental Health Journal, 21, 6774.<67::AID-IMHJ8>3.0.CO;2-23.0.CO;2-2>CrossRefGoogle Scholar
Tabachnick, B. G., & Fidell, L. S. (2012). Using multivariate statistics (6th ed.). Boston: Pearson.Google Scholar
Talge, N. M., Neal, C., & Glover, V. (2007). Antenatal maternal stress and long-term effects on child development: How and why? Journal of Child Psychology and Psychiatry, 48, 245261. ScholarPubMed
Thomas, J. C., Letourneau, N., Campbell, T. S., & Giesbrecht, G. F. (2018). Social buffering of the maternal and infant HPA axes: Mediation and moderation in the intergenerational transmission of adverse childhood experiences. Development and Psychopathology, 30, 921939. ScholarPubMed
Thomas, J. C., Magel, C., Tomfohr-Madsen, L., Madigan, S., Letourneau, N., Campbell, T. S., & Giesbrecht, G. F. (2018). Adverse childhood experiences and HPA axis function in pregnant women. Hormones and Behavior, 102, 1022. ScholarPubMed
Togher, K. L., O'Keefe, M. M., Khashan, A. S., Gutierrez, H., Kenny, L. C., & O'Keefe, G. W. (2014). Epigenetic regulation of the placental HSD11B2 barrier and its role as a critical regulator of fetal development. Epigenetics, 9, 816822. ScholarPubMed
Urizar, G. G. Jr., & Munoz, R. F. (2011). Impact of a prenatal cognitive-behavioral stress management intervention on salivary cortisol levels in low-income mothers and their infants. Psychoneuroendocrinology, 36, 14801494. ScholarPubMed
Varese, F., Smeets, F., Drukker, M., Lieverse, R., Lataster, T., Viechtbauer, W., … Bentall, R. P. (2012). Childhood adversities increase the risk of psychosis: A meta-analysis of patient-control, prospective- and cross-sectional cohort studies. Schizophrenia Bulletin, 38, 661671. ScholarPubMed
Weissbecker, I., Floyd, A., Dedert, E., Salmon, P., & Sephton, S. (2006). Childhood trauma and diurnal cortisol disruption in fibromyalgia syndrome. Psychoneuroendocrinology, 31, 312324. ScholarPubMed
Wessa, M., Rohleder, N., Kirschbaum, C., & Flor, H. (2006). Altered cortisol awakening response in posttraumatic stress disorder. Psychoneuroendocrinology, 31, 209215. ScholarPubMed
Zhang, H., & Emory, E. K. (2015). A mindfulness-based intervention for pregnant African-American women. Mindfulness, 6, 663674. Scholar
Zijlmans, M. A. C., Riksen-Walraven, J. M., & de Weerth, C. (2015). Associations between maternal prenatal cortisol concentrations and child outcomes: A systematic review. Neuroscience and Biobehavioral Reviews, 53, 124. ScholarPubMed
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The role of HPA-axis function during pregnancy in the intergenerational transmission of maternal adverse childhood experiences to child behavior problems
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The role of HPA-axis function during pregnancy in the intergenerational transmission of maternal adverse childhood experiences to child behavior problems