Emerging evidence suggests that antenatal exposure to maternal stress signals affects the development of the infant stress response systems. Animal studies indicate that maternal sensitive caregiving can reverse some of these effects. However, the generalizability of these findings to humans is unknown. This study investigated the role of maternal caregiving in the association between multiple markers of maternal antenatal stress and infant stress regulation.
The sample consisted of 94 mother-infant (N = 47 males, mean postnatal weeks = 12; SD = 1.84) dyads. Maternal levels of Interleukin-6, C-Reactive Protein (CRP), diurnal cortisol and alpha amylase, depressive and anxiety symptoms were assessed in late pregnancy (mean gestational age = 34.76; SD = 1.12), whereas postnatal symptomatology, caregiving, and infant cortisol response to the inoculation were evaluated at 3 months.
Hierarchical linear models (HLMs) showed a significant interaction between maternal antenatal cortisol, caregiving, and time on infant cortisol reactivity, while controlling for gender, maternal age, and postnatal depression. Specifically, higher levels of maternal antenatal cortisol were associated with greater cortisol response only among infants of less emotionally available mothers. All other markers of antenatal stress were not significantly associated with infant cortisol reactivity either independently or in interaction with maternal caregiving.
Albeit preliminary, results provide the first evidence in humans that maternal sensitive caregiving may eliminate the association between antenatal maternal cortisol and infant cortisol regulation.
Data availability statement
- Exposure to maternal stress signals during pregnancy is an emerging risk factor for the development of the infant stress response systems.
- Animal models indicate that early caregiving may buffer these effects, but the generalizability of these findings to human is unknown.
- We provided the first evidence for a buffering role of maternal emotional availability in the association between maternal antenatal cortisol levels and infant cortisol reactivity.
- Findings suggest that enhancing maternal sensitive caregiving, especially in situations of high stress in pregnancy, should be a key target of postnatal interventions. Further, they highlight the need to account for the role of variations in caregiving in future research, as they are likely to alter the unfolding of antenatal processes.
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- 2008). Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. Journal of Child Psychology and Psychiatry, 49, 97–103.
- 2005). When more is not better: The role of cumulative risk in child behavior outcomes. Journal of Child Psychology and Psychiatry, 46, 235–245.
- 1999). Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the "two hit hypothesis". Journal of Psychiatric Research, 33, 543–548.
- 1999). The Edinburgh Postnatal Depression Scale: validation for an Italian sample. Journal of Affective Disorders, 53, 137–141. http://dx.doi.org/10.1016/s0165-0327(98)00102-5
- 2010). Maternal prenatal cortisol and infant cognitive development: moderation by infant–mother attachment. Biological Psychiatry, 67, 1026–1032. http://dx.doi.org/10.1016/j.biopsych.2010.01.002
- 2008). The Emotional Availability (EA) Scales and EA Zones Evaluation: Infancy/early childhood version, 4th ed. Boulder, CO.
- 2014). Emotional availability (EA): Theoretical background, empirical research using the EA Scales, and clinical applications. Developmental Review, 34, 114–167. http://dx.doi.org/10.1016/j.dr.2014.01.002
- 2018). Hypothalamic-pituitary-adrenal axis and autonomic nervous system reactivity in children prenatally exposed to maternal depression: A systematic review of prospective studies. Neuroscience & Biobehavioral Reviews, 117, 243–252.
- 2011). Prenatal maternal stress programs infant stress regulation. Journal of Child Psychology and Psychiatry, 52, 119–129.
- 2013). Infant cortisol and behavioral habituation to weekly maternal separations: Links with maternal prenatal cortisol and psychosocial stress. Psychoneuroendocrinology, 38, 2863–2874.
- 2010). Maternal care counteracts behavioral effects of prenatal environmental stress in female rats. Behavioural Brain Research, 208, 593–602.
- 2017). Maternal interaction quality moderates effects of prenatal maternal emotional symptoms on girls' internalizing problems. Infant Mental Health Journal, 38, 634–644. http://dx.doi.org/10.1002/imhj.21662
- 2021). Antenatal maternal anxiety, maternal sensitivity and toddlers’ behavioral problems: An investigation of possible pathways. Early Hum Dev, 157, 105364.
- 2019). Emotional availability in samples of mothers at high risk for depression and with substance use disorder. Frontiers in Psychology, 10, 577.
- APrON Study Team. (2017). Sexually dimorphic and interactive effects of prenatal maternal cortisol and psychological distress on infant cortisol reactivity. Development and Psychopathology, 29, 805–818.
- 2010). Prenatal stress and the programming of the HPA axis. Neuroscience & Biobehavioral Reviews, 35, 17–22.
- 2009). Maternal prenatal anxiety, postnatal caregiving and infants' cortisol responses to the still-face procedure. Developmental Psychobiology, 51, 625–637. http://dx.doi.org/10.1002/dev.20397
- 2015). The social buffering of the hypothalamic–pituitary–adrenocortical axis in humans: Developmental and experiential determinants. Social Neuroscience, 10, 479–488. http://dx.doi.org/10.1080/17470919.2015.1070747
- 2009). Stress questionnaires and stress biomarkers during pregnancy. Journal of Women's Health, 18, 1425–1433.
- 2005). Estimating between- and within-individual variation in cortisol levels using multilevel models. Psychoneuroendocrinology, 30, 698–714.
- 2021). Maternal prenatal cortisol programs the infant hypothalamic–pituitary–adrenal axis. Psychoneuroendocrinology, 125, 105106.
- 2008). Effects of mothers' prenatal psychiatric status and postnatal caregiving on infant biobehavioral regulation: Can prenatal programming be modified? Early Human Development, 84, 249–256. http://dx.doi.org/10.1016/j.earlhumdev.2007.06.004
- 2018). Annual research review: Early adversity, the hypothalamic–pituitary–adrenocortical axis, and child psychopathology. Journal of Child Psychology and Psychiatry, 59, 327–346.
- 2017). Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease. Neuroscience and Biobehavioral Reviews, 80, 166–184.
- 1995). Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. Journal of Neuroscience, 15, 110–116.
- 2015). Causal effects of the early caregiving environment on development of stress response systems in children. Proceedings of the National Academy of Sciences, 112, 5637–5642.
- 2005). Stress responses at birth: determinants of cord arterial cortisol and links with cortisol response in infancy. BJOG: An International Journal of Obstetrics & Gynaecology, 112, 921–926.
- 2020a). Neuroendocrine and immune markers of maternal stress during pregnancy and infant cognitive development. Developmental Psychobiology, 62, 1100–1110. http://dx.doi.org/10.1002/dev.21967
- 2020b). The biological underpinnings of perinatal depressive symptoms: A multi-systems approach. Journal of Affective Disorders, 274, 1004–1012. http://dx.doi.org/10.1016/j.jad.2020.05.023
- 2019). Beyond the HPA-axis: Exploring maternal prenatal influences on birth outcomes and stress reactivity. Psychoneuroendocrinology, 101, 253–262.
- 2020). The programming role of maternal antenatal inflammation on infants’ early neurodevelopment: A review of human studies. Journal of Affective Disorders, 263, 739–746.
- 2012). Mismatch or cumulative stress: Toward an integrated hypothesis of programming effects. Physiology and Behavior, 106, 691–700.
- 2017). Fetal origins of mental health: The developmental origins of health and disease hypothesis. American Journal of Psychiatry, 174, 319–328.
- 2018). Antenatal depression programs cortisol stress reactivity in offspring through increased maternal inflammation and cortisol in pregnancy: The Psychiatry Research and Motherhood – Depression (PRAM-D) Study. Psychoneuroendocrinology, 98, 211–221. http://dx.doi.org/10.1016/j.psyneuen.2018.06.017
- 1989). Inventario per l’ansia di «Stato» e di «Tratto»: nuova versione italiana dello STAI Forma Y: Manuale. Firenze, Italy: Organizzazioni Speciali.
- 1998). What's wrong with Bonferroni adjustments. BMJ, 316, 1236–1238.
- 2011). Prenatal programming of postnatal plasticity? Development and Psychopathology, 23, 29–38.
- 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. http://dx.doi.org/10.1016/s0306-4530(02)00108-7
- 2017). Transfer of maternal psychosocial stress to the fetus. Neuroscience & Biobehavioral Reviews, 117, 185–197.
- APrON Study Team (2016). Developmental origins of infant stress reactivity profiles: A multi-system approach. Developmental psychobiology, 58, 578–599.
- 2015). The effects of parental behavior on infants' neural processing of emotion expressions. Child Development, 86, 877–888.
- 1999). Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. European Journal of Neuroscience, 11, 2906–2916.
- 2020). Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neuroscience & Biobehavioral Reviews, 117, 26–64. http://dx.doi.org/10.1016/j.neubiorev.2017.07.003
- 2012). Genetic and environmental influences on individual differences in cortisol level and circadian rhythm in middle childhood. Hormones and Behavior, 62, 36–42.
- 2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.