Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T12:58:05.690Z Has data issue: false hasContentIssue false
  • English
  • Français

Environmental determinants of physiological reactivity to stress: The interacting effects of early life deprivation, caregiving quality, and stressful life events

Published online by Cambridge University Press:  11 January 2021

Mark Wade ,
Margaret A. Sheridan ,
Charles H. Zeanah ,
Nathan A. Fox ,
Charles A. Nelson  and
Katie A. McLaughlin
Mark Wade*
Affiliation:
Deparment of Applied Psychology and Human Development, University of Toronto, Toronto, ON, Canada
Margaret A. Sheridan
Affiliation:
Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Charles H. Zeanah
Affiliation:
Department of Psychiatry and Behavioral Sciences, Tulane University School of Medicine, New Orleans, LA, USA
Nathan A. Fox
Affiliation:
Department of Human Development and Quantitative Methodology, University of Maryland, College Park, MD, USA
Charles A. Nelson
Affiliation:
Boston Children's Hospital of Harvard Medical School, Boston, MA, USA Harvard Graduate School of Education, Cambridge, MA, USA
Katie A. McLaughlin
Affiliation:
Department of Psychology, Harvard University, Cambridge, MA, USA
*
Author for Correspondence: Mark Wade, PhD, Department of Applied Psychology and Human Development, University of Toronto, 252 Bloor Street West, Toronto, ON, Canada, M5S1V6; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Children who spend their early lives in institutions experience profound psychosocial deprivation that is associated with altered stress response system development. Here, we used data from a longitudinal randomized controlled trial of foster care for institutionally reared children to examine whether caregiving quality and stressful life events (SLEs) in early adolescence (age 12) influence patterns of hypothalamic–pituitary–adrenal (HPA) axis and sympathetic nervous system (SNS) reactivity. Controlling for the effect of institutional care, higher caregiving quality at age 12 was associated with heightened cortisol and SNS reactivity. However, moderation analysis revealed that the latter effect was only observed among never-institutionalized children, whereas ever-institutionalized children demonstrated a persistently blunted SNS response regardless of recent caregiving quality. Among institutionally reared children, SLEs interacted with prior random assignment to foster care, such that those placed in foster care early in development had a SNS response that approximated never-institutionalized children when SLEs at age 12 were low. In contrast, SNS reactivity was persistently blunted among those with prolonged deprivation, regardless of recent SLEs. Early-life deprivation is associated with persistent blunting of stress response systems, but normalization may be achievable if SLEs are limited following placement into enriched family-based care.

Keywords

developmental psychobiologyHPA-axisinstitutional rearingneglectstress reactivitysympathetic nervous system
Type
Special Section 2: Early Adversity and Development: Contributions from the Field
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1732 - 1742
Check for updates
Copyright
Copyright © Cambridge University Press 2020

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.)

References

Alink, L. R. A., van Ijzendoorn, M. H., Bakermans-Kranenburg, M. J., Mesman, J., Juffer, F., & Koot, H. M. (2008). Cortisol and externalizing behavior in children and adolescents: Mixed meta-analytic evidence for the inverse relation of basal cortisol and cortisol reactivity with externalizing behavior. Developmental Psychobiology, 50, 427–450. doi:10.1002/dev.20300CrossRefGoogle ScholarPubMed
Alkon, A., Boyce, W. T., Tran, L., Harley, K. G., Neuhaus, J., & Eskenazi, B. (2014). Prenatal adversities and Latino children's autonomic nervous system reactivity trajectories from 6 months to 5 years of age. PloS one, 9(1), e86283.CrossRefGoogle ScholarPubMed
Badanes, L. S., Watamura, S. E., & Hankin, B. L. (2011). Hypocortisolism as a potential marker of allostatic load in children: Associations with family risk and internalizing disorders. Development and Psychopathology, 23, 881–896. doi:10.1017/S095457941100037XCrossRefGoogle ScholarPubMed
Bernard, K., Hostinar, C. E., & Dozier, M. (2015). Intervention effects on diurnal cortisol rhythms of Child Protective Services-referred infants in early childhood preschool follow-up results of a randomized clinical trial. JAMA Pediatrics, 169, 112–119. doi:10.1001/jamapediatrics.2014.2369CrossRefGoogle ScholarPubMed
Berntson, G. G., Lozano, D. L., Chen, Y. J., & Cacioppo, J. T. (2004). Where to Q in PEP. Psychophysiology, 41, 333–337. doi:10.1111/j.1469-8986.2004.00156.xCrossRefGoogle Scholar
Berry, D., Blair, C., Granger, D. A., Vernon-Feagans, L., Cox, M., Burchinal, P., … Crnic, K. (2016). Child care and cortisol across infancy and toddlerhood: Poverty, peers, and developmental timing. Family Relations, 65, 51–72. doi:10.1111/fare.12184CrossRefGoogle ScholarPubMed
Bosch, N. M., Riese, H., Reijneveld, S. A., Bakker, M. P., Verhulst, F. C., Ormel, J., & Oldehinkel, A. J. (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. doi:10.1016/j.psyneuen.2012.01.013CrossRefGoogle ScholarPubMed
Boyce, W. T., & Ellis, B. J. (2005, March). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271–301. doi:10.1017/S0954579405050145CrossRefGoogle ScholarPubMed
Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. (2009). Morning cortisol levels in preschool-aged foster children: Differential effects of maltreatment type. Developmental Psychobiology, 51, 14–23. doi:10.1002/dev.20333CrossRefGoogle ScholarPubMed
Busso, D. S., McLaughlin, K. A., & Sheridan, M. A. (2017). Dimensions of adversity, physiological reactivity, and externalizing psychopathology in adolescence: Deprivation and threat. Psychosomatic Medicine, 79, 162–171. doi:10.1097/PSY.0000000000000369CrossRefGoogle ScholarPubMed
Cantave, C. Y., Langevin, S., Marin, M. F., Brendgen, M., Lupien, S., & Ouellet-Morin, I. (2019). Impact of maltreatment on depressive symptoms in young male adults: The mediating and moderating role of cortisol stress response and coping strategies. Psychoneuroendocrinology, 103, 41–48.CrossRefGoogle ScholarPubMed
Cicchetti, D., Rogosch, F. A., Toth, S. L., & Sturge-Apple, M. L. (2011). Normalizing the development of cortisol regulation in maltreated infants through preventive interventions. Development and Psychopathology, 23, 789–800. doi:10.1017/S0954579411000307CrossRefGoogle ScholarPubMed
Dahl, R. E., & Gunnar, M. R. (2009). Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21, 1–6. doi:10.1017/S0954579409000017CrossRefGoogle ScholarPubMed
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011, June). The adaptive calibration model of stress responsivity. Neuroscience and Biobehavioral Reviews, 35, 1562–1592. doi:10.1016/j.neubiorev.2010.11.007CrossRefGoogle ScholarPubMed
Depasquale, C, Donzella, B., & Gunnar, M. R.. (2019). Pubertal recalibration of cortisol reactivity following early life stress: A cross-sectional analysis. Journal of Child Psychology and Psychiatry, 60(5), 566–577.CrossRefGoogle ScholarPubMed
DePasquale, C. E., Raby, K. L., Hoye, J., & Dozier, M. (2018). Parenting predicts strange situation cortisol reactivity among children adopted internationally. Psychoneuroendocrinology, 89, 86–91. doi:10.1016/j.psyneuen.2018.01.003CrossRefGoogle ScholarPubMed
Doom, J. R., Doyle, C. M., & Gunnar, M. R. (2017). Social stress buffering by friends in childhood and adolescence: Effects on HPA and oxytocin activity. Social Neuroscience, 12, 8–21. doi:10.1080/17470919.2016.1149095CrossRefGoogle ScholarPubMed
Doom, J. R., Hostinar, C. E., VanZomeren-Dohm, A. A., & Gunnar, M. R. (2015). The roles of puberty and age in explaining the diminished effectiveness of parental buffering of HPA reactivity and recovery in adolescence. Psychoneuroendocrinology, 59, 102–111. doi:10.1016/j.psyneuen.2015.04.024CrossRefGoogle 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, 892–905. doi:10.1016/j.psyneuen.2007.06.008CrossRefGoogle ScholarPubMed
Fries, A. B. W., Ziegler, T. E., Kurian, J. R., Jacoris, S., & Pollak, S. D. (2005). Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. Proceedings of the National Academy of Sciences of the United States of America, 102, 17237–17240. doi:10.1073/pnas.0504767102CrossRefGoogle Scholar
Fuhrmann, D., Knoll, L. J., & Blakemore, S. J. (2015, October 1). Adolescence as a sensitive period of brain development. Trends in Cognitive Sciences, 19, 558–566. doi:10.1016/j.tics.2015.07.008CrossRefGoogle ScholarPubMed
Gunnar, M. R., DePasquale, C. E., Reid, B. M., Donzella, B., & Miller, B. S. (2019). Pubertal stress recalibration reverses the effects of early life stress in postinstitutionalized children. Proceedings of the National Academy of Sciences, 116(48), 23984–23988.CrossRefGoogle ScholarPubMed
Gunnar, M. R., Frenn, K., Wewerka, S. S., & Van Ryzin, M. J. (2009). Moderate versus severe early life stress: Associations with stress reactivity and regulation in 10-12-year-old children. Psychoneuroendocrinology, 34, 62–75. doi:10.1016/j.psyneuen.2008.08.013CrossRefGoogle ScholarPubMed
Hackman, D. A., Betancourt, L. M., Brodsky, N. L., Kobrin, L., Hurt, H., & Farah, M. J. (2013). Selective impact of early parental responsivity on adolescent stress reactivity. PLoS ONE, 8, e58250. doi:10.1371/journal.pone.0058250CrossRefGoogle ScholarPubMed
Hagan, M. J., Roubinov, D. S., Mistler, A. K., & Luecken, L. J. (2014). Mental health outcomes in emerging adults exposed to childhood maltreatment: The moderating role of stress reactivity. Child Maltreatment, 19, 156–167.CrossRefGoogle ScholarPubMed
Hartman, C. A., Hermanns, V. W., de Jong, P. J., & Ormel, J. (2013). Self- or parent report of (co-occurring) internalizing and externalizing problems, and basal or reactivity measures of HPA-axis functioning: A systematic evaluation of the internalizing-hyperresponsivity versus externalizing-hyporesponsivity HPA-axis hypothesis. Biological Psychology, 94, 175–184. doi:10.1016/j.biopsycho.2013.05.009CrossRefGoogle ScholarPubMed
Heim, C. M., Entringer, S., & Buss, C. (2019, July 1). Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health. Psychoneuroendocrinology, 105, 123–137. doi:10.1016/j.psyneuen.2018.12.011CrossRefGoogle ScholarPubMed
Hostinar, C. E., Johnson, A. E., & Gunnar, M. R. (2015a). Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Developmental Science, 18, 281–297. doi:10.1111/desc.12195CrossRefGoogle Scholar
Hostinar, C. E., Johnson, A. E., & Gunnar, M. R. (2015b). Early social deprivation and the social buffering of cortisol stress responses in late childhood: An experimental study. Developmental Psychology, 51, 1597–1608. doi:10.1037/dev0000029CrossRefGoogle Scholar
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: A review of animal models and human studies across development. Psychological Bulletin, 140, 256–282. doi:10.1037/a0032671CrossRefGoogle ScholarPubMed
Humphreys, K. L., Gleason, M. M., Drury, S. S., Miron, D., Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2015). Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: Follow-up of an open, randomised controlled trial. The Lancet Psychiatry, 2, 625–634. doi:10.1016/S2215-0366(15)00095-4CrossRefGoogle ScholarPubMed
Jaffee, S. R., McFarquhar, T., Stevens, S., Ouellet-Morin, I., Melhuish, E., & Belsky, J. (2015). Interactive effects of early and recent exposure to stressful contexts on cortisol reactivity in middle childhood. Journal of Child Psychology and Psychiatry and Allied Disciplines, 56, 138–146. doi:10.1111/jcpp.12287CrossRefGoogle ScholarPubMed
Koss, K. J., & Gunnar, M. R. (2018, April 1). Annual research review: Early adversity, the hypothalamic–pituitary–adrenocortical axis, and child psychopathology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 59, 327–346. doi:10.1111/jcpp.12784CrossRefGoogle ScholarPubMed
Koss, K. J., Hostinar, C. E., Donzella, B., & Gunnar, M. R. (2014). Social deprivation and the HPA axis in early development. Psychoneuroendocrinology, 50, 1–13. doi:10.1016/j.psyneuen.2014.07.028CrossRefGoogle ScholarPubMed
Koss, K. J., Mliner, S. B., Donzella, B., & Gunnar, M. R. (2016). Early adversity, hypocortisolism, and behavior problems at school entry: A study of internationally adopted children. Psychoneuroendocrinology, 66, 31–38. doi:10.1016/j.psyneuen.2015.12.018CrossRefGoogle ScholarPubMed
Larsen, B., & Luna, B. (2018, November 1). Adolescence as a neurobiological critical period for the development of higher-order cognition. Neuroscience and Biobehavioral Reviews, 94, 179–195. doi:10.1016/j.neubiorev.2018.09.005CrossRefGoogle ScholarPubMed
Leneman, K. B., Donzella, B., Desjardins, C. D., Miller, B. S., & Gunnar, M. R. (2018). The slope of cortisol from awakening to 30 min post-wake in post-institutionalized children and early adolescents. Psychoneuroendocrinology, 96, 93–99. doi:10.1016/j.psyneuen.2018.06.011CrossRefGoogle ScholarPubMed
Loman, M. M., & Gunnar, M. R. (2010, May). Early experience and the development of stress reactivity and regulation in children. Neuroscience and Biobehavioral Reviews, 34, 867–876. doi:10.1016/j.neubiorev.2009.05.007CrossRefGoogle ScholarPubMed
Lozano, D. L., Norman, G., Knox, D., Wood, B. L., Miller, B. D., Emery, C. F., & Berntson, G. G. (2007). Where to B in dZ/dt. Psychophysiology, 44, 113–119. doi:10.1111/j.1469-8986.2006.00468.xCrossRefGoogle Scholar
Luecken, L. J., Kraft, A., & Hagan, M. J. (2009). Negative relationships in the family-of-origin predict attenuated cortisol in emerging adults. Hormones and Behavior, 55, 412–417. doi:10.1016/j.yhbeh.2008.12.007CrossRefGoogle ScholarPubMed
Martinez-Torteya, C., Bogat, G. A., Levendosky, A. A., & Von Eye, A. (2016). The influence of prenatal intimate partner violence exposure on hypothalamic-pituitary-adrenal axis reactivity and childhood internalizing and externalizing symptoms. Development and Psychopathology, 28, 55–72. doi:10.1017/S0954579415000280CrossRefGoogle ScholarPubMed
Mazurka, R., Wynne-Edwards, K. E., & Harkness, K. L. (2016). Stressful life events prior to depression onset and the cortisol response to stress in youth with first onset versus recurrent depression. Journal of Abnormal Child Psychology, 44, 1173–1184. doi:10.1007/s10802-015-0103-yCrossRefGoogle ScholarPubMed
McClelland, G. H., & Judd, C. M. (1993). Statistical difficulties of detecting interactions and moderator effects. Psychological Bulletin, 114, 376–390. doi:10.1037/0033-2909.114.2.376CrossRefGoogle ScholarPubMed
McEwen, B. S. (2008, April 7). Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. European Journal of Pharmacology, 583, 174–185. doi:10.1016/j.ejphar.2007.11.071CrossRefGoogle ScholarPubMed
McEwen, B. S. (2012). Brain on stress: How the social environment gets under the skin. Proceedings of the National Academy of Sciences of the United States of America, 109(Suppl.2), 17180–17185. doi:10.1073/pnas.1121254109CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Kubzansky, L. D., Dunn, E. C., Waldinger, R., Vaillant, G., & Koenen, K. C. (2010). Childhood social environment, emotional reactivity to stress, and mood and anxiety disorders across the life course. Depression and Anxiety, 27, 1087–1094. doi:10.1002/da.20762CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Sheridan, M. A., Tibu, F., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (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.CrossRefGoogle ScholarPubMed
Miller, R., & Kirschbaum, C. (2019). Cultures under stress: A cross-national meta-analysis of cortisol responses to the Trier Social Stress Test and their association with anxiety-related value orientations and internalizing mental disorders. Psychoneuroendocrinology, 105, 147–154. doi:10.1016/j.psyneuen.2018.12.236CrossRefGoogle Scholar
Reilly, E. B., & Gunnar, M. R. (2019, November 1). Neglect, HPA axis reactivity, and development. International Journal of Developmental Neuroscience, 78, 100–108. doi:10.1016/j.ijdevneu.2019.07.010CrossRefGoogle ScholarPubMed
Ruttle, P. L., Shirtcliff, E. A., Serbin, L. A., Ben-Dat Fisher, D., Stack, D. M., & Schwartzman, A. E. (2011). Disentangling psychobiological mechanisms underlying internalizing and externalizing behaviors in youth: Longitudinal and concurrent associations with cortisol. Hormones and Behavior, 59, 123–132. doi:10.1016/j.yhbeh.2010.10.015CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Peres, J. C., Dismukes, A. R., Lee, Y., & Phan, J. M. (2014). Riding the physiological roller coaster: Adaptive significance of cortisol stress reactivity to social contexts. Journal of Personality Disorders, 28, 40–51. doi:10.1521/pedi.2014.28.1.40CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Skinner, M. L., Obasi, E. M., & Haggerty, K. P. (2017). Positive parenting predicts cortisol functioning six years later in young adults. Developmental Science, 20, e12461. doi:10.1111/desc.12461CrossRefGoogle ScholarPubMed
Slopen, N., McLaughlin, K. A., & Shonkoff, J. P. (2014, February). Interventions to improve cortisol regulation in children: A systematic review. Pediatrics, 133, 312–326. doi:10.1542/peds.2013-1632CrossRefGoogle ScholarPubMed
van der Vegt, E. J. M., van der Ende, J., Kirschbaum, C., Verhulst, F. C., & Tiemeier, H. (2009). Early neglect and abuse predict diurnal cortisol patterns in adults. A study of international adoptees. Psychoneuroendocrinology, 34, 660–669. doi:10.1016/j.psyneuen.2008.11.004CrossRefGoogle ScholarPubMed
Wade, M., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2018). Effect of foster care intervention on trajectories of general and specific psychopathology among children with histories of institutional rearing: A randomized clinical trial. JAMA Psychiatry, 75, 1137–1145. doi:10.1001/jamapsychiatry.2018.2556CrossRefGoogle ScholarPubMed
Wade, M., Zeanah, C. H., Fox, N. A., Tibu, F., Ciolan, L. E., & Nelson, C. A. (2019). Stress sensitization among severely neglected children and protection by social enrichment. Nature Communications, 10, 1–8.CrossRefGoogle ScholarPubMed
Wadsworth, M. E., Broderick, A. V., Loughlin-Presnal, J. E., Bendezu, J. J., Joos, C. M., Ahlkvist, J. A., … McDonald, A. (2019). Co-activation of SAM and HPA responses to acute stress: A review of the literature and test of differential associations with preadolescents’ internalizing and externalizing. Developmental Psychobiology, 61, 1079–1093. doi:10.1002/dev.21866CrossRefGoogle ScholarPubMed
Young, E. S., Farrell, A. K., Carlson, E. A., Englund, M. M., Miller, G. E., Gunnar, M. R., … Simpson, J. A. (2019). The dual impact of early and concurrent life stress on adults’ diurnal cortisol patterns: A prospective study. Psychological Science, 30, 739–747. doi:10.1177/0956797619833664CrossRefGoogle ScholarPubMed
Zorn, J. V., Schür, R. R., Boks, M. P., Kahn, R. S., Joëls, M., & Vinkers, C. H. (2017, March 1). Cortisol stress reactivity across psychiatric disorders: A systematic review and meta-analysis. Psychoneuroendocrinology, 77, 25–36. doi:10.1016/j.psyneuen.2016.11.036CrossRefGoogle ScholarPubMed