Skip to main content Accessibility help

Poverty, early care, and stress reactivity in adolescence: Findings from a prospective, longitudinal study in South Africa

  • R. M. Pasco Fearon (a1), Mark Tomlinson (a2) (a3), Robert Kumsta (a4), Sarah Skeen (a2), Lynne Murray (a2) (a5) (a6), Peter J. Cooper (a2) (a5) (a6) and Barak Morgan (a3) (a6) (a7)...


A considerable body of evidence suggests that early caregiving may affect the short-term functioning and longer term development of the hypothalamic–pituitary–adrenocortical axis. Despite this, most research to date has been cross-sectional in nature or restricted to relatively short-term longitudinal follow-ups. More important, there is a paucity of research on the role of caregiving in low- and middle-income countries, where the protective effects of high-quality care in buffering the child's developing stress regulation systems may be crucial. In this paper, we report findings from a longitudinal study (N = 232) conducted in an impoverished periurban settlement in Cape Town, South Africa. We measured caregiving sensitivity and security of attachment in infancy and followed children up at age 13 years, when we conducted assessments of hypothalamus–pituitary–adrenocortical axis reactivity, as indexed by salivary cortisol during the Trier Social Stress Test. The findings indicated that insecure attachment was predictive of reduced cortisol responses to social stress, particularly in boys, and that attachment status moderated the impact of contextual adversity on stress responses: secure children in highly adverse circumstances did not show the blunted cortisol response shown by their insecure counterparts. Some evidence was found that sensitivity of care in infancy was also associated with cortisol reactivity, but in this case, insensitivity was associated with heightened cortisol reactivity, and only for girls. The discussion focuses on the potentially important role of caregiving in the long-term calibration of the stress system and the need to better understand the social and biological mechanisms shaping the stress response across development in low- and middle-income countries.


Corresponding author

Address correspondence and reprint requests to: R. M. Pasco Fearon, Research Department of Clinical, Educational and Health Psychology, University College London, 1-19 Torrington Place, London WC1E 7HB, UK; E-mail:


Hide All

This study was supported by a grant from Grand Challenges Canada (Grant 0066-03). Mark Tomlinson is supported by the National Research Foundation, South Africa, for his role as a Lead Investigator with the Centre of Excellence in Human Development, University of the Witwatersrand, South Africa.



Hide All
Ainsworth, M. S., Blehar, M. C., Waters, E., & Wall, S. (1978). Patterns of attachment: A psychological study of the Strange Situation (Vol. 18). Hillsdale, NJ: Erlbaum.
Albers, E. M., Riksen-Walraven, J. M., Sweep, F. C., & Weerth, C. D. (2008). Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. Journal of Child Psychology and Psychiatry, 49, 97103.
Alink, L. R., 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, 427450.
Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Mesman, J., Alink, L. R., & Juffer, F. (2008). Effects of an attachment-based intervention on daily cortisol moderated by dopamine receptor D4: A randomized control trial on 1- to 3-year-olds screened for externalizing behavior. Development and Psychopathology, 20, 805820.
Barry, T. J., Murray, L., Fearon, R. P., Moutsiana, C., Cooper, P., Goodyer, I. M., … Halligan, S. L. (2015). Maternal postnatal depression predicts altered offspring biological stress reactivity in adulthood. Psychoneuroendocrinology, 52, 251260.
Bernard, K., Dozier, M., Bick, J., & Gordon, M. K. (2015). Intervening to enhance cortisol regulation among children at risk for neglect: Results of a randomized clinical trial. Development and Psychopathology, 27, 829841.
Berry, D., Blair, C., Willoughby, M., Granger, D. A., & Family Life Project Key Investigators. (2012). Salivary alpha-amylase and cortisol in infancy and toddlerhood: Direct and indirect relations with executive functioning and academic ability in childhood. Psychoneuroendocrinology, 37, 17001711.
Blair, C., Berry, D., Mills-Koonce, R., Granger, D., & Family Life Project Key Investigators. (2013). Cumulative effects of early poverty on cortisol in young children: Moderation by autonomic nervous system activity. Psychoneuroendocrinology, 38, 26662675.
Blair, C., Granger, D., & Peters Razza, R. (2005). Cortisol reactivity is positively related to executive function in preschool children attending head start. Child Development, 76, 554567.
Blair, C., Granger, D., Willoughby, M., & Kivlighan, K. (2006). Maternal sensitivity is related to hypothalamic–pituitary–adrenal axis stress reactivity and regulation in response to emotion challenge in 6-month-old infants. Annals of the New York Academy of Sciences, 1094, 263267.
Blair, C., Granger, D. A., Willoughby, M., Mills-Koonce, R., Cox, M., Greenberg, M. T., … Fortunato, C. K. (2011). Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood. Child Development, 82, 19701984.
Bouma, E. M., Riese, H., Ormel, J., Verhulst, F. C., & Oldehinkel, A. J. (2009). Adolescents' cortisol responses to awakening and social stress; effects of gender, menstrual phase and oral contraceptives. The TRAILS study. Psychoneuroendocrinology, 34, 884893.
Boyle, M. H., & Willms, J. D. (2001). Multilevel modelling of hierarchical data in developmental studies. Journal of Child Psychology and Psychiatry, 42, 141162.
Burgess, K. B., Marshall, P. J., Rubin, K. H., & Fox, N. A. (2003). Infant attachment and temperament as predictors of subsequent externalizing problems and cardiac physiology. Journal of Child Psychology and Psychiatry, 44, 819831.
Cicchetti, D., Rogosch, F. A., Gunnar, M. R., & Toth, S. L. (2010). The differential impacts of early physical and sexual abuse and internalizing problems on daytime cortisol rhythm in school-aged children. Child Development, 81, 252269.
Conradt, E., Hawes, K., Guerin, D., Armstrong, D. A., Marsit, C. J., Tronick, E., & Lester, B. M. (2016). The contributions of maternal sensitivity and maternal depressive symptoms to epigenetic processes and neuroendocrine functioning. Child Development, 87, 7385.
Cooper, P. J., Tomlinson, M., Swartz, L., Landman, M., Molteno, C., Stein, A., … Murray, L. (2009). Improving quality of mother-infant relationship and infant attachment in socioeconomically deprived community in South Africa: Randomised controlled trial. British Medical Journal, 338, 974.
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 15621592.
De Wolff, M., & van IJzendoorn, M. H. (1997). Sensitivity and attachment: A meta-analysis on parental antecedents of infant attachment. Child Development, 68, 571591.
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355391.
Doan, S. N., Tardif, T., Miller, A., Olson, S., Kessler, D., Felt, B., & Wang, L. (2016). Consequences of “tiger” parenting: A cross-cultural study of maternal psychological control and children's cortisol stress response. Developmental Science. Advance online publication. doi:10.1111/desc.12404
Fearon, R. M. P., & Belsky, J. (2016). Precursors of attachment. In Cassidy, J. & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research and clinical applications (3rd ed., pp. 291313). New York: Guilford Press.
Fernald, L. C., & Gunnar, M. R. (2009). Poverty-alleviation program participation and salivary cortisol in very low-income children. Social Science & Medicine, 68, 21802189.
Flinn, M. V., & England, B. G. (1997). Social economics of childhood glucocorticoid stress response and health. American Journal of Physical Anthropology, 102, 3353.
Frodl, T., & O'Keane, V. (2013). How does the brain deal with cumulative stress? A review with focus on developmental stress, HPA axis function and hippocampal structure in humans. Neurobiology of Disease, 52, 2437.
Gotlib, I. H., Joormann, J., Minor, K. L., & Hallmayer, J. (2008). HPA axis reactivity: A mechanism underlying the associations among 5-HTTLPR, stress, and depression. Biological Psychiatry, 63, 847851.
Guerry, J. D., & Hastings, P. D. (2011). In search of HPA axis dysregulation in child and adolescent depression. Clinical Child and Family Psychology Review, 14, 135160.
Gunnar, M. R. (1998). Quality of early care and buffering of neuroendocrine stress reactions: Potential effects on the developing human brain. Preventive Medicine, 27, 208211.
Gunnar, M. R., Brodersen, L., Nachmias, M., Buss, K., & Rigatuso, J. (1996). Stress reactivity and attachment security. Developmental Psychobiology, 29, 191204.
Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199220.
Gunnar, M. R., & Fisher, P. A. (2006). Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Development and Psychopathology, 18, 651677.
Gunnar, M. R., & Quevedo, K. M. (2007). Early care experiences and HPA axis regulation in children: A mechanism for later trauma vulnerability. Progress in Brain Research, 167, 137149.
Haley, D. W., & Stansbury, K. (2003). Infant stress and parent responsiveness: Regulation of physiology and behavior during still-face and reunion. Child Development, 74, 15341546.
Halligan, S. L., Herbert, J., Goodyer, I., & Murray, L. (2007). Disturbances in morning cortisol secretion in association with maternal postnatal depression predict subsequent depressive symptomatology in adolescents. Biological Psychiatry, 62, 4046.
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, 256282.
Kertes, D. A., Donzella, B., Talge, N. M., Garvin, M. C., Van Ryzin, M. J., & Gunnar, M. R. (2009). Inhibited temperament and parent emotional availability differentially predict young children's cortisol responses to novel social and nonsocial events. Developmental Psychobiology, 51, 521532.
Loman, M. M., & Gunnar, M. R. (2010). Early experience and the development of stress reactivity and regulation in children. Neuroscience & Biobehavioral Reviews, 34, 867876.
Lopez-Duran, N. L., Kovacs, M., & George, C. J. (2009). Hypothalamic-pituitary-adrenal axis dysregulation in depressed children and adolescents: A meta-analysis. Psychoneuroendocrinology, 34, 12721283.
Luijk, M. P., Saridjan, N., Tharner, A., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Jaddoe, V. W., … Tiemeier, H. (2010). Attachment, depression, and cortisol: Deviant patterns in insecure-resistant and disorganized infants. Developmental Psychobiology, 52, 441452.
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434445.
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 3344.
McLaughlin, K. A., Sheridan, M. A., Tibu, F., Fox, N. A., Zeanah, C. H., & Nelson III, 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, 56375642.
Mesman, J., van IJzendoorn, M. H., & Sagi-Schwartz, A. (2016). Cross-cultural patterns of attachment: Universal and contextual dimensions. In Cassidy, J. & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research and clinical application (3rd ed., pp. 852877). New York: Guilford Press.
Murray, L., Fiori-Cowley, A., Hooper, R., & Cooper, P. (1996). The impact of postnatal depression and associated adversity on early mother-infant interactions and later infant outcome. Child Development, 67, 25122526.
Nachmias, M., Gunnar, M., Mangelsdorf, S., Parritz, R. H., & Buss, K. (1996). Behavioral inhibition and stress reactivity: The moderating role of attachment security. Child Development, 67, 508522.
Panter-Brick, C., Worthman, C., Lunn, P., Baker, R., & Todd, A. (1996). Urban-rural and class differences in biological markers of stress among Nepali children. Paper presented at the American Journal of Human Biology Conference.
Roisman, G. I., Susman, E., Barnett-Walker, K., Booth-LaForce, C., Owen, M. T., Belsky, J., … NICHD Early Child Care Research Network. (2009). Early family and child-care antecedents of awakening cortisol levels in adolescence. Child Development, 80, 907920.
Rosmond, R. (2003). Stress induced disturbances of the HPA axis: A pathway to type 2 diabetes? Medical Science Monitor Basic Research, 9, RA35RA39.
Rosmond, R., Dallman, M. F., & Bjorntorp, P. (1998). Stress-related cortisol secretion in men: Relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities 1. Journal of Clinical Endocrinology & Metabolism, 83, 18531859.
Schieche, M., & Spangler, G. (2005). Individual differences in biobehavioral organization during problem-solving in toddlers: The influence of maternal behavior, infant-mother attachment, and behavioral inhibition on the attachment-exploration balance. Developmental Psychobiology, 46, 293306.
Schoofs, D., Wolf, O. T., & Smeets, T. (2009). Cold pressor stress impairs performance on working memory tasks requiring executive functions in healthy young men. Behavioral Neuroscience, 123, 1066.
Shields, G. S., Bonner, J. C., & Moons, W. G. (2015). Does cortisol influence core executive functions? A meta-analysis of acute cortisol administration effects on working memory, inhibition, and set-shifting. Psychoneuroendocrinology, 58, 91103.
Spangler, G. (1998). Emotional and adrenocortical responses of infants to the strange situation: The differential function of emotional expression. International Journal of Behavioral Development, 22, 681706.
Spangler, G., & Grossmann, K. E. (1993). Biobehavioral organization in securely and insecurely attached infants. Child Development, 64, 14391450.
Spangler, G., & Zimmermann, P. (2014). Emotional and adrenocortical regulation in early adolescence: Prediction by attachment security and disorganization in infancy. International Journal of Behavioral Development, 38, 142154.
Sturge-Apple, M. L., Davies, P. T., Cicchetti, D., & Manning, L. G. (2012). Interparental violence, maternal emotional unavailability and children's cortisol functioning in family contexts. Developmental Psychology, 48, 237.
Takai, N., Yamaguchi, M., Aragaki, T., Eto, K., Uchihashi, K., & Nishikawa, Y. (2007). Gender-specific differences in salivary biomarker responses to acute psychological stress. Annals of the New York Academy of Sciences, 1098, 510515.
Thompson, L. A., & Trevathan, W. R. (2008). Cortisol reactivity, maternal sensitivity, and learning in 3-month-old infants. Infant Behavior and Development, 31, 92106.
Tout, K., de Haan, M., Campbell, E. K., & Gunnar, M. R. (1998). Social behavior correlates of cortisol activity in child care: Gender differences and time-of-day effects. Child Development, 69, 12471262.
van IJzendoorn, M. H. (1995). Adult attachment representations, parental responsiveness, and infant attachment: A meta-analysis on the predictive validity of the Adult Attachment Interview. Psychological Bulletin, 117, 387403.
Verhage, M. L., Schuengel, C., Madigan, S., Fearon, R. M., Oosterman, M., Cassibba, R., … van IJzendoorn, M. H. (2016). Narrowing the transmission gap: A synthesis of three decades of research on intergenerational transmission of attachment. Psychological Bulletin, 142, 337366.
Wolf, O. (2003). HPA axis and memory. Best Practice & Research Clinical Endocrinology & Metabolism, 17, 287299.


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed