Cortisol Stress Response Variability in Early Adolescence: Attachment, Affect and Sex
Attachment, affect, and sex shape responsivity to psychosocial stress. Concurrent social contexts influence cortisol secretion, a stress hormone and biological marker of hypothalamic–pituitary–adrenal axis activity. Patterns of attachment, emotion status, and sex were hypothesized to relate to bifurcated, that is, accentuated and attenuated, cortisol reactivity. The theoretical framework for this study posits that multiple individual differences mediate a cortisol stress response. The effects of two psychosocial stress interventions, a modified Trier Social Stress Test for Teens and the Frustration Social Stressor for Adolescents were developed and investigated with early adolescents. Both of these protocols induced a significant stress reaction and evoked predicted bifurcation in cortisol responses; an increase or decrease from baseline to reactivity. In Study I, 120 predominantly middle-class, Euro-Canadian early adolescents with a mean age of 13.43 years were studied. The girls’ attenuated cortisol reactivity to the public performance stressor related significantly to their self-reported lower maternal-attachment and higher trait-anger. In Study II, a community sample of 146 predominantly Euro-Canadian middle-class youth, with an average age of 14.5 years participated. Their self-reports of higher trait-anger and trait-anxiety, and lower parental attachment by both sexes related differentially to accentuated and attenuated cortisol reactivity to the frustration stressor. Thus, attachment, affect, sex, and the stressor contextual factors were associated with the adrenal-cortical responses of these adolescents through complex interactions. Further studies of individual differences in physiological responses to stress are called for in order to clarify the identities of concurrent protective and risk factors in the psychosocial stress and physiological stress responses of early adolescents.
KeywordsCortisol Adolescence Stress Attachment Affect Sex
We thank the adolescent participants in this study and appreciate the cooperation of their teachers and parents who assisted in supporting the data collection in Fredericton NB and Vancouver BC Canada. We also thank the numerous research assistants who made the research possible. We also offer thanks to E. Leslie Cameron for drawing the figures.
C.A.C. conceived of the two studies in collaboration with J.M.W. for Study I and S.M. for Study II. She also wrote first drafts of the manuscript and coordinated the development of its final form. J.M.W. designed and conducted Study I. S.M. designed and conducted Study II. She also performed the final statistical analyses of both Studies I and II and co-wrote the manuscript. E.J.S. collaborated in the design of both Studies I and II and the analyses of Study I. K.W.-E. and J.W. provided guidance in the conduct and analysis of Study II. All authors were consulted and they approved the final version of this paper.
Conflicts of interest
The authors report no conflict of interests.
Funding was generously provided by MindCareNew Brunswick for Study I and the Healthy Early Learning Partnership (HELP) at UBC for Study II.
Institutional Ethics Review Boards at the University of New Brunswick and the Fredericton NB School Board and the University of British Columbia and the Vancouver BC School Board approved the conduct of Studies I and II respectively. The ethical standards of the Canadian Psychological Association and the guidelines of the Society for Research in Child Development were rigorously adhered to.
Written informed consent was obtained from the parents/guardians of all participants and informed assent was obtained from all participants.
- Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: Sage.Google Scholar
- Ainsworth, M. D. S., Blehar, M. C., Waters, E., & Wall, S. (1978). Patterns of attachment: A psychological study of the strange situation. Hillsdale, NJ: Laurence Erlbaum.Google Scholar
- Allen, J. P., Hauser, S. T., O’Connor, T. G., & Bell, K. L. (2002). Prediction of peer-rated adult hostility from autonomy struggles in adolescent-family interactions. Development and Psychopathology, 14, 123–137. ISSN: 0954-5794.Google Scholar
- Beaton, E. A., Schmidt, L. A., Ashbaugh, A. R., Santesso, D. L., Antony, M. M., McCabe, R. E., et al. (2006). Low salivary cortisol levels among socially anxious young adults: Preliminary evidence from a selected and non-selected sample. Personality and Individual Differences, 41, 1217–1228. doi: 10.1016/j.paid.2006.02.020.CrossRefGoogle Scholar
- Bowlby, J. (1973). Attachment and loss: Vol. 2. Separation: Anxiety and anger. New York: Basic Books.Google Scholar
- Brain, P. F., & Susman, E. J. (1997). Hormonal aspects of aggression and violence. In D. M. Stoff, J. Breiling, & J. D. Maser (Eds.), Handbook of antisocial behavior (pp. 314–323). New York, NY: Wiley.Google Scholar
- Burghy, C. A., Stodola, D. E., Ruttle, P. L., Molloy, E. K., Armstrong, J. M., Oler, J. A., et al. (2012). Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nature Neuroscience, 15(12), 1736–1741. doi: 10.1038/nn.3257.PubMedPubMedCentralCrossRefGoogle Scholar
- Cohen, J., & Cohen, P. (1983). Applied multiple regression/correlation analysis for the behavioral sciences (2nd ed.). New Jersey, NY: Lawrence Erlbaum.Google Scholar
- Deffenbacher, J. L. (1992). Trait-anger: Theory, findings and implications. In J. N. Butcher & C. D. Spielberger (Eds.), Advances in personality assessment (Vol. 9, pp. 177–201). Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
- Essex, M. J., Boyce, T. W., Hertzman, C., Lam, L. L., Armstrong, J. M., Neumann, S. M. A., et al. (2011a). Epigenetic vestiges of early developmental adversity: Childhood exposure and methylation in adolescence. Child Development, 84(1), 58–75. doi: 10.1111/j.1467-8624.2011.01641.x.PubMedPubMedCentralCrossRefGoogle Scholar
- Essex, M. J., Shirtcliff, E. A., Burk, L. R., Ruttle, P. L., Klein, M. H., Slattery, M. J., et al. (2011b). Influence of early life stress on later hypothalamic–pituitary–adrenal axis functioning and its covariation with mental health symptoms: A study of the allostatic process from childhood into adolescence. Development and Psychopathology, 23, 1039–1058. doi: 10.1017/S0954579411000484.PubMedPubMedCentralCrossRefGoogle Scholar
- Fivush, R., & Waters, T. E. A. (2015). Patterns of attachments across the lifespan. In R. A. Scott & S. M. Kosselyn (Eds.), Emerging trends in the behavioral sciences: An interdisciplinary, searchable, and linkable resource. Wiley Online Library. doi: 10.1002/9781118900772.
- Gordis, E. B., Granger, D. A., Susman, E. J., & Tricket, P. K. (2006). Salivary alpha-amylase and cortisol response to social stress among maltreated and comparison youth. Paper presented at Biennial Meeting of the Society for Research on Adolescence, San Francisco, CA.Google Scholar
- Granger, D., Serbin, L., Schwartzman, A., Lehoux, P., Cooperman, J., & Ikeda, S. (1998). Children’s salivary cortisol, internalising behaviour problems, and family environment: Results from the Concordia Longitudinal Risk Project. International Journal of Behavioral Development, 22, 707–728. doi: 10.1080/016502598384135.CrossRefGoogle Scholar
- Gunnar, M. R., Wewerka, S., Frenn, K., Long, J. D., & Griggs, C. (2009). Developmental changes in hypothalamus–pituitary–adrenal activity over transition to adolescence: Normative changes and associations with puberty. Developmental Psychopathology, 21, 69–85. doi: 10.1017/S0954579409000054.CrossRefGoogle Scholar
- Hammerfald, K., Eberle, C., Grau, M., Kinsperger, A., Zimmerman, A., Ehlert, U., et al. (2006). Persistent effects of cognitive-behavioral stress management on cortisol responses to acute stress in healthy subjects: A randomized controlled trial. Psychoneuroendocrinology, 31, 333–339. doi: 10.1016/j.psyneuen.2005.08.007.PubMedCrossRefGoogle Scholar
- Howe, D. (2011). Attachment across the lifecourse: A brief introduction. Basingstoke UK: Palgrave Macmillan.Google Scholar
- Jeliki, H., Bobek, D. L., Phelps, E., Lerner, R. M., & Lerner, J. V. (2007). Using positive youth development to predict contribution and risk behaviors in early adolescence: Findings from the first two waves of the 4-H Study of Positive Youth Development. International Journal of Behavioral Development, 31, 263–273. doi: 10.1177/0165025407076439.CrossRefGoogle Scholar
- Kassinove, H., & Sukhodolsky, D. G. (1995). Anger disorders: Basic science and practice issues. In H. Kassinove (Ed.), Anger disorders: Definition, diagnosis, and treatment (pp. 1–26). Washington, DC: Taylor & Francis.Google Scholar
- Kirschbaum, C. (2010). Trier Social Stress Test. In I. P. Stolerman (Ed.), Encyclopedia of psychopharmacology (pp. 1–3). Berlin: Springer.Google Scholar
- Kirschbaum, C., & Hellhammer, D. H. (2007). Salivary cortisol. In G. Fink (Editor-in-Chief), Encyclopedia of stress, 2nd Ed. (Vol. 3, pp. 405–409). Oxford: Academic Press.Google Scholar
- Klein, L. C., & Corwin, E. J. (2002). Seeing the unexpected: How sex differences in stress responses may provide a new perspective on the manifestation of psychiatric disorders. Current Psychiatry Reports, 4(6), 441–448. doi: 10.1007/s11920-002-0072-z.
- Klimes-Dougan, B., Hastings, P. D., Granger, D. A., Usher, B. A., & Zahn-Waxler, C. (2001). Adrenocortical activity in at-risk and normally developing adolescents: Individual differences in salivary cortisol basal levels, diurnal variation, and responses to social challenges. Development and Psychopathology, 13(3), 695–719.PubMedCrossRefGoogle Scholar
- Kudielka, B. M., Hellhammer, D. H., & Kirschbaum, C. (2007). Sex differences in human stress response. In G. Fink (Editor-in-Chief), Encyclopedia of stress, 2nd Ed. (Vol. 3, pp. 469–473). Oxford: Academic Press.Google Scholar
- Kudielka, B. M., Wüst, S., Kirschbaum, C., & Hellhammer, D. H. (2007). Trier Social Stress Test. In G. Fink (Editor-in-Chief), Encyclopedia of stress, 2nd Ed. (Vol. 3, pp. 776–781). Oxford: Academic Press.Google Scholar
- Löckenhoff, C. E., Costa Jr., P. T. & Lane, R. D. (2008). Age differences in descriptions of experiences in oneself and others. Journal of Gerontology: Psychological Sciences, 63B(2), 92–99. Online ISSN 1758-5368, Print ISSN 1079-5014.Google Scholar
- Luthar, S. S. (Ed.). (2003). Resilience and vulnerability: Adaptation in the context of childhood adversities. Cambridge: Cambridge University Press.Google Scholar
- Martorell, G. A. (2002). Maternal and child adrenocortical responses as a function of attachment classification, temperament, and maternal care giving attributions. Dissertation Abstracts International, 62(7-B), 3401.Google Scholar
- Natsuaki, M. N., Klimes-Dougan, B., Ge, X., Shirtcliff, E. A., Hastings, P. D., & Zahn-Waxler, C. (2009). Early pubertal maturation and internalizing problems in adolescence: Sex differences in the role of cortisol reactivity to interpersonal stress. Journal of Clinical Child & Adolescent Psychology, 38(4), 513–524. doi: 10.1080/15374410902976320.CrossRefGoogle Scholar
- Perry, B. D. (2001). The neurodevelopmental impact of violence in childhood. In D. Schetky & E. Benedek (Eds.), Textbook of child and adolescent forensic psychiatry (pp. 221–238). Washington, DC: American Psychiatric Press Inc.Google Scholar
- Pesonen, A.-K., & Räikkönen, K. (2011). Mental health of children evacuated during World War II. In H. E. Fitzgerald, K. Puura, M. Tomlinson, & C. Paul (Eds.), International perspectives on children and mental health, Volume 1: Development and context (pp. 197–216). Santa Barbara, CA: Praeger Publishers.Google Scholar
- Petersen, A. C., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of puberty status: Reliability, validity, and initial norms. Journal of Youth and Adolescence, 17(2), 117–133. doi: 10.1007/BF01537962.
- 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. doi: 10.1016/S0306-4530(02)00108-7.PubMedCrossRefGoogle Scholar
- Ruttle, P. L., Shirtcliff, E. A., Serbin, L. A., Fisher, D. B.-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.2010.10.015.PubMedCrossRefGoogle Scholar
- Schore, A. N. (2012). The science of the art of psychotherapy. New York NY: Norton.Google Scholar
- Shih, J. H., Eberhart, N. K., Haammen, C. L., & Brennan, P. A. (2006). Differential exposure and reactivity to interpersonal stress predict sex differences in adolescent depression. Journal of Clinical Child & Adolescent Psychology, 35(1), 103–115. doi: 10.1207/s15374424jccp3501_9.CrossRefGoogle Scholar
- Spielberger, C. D. (1988). STAI: State-Trait Anxiety Inventory (self-evaluation questionnaire). Palo Alto, CA: Consulting Psychologists Press.Google Scholar
- Spielberger, C. D. (1999). STAXI-2: State-Trait Anger Expression Inventory—2 (professional manual). Lutz, FL: Psychological Assessment Resources.Google Scholar
- Steiner, H., Ryst, E., Berkowitz, J., Gschwendt, M. A., & Koopman, C. (2002). Boys’ and girls’ responses to stress: Affect and heart rate during a speech task. Journal of Adolescent Health, 30, 14–21.Google Scholar
- Susman, E. J., & Pajer, K. (2004). Biology-behavior integration and antisocial behavior in girls. In M. Putallaz & K. Bierman (Eds.), Aggression, antisocial behavior and violence among girls: A developmental perspective. New York: Guilford Publications.Google Scholar
- Susman, E. J., & Rogol, A. (2004). Puberty and psychological development. In R. M. Lerner & L. Steinberg (Eds.), Handbook of adolescent psychology (pp. 15–44). New York: Wiley.Google Scholar
- Tabachnick, B. G., & Fidell, L. S. (2001). Using multivariate statistics (4th ed.). Needham Heights, MA: Allyn and Bacon.Google Scholar
- Takahashi, T., Ikeda, K., Ishikawa, M., Kitamura, N., Tsukasaki, T., Nakama, D., et al. (2006). Anxiety, reactivity, and social stress-induced cortisol elevations in humans. Neuroendocrinology Letters, 26(4), 351–354.Google Scholar
- van den Bos, E., de Rooij, M., Miers, A. C., Bokhorst, C. L., & Westenberg, P. M. (2014). Adolescents’ increasing stress response to social evaluation: Pubertal effects on cortisol and alpha-amylase during public speaking. Child Development, 85(1), 220–236. doi: 10.1111/cdev.12118.PubMedCrossRefGoogle Scholar
- van de Wiel, N. M., van Goozen, S. H., Matthys, W., Snoek, H., & van Engeland, H. (2004). Cortisol and treatment effect in children with disruptive behavior disorders: A preliminary study. Journal of the American Academy of Child and Adolescent Psychiatry, 43(8), 1011–1018. doi: 10.1097/01.chi.0000126976.56955.43.PubMedCrossRefGoogle Scholar
- van de Wiel, N. M., Matthys, S. H., Snoek, H., & van Engeland, H. (2004). Cortisol and treatment effect in children with disruptive behavior disorders: A preliminary study. Journal of the American Academy of Child and Adolescent Psychiatry, 43(8), 1011–1018. doi: 10.1097/01.chi.0000126976.56955.43.PubMedCrossRefGoogle Scholar
- Weinfield, N. S., Sroufe, L. A., Egeland, B., & Carlson, E. A. (1999). The nature of individual differences in infant-caregiver attachment. In J. Cassidy & P. R. Shaver (Eds.), Handbook of attachment: Theory, research and clinical practice (pp. 68–88). New York, NY: Guilford.Google Scholar