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Developmental changes in hypothalamus–pituitary–adrenal activity over the transition to adolescence: Normative changes and associations with puberty

Published online by Cambridge University Press:  15 January 2009

Megan R. Gunnar*
Affiliation:
University of Minnesota
Sandi Wewerka
Affiliation:
University of Minnesota
Kristin Frenn
Affiliation:
University of Minnesota
Jeffrey D. Long
Affiliation:
University of Minnesota
Christopher Griggs
Affiliation:
University of Minnesota
*
Address correspondence and reprint requests to: Megan R. Gunnar, Institute of Child Development, 51 East River Rd., University of Minnesota, Minneapolis, MN 55455; E-mail: gunnar@umn.edu.

Abstract

Home baseline and laboratory stressor (Trier Social Stress Test for Children) measures of salivary cortisol were obtained from 82 participants (40 girls) aged 9, 11, 13, and 15 years. Measures of pubertal development, self-reported stress, parent reports of child depressive symptoms and fearful temperament, and cardiac measures of sympathetic and parasympathetic activity were also obtained. Significant increases in the home cortisol baselines were found with age and pubertal development. Cortisol stress reactivity differed by age group with 11-year-olds and 13-year-old boys showing blunted reactivity and 9-year-olds, 13-year-old girls, and 15-year-olds showing significant cortisol reactions. Cortisol reactivity correlated marginally with sexual maturation. Measures of sympathetic activity revealed increased sympathetic modulation with age. Higher sympathetic tone was associated with more fearful temperament, whereas greater cortisol reactivity was associated with more anxious and depressed symptoms for girls. The importance of these findings for the hypothesis that puberty-associated increases in hypothalamic–pituitary–adrenal axis activity heightens the risk of psychopathology is discussed.

Type
Special Section Articles
Copyright
Copyright © Cambridge University Press 2009

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References

Achenbach, T. M., & Rescorla, L. A. (2001). Manual for the ASEBA school-age forms & profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, & Families.Google Scholar
Adam, E. K. (2006). Transactions among trait and state emotion and adolescent diurnal and momentary cortisol activity in naturalistic settings. Psychoneuroendocrinology, 31, 664679.CrossRefGoogle ScholarPubMed
Angold, A., & Costello, E. J. (2006). Puberty and depression. Child and Adolescent Psychiatric Clinics of North America, 15, 919937.CrossRefGoogle ScholarPubMed
Bakeman, R. (2005). Recommended effect size statistics for repeated measures designs. Behavioral Research Methods, 37, 379384.CrossRefGoogle ScholarPubMed
Blair, C. (2003). Behavioral inhibition and behavioral activation in young children: Relations with self-regulation and adaptation to preschool in children attending head start. Developmental Psychobiology, 42, 301311.CrossRefGoogle ScholarPubMed
Buske-Kirschbaum, A., Jobst, S., Psych, D., Wustmans, A., Kirschbaum, C., Rauh, W., et al. (1997). Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosomatic Medicine, 59, 419426.CrossRefGoogle ScholarPubMed
Buske-Kirschbaum, A., von Auer, K., Krieger, S., Weis, S., Rauh, W., & Hellhammer, D. (2003). Blunted cortisol responses to psychosocial stress in asthmatic children: A general feature of atopic disease? Psychosomatic Medicine, 65, 806810.CrossRefGoogle ScholarPubMed
Buss, A. H., & Plomin, R. (1984). Temperament: Early developing personality traits. Mahwah, NJ: Erlbaum.Google Scholar
Carver, C. S., & White, T. L. (1994). Behavioral inhibition, behavioral activation, and affective responses to reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology, 67, 319333.CrossRefGoogle Scholar
Clements, A. D., & Parker, R. C. (1998). The relationship between salivary cortisol concentrations in frozen versus mailed samples. Psychoneuroendocrinology, 23, 613616.CrossRefGoogle ScholarPubMed
Dahl, R. (2004). Adolescent brain development: A period of opportunities and vulnerabilities. Annals of the New York Academy of Science, 1021.CrossRefGoogle ScholarPubMed
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355391.CrossRefGoogle ScholarPubMed
Fitzmaurice, G. M., Laird, N. M., & Ware, J. H. (2004). Applied longitudinal analysis. New York: Wiley.Google Scholar
Gunnar, M. R., & Vazquez, D. (2006). Stress neurobiology and developmental psychopathology. In Cicchetti, D. & Cohen, D. (Eds.), Developmental psychopathology: Vol. 2. Developmental neuroscience (2nd ed., pp. 533577). New York: Wiley.Google Scholar
Hasler, G., Drevets, W., Manji, H., & Charney, D. (2004). Discovering endophenotypes of major depression. Neuropsychopharmacology, 29, 17651781.CrossRefGoogle ScholarPubMed
Kenny, F. M., Preeyasombat, C., & Migeon, C. J. (1966). Cortisol production rate. II. Normal infants, children and adults. Pediatrics, 37, 3442.CrossRefGoogle ScholarPubMed
Kenward, M. G., & Roger, J. J. (1997). Small sample inference for fixed effects form restricted maximum likelihood. Biometrics, 53, 983997.CrossRefGoogle Scholar
Kiess, W., Meidert, R. A., Dressensorfer, K., Schriever, U., Kessler, A., Konig, A., et al. (1995). Salivary cortisol levels throughout childhood and adolescence: Relation with age, pubertal stage, and weight. Pediatric Research, 37, 502506.CrossRefGoogle ScholarPubMed
Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999). Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus–pituitary–adrenal axis. Psychosomatic Medicine, 61, 154162.CrossRefGoogle ScholarPubMed
Kirschbaum, C., Pirke, K. M., & Hellhammer, D. (1993). The “Trier Social Stress Test”—A tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 7681.CrossRefGoogle Scholar
Kirschbaum, C., Wust, S., & Hellhammer, D. (1992). Consistent sex differences in cortisol responses to psychological stress. Psychosomatic Medicine, 54, 648657.CrossRefGoogle ScholarPubMed
Knutsson, U., Dahlgren, J., Marcus, C., Rosberg, S., Bronnegard, M., Stierna, P., et al. (1997). Circadian cortisol rhythms in healthy boys and girls: Relationship with age, growth, body composition and pubertal development. Journal of Clinical Endocrinology and Metabolism, 82, 536540.Google ScholarPubMed
Kudielka, B. M., Buske-Kirschbaum, A., Hellhammer, D. H., & Kirschbaum, C. (2004). HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: Impact of age and gender. Psychoneuroendocrinology, 29, 8398.CrossRefGoogle ScholarPubMed
Lang, P. J. (1980). Behavioral treatment and bio-behavior assessment: Computer applications. In Sidowski, J. B., Johnson, J. H., & Williams, T. A. (Eds.), Technology in mental health care delivery systems (pp. 119137). Norwood, NJ: Ablex.Google Scholar
Legro, R. S., Lin, H. M., Demers, L. M., & Lloyd, T. (2003). Urinary free cortisol increases in adolescent Caucasian females during perimenarche. Journal of Clinical Endocrinology and Metabolism, 88, 215219.CrossRefGoogle ScholarPubMed
Lenard, Z., Studinger, P., Merisch, B., Kocsis, L., & Kollai, M. (2004). Maturation of cardiovagal function from childhood to young adult age. Circulation, 110, 2307–2011.CrossRefGoogle ScholarPubMed
Lindahl, M., Theorell, T., & Lindblad, F. (2005). Test performance and self-esteem in relation to experienced stress in Swedish sixth and ninth graders: Salivary cortisol levels and psychological reactions to demands. Acta Pediatrica, 94, 489495.CrossRefGoogle Scholar
Massin, M., & von Bernuth, G. (1997). Normal ranges of heart rate variability during infancy and childhood. Pediatric Cardiology, 18, 297302.CrossRefGoogle ScholarPubMed
Meyer, S., Chrousos, G. P., & Gold, A. (2001). Major depression and the stress system: A life span perspective. Development and Psychopathology, 13, 565580.CrossRefGoogle ScholarPubMed
Netherton, C., Goodyer, I., Tamplin, A., & Herbert, J. (2004). Salivary cortisol and dehydroepiandrosterone in relation to puberty and gender. Psychoneuroendocrinology, 29, 125140.CrossRefGoogle ScholarPubMed
Petersen, A. C., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Reliability, validity, and initial norms. Journal of Youth and Adolescence, 17, 117133.CrossRefGoogle ScholarPubMed
Porges, S. W. (1985). U.S. Patent No. 4,510,944. Washington, DC: US Patent and Trademark Office.Google Scholar
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependant change. Psychoneuroendocrinology, 28, 916931.CrossRefGoogle Scholar
Scheifbein, V. L., & Susman, E. (2006). Cortisol levels and longitudinal cortisol change as predictors of anxiety in adolescents. Journal of Early Adolescence, 26, 397413.Google Scholar
Schwartz, E. B., Granger, D. A., Susman, E. J., Gunnar, M. R., & Laird, B. (1998). Assessing salivary cortisol in studies of child development. Child Development, 69, 15031513.CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17, 167184.CrossRefGoogle ScholarPubMed
Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417463.CrossRefGoogle ScholarPubMed
Stroud, L., Foster, E., Handwerger, K., Papandonatos, G. D., Granger, D., Kivlighan, K. T., et al. (2009). Stress response and the adolescent transition: Performance versus peer rejection stress. Development and Psychopathology, 21, 4768.CrossRefGoogle Scholar
Stroud, L., Papandonatos, G. D., Williamson, D. E., & Dahl, R. E. (2004). Sex differences in the effects of pubertal development on responses to corticotropin-releasing hormone challenge. Annals of the New York Academy of Science, 1021, 348351.CrossRefGoogle ScholarPubMed
Walker, E. F., Walder, D. J., & Reynolds, R. (2001). Developmental changes in cortisol secretion in normal and at-risk youth. Development and Psychopathology, 13, 721732.CrossRefGoogle ScholarPubMed
Weinstein, D. D., Diforio, D., Schiffman, J., Walker, E., & Bonsall, R. (1999). Minor physical anomalies, dermatoglyphic asymmetries, and cortisol levels in adolescents with schizotypal personality disorder. American Journal of Psychiatry, 156, 617623.CrossRefGoogle ScholarPubMed