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Low salivary cortisol levels and externalizing behavior problems in youth

Published online by Cambridge University Press:  07 April 2005

ELIZABETH A. SHIRTCLIFF ,
DOUGLAS A. GRANGER ,
ALAN BOOTH  and
DAVID JOHNSON
ELIZABETH A. SHIRTCLIFF
Affiliation:
University of Wisconsin
DOUGLAS A. GRANGER
Affiliation:
Pennsylvania State University
ALAN BOOTH
Affiliation:
Pennsylvania State University
DAVID JOHNSON
Affiliation:
Pennsylvania State University
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Abstract

Research linking basal cortisol levels with internalizing and externalizing behavior problems in youths has yielded inconsistent results. We hypothesize that the high moment to moment variation in adrenocortical activity requires an analytical strategy that separates variance in cortisol levels attributable to “stable traitlike” versus “state or situationally specific” sources. Early morning saliva samples were obtained from 724 youths (M age = 13.5 years; range = 6–16 years in Year 1) on 2 successive days 1 year apart. Latent state–trait modeling revealed that 70% of the variance in cortisol levels could be attributed to statelike sources, and 28% to traitlike sources. For boys only, higher levels of externalizing problem behaviors were consistently associated with lower cortisol attributable to traitlike sources across 3 years of behavioral assessment. The inverse association between individual differences in cortisol and externalizing problem behavior has previously only been reported in studies of at-risk or clinical groups. The present findings suggest the relationship is a stable phenomenon that spans both normative and atypical child development. Studies are needed to reveal the biosocial mechanisms involved in the establishment and maintenance of this phenomenon, and to decipher whether individual differences in this hormone–behavior link confers risk or resilience.This research was supported in part by the Behavioral Endocrinology Laboratory, and the Population Research Institute (PRI) at Pennsylvania State University, as well as the W. T. Grant Foundation (Grant 9617796). PRI has core support from the National Institute of Child Health and Development (Grant 1-HD28263). Collection of data on family process and child psychosocial functioning was supported by two grants from the National Institute of Child Health and Human Development (HD 32336 and HD 29409) to Ann Crouter and Susan McHale.

Type
Research Article
Information
Development and Psychopathology , Volume 17 , Issue 1 , March 2005 , pp. 167 - 184
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Adam, E. K. (2002, April). Momentary emotion and cortisol activity in adolescents' everyday lives. Paper presented at the Society for Research on Adolescents, New Orleans, LA.
Ashman, S. B., Dawson, G., Panagiotides, H., Yamada, E., & Wilkinson, C. W. (2002). Stress hormone levels of children of depressed mothers. Development and Psychopathology 14, 333–349.Google Scholar
Bollen, K. A. (1989). Structural equations with latent variables. New York: Wiley.
Booth, A., Carver, K., & Granger, D. A. (2000). Biosocial perspectives on the family. Journal of Marriage and Family 62, 1018–1034.Google Scholar
Booth, A., Johnson, D., Granger, D. A., Crouter, A., & McHale, S. (2003). Testosterone and child and adolescent adjustment: The moderating role of parent–child relationships. Developmental Psychology 39, 85–98.Google Scholar
Brennan, P., & Raine, A. (1997). Biosocial bases of antisocial behavior: Psychophysiological, neurological, and cognitive factors. Clinical Psychology Review 17, 589–604.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology 13, 783–804.Google Scholar
Colomina, M. T., Canals, J., Carbajo, G., & Domingo, J. L. (1997). Salivary cortisol in a young population: Relationship with psychopathological disorders. Research Communications in Biological Psychology and Psychiatry 22, 1–10.Google Scholar
Dabbs, J. M., Jr. (1991). Salivary testosterone measurements: Collecting, storing, and mailing saliva samples. Physiology and Behavior 49, 815–817.Google Scholar
Dahl, R. E., Puig–Antich, J., Ryan, N., Nelson, B., Novacenko, H., Twomey, J., Williamson, D., Goetz, R., & Amrosini, P. (1989). Cortisol secretion in adolescents with major depressive disorder. Acta Psychiatrica Scandinavia 80, 18–21.Google Scholar
Dahl, R. E., Ryan, N. D., Nguyen, N. A., Al-Shabbout, M., Meyer, V. A., & Perel, J. (1991). 24-hour cortisol measures in adolescents with major depression: A controlled study. Biological Psychiatry 30, 26–36.Google Scholar
Davis, E. P., Donzella, B., Krueger, W. K., & Gunnar, M. R. (1999). The start of a new school year: Individual differences in salivary cortisol response in relation to child temperament. Developmental Psychobiology 35, 188–196.Google Scholar
de Haan, M., Gunnar, M. R., Tout, K., Hart, J., & Stansbury, K. (1998). Familiar and novel contexts yield different associations between cortisol and behavior among 2-year-old children. Developmental Psychobiology 33, 93–101.Google Scholar
Deinzer, R., Steyer, R., Eid, M., Notz, P., Schwenkmezger, P., Ostendorf, F., & Neubauer, A. (1995). Situational effects in psychological assessment of traits: The FPI, NEOFFI, and EPI questionnaires. European Journal of Personality 9, 1–23.Google Scholar
Devins, G., & Ore, C. (1985). Center for Epidemiological Studies Depression Scale. In D. Keyser & R. Sweetland (Eds.), Test critiques (pp. 144–160). Kansas City, MO: Test Corporation of America.
Dumenci, L., & Windle, M. (1998). A multitrait-multioccasion generalization of the latent trait–state model: Description and application. Structural Equation Modeling 5, 391–410.Google Scholar
Eccles, J., & Barber, B. (1990). The risky behavior scale. Unpublished manuscript, University of Michigan.
Essman, W. B. (1981). Drug effects upon aggressive behavior. In I. Valzelli & I. Morgese (Eds.), Aggression and violence: A psychobiological and clinical approach (pp. 150–175). Edizioni Saint Vincent: Edizioni Centro Culturale E Congressi Saint Vincent.
Finkelstein, J. W., Susman, E. J., Chinchilli, V. M., Kunselman, S. J., D'Arcangelo, M. R., Schwab, J., Demers, L. M., Liben, L. S., Lookingbill, G., & Kulin, H. E. (1997). Estrogen or testosterone increases self-reported aggressive behaviors in hypogonadal adolescents. Journal of Clinical Endocrinology and Metabolism 82, 2433–2438.Google Scholar
Flinn, M. V., & England, B. G. (1995). Childhood stress and family environment. Current Anthropology 36, 854–866.Google Scholar
Gimbel, C., & Booth, A. (1996). Who fought in Vietnam? Social Forces 786, 1137–1157.Google Scholar
Goodyer, I. M., Herbert, J., & Altham, P. M. (1998). Adrenal steroid secretion and major depression in 8- to 16-year-olds, III. Influence of cortisol/DHEA ratio at presentation on subsequent rates of disappointing life events and persistent major depression. Psychological Medicine 28, 265–273.Google Scholar
Goodyer, I. M., Herbert, J., Altham, P. M., Pearson, J., Secher, S. M., & Shiers, H. M. (1996). Adrenal secretion during major depression in 8- to 16-year-olds, I. Altered diurnal rhythms in salivary cortisol and dehydroepiandrosterone (DHEA) at presentation. Psychological Medicine 26, 245–256.Google Scholar
Goodyer, I. M., Herbert, J., Moor, S., & Altham, P. M. (1991). Cortisol hypersecretion in depressed school-aged children and adolescents. Psychiatry Research 37, 237–244.Google Scholar
Goodyer, I. M., Herbert, J., Tamplin, A., & Altham, P. M. (2000). Recent life events, cortisol, dehydroepiandrosterone and the onset of major depression in high-risk adolescents. British Journal of Psychiatry 177, 499–504.Google Scholar
Goodyer, I. M., Park, R. J., & Herbert, J. (2001). Psychosocial and endocrine features of chronic first-episode major depression in 8–16 year olds. Biological Psychiatry 50, 351–357.Google Scholar
Granger, D. A., & Kivlighan, K. T. (2003). The biosocial model and child development research. Child Development 74, 1058–1063Google Scholar
Granger, D. A., Serbin, L. A., Schwartzman, A. E., Lehoux, P. M., Cooperman, J. M., & Ikeda, S. (1998). Children's salivary cortisol, internalizing behavior problems, and family environment: Results from the Concordia Longitudinal Risk Project. International Journal of Behavioral Development 22, 707–728.Google Scholar
Granger, D. A., Shirtcliff, E. A., Zahn–Waxler, C., Usher, B. A., Klimes–Dougan, B., & Hastings, P. D. (2003). Adolescent internalizing and externalizing behavior problems predict individual differences in testosterone diurnal variation. Development and Psychopathology 15, 431–449.Google Scholar
Granger, D. A., Stansbury, K., & Henker, B. (1994). Preschooler's behavioral and neuroendocrine responses to social challenge. Merrill–Palmer Quarterly 40, 20–41.Google Scholar
Granger, D. A., Weisz, J. R., & Kauneckis, D. (1994). Neuroendocrine reactivity, internalizing behavior problems and control-related cognitions in clinic-referred children and adolescents. Journal of Abnormal Psychology 103, 267–276.Google Scholar
Granger, D. A., Weisz, J. R., McCracken, J. T., Ikeda, S. C., & Douglas, P. (1996). Reciprocal influences among adrenocortical activation, psychosocial processes, and the behavioral adjustment of clinic-referred children. Child Development 67, 3250–3262.Google Scholar
Gunnar, M. (2001). The role of glucocorticoids in anxiety disorders: A critical analysis. In M. V. Vasey & M. R. Dadds (Eds.), The developmental psychopathology of anxiety (pp. 143–159). New York: Oxford University Press.
Gunnar, M., Bruce, J., & Donzella, B. (2000). Stress physiology, health, and behavioral development. In A. Thornton (Ed.), The well-being of children and families: Research and data needs (pp. 188–212). Ann Arbor, MI: University of Michigan Press.
Gunnar, M. R., Tout, K., de Haan, M., Pierce, S., & Stansbury, K. (1997). Temperament, social competence, and adrenocortical activity in preschoolers. Developmental Psychobiology 31, 65–85.Google Scholar
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology 13, 515–538.Google Scholar
Hammen, C., Henry, R., & Daley, S. E. (2000). Depression and sensitization to stressors among young women as a function of childhood adversity. Journal of Consulting and Clinical Psychology 68, 782–787.Google Scholar
Heim, C., Ehlert, U., & Hellhammer, D. H. (2000). The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology 25, 1–35.Google Scholar
Hofer, S. M. (1999). Assessing personality structure using factor invariance procedures. In I. Merviede, I. Deary, F. DeFruyt, & F. Ostendorf (Eds.), Personality psychology in Europe (Vol. 7, pp. 35–49). Amsterdam: Tilburg University Press.
Johnson, D., & Elliot, L. (1998). Sampling design effects: Do they affect the analyses of data from the National Survey of Families and Households? Journal of Marriage and the Family 60, 993–1001.Google Scholar
Kalin, N. H. (1999a). Primate models and aggression. Journal of Clinical Psychiatry Monograph Series 17, 22–24.Google Scholar
Kalin, N. H. (1999b). Primate models to understand human aggression. Journal of Clinical Psychiatry 60, 29–32.Google Scholar
Kenny, D. A., & Zautra, A. (2001). Trait–state models for longitudinal data. In L. M. Collins & A. G. Sayer (Eds.), New methods for the analysis of change (pp. 243–263). Washington, DC: American Psychological Association.
Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1993). The “Trier Social Stress Test”—A tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 76–81.Google Scholar
Kirschbaum, C., Steyer, R., Eid, M., Patalla, U., Schwenkmezger, P., & Hellhammer, D. H. (1990). Cortisol and behavior: 2. Application of a latent state–trait model to salivary cortisol. Psychoneuroendocrinology 15, 297–307.Google Scholar
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, 695–719.Google Scholar
Kovacs, M. (1980). Rating scales to assess depression in school-aged children. Acta Paedopsychiatrica 46, 306–315.Google Scholar
Kruesi, M. J. P., Schmidt, M. E., Donnelly, H., Hibbs, E. D., & Hamburger, S. P. (1989). Urinary free cortisol output and disruptive behavior in children. Journal of the American Academy of Child and Adolescent Psychiatry 28, 441–443.Google Scholar
Kutcher, S., Malkin, D., Silverberg, J., & Marton, P. (1991). Nocturnal cortisol, thyroid stimulating hormone, and growth hormone secretory profiles in depressed adolescents. Journal of the American Academy of Child and Adolescent Psychiatry 30, 407–141.Google Scholar
Lewis, M. (1992). Individual differences in response to stress. Pediatrics 3, 487–490.Google Scholar
Li, F., Duncan, S. C., Duncan, T. E., Yang–Wallentin, F., Acock, A. C., & Hops, H. (2001). Interaction models in latent growth curves. In G. A. Marcoulides & R. E. Schumacker (Eds.), New developments and techniques in structural equation modeling (pp. 561–614). Hillsdale, NJ: Erlbaum.
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2001). Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status. Development and Psychopathology 13, 653–676.Google Scholar
Magnano, C. L., Diamond, E. J., & Gardner, J. M. (1989). Use of salivary cortisol measurements in young infants: A note of caution. Child Development 60, 1099–1101.Google Scholar
Mazur, A., & Booth, A. (1998). Testosterone and dominance in men. Behavioral and Brain Sciences 21, 353–363.Google Scholar
McBurnett, K. M., Lahey, B. B., Frick, P. J., Risch, C., Loeber, R., Hart, E. L., Christ, M. A. G., & Hanson, K. S. (1991). Anxiety, inhibition, and conduct disorder in children: II. Relation to salivary cortisol. Journal of the American Academy of Child and Adolescent Psychiatry 38, 547–555.Google Scholar
McBurnett, K. M., Lahey, B. B., Rathouz, P. J., & Loeber, R. (2000). Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Archives of General Psychiatry 57, 38–43.Google Scholar
McClintock, M., & Herdt, G. (1996). Rethinking puberty: The development of sexual attraction. Current Directions in Psychological Science 5, 178–183.Google Scholar
Meredith, W. (1993). Measurement invariance, factor analysis and factorial invariance. Psychometrika 58, 525–543.Google Scholar
Meredith, W., & Horn, J. L. (2001). The role of factorial invariance in modeling growth and change. In L. M. Collins & A. G. Sayer (Eds.), New methods for the analysis of change (pp. 204–240). Washington, DC: American Psychological Association.
Moss, H. B., Vanyukov, M. M., & Martin, C. S. (1995). Salivary cortisol responses and the risk for substance abuse in prepubertal boys. Biological Psychiatry 38, 547–555.Google Scholar
Nesselroade, J. R. (1988). Some implications of the trait–state distinction for the study of development over the life span: The case of personality. In P. B. Baltes, D. L. Featherman, & R. M. Lerner (Eds.), Life-span development and behavior. Hillsdale, NJ: Erlbaum.
Pajer, K., Gardner, W., Kirillova, G. P., & Vanyukov, M. (2001). Sex differences in cortisol levels and neurobehavioral disinhibition in children of substance abusers. Journal of Child and Adolescent Substance Abuse 10, 65–76.Google Scholar
Parker, L. N. (1991). Adrenarche. Endocrinology and Metabolism Clinics of North America 20, 71–83.Google Scholar
Petersen, A., 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, 117–133.Google Scholar
Puig–Antich, J., Dahl, R. E., Ryan, N., Novacenko, H., Goetz, D., Goetz, R., Twomey, J., & Klepper, T. (1989). Cortisol secretion in prepubertal children with major depressive disorder. Archives of General Psychiatry 6, 801–809.Google Scholar
Raine, A. (2002). Biosocial studies of antisocial and violent behavior in children and adults: A review. Journal of Abnormal Child Psychology 30, 311–326.Google Scholar
Ridgon, E. E., Schumacker, R. E., & Wothke, W. (1998). A comparative review of interaction and nonlinear modeling. In R. E. Schumacker & G. A. Marcoulides (Eds.), Interaction and non-linear effects in structural equation (pp. 1–16). Hillsdale, NJ: Erlbaum.
Schaal, B., Tremblay, R. E., Soussignan, R., & Susman, E. J. (1996). Male testosterone linked to high social dominance but low physical aggression in early adolescence. Journal of the American Academy of Child and Adolescent Psychiatry 35, 1322–1330.Google Scholar
Schafer, J. L., & Graham, J. W. (2002). Missing data: Our view of the state of the art. Psychological Methods 7, 147–177.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, 1503–1513.Google Scholar
Smider, N. A., Essex, M. J., Kalin, N. H., Buss, K. A., Klein, M. H., Davidson, R. J., & Goldsmith, H. H. (2002). Salivary cortisol as a predictor of socioemotional adjustment during kindergarten: A prospective study. Child Development 73, 75–92.Google Scholar
Smyth, J., Ockenfels, M. C., Porter, L., Kirschbaum, C., Hellhammer, D. H., & Stone, A. A. (1998). Stressors and mood measured on a momentary basis are associated with salivary cortisol secretion. Psychoneuroendocrinology 23, 353–370.Google Scholar
Stansbury, K., & Gunnar, R. (1994). Adrenocortical activity and emotion regulation. Monographs of the Society for Research in Child Development 59, 108–134.Google Scholar
Steyer, R., Eid, M., & Schwenkmezger, P. (1997). Modeling true intraindividual change: True change as a latent variable. Methods of Psychological Research Online 2, 1–33.Google Scholar
Steyer, R., Partchev, I., & Shanahan, M. J. (2000). Modeling true intraindividual change in structural equation models: The case of poverty and children's psychosocial adjustment. In T. D. Little, K. U. Schnabel, & J. Baumert (Eds.), Modeling longitudinal and multilevel data: Practical issues, applied approaches and specific examples (pp. 109–126). Mahwah, NJ: Erlbaum.
Steyer, R., Schmitt, M., & Eid, M. (1999). Latent state–trait theory and research in personality and individual differences. European Journal of Personality 13, 389–408.Google Scholar
Steyer, R., Schwenkmezger, P., & Auer, A. (1990). The emotional and cognitive components of trait anxiety: A latent state–trait model. Personality and Individual Differences 11, 125–134.Google Scholar
Susman, E. J., Nottelmann, E. D., Dorn, L. D., Inoff–Germain, G., & Chrousos, G. P. (1988). Physiological and behavioral aspects of stress in adolescence. Advances in Experimental Medicine and Biology 245, 341–352.Google Scholar
Taylor, S., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A. R., & Updegraff, J. A. (2000). Biobehavioral response to stress in females: Tend and befriend, not fight-or-flight. Psychological Review 107, 411–429.Google Scholar
Tennes, K., & Kreye, M. (1985). Children's adrenocortical responses to classroom activities and tests in elementary school. Psychosomatic Medicine 47, 451–460.Google Scholar
Tennes, K., Kreye, M., Avitable, N., & Wells, R. (1986). Behavioral correlations of excreted catecholamines and cortisol in second-grade children. Journal of the American Academy of Child and Adolescent Psychiatry 25, 764–770.Google Scholar
Tremblay, R. E., Schaal, B., Boulerice, B., Arseneault, L., Soussignan, R., Paquette, D., & Lauret, D. (1998). Testosterone, physical aggression, dominance and physical development in early adolescence. International Journal of Behavioral Development 22, 753–777.Google Scholar
Van Goozen, S. H. M., Matthys, W., Cohen–Kettenis, P. T., Buitelaar, J. K., & Van Engeland, H. (2000). Hypothalamic–pituitary–adrenal axis and autonomic nervous system activity in disruptive children and matched controls. Journal of the American Academy of Child and Adolescent Psychiatry 39, 1438–1445.Google Scholar
Van Goozen, S. H. M., Matthys, W., Cohen–Kettenis, P. T., Gispen–de Weid, C., Wiegant, V. M., & Van Engeland, H. (1998). Salivary cortisol and cardiovascular activity during stress in oppositional defiant disorder boys and normal controls. Biological Psychiatry 43, 531–539.Google Scholar
Vanyukov, M. M., Moss, H. B., Plail, J. A., Blackson, T., Mezzich, A. C., & Tarter, R. E. (1993). Antisocial symptoms in preadolescent boys and in their parents: Associations with cortisol. Psychiatry Research 46, 9–17.Google Scholar
Viau, V. (2002). Functional cross-talk between the hypothalamic–pituitary–gonadal and –adrenal axes. Journal of Neuroendocrinology 14, 506–513.Google Scholar
Virkkunen, M. (1985). Urinary free cortisol secretion in habitually violent offenders. Acta Psychiatrica Scandinavia 72, 40–44.Google Scholar
Walker, E. F., Walder, D. J., & Reynolds, F. (2001). Developmental changes in cortisol secretion in normal and at-risk youth. Development and Psychopathology 13, 721–732.Google Scholar
Wohlwill, J. (1973). The study of behavioral development. New York: Academic Press.
Zahn–Waxler, C. (2000). The development of empathy, guilt, and internalization of distress: Implications for gender differences in internalizing and externalizing problems. In R. J. Davidson (Ed.), Anxiety, depression, and emotion: Wisconsin Symposium on Emotion (Vol. 1, pp. 222–265). New York: Oxford University Press.
Zahn–Waxler, C., Klimes–Dougan, B., & Slattery, M. J. (2000). Internalizing problems of childhood and adolescence: Prospects, pitfalls, and progress in understanding the development of anxiety and depression. Development and Psychopathology 12, 443–466.Google Scholar