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Cortisol Rhythm in Preschoolers: Relations with Maternal Depression and Child Temperament

  • Katherine A. Leppert
  • Victoria C. Smith
  • Stephanie M. Merwin
  • Marissa Kushner
  • Lea R. Dougherty
Article

Abstract

Evidence supports associations between deviations from the normative daily cortisol rhythm and depression. We examined associations between multiple indices of daily cortisol in 146 preschool-aged children and two well-established risk factors for depression: maternal depression and early child temperament (negative emotionality/NE and positive emotionality/PE). Offspring of mothers with current depression demonstrated lower waking cortisol and lower total post-awakening cortisol. Child PE was negatively associated with waking cortisol. The combination of maternal depression history and high child NE was associated with higher levels of evening cortisol. Findings suggest that an interplay between familial risk for depression and child temperamental vulnerability may be related to neuroendocrine functioning in young children and highlight important methodological considerations in the assessment of children’s basal cortisol activity. It will be critical for future research to map the developmental progression from early disruptions in children’s cortisol rhythm to the emergence of psychopathology.

Keywords

Cortisol Cortisol awakening response Preschool Depression Temperament Maternal psychopathology 

Notes

Acknowledgements

This research was supported by the University of Maryland (UMD) College of Behavioral and Social Sciences Dean’s Research Initiative Award (LRD) and the UMD Research and Scholars Award (LRD). We are indebted to the families and staff who made this study possible. We are especially grateful to Caitlin Condit for all her efforts in recruiting families and running participants.

Compliance with Ethical Standards

Conflict of Interest

Katherine A. Leppert, Victoria C. Smith, Stephanie M. Merwin, Marissa Kushner, and Lea Rose Dougherty declare that they have no conflict of interest.

Experiment Participants

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

References

  1. Adam, E. K., & Kumari, M. (2009). Assessing salivary cortisol in largescale epidemiological research. Psychoneuroendocrinology, 34, 1423–1436.PubMedGoogle Scholar
  2. Adam, E. K., Hawkley, L. C., Kudielka, B. M., & Cacioppo, J. T. (2006). Day-to-day dynamics of experience–cortisol associations in a population-based sample of older adults. Proceedings of the National Academy of Sciences, 103(45), 17058–17063.f.Google Scholar
  3. Adam, E. K., Doane, L. D., Zinbarg, R. E., Mineka, S., Craske, M. G., & Griffith, J. W. (2010). Prospective prediction of major depressive disorder from cortisol awakening responses in adolescence. Psychoneuroendocrinology, 35, 921–931.PubMedPubMedCentralGoogle Scholar
  4. Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park: Sage.Google Scholar
  5. Anthony, J. L., Lonigan, C. J., Hooe, E. S., & Phillips, B. M. (2002). An affect-based, hierarchical model of temperament and its relations with internalizing symptomatology. Journal of Clinical Child and Adolescent Psychology, 31(4), 480–490.PubMedGoogle Scholar
  6. Bartels, M., de Geus, E. J., Kirschbaum, C., Sluyter, F., & Boomsma, D. I. (2003a). Heritability of daytime cortisol levels in children. Behavior Genetics, 33(4), 421–433.PubMedGoogle Scholar
  7. Bartels, M., Van den Berg, M., Sluyter, F., Boomsma, D. I., & de Geus, E. J. (2003b). Heritability of cortisol levels: review and simultaneous analysis of twin studies. Psychoneuroendocrinology, 28(2), 121–137.PubMedGoogle Scholar
  8. Bäumler, D., Kirschbaum, C., Kliegel, M., Alexander, N., & Stalder, T. (2013). The cortisol awakening response in toddlers and young children. Psychoneuroendocrinology, 38(11), 2485–2492.PubMedGoogle Scholar
  9. Bhagwagar, Z., Hafizi, S., & Cowen, P. J. (2003). Increase in concentration of waking salivary cortisol in recovered patients with depression. The American Journal of Psychiatry, 160, 1890–1891.PubMedGoogle Scholar
  10. Bhagwagar, Z., Hafizi, S., & Cowen, P. J. (2005). Increased salivary cortisol after waking in depression. Psychopharmacology, 182, 54–57.PubMedGoogle Scholar
  11. Bockting, C. L., Lok, A., Visser, I., Assies, J., Koeter, M. W., Schene, A. H., & DELTA Study Group. (2012). Lower cortisol levels predict recurrence in remitted patients with recurrent depression: a 5.5 year prospective study. Psychiatry Research, 200(2), 281–287.PubMedGoogle Scholar
  12. Broderick, J. E., Arnold, D., Kudielka, B. M., & Kirschbaum, C. (2004). Salivary cortisol sampling compliance: comparison of patients and healthy volunteers. Psychoneuroendocrinology, 29, 636–650.PubMedGoogle Scholar
  13. Burke, L. (2003). The impact of maternal depression on familial relationships. International Review of Psychiatry, 15(3), 243–255.PubMedGoogle Scholar
  14. Caspi, A., Moffitt, T. E., Newman, D. L., & Silva, P. A. (1996). Behavioral observations at age 3 years predict adult psychiatric disorders. Archives of General Psychiatry, 53, 1033–1039.PubMedGoogle Scholar
  15. Clow, A., Thorn, L., Evans, P., & Hucklebridge, F. (2004). The awakening cortisol response: methodological issues and significance. Stress, 7, 29–37.PubMedGoogle Scholar
  16. Connell, A. M., & Goodman, S. H. (2002). The association between psychopathology in fathers versus mothers and children's internalizing and externalizing behavior problems: a meta-analysis. Psychological Bulletin, 128(5), 746–773.PubMedGoogle Scholar
  17. De Moor, M. H., Van Den Berg, S. M., Verweij, K. J., Krueger, R. F., Luciano, M., Vasquez, A. A., et al. (2015). Meta-analysis of genome-wide association studies for neuroticism, and the polygenic association with major depressive disorder. JAMA Psychiatry, 72(7), 642–650.PubMedPubMedCentralGoogle Scholar
  18. Degnan, K. A., Hane, A. A., Henderson, H. A., Moas, O. L., Reeb-Sutherland, B. C., & Fox, N. A. (2011). Longitudinal stability of temperamental exuberance and social–emotional outcomes in early childhood. Developmental Psychology, 47(3), 765–780.PubMedPubMedCentralGoogle Scholar
  19. Dettling, A. C., Gunnar, M. R., & Donzella, B. (1999). Cortisol levels of young children in full-day childcare centers: Relations with age and temperament. Psychoneuroendocrinology, 24, 519–536.PubMedGoogle Scholar
  20. Dougherty, L. R., Klein, D. N., Olino, T. M., Dyson, M., & Rose, S. (2009). Increased waking salivary cortisol and depression risk in preschoolers: the role of maternal history of melancholic depression and early child temperament. Journal of Child Psychology and Psychiatry, 50, 1495–1503.PubMedGoogle Scholar
  21. Dougherty, L. R., Klein, D. N., Durbin, C. E., Hayden, E. P., & Olino, T. M. (2010). Temperamental positive and negative emotionality and children's depressive symptoms: a longitudinal prospective study from age three to age ten. Journal of Social and Clinical Psychology, 29, 462–488.Google Scholar
  22. Dougherty, L. R., Bufferd, S. J., Carlson, G. A., Dyson, M., Olino, T. M., Durbin, C. E., & Klein, D. N. (2011). Preschoolers' observed temperament and psychiatric disorders assessed with a parent diagnostic interview. Journal of Clinical Child & Adolescent Psychology, 40(2), 295–306.Google Scholar
  23. Dougherty, L. R., Smith, V. C., Olino, T. M., Dyson, M. W., Bufferd, S. J., Rose, S. A., & Klein, D. N. (2013). Maternal psychopathology and early child temperament predict young children’s salivary cortisol 3 years later. Journal of Abnormal Child Psychology, 41, 531–542.PubMedGoogle Scholar
  24. Durbin, C. E., Klein, D. N., Hayden, E. P., Buckley, M. E., & Moerk, K. C. (2005). Temperamental emotionality in preschoolers and parental mood disorders. Journal of Abnormal Psychology, 114, 28–37.PubMedGoogle Scholar
  25. Durbin, C. E., Hayden, E. P., Klein, D. N., & Olino, T. M. (2007). Stability of laboratory-assessed temperamental emotionality traits from ages 3 to 7. Emotion, 7(2), 388–399.PubMedGoogle Scholar
  26. Egger, H. L., Ascher, B. H., & Angold, A. (1999). The preschool age psychiatric assessment: Version 1.1. Durham: Center for Developmental Epidemiology, Department of Psychiatry and Behavioral Sciences, Duke University Medical Center.Google Scholar
  27. Elder, G. J., Ellis, J. G., Barclay, N. L., & Wetherell, M. A. (2016). Assessing the daily stability of the cortisol awakening response in a controlled environment. BMC Psychology, 4(1), 3–13.PubMedPubMedCentralGoogle Scholar
  28. Ertel, K. A., Rich-Edwards, J. W., & Koenen, K. C. (2011). Maternal depression in the United States: nationally representative rates and risks. Journal of Women's Health, 20(11), 1609–1617.PubMedPubMedCentralGoogle Scholar
  29. Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., & Gilboa-Schechtman, E. (2009). Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. Journal of the American Academy of Child & Adolescent Psychiatry, 48(9), 919–927.Google Scholar
  30. Fernald, L. C., Burke, H. M., & Gunnar, M. R. (2008). Salivary cortisol levels in children of low-income women with high depressive symptomatology. Development and Psychopathology, 20(2), 423–436.PubMedGoogle Scholar
  31. First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1996). Structured clinical interview for DSM-IV Axis I disorders: non-patient edition (version 2.0). New York: New York State Psychiatric Institute, Biometrics Research.Google Scholar
  32. Foland-Ross, L. C., Kircanski, K., & Gotlib, I. H. (2014). Coping with having a depressed mother: The role of stress and coping in hypothalamic-pituitary-adrenal axis dysfunction in girls at familial risk for major depression. Development and Psychopathology, 26, 1401–1409.PubMedGoogle Scholar
  33. Fries, E., Dettenborn, L., & Kirschbaum, C. (2009). The cortisol awakening response (CAR): Facts and future directions. International Journal of Psychophysiology, 72, 67–73.PubMedGoogle Scholar
  34. Gagne, J. R., Van Hulle, C. A., Aksan, N., Essex, M. J., & Goldsmith, H. H. (2011). Deriving childhood temperament measures from emotion-eliciting behavioral episodes: Scale construction and initial validation. Psychological Assessment, 23(2), 337–353.PubMedPubMedCentralGoogle Scholar
  35. Garde, A. H., & Hansen, Å. M. (2005). Long-term stability of salivary cortisol. Scandinavian Journal of Clinical and Laboratory Investigation, 65(5), 433–436.PubMedGoogle Scholar
  36. Gillespie, C. F., Phifer, J., Bradley, B., & Ressler, K. J. (2009). Risk and resilience: genetic and environmental influences on development of the stress response. Depression and Anxiety, 26(11), 984–992.PubMedPubMedCentralGoogle Scholar
  37. Gold, P. W., & Chrousos, G. P. (2002). Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Molecular Psychiatry, 7, 254–275.PubMedGoogle Scholar
  38. Goldsmith, H. H., Reilly, J., Lemery, K.S., Longley, S., & Prescott, A. (1995). The laboratory temperament assessment battery: Preschool version. Unpublished manuscript.Google Scholar
  39. Goldstein, B. L., Perlman, G., Kotov, R., Broderick, J. E., Liu, K., Ruggero, C., & Klein, D. N. (2017). Etiologic specificity of waking cortisol: links with maternal history of depression and anxiety in adolescent girls. Journal of Affective Disorders, 208, 103–109.PubMedGoogle Scholar
  40. Goodman, S. H., & Gotlib, I. H. (1999). Risk for psychopathology in the children of depressed mothers: a developmental model for understanding mechanisms of transmission. Psychological Review, 106(3), 458–490.PubMedGoogle Scholar
  41. Goodyer, I. M., Herbert, J., Altham, P. M. E., 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(02), 245–256.PubMedGoogle Scholar
  42. Goodyer, I. M., Herbert, J., Tamplin, A., & Altham, P. M. E. (2000). Recent life events, cortisol, dehydroepiandrosterone and the onset of major depression in high-risk adolescents. The British Journal of Psychiatry, 177(6), 499–504.PubMedGoogle Scholar
  43. 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(5), 351–357.PubMedGoogle Scholar
  44. Granger, D. A., Hibel, L. C., Fortunato, C. K., & Kapelewski, C. H. (2009). Medication effects on salivary cortisol: Tactics and strategy to minimize impact in behavioral and developmental science. Psychoneuroendocrinology, 34, 1437–1448.PubMedGoogle Scholar
  45. Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27(1), 199–220.PubMedGoogle Scholar
  46. Gunnar, M. R., & Talge, N. M. (2007). Neuroendocrine measures in developmental research. In L. A. Schmidt & S. J. Segalowitz (Eds.), Developmental psychophysiology: Theory, systems, and methods (pp. 343–366). Cambridge: University Press.Google Scholar
  47. Gunnar, M. R., & White, B. (2001). Salivary cortisol measures in infant and child assessment. In L. T. Singer & P. S. Zeskind (Eds.), Biobehavioral assessment of the newborn (pp. 167–189). New York: Guilford Press.Google Scholar
  48. Gunnar, M. R., Broderson, L., Krueger, K., & Rigatuso, J. (1996). Dampening of adrenocortisol responses during infancy: Normative changes and individual differences. Child Development, 67(3), 877–889.PubMedGoogle Scholar
  49. Halligan, S. L., Herbert, J., Goodyer, I. M., & Murray, L. (2004). Exposure to postnatal depression predicts elevated cortisol in adolescent offspring. Biological Psychiatry, 55, 376–381.PubMedGoogle Scholar
  50. 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(1), 40–46.PubMedGoogle Scholar
  51. Harris, T. O., Borsanyi, S., Messari, S., Standord, K., Cleary, S. E., Shiers, H. M., et al. (2000). Morning cortisol as a risk factor for subsequent major depressive disorder in adult women. British Journal of Psychiatry, 177, 505–510.PubMedGoogle Scholar
  52. Hauner, K. K., Adam, E. K., Mineka, S., Doane, L. D., DeSantis, A. S., Zinbarg, R., et al. (2008). Neuroticism and introversion are associated with salivary cortisol patterns in adolescents. Psychoneuroendocrinology, 33(10), 1344–1356.PubMedPubMedCentralGoogle Scholar
  53. Hayden, E. P., Klein, D. N., & Durbin, C. E. (2005). Parent reports and laboratory assessments of child temperament: a comparison of their associations with risk for depression and externalizing disorders. Journal of Psychopathology and Behavioral Assessment, 27(2), 89–100.Google Scholar
  54. Hayden, E. P., Klein, D. N., Durbin, C. E., & Olino, T. M. (2006). Positive emotionality at age 3 predicts cognitive styles in 7-year-old children. Development and Psychopathology, 18(2), 409–423.PubMedGoogle Scholar
  55. Hayes, A. F., & Matthes, J. (2009). Computational procedures for probing interactions in OLS and logistic regression: SPSS and SAS implementations. Behavior Research Methods, 41(3), 924–936.PubMedGoogle Scholar
  56. Heim, C., Ehlert, U., & Hellhammer, D. H. (2000). The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology, 25(1), 1–35.PubMedGoogle Scholar
  57. Hellhammer, J., Fries, E., Schweisthal, O. W., Schlotz, W., Stone, A. A., & Hagemann, D. (2007). Several daily measurements are necessary to reliably assess the cortisol rise after awakening: State-and trait components. Psychoneuroendocrinology, 32(1), 80–86.PubMedGoogle Scholar
  58. Hettema, J. M., Neale, M. C., Myers, J. M., Prescott, C. A., & Kendler, K. S. (2006). A population-based twin study of the relationship between neuroticism and internalizing disorders. American Journal of Psychiatry, 163(5), 857–864.PubMedGoogle Scholar
  59. Kagan, J., Reznick, J. S., & Snidman, N. (1987). The physiology and psychology of behavioral inhibition in children. Child Development, 58, 1459–1473.PubMedGoogle Scholar
  60. Kendler, K. S., Gatz, M., Gardner, C. O., & Pedersen, N. L. (2006). Personality and major depression: a Swedish longitudinal, population-based twin study. Archives of General Psychiatry, 63(10), 1113–1120.PubMedGoogle Scholar
  61. Kendler, K. S., Gatz, M., Gardner, C. O., & Pedersen, N. L. (2007). Clinical indices of familial depression in the Swedish twin registry. Acta Psychiatrica Scandinavica, 115(3), 214–220.PubMedGoogle Scholar
  62. Klein, D. N., Durbin, C. E., & Shankman, S. A. (2009). Personality and mood disorders. In I. H. Gotlib & C. L. Hammen (Eds.), Handbook of depression (2nd ed., pp. 93–112). New York: Guilford.Google Scholar
  63. Knorr, U., Vinberg, M., Kessing, L. V., & Wetterslev, J. (2010). Salivary cortisol in depressed patients versus control persons: a systematic review and meta-analysis. Psychoneuroendocrinology, 35, 1275–1286.PubMedGoogle Scholar
  64. Kudielka, B. M., & Kirschbaum, C. (2003). Awakening cortisol responses are influenced by health status and awakening time but not by menstrual cycle phase. Psychoneuroendocrinology, 28(1), 35–47.PubMedGoogle Scholar
  65. Kudielka, B. M., Hawkley, L. C., Adam, E. K., & Cacioppo, J. T. (2007). Compliance with ambulatory saliva sampling in the Chicago health, aging, and social relations study and associations with social support. Annals of Behavioral Medicine, 34, 209–216.PubMedGoogle Scholar
  66. Kudielka, B. M., Gierens, A., Hellhammer, D. H., Wüst, S., & Schlotz, W. (2012). Salivary cortisol in ambulatory assessment—some dos, some don’ts, and some open questions. Psychosomatic Medicine, 74(4), 418–431.PubMedGoogle Scholar
  67. Kunz-Ebrecht, S. R., Kirschbaum, C., Marmot, M., & Steptoe, A. (2004). Differences in cortisol awakening response on work days and weekends in women and men from the Whitehall II cohort. Psychoneuroendocrinology, 29, 516–528.PubMedGoogle Scholar
  68. Kushner, M. R., Barrios, C., Smith, V. C., & Dougherty, L. R. (2016). Physiological and behavioral vulnerability markers increase risk to early life stress in preschool-aged children. Journal of Abnormal Child Psychology, 44(5), 859–870.PubMedGoogle Scholar
  69. Laceulle, O. M., Nederhof, E., van Aken, M. A. G., & Ormel, J. (2015). Adolescent personality: Associations with basal, awakening, and stress-induced cortisol responses. Journal of Personality, 83(3), 262–273.PubMedGoogle Scholar
  70. LeMoult, J., Chen, M. C., Foland-Ross, L. C., Burley, H. W., & Gotlib, I. H. (2015). Concordance of mother–daughter diurnal cortisol production: Understanding the intergenerational transmission of risk for depression. Biological Psychology, 108, 98–104.PubMedPubMedCentralGoogle Scholar
  71. Liang, K. Y., & Zeger, S. L. (1986). Longitudinal data analysis using generalized linear models. Biometrika, 73(1), 13–22.Google Scholar
  72. Lippold, M. A., Davis, K. D., McHale, S. M., Buxton, O. M., & Almeida, D. M. (2016a). Daily stressor reactivity during adolescence: The buffering role of parental warmth. Health Psychology, 35(9), 1027–1035.PubMedPubMedCentralGoogle Scholar
  73. Lippold, M. A., McHale, S. M., Davis, K. D., Almeida, D. M., & King, R. B. (2016b). Experiences with parents and youth physical health symptoms and cortisol: A daily diary investigation. Journal of Research on Adolescence, 26(2), 226–240.PubMedGoogle Scholar
  74. Lo, S. L., Vroman, L. N., & Durbin, C. E. (2015). Ecological validity of laboratory assessments of child temperament: evidence from parent perspectives. Psychological Assessment, 27(1), 280–290.PubMedGoogle Scholar
  75. Lovejoy, M. C., Graczyk, P. A., O'Hare, E., & Neuman, G. (2000). Maternal depression and parenting behavior: a meta-analytic review. Clinical Psychology Review, 20(5), 561–592.PubMedGoogle Scholar
  76. Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2000). Child’s stress hormone levels correlate with mother’s socioeconomic status and depressive state. Biological Psychiatry, 48(10), 976–980.PubMedGoogle Scholar
  77. 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(3), 653–676.Google Scholar
  78. Mannie, Z. N., Harmer, C. J., & Cowen, P. J. (2007). Increased waking salivary cortisol levels in young people at familial risk of depression. American Journal of Psychiatry, 164, 617–621.PubMedGoogle Scholar
  79. McMakin, D. L., Burkhouse, K. L., Olino, T. M., Siegle, G. J., Dahl, R. E., & Silk, J. S. (2011). Affective functioning among early adolescents at high and low familial risk for depression and their mothers: a focus on individual and transactional processes across contexts. Journal of Abnormal Child Psychology, 39(8), 1213–1225.PubMedGoogle Scholar
  80. Merikangas, K. R., He, J. P., Burstein, M., Swanson, S. A., Avenevoli, S., Cui, L., et al. (2010). Lifetime prevalence of mental disorders in U.S. adolescents: Results from the National Comorbidity Survey Replication--Adolescent Supplement (NCS-A). Journal of the American Academy of Child and Adolescent Psychiatry, 49, 980–989.PubMedPubMedCentralGoogle Scholar
  81. Mikolajewski, A. J., Allan, N. P., Hart, S. A., Lonigan, C. J., & Taylor, J. (2013). Negative affect shares genetic and environmental influences with symptoms of childhood internalizing and externalizing disorders. Journal of Abnormal Child Psychology, 41(3), 411–423.PubMedPubMedCentralGoogle Scholar
  82. Morris, B. H., Bylsma, L. M., & Rottenberg, J. (2009). Does emotion predict the course of major depressive disorder? A review of prospective studies. British Journal of Clinical Psychology, 48, 255–273.PubMedGoogle Scholar
  83. Naragon-Gainey, K., Watson, D., & Markon, K. E. (2009). Differential relations of depression and social anxiety symptoms to the facets of extraversion/positive emotionality. Journal of Abnormal Psychology, 118(2), 299–310.PubMedPubMedCentralGoogle Scholar
  84. O’Donnell, K. J., Glover, V., Jenkins, J., Browne, D., Ben-Shlomo, Y., Golding, J., & O’Connor, T. G. (2013). Prenatal maternal mood is associated with altered diurnal cortisol in adolescence. Psychoneuroendocrinology, 38(9), 1630–1638.PubMedPubMedCentralGoogle Scholar
  85. O’Neal, C. R., Brotman, L. M., Huang, K. Y., Gouley, K. K., Kamboukos, D., Calzada, E. J., & Pine, D. S. (2010). Understanding relations among early family environment, cortisol response, and child aggression via a prevention experiment. Child Development, 81(1), 290–305.PubMedPubMedCentralGoogle Scholar
  86. Olino, T. M., Klein, D. N., Dyson, M. W., Rose, S. A., & Durbin, C. E. (2010). Temperamental emotionality in preschool-aged children and depressive disorders in parents: associations in a large community sample. Journal of Abnormal Psychology, 119, 468–478.PubMedPubMedCentralGoogle Scholar
  87. Olino, T. M., Lopez-Duran, N. L., Kovacs, M., George, C. J., Gentzler, A. L., & Shaw, D. S. (2011). Developmental trajectories of positive and negative affect in children at high and low familial risk for depressive disorder. Journal of Child Psychology and Psychiatry, 52, 792–799.PubMedGoogle Scholar
  88. Polk, D. E., Cohen, S., Doyle, W. J., Skoner, D. P., & Kirschbaum, C. (2005). State and trait affect as predictors of salivary cortisol in healthy adults. Psychoneuroendocrinology, 30, 261–272.PubMedGoogle Scholar
  89. 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.PubMedGoogle Scholar
  90. Rohde, P., Lewinsohn, P. M., & Seeley, J. R. (1997). Comparability of telephone and face-to-face interviews in assessing Axis I and II disorders. American Journal of Psychiatry, 154, 1593–1598.PubMedGoogle Scholar
  91. Ross, K. M., Murphy, M. L., Adam, E. K., Chen, E., & Miller, G. E. (2014). How stable are diurnal cortisol activity indices in healthy individuals? Evidence from three multi-wave studies. Psychoneuroendocrinology, 39, 184–193.PubMedGoogle Scholar
  92. Rotenberg, S., McGrath, J. J., Roy-Gagnon, M. H., & Tu, M. T. (2012). Stability of the diurnal cortisol profile in children and adolescents. Psychoneuroendocrinology, 37(12), 1981–1989.PubMedPubMedCentralGoogle Scholar
  93. Rousseeuw, P. J., & Van Zomeren, B. C. (1990). Unmasking multivariate outliers and leverage points. Journal of the American Statistical Association, 85(411), 633–651.Google Scholar
  94. Schmidt, L. A., Fox, N. A., Rubin, K. H., Sternberg, E. M., Gold, P. W., Smith, C. C., & Schulkin, J. (1997). Behavioral and neuroendocrine responses in shy children. Developmental Psychobiology, 30(2), 127–140.PubMedGoogle Scholar
  95. Shankman, S. A., & Klein, D. N. (2003). The relation between depression and anxiety: an evaluation of the tripartite, approach-withdrawal and valence-arousal models. Clinical Psychology Review, 23(4), 605–637.PubMedGoogle Scholar
  96. Shankman, S. A., Tenke, C. E., Bruder, G. E., Durbin, C. E., Hayden, E. P., & Klein, D. N. (2005). Low positive emotionality in young children: association with EEG asymmetry. Development and Psychopathology, 17(1), 85–98.PubMedGoogle Scholar
  97. Shankman, S. A., Klein, D. N., Torpey, D. C., Olino, T. M., Dyson, M. W., Kim, J., et al. (2013). Do positive and negative temperament traits interact in predicting risk for depression? A resting EEG study of 329 preschoolers. Development and Psychopathology, 23(2), 551–562.Google Scholar
  98. Silk, J. S., Shaw, D. S., Forbes, E. E., Lane, T. L., & Kovacs, M. (2006). Maternal depression and child internalizing: the moderating role of child emotion regulation. Journal of Clinical Child and Adolescent Psychology, 35(1), 116–126.PubMedGoogle Scholar
  99. Smith, V. C., & Dougherty, L. R. (2014). Noisy spit: parental noncompliance with child salivary cortisol sampling. Developmental Psychobiology, 56, 647–656.PubMedGoogle Scholar
  100. Stalder, T., Bäumler, D., Miller, R., Alexander, N., Kliegel, M., & Kirschbaum, C. (2013). The cortisol awakening response in infants: ontogeny and associations with development-related variables. Psychoneuroendocrinology, 38(4), 552–559.PubMedGoogle Scholar
  101. Stalder, T., Kirschbaum, C., Kudielka, B. M., Adam, E. K., Pruessner, J. C., Wüst, S., et al. (2016). Assessment of the cortisol awakening response: expert consensus guidelines. Psychoneuroendocrinology, 63, 414–432.PubMedGoogle Scholar
  102. Stetler, C., & Miller, G. E. (2005). Blunted cortisol response to awakening in mild to moderate depression: Regulatory influences of sleep patterns and social contacts. Journal of Abnormal Psychology, 114, 697–705.PubMedGoogle Scholar
  103. Stifter, C. A., Putnam, S., & Jahromi, L. (2008). Exuberant and inhibited toddlers: stability of temperament and risk for problem behavior. Development and Psychopathology, 20(2), 401–421.PubMedPubMedCentralGoogle Scholar
  104. Stone, A. A., Schwartz, J. E., Smyth, J., Kirschbaum, C., Cohen, S., Hellhammer, D., & Grossman, S. (2001). Individual differences in the diurnal cycle of salivary free cortisol: a replication of flattened cycles for some individuals. Psychoneuroendocrinology, 26, 295–306.PubMedGoogle Scholar
  105. Thorn, L., Hucklebridge, F., Evans, P., & Clow, A. (2009). The cortisol awakening response, seasonality, stress and arousal: a study of trait and state influences. Psychoneuroendocrinology, 34(3), 299–306.PubMedGoogle Scholar
  106. Toone, R. J., Peacock, O. J., Smith, A. A., Thompson, D., Drawer, S., Cook, C., & Stokes, K. A. (2013). Measurement of steroid hormones in saliva: effects of sample storage condition. Scandinavian Journal of Clinical and Laboratory Investigation, 73(8), 615–621.PubMedGoogle Scholar
  107. Tugade, M. M., & Fredrickson, B. L. (2004). Resilient individuals use positive emotions to bounce back from negative emotional experiences. Journal of Personality and Social Psychology, 86(2), 320–333.PubMedPubMedCentralGoogle Scholar
  108. Ulrike, S., Reinhold, L., & Dirk, H. (2013). Major depression in young girls is related to altered cortisol awakening response. European Child & Adolescent Psychiatry, 22(6), 379–384.Google Scholar
  109. Vreeburg, S. A., Hoogendijk, W. J., van Pelt, J., DeRijk, R. H., Verhagen, J. C., van Dyck, R., et al. (2009). Major depressive disorder and hypothalamic-pituitary-adrenal axis activity: results from a large cohort study. Archives of General Psychiatry, 66(6), 617–626.PubMedGoogle Scholar
  110. Vreeburg, S. A., Hartman, C. A., Hoogendijk, W. J., van Dyck, R., Zitman, F. G., Ormel, J., & Penninx, B. W. (2010). Parental history of depression or anxiety and the cortisol awakening response. The British Journal of Psychiatry, 197(3), 180–185.PubMedGoogle Scholar
  111. Vreeburg, S. A., Hoogendijk, W. J., DeRijk, R. H., van Dyck, R., Smit, J. H., Zitman, F. G., & Penninx, B. W. (2013). Salivary cortisol levels and the 2-year course of depressive and anxiety disorders. Psychoneuroendocrinology, 38, 1494–1502.PubMedGoogle Scholar
  112. Watamura, S. E., Donzella, B., Alwin, J., & Gunnar, M. R. (2003). Morning-to-afternoon increases in cortisol concentrations for infants and toddlers at child care: age differences and behavioral correlates. Child Development, 74(4), 1006–1020.PubMedGoogle Scholar
  113. Weissman, M. M., Wickramaratne, P., Nomura, Y., Warner, V., Pilowsky, D., & Verdeli, H. (2006). Offspring of depressed parents: 20 years later. American Journal of Psychiatry, 163, 1001–1008.PubMedGoogle Scholar
  114. Weissman, M. M., Wickramaratne, P., Gameroff, M. J., Warner, V., Pilowsky, D., Kohad, R. G., et al. (2016). Offspring of depressed parents: 30 years later. American Journal of Psychiatry, 173(10), 1024–1032.PubMedGoogle Scholar
  115. Wichers, M., Jacobs, N., Derom, C., Thiery, E., & van Os, J. (2007). Depression: Too much negative affect or too little positive affect? Twin Research and Human Genetics, 10(S1), 19–20.Google Scholar
  116. Wust, S., Federenko, I., Hellhammer, D., & Kirschbaum, C. (2000a). Genetic factors, perceived chronic stress and the free cortisol response to awakening. Psychoneuroendocrinology, 25, 707–720.PubMedGoogle Scholar
  117. Wust, S., Wolf, J., Hellhammer, D. H., Federenko, I., Schommer, N., & Kirschbaum, C. (2000b). The cortisol awakening response-normal values and confounds. Noise and Health, 2(7), 79–88.PubMedGoogle Scholar
  118. Young, E. A., Vazquez, D., Jiang, H., & Pfeffer, C. R. (2006). Saliva cortisol and response to dexamethasone in children of depressed parents. Biological Psychiatry, 60(8), 831–836.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Katherine A. Leppert
    • 1
  • Victoria C. Smith
    • 1
  • Stephanie M. Merwin
    • 1
  • Marissa Kushner
    • 1
  • Lea R. Dougherty
    • 1
  1. 1.Department of PsychologyUniversity of MarylandCollege ParkUSA

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