Psychoneuroendocrinology
Volume 35, Issue 8 , Pages 1167-1177 , September 2010

Behavioral adjustment in a community sample of boys: Links with basal and stress-induced salivary cortisol concentrations

  • Audrey R. Tyrka

      Affiliations

    • Mood Disorders Research Program and Laboratory for Clinical Neuroscience, Butler Hospital, Providence, RI, United States
    • Department of Psychiatry and Human Behavior, Warren Alpert Medical School of Brown University, Providence, RI, United States
    • Corresponding Author InformationCorresponding author at: Butler Hospital, 345 Blackstone Blvd., Providence, RI 02906, United States. Tel.: +1 401 455 6520; fax: +1 401 455 6534.
    • ,
  • Megan M. Kelly

      Affiliations

    • Mood Disorders Research Program and Laboratory for Clinical Neuroscience, Butler Hospital, Providence, RI, United States
    • Department of Psychiatry and Human Behavior, Warren Alpert Medical School of Brown University, Providence, RI, United States
    • ,
  • Julia A. Graber

      Affiliations

    • Department of Psychology, University of Florida, Gainesville, FL, United States
    • ,
  • Laura DeRose

      Affiliations

    • Department of Developmental Psychology, Adelphi University, Garden City, NY, United States
    • ,
  • Janet K. Lee

      Affiliations

    • Mood Disorders Research Program and Laboratory for Clinical Neuroscience, Butler Hospital, Providence, RI, United States
    • ,
  • Michelle P. Warren

      Affiliations

    • College of Physicians & Surgeons, Columbia University, New York, NY, United States
    • ,
  • Jeanne Brooks-Gunn

      Affiliations

    • College of Physicians & Surgeons, Columbia University, New York, NY, United States
    • National Center for Children and Families, Teachers College, Columbia University, New York, NY, United States

Received 4 December 2008 ,Revised 20 November 2009 ,Accepted 2 February 2010.

References 

  1. Achenbach TM. Child Behavior Checklist for Ages 6 to 18. Burlington: University of Vermont Research Center for Children, Youth, & Families; 2001;
  2. Achenbach TM, Dumenci L. Advances in empirically based assessment: revised cross-informant syndromes and new DSM-oriented scales for the CBCL, YSR, and TRF: comment on Lengua, Sadowksi, Friedrich, and Fischer (2001). J. Consult. Clin. Psychol. 2001;69(4):699–702
  3. Achenbach TM, Howell CT, Quay HC, Conners CK. National survey of problems and competencies among four- to sixteen-year-olds: parents’ reports for normative and clinical samples. Monogr. Soc. Res. Child Dev. 1991;56(3):1–131
  4. Achenbach TM, Rescorla LA. Manual for the ASEBA School Age Forms & Profiles. Burlington: University of Vermont Research Center for children, Youth & Families; 2001;
  5. Adam EK. Transactions among adolescent trait and state emotion and diurnal and momentary cortisol activity in naturalistic settings. Psychoneuroendocrinology. 2006;31(5):664–679
  6. Ashman SB, Dawson G, Panagiotides H, Yamada E, Wilkinson CW. Stress hormone levels of children of depressed mothers. Dev. Psychopathol. 2002;14(2):333–349
  7. Bennett GG, Merritt MM, Wolin KY. Ethnicity, education, and the cortisol response to awakening: a preliminary investigation. Ethn. Health. 2004;9(4):337–347
  8. Bierman KL, Smoot DL, Aumiller K. Characteristics of aggressive-rejected, aggressive (nonrejected), and rejected (nonaggressive) boys. Child Dev. 1993;64(1):139–151
  9. Birmaher B, Dahl RE, Perel J, Williamson DE, Nelson B, Stull S, et al. Corticotropin-releasing hormone challenge in prepubertal major depression. Biol. Psychiatry. 1996;39(4):267–277
  10. Birmaher B, Ryan ND, Dahl R, Rabinovich H, Ambrosini P, Williamson DE, et al. Dexamethasone suppression test in children with major depressive disorder. J. Am. Acad. Child Adolesc. Psychiatry. 1992;31(2):291–297
  11. Blair C, Peters R, Granger D. Physiological and neuropsychological correlates of approach/withdrawal tendencies in preschool: further examination of the behavioral inhibition system/behavioral activation system scales for young children. Dev. Psychobiol. 2004;45(3):113–124
  12. Boyce WT, Essex MJ, Alkon A, Goldsmith HH, Kraemer HC, Kupfer DJ. Early father involvement moderates biobehavioral susceptibility to mental health problems in middle childhood. J. Am. Acad. Child Adolesc. Psychiatry. 2006;45(12):1510–1520
  13. Brooks-Gunn J, Warren MP, Rosso J, Gargiulo J. Validity of self-report measures of girls’ pubertal status. Child Dev. 1987;58(3):829–841
  14. Buss AH, Plomin R. Temperament: Early Developing Personality Traits. Hillsdale, New Jersey: Lawrence Erlbaum Associates, Inc.; 1984;
  15. Chong RY, Uhart M, McCaul ME, Johnson E, Wand GS. Whites have a more robust hypothalamic–pituitary–adrenal axis response to a psychological stressor than Blacks. Psychoneuroendocrinology. 2008;33(2):246–254
  16. Cicchetti D, Rogosch FA. The impact of child maltreatment and psychopathology on neuroendocrine functioning. Dev. Psychopathol. 2001;13(4):783–804
  17. Clingempeel WG, Colyar JJ, Brand E, Hetherington EM. Children's relationships with maternal grandparents: a longitudinal study of family structure and pubertal status effects. Child Dev. 1992;63(6):1404–1422
  18. Cohen S, Doyle WJ, Baum A. Socioeconomic status is associated with stress hormones. Psychosom. Med. 2006;68(3):414–420
  19. Dahl R, Puig-Antich J, Ryan N, Nelson B, Novacenko H, Twomey J, et al. Cortisol secretion in adolescents with major depressive disorder. Acta Psychiatr. Scand. 1989;80(1):18–26
  20. Dahl RE, Ryan ND, Puig-Antich J, Nguyen NA, al-Shabbout M, Meyer VA, et al. 24-hour cortisol measures in adolescents with major depression: a controlled study. Biol. Psychiatry. 1991;30(1):25–36
  21. Davis EP, Donzella B, Krueger WK, Gunnar MR. The start of a new school year: individual differences in salivary cortisol response in relation to child temperament. Dev. Psychobiol. 1999;35(3):188–196
  22. de Haan M, Gunnar MR, Tout K, Hart J, Stansbury K. Familiar and novel contexts yield different associations between cortisol and behavior among 2-year-old children. Dev. Psychobiol. 1998;33(1):93–101
  23. DeSantis AS, Adam EK, Doane LD, Mineka S, Zinbarg RE, Craske MG. Racial/ethnic differences in cortisol diurnal rhythms in a community sample of adolescents. J. Adolesc. Health. 2007;41(1):3–13
  24. Dorn LD, Burgess ES, Susman EJ, von Eye A, DeBellis MD, Gold PW, et al. Response to oCRH in depressed and nondepressed adolescents: does gender make a difference?. J. Am. Acad. Child Adolesc. Psychiatry. 1996;35(6):764–773
  25. Dorn LD, Susman EJ, Nottelmann ED, Inoff-Germain G, Chrousos GP. Perceptions of puberty: adolescent, parent, and health care personnel. Dev. Psychol. 1990;26(2):322–329
  26. Duman RS, Monteggia LM. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry. 2006;59(12):1116–1127
  27. Fanurik D, Zeltzer LK, Roberts MC, Blount RL. The relationship between children's coping styles and psychological interventions for cold pressor pain. Pain. 1993;53(2):213–222
  28. Forbes EE, Williamson DE, Ryan ND, Birmaher B, Axelson DA, Dahl RE. Peri-sleep-onset cortisol levels in children and adolescents with affective disorders. Biol. Psychiatry. 2006;59(1):24–30
  29. Geller B, Rogol AD, Knitter EF. Preliminary data on the dexamethasone suppression test in children with major depressive disorder. Am. J. Psychiatry. 1983;140(5):620–622
  30. Gispen-de Wied CC, Jansen LM, Duyx JH, Thijssen JH, van Engeland H. Pituitary–adrenal function in adolescent psychiatric patients: impact of depressive symptoms. J. Affect. Disord. 2000;59(1):71–76
  31. Goodyer IM, Herbert J, Altham PM, Pearson J, Secher SM, Shiers HM. Adrenal secretion during major depression in 8- to 16-year-olds. I. Altered diurnal rhythms in salivary cortisol and dehydroepiandrosterone (DHEA) at presentation. Psychol. Med. 1996;26(2):245–256
  32. Goodyer IM, Herbert J, Tamplin A. Psychoendocrine antecedents of persistent first-episode major depression in adolescents: a community-based longitudinal enquiry. Psychol. Med. 2003;33(4):601–610
  33. Goodyer IM, Herbert J, Tamplin A, Altham PM. Recent life events, cortisol, dehydroepiandrosterone and the onset of major depression in high-risk adolescents. Br. J. Psychiatry. 2000;177:499–504
  34. Goodyer IM, Park RJ, Herbert J. Psychosocial and endocrine features of chronic first-episode major depression in 8–16 year olds. Biol. Psychiatry. 2001;50(5):351–357
  35. Granger DA, Weisz JR, Kauneckis D. Neuroendocrine reactivity, internalizing behavior problems, and control-related cognitions in clinic-referred children and adolescents. J. Abnorm. Psychol. 1994;103(2):267–276
  36. Gunnar MR, Sebanc AM, Tout K, Donzella B, van Dulmen MM. Peer rejection, temperament, and cortisol activity in preschoolers. Dev. Psychobiol. 2003;43(4):346–358
  37. Gunnar MR, Tout K, de Haan M, Pierce S, Stansbury K. Temperament, social competence, and adrenocortical activity in preschoolers. Dev. Psychobiol. 1997;31(1):65–85
  38. Ha H, Kaplan S, Foley C. The dexamethasone suppression test in adolescent psychiatric patients. Am. J. Psychiatry. 1984;141(3):421–423
  39. Harmon AG, Hibel LC, Rumyantseva O, Granger DA. Measuring salivary cortisol in studies of child development: watch out—what goes in may not come out of saliva collection devices. Dev. Psychobiol. 2007;49(5):495–500
  40. Hasler G, Drevets WC, Manji HK, Charney DS. Discovering endophenotypes for major depression. Neuropsychopharmacology. 2004;29(10):1765–1781
  41. Hollingshead AB. Four Factor Index of Social Status. Yale University; 1975;
  42. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology. 2000;23(5):477–501
  43. Kagan J, Reznick JS, Snidman N. The physiology and psychology of behavioral inhibition in children. Child Dev. 1987;58(6):1459–1473
  44. Kaufman J, Charney D. Effects of early stress on brain structure and function: implications for understanding the relationship between child maltreatment and depression. Dev. Psychopathol. 2001;13(3):451–471
  45. Kenny FM, Gancayco GP, Heald FP, Hung W. Cortisol production rate in adolescent males in different stages of sexual maturation. J. Clin. Endocrinol. Metab. 1966;26(11):1232–1236
  46. Kenny FM, Preeyasombat C, Migeon CJ. Cortisol production rate. II. Normal infants, children, and adults. Pediatrics. 1966;37(1):34–42
  47. Kiess W, Meidert A, Dressendorfer RA, Schriever K, Kessler U, Konig A, et al. Salivary cortisol levels throughout childhood and adolescence: relation with age, pubertal stage, and weight. Pediatr. Res. 1995;37(4 Pt 1):502–506
  48. Klimes-Dougan B, Hastings PD, Granger DA, Usher BA, Zahn-Waxler C. Adrenocortical activity in at-risk and normally developing adolescents: individual differences in salivary cortisol basal levels, diurnal variation, and responses to social challenges. Dev. Psychopathol. 2001;13(3):695–719
  49. Kovacs M. Children's Depression Inventory Manual. North Tonawanda, New York: Multi-Health Systems, Inc.; 1992;
  50. Kutcher S, Malkin D, Silverberg J, Marton P, Williamson P, Malkin A, et al. Nocturnal cortisol, thyroid stimulating hormone, and growth hormone secretory profiles in depressed adolescents. J. Am. Acad. Child Adolesc. Psychiatry. 1991;30(3):407–414
  51. La Greca AM. Peer acceptance: the correspondence between children's sociometric scores and teachers’ rating of peer interactions. J. Abnorm. Child Psychol. 1981;9(2):167–178
  52. Ledingham JE. Developmental patterns of aggressive and withdrawn behavior in childhood: a possible method for identifying preschizophrenics. J. Abnorm. Child Psychol. 1981;9(1):1–22
  53. Ledingham JE, Younger AJ. The influence of the evaluator on assessments of children's social skills. In:  Schneider BH, et al. editor. Social Competence in Developmental Perspective. Dordrecht: Kluwer; 1985;
  54. Luby JL, Heffelfinger A, Mrakotsky C, Brown K, Hessler M, Spitznagel E. Alterations in stress cortisol reactivity in depressed preschoolers relative to psychiatric and no-disorder comparison groups. Arch. Gen. Psychiatry. 2003;60(12):1248–1255
  55. Luby JL, Mrakotsky C, Heffelfinger A, Brown K, Spitznagel E. Characteristics of depressed preschoolers with and without anhedonia: evidence for a melancholic depressive subtype in young children. Am. J. Psychiatry. 2004;161(11):1998–2004
  56. Lupie SJ, King S, Meaney MJ, McEwen BS. Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status. Dev. Psychopathol. 2001;13(3):653–676
  57. Mathew SJ, Coplan JD, Goetz RR, Feder A, Greenwald S, Dahl RE, et al. Differentiating depressed adolescent 24h cortisol secretion in light of their adult clinical outcome. Neuropsychopharmacology. 2003;28(7):1336–1343
  58. McBurnett K, Lahey BB, Frick PJ, Risch C, Loeber R, Hart EL, et al. Anxiety, inhibition, and conduct disorder in children. II. Relation to salivary cortisol. J. Am. Acad. Child Adolesc. Psychiatry. 1991;30(2):192–196
  59. McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 2007;87(3):873–904
  60. Mechlin MB, Maixner W, Light KC, Fisher JM, Girdler SS. African Americans show alterations in endogenous pain regulatory mechanisms and reduced pain tolerance to experimental pain procedures. Psychosom. Med. 2005;67(6):948–956
  61. Morris NM, Udry JR. Validation of a self-administered instrument to assess stage of adolescent development. J. Youth Adolesc. 1980;9(3):271–280
  62. Moss HB, Vanyukov M, Yao JK, Kirillova GP. Salivary cortisol responses in prepubertal boys: the effects of parental substance abuse and association with drug use behavior during adolescence. Biol. Psychiatry. 1999;45(10):1293–1299
  63. Moss HB, Vanyukov MM, Martin CS. Salivary cortisol responses and the risk for substance abuse in prepubertal boys. Biol. Psychiatry. 1995;38(8):547–555
  64. Pekarik EG, Prinz RJ, Liebert DE, Weintraub S, Neale JM. The Pupil Evaluation Inventory. A sociometric technique for assessing children's social behavior. J. Abnorm. Child Psychol. 1976;4(1):83–97
  65. Petty LK, Asarnow JR, Carlson GA, Lesser L. The dexamethasone suppression test in depressed, dysthymic, and nondepressed children. Am. J. Psychiatry. 1985;142(5):631–633
  66. Puig-Antich J, Dahl R, Ryan N, Novacenko H, Goetz D, Goetz R, et al. Cortisol secretion in prepubertal children with major depressive disorder. Episode and recovery. Arch. Gen. Psychiatry. 1989;46(9):801–809
  67. Rao U, Dahl RE, Ryan ND, Birmaher B, Williamson DE, Giles DE, et al. The relationship between longitudinal clinical course and sleep and cortisol changes in adolescent depression. Biol. Psychiatry. 1996;40(6):474–484
  68. Rickels K, Garcia CR, Lipman RS, Derogatis LR, Fisher EL. The Hopkins Symptom Checklist. Assessing emotional distress in obstetric-gynecologic practice. Prim. Care. 1976;3(4):751–764
  69. Risbrough VB, Stein MB. Role of corticotropin releasing factor in anxiety disorders: a translational research perspective. Horm. Behav. 2006;50(4):550–561
  70. Rogeness GA, Cepeda C, Macedo CA, Fischer C, Harris WR. Differences in heart rate and blood pressure in children with conduct disorder, major depression, and separation anxiety. Psychiatry Res. 1990;33(2):199–206
  71. Ronsaville DS, Municchi G, Laney C, Cizza G, Meyer SE, Haim A, et al. Maternal and environmental factors influence the hypothalamic–pituitary–adrenal axis response to corticotropin-releasing hormone infusion in offspring of mothers with or without mood disorders. Dev. Psychopathol. 2006;18(1):173–194
  72. Rosmalen JG, Oldehinkel AJ, Ormel J, de Winter AF, Buitelaar JK, Verhulst FC. Determinants of salivary cortisol levels in 10–12 year old children; a population-based study of individual differences. Psychoneuroendocrinology. 2005;30(5):483–495
  73. Scerbo AS, Kolko DJ. Salivary testosterone and cortisol in disruptive children: relationship to aggressive, hyperactive, and internalizing behaviors. J. Am. Acad. Child Adolesc. Psychiatry. 1994;33(8):1174–1184
  74. Schmidt LA, Fox NA, Rubin KH, Sternberg EM, Gold PW, Smith CC, et al. Behavioral and neuroendocrine responses in shy children. Dev. Psychobiol. 1997;30(2):127–140
  75. Shirtcliff EA, Granger DA, Booth A, Johnson D. Low salivary cortisol levels and externalizing behavior problems in youth. Dev. Psychopathol. 2005;17(1):167–184
  76. Shoal GD, Giancola PR, Kirillova GP. Salivary cortisol, personality, and aggressive behavior in adolescent boys: a 5-year longitudinal study. J. Am. Acad. Child Adolesc. Psychiatry. 2003;42(9):1101–1107
  77. Smider NA, Essex MJ, Kalin NH, Buss KA, Klein MH, Davidson RJ, et al. Salivary cortisol as a predictor of socioemotional adjustment during kindergarten: a prospective study. Child Dev. 2002;73(1):75–92
  78. Sondeijker FE, Ferdinand RF, Oldehinkel AJ, Tiemeier H, Ormel J, Verhulst FC. HPA-axis activity as a predictor of future disruptive behaviors in young adolescents. Psychophysiology. 2008;45(3):398–404
  79. Szanton SL, Gill JM, Allen JK. Allostatic load: a mechanism of socioeconomic health disparities?. Biol. Res. Nurs. 2005;7(1):7–15
  80. Targum SD, Capodanno AE. The dexamethasone suppression test in adolescent psychiatric inpatients. Am. J. Psychiatry. 1983;140(5):589–591
  81. Tennes K, Kreye M. Children's adrenocortical responses to classroom activities and tests in elementary school. Psychosom. Med. 1985;47(5):451–460
  82. Tout K, de Haan M, Campbell EK, Gunnar MR. Social behavior correlates of cortisol activity in child care: gender differences and time-of-day effects. Child Dev. 1998;69(5):1247–1262
  83. Tyrka AR, Wier LM, Anderson GM, Wilkinson CW, Price LH, Carpenter LL. Temperament and response to the Trier Social Stress Test. Acta Psychiatr. Scand. 2007;115(5):395–402
  84. Tyrka AR, Wier LM, Price LH, Rikhye K, Ross NS, Anderson GM, et al. Cortisol and ACTH responses to the Dex/CRH test: influence of temperament. Horm. Behav. 2008;53(4):518–525
  85. Van den Bergh BR, Van Calster B, Pinna Puissant S, Van Huffel S. Self-reported symptoms of depressed mood, trait anxiety and aggressive behavior in post-pubertal adolescents: associations with diurnal cortisol profiles. Horm. Behav. 2008;54(2):253–257
  86. van Goozen SH, Matthys W, Cohen-Kettenis PT, Buitelaar JK, van Engeland H. Hypothalamic–pituitary–adrenal axis and autonomic nervous system activity in disruptive children and matched controls. J. Am. Acad. Child Adolesc. Psychiatry. 2000;39(11):1438–1445
  87. van Goozen SH, Matthys W, Cohen-Kettenis PT, Gispen-de Wied C, Wiegant VM, van Engeland H. Salivary cortisol and cardiovascular activity during stress in oppositional-defiant disorder boys and normal controls. Biol. Psychiatry. 1998;43(7):531–539
  88. Viru A, Laaneots L, Karelson K, Smirnova T, Viru M. Exercise-induced hormone responses in girls at different stages of sexual maturation. Eur. J. Appl. Physiol. Occup. Physiol. 1998;77(5):401–408
  89. Walker EF, Walder DJ, Reynolds F. Developmental changes in cortisol secretion in normal and at-risk youth. Dev. Psychopathol. 2001;13(3):721–732
  90. Wechsler D. The Wechsler Intelligence Scale for Children. Third Edition. New York: The Psychological Corporation; 1991;
  91. Zobel A, Barkow K, Schulze-Rauschenbach S, Von Widdern O, Metten M, Pfeiffer U, et al. High neuroticism and depressive temperament are associated with dysfunctional regulation of the hypothalamic–pituitary–adrenocortical system in healthy volunteers. Acta Psychiatr. Scand. 2004;109(5):392–399

PII: S0306-4530(10)00033-8

doi: 10.1016/j.psyneuen.2010.02.002

Psychoneuroendocrinology
Volume 35, Issue 8 , Pages 1167-1177 , September 2010

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