Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-19T14:31:02.820Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  10 February 2006

DONNA S. RONSAVILLE ,
GIOVANNA MUNICCHI ,
CAROLYN LANEY ,
GIOVANNI CIZZA ,
STEPHANIE E. MEYER ,
ADAM HAIM ,
MARIAN RADKE-YARROW ,
GEORGE CHROUSOS ,
PHILLIP W. GOLD  and
PEDRO E. MARTINEZ
DONNA S. RONSAVILLE
Affiliation:
NIMH
GIOVANNA MUNICCHI
Affiliation:
NICHD
CAROLYN LANEY
Affiliation:
NIMH
GIOVANNI CIZZA
Affiliation:
NIDDK
STEPHANIE E. MEYER
Affiliation:
NIMH University of California
ADAM HAIM
Affiliation:
NIMH
MARIAN RADKE-YARROW
Affiliation:
NIMH
GEORGE CHROUSOS
Affiliation:
NICHD
PHILLIP W. GOLD
Affiliation:
NIMH
PEDRO E. MARTINEZ
Affiliation:
NIMH
Get access Rights & Permissions [Opens in a new window]

Abstract

Individuals with melancholic major depression exhibit basal hypercortisolism and an attenuated ACTH response to exogenous corticotropin-releasing hormone (CRH) infusion. Given the greater incidence of depression in children of depressed parents, we examined the ACTH and cortisol responses to ovine CRH (oCRH) infusion in 63 adolescent offspring of mothers with major depression, bipolar illness, or no psychiatric illness. Psychiatric and observational assessments of these families had been conducted over the course of 10 years preceding this study. We examined the children's responses to CRH in relation to maternal characteristics and family environment and found the following: (a) cortisol responses were negatively related to chronic family stress and (b) offspring of depressed mothers with an avoidant personality disorder showed an exaggerated ACTH response. In addition, adolescents in late puberty (Tanner 4 and 5) had lower ACTH and cortisol responses to oCRH infusion than those in early puberty. Further, offspring with early histories of mood problems, and those who developed major depressive disorder as young adults, did not exhibit basal hypercortisolism but did show an attenuated ACTH response to CRH. Our results add to the growing body of literature showing the influence of maternal characteristics and environmental factors on hypothalamic–pituitary–adrenal axis patterns in children.We acknowledge the efforts of our predecessors on this project, whose work made this study possible. In addition, we thank Ann Mayfield, Sara Torvik, and Patricia Kasdan for their recruitment efforts and Sue Harris and Hayley Kleitz for their editorial comments on the manuscript. Finally, we thank all of the mothers and their children who have dedicated their time to this study over the course of 20 years.

Type
Research Article
Information
Development and Psychopathology , Volume 18 , Issue 1 , March 2006 , pp. 173 - 194
Copyright
© 2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Achenbach, T., & Edelbrock, C. (1983). Manual for the Child Behavior Checklist and revised child behavior profile. Burlington, VT: University of Vermont, Department of Psychology.
Alden, L., Laposa, J., Taylor, C., & Ryder, A. (2002). Avoidant personality disorder: Current status and future directions. Journal of Personality Disorders, 16, 1–29.CrossRefGoogle Scholar
Alpert, J. E., Uebelacke, L. A., McLean, N. E., Nierenberg, A. A., Pava, J. A., Worthington, J. J., et al. (1997). Social phobia, avoidant personality disorder and atypical depression: Co-occurrence and clinical implications. Psychological Medicine, 27, 627–633.CrossRefGoogle Scholar
Angold, A., Costello, E. J., & Worthman, C. M. (1998). Puberty and depression: The roles of age, pubertal status and pubertal timing. Psychological Medicine, 28, 51–61.CrossRefGoogle Scholar
Arborelius, L., Owens, M. J., Plotsky, P. M., & Nemeroff, C. B. (1999). The role of corticotropin-releasing factor in depression and anxiety disorders. Journal of Endocrinology, 160, 1–12.Google Scholar
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.CrossRefGoogle Scholar
Atko, V., Laaneots, L., Karelson, K., Smirnova, T., & Viru, M. (1998). Exercise-induced hormone responses in girls at different stages of sexual maturation. European Journal of Applied Physiology, 77, 401–408.Google Scholar
Attanasio, A., Rosskamp, R., Bernasconi, S., Terzi, C., Ranke, M., Giovanelli, G., et al. (1987). Plasma adrenocorticotropin, cortisol, and dehydroepiandrosterone response to cortocotropin-releasing factor in normal children during pubertal development. Pediatric Research, 22, 41–44.CrossRefGoogle Scholar
Beardslee, W., Bemporad, J., Keller, M., & Klerman, G. (1983). Children of parents with major affective disorder: A review. American Journal of Psychiatry, 140, 825–832.Google Scholar
Beck, A. T., & Steer, R. A. (1988). Beck Hopelessness Scale (BHS). San Antonio, TX: Psychological Association/Harcourt Brace Jovanovich.
Birmaher, B., Dahl, R. E., Perel, J., Williamson, D. E., Nelson, B., Stull, S., et al. (1996). Corticotropin-releasing hormone challenge in prepubertal major depression. Biological Psychiatry, 39, 267–277.CrossRefGoogle Scholar
Brown, G., & Harris, T. (1978). Social origins of depression. A study of psychiatric disorders in women. London: Tavistock.
Caldji, C., Diorio, J., & Meaney, M. J. (2000). Variations in maternal care in infancy regulate the development of stress reactivity. Biological Psychiatry, 48, 1164–1174.CrossRefGoogle Scholar
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Sciences of the United States of America, 95, 5335–5340.CrossRefGoogle Scholar
Chrousos, G. P., & Gold, P. W. (1992). The concepts of stress and stress system disorders: Overview of physical and behavioral homeostasis. Journal of the American Medical Association, 267, 1244–1252.CrossRefGoogle Scholar
Chrousos, G. P., Schulte, H. M., Oldfield, E. H., Gold, P. W., Cutler, G. B., Jr., & Loriaux, D. L. (1984). The CRF stimulation test: Aid in the differential diagnosis of Cushing's disease. New England Journal of Medicine, 310, 622–627.CrossRefGoogle Scholar
Clarke, A. S., Wittwer, D. J., Abbott, D. H., & Schneider, M. L. (1994). Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Developmental Psychobiology, 27, 257–269.CrossRefGoogle Scholar
Coplan, J. D., Andrews, M. W., Rosenblum, L. A., Owens, M. J., Friedman, S., Gorman, J. M., et al. (1996). Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: Implications for the pathophysiology of mood and anxiety disorders. Proceedings of the National Academy of Sciences of the United States of America, 93, 1619–1623.CrossRefGoogle Scholar
Coplan, J. D., Trost, R. C., Owens, M. J., Cooper, T. B., Gorman, J. M., Nemeroff, C. B., et al. (1998). Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Archives of General Psychiatry, 55, 473–477.CrossRefGoogle Scholar
Darlington, D. N., & Dallman, M. F. (2001). Feedback control in endocrine systems. In K. L. Becker (Ed.), Principles and practice of endocrinology and metabolism (3rd ed., pp. 50–56). Philadelphia, PA: Lippincott Williams & Wilkins.
De Bellis, M. D., Chrousos, G. P., Dorn, L. D., Burke, L., Helmers, K., Kling, M. A., et al. (1994). Hypothalamic–pituitary–adrenal axis dyregulation in sexually abused girls. Journal of Clinical Endocrinology and Metabolism, 78, 249–255.Google Scholar
Dorn, L. D., Burgess, E. S., Susman, E. J., von Eye, A., De Bellis, M. D., Gold, P. W., et al. (1996). Response to oCRH in depressed and nondepressed adolescents: Does gender make a difference? Journal of the American Academy of Child and Adolescent Psychiatry, 35, 764–773.Google Scholar
Ellenbogen, M. A., Hodgins, S., & Walker, C. D. (2004). High levels of cortisol among adolescent offspring of parents with bipolar disorder: A pilot study. Psychoneuroendocrinology, 29, 99–106.CrossRefGoogle Scholar
Endicott, J., Spitzer, R., Fleiss, J., & Cohen, J. (1976). The global assessment scale. Archives of General Psychiatry, 33, 766–771.CrossRefGoogle Scholar
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002). Maternal stress beginning in infancy may sensitize children to later stress exposure: Effects on cortisol and behavior. Biological Psychiatry, 52, 776–784.CrossRefGoogle Scholar
Fahlke, C., Lorenz, J. G., Long, J., Champoux, M., Soumi, S. J., & Higley, J. D. (2000). Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcoholism: Clinical and Experimental Research, 24, 644–650.CrossRefGoogle Scholar
Flinn, M. V., & England, B. G. (1997). Social economics of childhood glucocorticoid stress response and health. American Journal of Physical Anthropology, 102, 33–53.3.0.CO;2-E>CrossRefGoogle Scholar
Francis, D. D., Diorio, J., Liu, D., & Meaney, M. J. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science, 286, 1155–1158.CrossRefGoogle Scholar
Francis, D. D., & Meaney, M. J. (1999). Maternal care and the development of the stress response. Current Opinions in Neurobiology, 9, 128–134.CrossRefGoogle Scholar
Gold, P. W., Calabrese, J. R., Kling, M. A., Avgerinos, P., Khan, I., Gallucci, W. T., et al. (1986). Abnormal ACTH and cortisol responses to ovine corticotropin releasing factor in patients with primary affective disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 10, 57–65.CrossRefGoogle Scholar
Gold, P. W., Licinio, J., Wong, M. L., & Chrousos, G. P. (1995). Corticotropin releasing hormone in the pathophysiology of melancholic and atypical depression and in the mechanism of action of antidepressant drugs. Annals of the New York Academy of Sciences, 771, 716–729.CrossRefGoogle Scholar
Gold, P. W., Loriaux, D. L., Roy, A., Kling, M. A., Calabrese, J. R., Kellner, C. H., et al. (1986). Responses to corticotropin-releasing hormone in the hypercortisolism of depression and Cushing's disease. Pathophysiologic and diagnostic implications. New England Journal of Medicine, 314, 1329–1335.CrossRefGoogle 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.CrossRefGoogle Scholar
Granger, D. A., Serbin, L. A., Schwartzman, A., Lehoux, P., Cooperman, J., & Ikeda, S. (1998). Children's salivary cortisol, internalising behavior problems, and family environment: Results from the Concordia Longitudinal Risk Project. International Journal of Behavioral Development, 22, 707–728.CrossRefGoogle 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.CrossRefGoogle Scholar
Gunnar, M. R., Brodersen, L., Krueger, K., & Rigatuso, J. (1996). Dampening of adrenocortical responses during infancy: Normative changes and individual differences. Child Development, 67, 844–889.CrossRefGoogle Scholar
Gunnar, M. R., Brodersen, L., Nachmias, M., Buss, K., & Rigatuso, J. (1996). Stress reactivity and attachment security. Developmental Psychobiology, 29, 191–204.3.0.CO;2-M>CrossRefGoogle Scholar
Gunnar, M. R., Larson, M. C., Hertsgaard, L., Harris, M. L., & Brodersen, L. (1992). The stressfulness of separation among nine-month-old infants: Effects of social context variables and infant temperament. Child Development, 63, 290–303.CrossRefGoogle Scholar
Gunnar, M. R., Morison, S. J., Chisholm, K., & Schuder, M. (2001). Salivary cortisol levels in children adopted from romanian orphanages. Development and Psychopathology, 13, 611–628.CrossRefGoogle Scholar
Gunnar, M. R., & Vasquez, 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.CrossRefGoogle Scholar
Harlow, H. F., Rowland, G. L., & Griffin, G. A. (1964). The effect of total social deprivation on the development of monkey behavior. Psychiatry Research Report American Psychiatry Association, 19, 116–135.Google Scholar
Hauger, R. L., Shelt, S. G., & Redei, E. E. (2002). Decreased corticotropin-releasing factor receptor expression and adrenocorticotropic hormone responsiveness in anterior pituitary cells of Wistar–Kyoto rats. Journal of Neuroendocrinology, 14, 126–134.CrossRefGoogle Scholar
Heim, C., Newport, D. J., Bonsall, R., Miller, A. H., & Nemeroff, C. B. (2001). Altered pituitary–adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. Americal Journal of Psychiatry, 158, 575–581.CrossRefGoogle Scholar
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., et al. (2000). Pituitary–adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association, 284, 592–597.CrossRefGoogle Scholar
Herjanic, B., & Reich, W. (1982). Development of a structured psychiatric interview for children: Agreement between child and parent on individual symptoms. Journal of Abnormal Child Psychology, 19, 307–324.CrossRefGoogle Scholar
Hodges, K., Kline, J., Fitch, P., McKnew, D., & Cytryn, L. (1981). The Child Assessment Schedule: A diagnostic interview for research and clinical use. Catalogue of Selected Documents in Psychology, 11, 56.Google Scholar
Hollingshead, A. B. (1975). Four factor index of social status. Unpublished manuscript. Department of Sociology, Yale University.
Holsboer, F., Lauer, C. J., Schreiber, W., & Krieg, J. C. (1995). Altered hypothalamic–pituitary–adrenocortical regulation in healthy subjects at high familial risk for affective disorders. Neuroendocrinology, 62, 340–347.Google Scholar
Holsboer, F., Vonbardeleben, U., Girken, A., Stalla, G. K., & Muller, O. A. (1984). Blunted corticotropin and normal cortisol response to human corticotropin-releasing factor in depression. New England Journal of Medicine, 311, 1127.Google Scholar
Huot, R. L., Gonzalez, M. E., Ladd, C. O., Thrivikraman, K. V., & Plotsky, P. M. (2004). Foster litters prevent hypothalamic–pituitary–adrenal axis sensitization mediated by neonatal maternal separation. Psychoneuroendocrinology, 29, 279–289.CrossRefGoogle Scholar
Kaufman, J., Birmaher, B., Perel, J., Dahl, R. E., Moreci, P., Nelson, B., et al. (1997). The corticotropin-releasing hormone challenge in depressed abused, depressed nonabused, and normal control children. Biological Psychiatry, 42, 669–679.CrossRefGoogle Scholar
Kaufman, J., Martin, A., King, R., & Charney, D. (2001). Are child-, adolescent-, and adult-onset depression one and the same disorder? Biological Psychiatry, 49, 980–1001.Google Scholar
Kaufman, J., & Ryan, N. (1999). The neurobiology of child and adolescent depression. In D. Charney, D. Nestler, & B. Bunny (Eds.), The Neurobiological Foundation of Mental Illness (pp. 810–822). New York: Oxford University Press.
Kiess, W., Meidert, A., Dressendorfer, R., Schriever, K., Kessler, U., Konig, K., et al. (1995). Salivary cortisol levels throughout childhood and adolescence: Relation with age, pubertal stage, and weight. Pediatric Research, 37, 502–506.CrossRefGoogle Scholar
King, J. A., Barkley, R. A., & Barrett, S. (1998). Attention-deficit hyperactivity disorder and the stress response. Biological Psychiatry, 44, 72–74.CrossRefGoogle Scholar
King, J. A., & Edwards, E. (1999). Early stress and genetic influences on hypothalamic–pituitary–adrenal axis functioning in adulthood. Hormones and Behavior, 36, 79–85.CrossRefGoogle 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.CrossRefGoogle Scholar
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, 536–540.Google Scholar
Kovacs, M. (1992). The Children's Depression Inventory (CDI) manual. Toronto: Multi-Health Systems.
Levine, S. (2000). Influence of psychological variables on the activity of the hypothalamic–pituitary–adrenal axis. European Journal of Pharmacology, 405, 149–160.CrossRefGoogle Scholar
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., et al. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science, 277, 1659–1662.CrossRefGoogle Scholar
Loranger, A. (1988). Personality Disorder Examination (PDE) manual. Yonkers, NY: DV Communications.
Luby, J. L., Heffelfinger, A., Mrakotsky, C., Brown, K., Hessler, M., & Spitznagel, E. (2003). Alterations in stress cortisol reactivity in depressed preschoolers relative to psychiatric and no-disorder comparison groups. Archives of General Psychiatry, 60, 1248–1255.CrossRefGoogle Scholar
Ma, X. M., Levy, A., & Lightman, S. L. (1997). Emergence of an isolated arginine vasopressin (AVP) response to stress after repeated restraint: A study of both AVP and corticotropin-releasing hormone messenger ribonucleic acid (RNA) and heteronuclear RNA. Endocrinology, 138, 4351–4357.CrossRefGoogle Scholar
Ma, X. M., Lightman, S. L., & Aguilera, G. (1999). Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint. Endocrinology, 140, 3623–3632.CrossRefGoogle Scholar
Mamalaki, E., Kvetnansky, R., Brady, L. S., Gold, P. W., & Herkenham, M. (1992). Repeated immobilization stress alters tyrosine hydroxylase corticotropin-releasing hormone and corticosteroid receptor messenger ribonucleic acid levels in rat brain. Journal of Neuroendocrinology, 4, 689–699.CrossRefGoogle Scholar
Marshall, W. A., & Tanner, J. M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291–303.CrossRefGoogle Scholar
Martinez, P., Ronsaville, D., Torvik, S., Eskandari, F., Kotila, C., Mistry, S., et al. (2003). Women aged 21 to 45 with atypical depression exhibit greater plasma ACTH, and delayed ACTH and cortisol nocturnal nadirs compared to melancholic, and mixed subtypes and control subjects. Potential implications for the pathophysiology and medical consequences of major depressive subtypes. Poster presented at NIH Research Festival, October, 2003.
Meyer, S. E., Chrousos, G. P., & Gold, P. W. (2001). Major depression and the stress system: A life span perspective. Development and Psychopathology, 13, 565–580.CrossRefGoogle Scholar
Newport, D. J., Heim, C., Owens, M. J., Ritchie, J. C., Ramsey, C. H., Bonsall, R., et al. (2003). Cerebrospinal fluid corticotropin-releasing factor (CRF) and vasopressin concentrations predict pituitary response in the CRF stimulation test: A multiple regression analysis. Neuropsychopharmacology, 28, 569–576.CrossRefGoogle Scholar
Ohta, R., Shirota, M., Adachi, T., Tohei, A., & Taya, K. (1999). Plasma ACTH levels during early, two-way avoidance acquisition in high- and low-avoidance rats (Hatano strains). Behavior Genetics, 29, 137–144.CrossRefGoogle Scholar
Orvaschel, H., Walsh-Allis, G., & Ye, W. (1988). Psychopathology in children of parents with recurrent depression. Journal of Abnormal Child Psychology, 16, 17–28.CrossRefGoogle Scholar
Plotsky, P. M., & Meaney, M. J. (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research, 18, 195–200.CrossRefGoogle Scholar
Radke-Yarrow, M., Martinez, P., Mayfield, A., & Ronsaville, D. (1998). Children of depressed mothers: From early childhood to maturity. New York: Cambridge University Press.
Radke-Yarrow, M., Nottelmann, E., Martinez, P., Fox, M. B., & Belmont, B. (1992). Young children of affectively ill parents: A longitudinal study of psychosocial development. Journal of the American Academy of Child and Adolescent Psychiatry, 31, 68–77.CrossRefGoogle Scholar
Rao, U., McCracken, J. T., Lutchmansingh, P., Edwards, C., & Poland, R. E. (1997). Electroencephalographic sleep and urinary free cortisol in adolescent depression: A preliminary report of changes from episode to recovery. Biological Psychiatry, 41, 369–373.CrossRefGoogle Scholar
Ross, J., Schulte, H., Gallucci, W., Cutler, G., Loriaux, D., & Chrousos, G. (1986). Ovine corticotropin-releasing hormone stimulation test in normal children. Journal of Clinical Endocrinology and Metabolism, 62, 390–392.CrossRefGoogle Scholar
Rutter, M., & Quinton, D. (1984). Parental psychiatric disorder: Effects on children. Psychological Medicine, 14, 855–880.CrossRefGoogle Scholar
Ryan, N. D., & Dahl, R. E. (1993). The biology of depression in children and adolescents. In J. J. Mann & D. J. Kupfer (Eds.), Biology of depressive disorders, Part B: Subtypes of depression and comorbid disorders (Vol. 4, pp. 37–58). New York: Plenum Press.
SAS Institute. (1990). SAS/Stat users guide. Version 6 (4th ed., Vol. 1). Cary, NC: SAS Institute.
Schulte, H. M., Chrousos, G. P., Oldfield, E. H., Gold, P. W., Cutler, G. B., Jr., & Loriaux, D. L. (1982). The effects of corticotropin releasing factor on the anterior pituitary function of stalk-sectioned cynomolgus macaques: Dose response of cortical secretion. Journal of Clinical Endocrinology and Metabolism, 55, 810–812.CrossRefGoogle Scholar
Shannon, C., Champoux, M., & Suomi, S. (1998). Rearing condition and plasma cortisol in rhesus monkey infants. American Journal of Primatology, 46, 311–321.3.0.CO;2-L>CrossRefGoogle Scholar
Shoal, G. D., Giancola, P. R., & Kirillova, G. P. (2003). Salivary cortisol, personality, and aggressive behavior in adolescent boys: A 5-year longitudinal study. Journal of the American Academy of Child and Adolescent Psychiatry, 42, 1101–1107.CrossRefGoogle Scholar
Singer, J. (1998). Using SAS PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. Journal of Educational and Behavioral Statistics, 24, 323–355.CrossRefGoogle Scholar
Spitzer, R. L., & Endicott, J. (1977). The Schedule for Affective Disorders and Schizophrenia: Lifetime version. New York: New York State Psychiatric Institute, Biometrics Research.
Spitzer, R. L., Williams, T. B. W., Gibbon, M., & First, M. B. (1989). Structured Clinical Interview for DSM-III-R, nonpatient version. New York: New York State Psychiatric Institute, Biometrics Research.
Stuart, S., Pfohl, B., Battaglia, M., Bellodi, L., Grove, W., & Cadoret, R. (1998). The co-occurrence of DSM-III-R personality disorders. Journal of Personality Disorders, 12, 302–315.CrossRefGoogle Scholar
Suomi, S. J. (1999). Attachment in rhesus monkeys. In J. Cassidy & P. R. Shaver (Eds.), Handbook of attachment: Theory, research, and clinical application (pp. 181–197). New York: Guilford Press.
Suomi, S. J., & Levine, S. (1998). Psychobiology of intergenerational effects of trauma. Evidence from animal studies. In Y. Danieli (Ed.), International handbook of multigenerational legacies of trauma (pp. 623–637). New York: Plenum Press.
Tennes, K., & Kreye, M. (1985). Children's adrenocortical responses to classroom activities and tests in elementary school. Psychosomatic Medicine, 47, 451–460.CrossRefGoogle Scholar
Tennes, K., Kreye, M., Avitable, N., & Wells, R. (1986). Behavioral correlates of excreted catecholamines and cortisol in second-grade children. Journal of the American Academy of Child Psychiatry, 25, 764–770.CrossRefGoogle Scholar
Van Cauter, E. (2001). Endocrine rhythms. In K. L. Becker (Ed.), Principles and practice of endocrinology and metabolism (3rd ed., pp. 57–68). Philadelphia, PA: Lippincott Williams & Wilkins.
van Goozen, S. H., 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Weise, M., Eisenhofer, G., & Merke, D. P. (2002). Pubertal and gender-related changes in the sympathoadrenal system in healthy children. Journal of Clinical Endocrinology and Metabolism, 87, 5038–5043.CrossRefGoogle Scholar
Yehuda, R., Bierer, L. M., Schmeidler, J., Aferiat, D. H., Breslau, I., & Dolan, S. (2000). Low cortisol and risk for PTSD in adult offspring of Holocaust survivors. American Journal of Psychiatry, 157, 1252–1259.CrossRefGoogle Scholar
Yehuda, R., Southwick, S. M., Krystal, J. H., Bremner, D., Charney, D. S., & Mason, J. W. (1993). Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder. American Journal of Psychiatry, 150, 83–86.Google Scholar
Young, E. A., Carlson, N. E., & Brown, M. B. (2002). Twenty-four-hour ACTH and cortisol pulsatility in depressed women. Neuropsychopharmacology, 25, 267–276.Google Scholar
Young, E. A., Haskett, R. F., Murphy-Weinberg, V., Watson, S. J., & Akil, H. (1991). Loss of glucocorticoid fast feedback in depression. Archives of General Psychiatry, 48, 693–699.CrossRefGoogle Scholar
Zachmann, M., Prader, A., Kind, H. P., Hafliger, H., & Budliger, H. (1974). Testicular volume during adolescence. Cross-sectional and longitudinal studies. Helvica Paediatric Acta, 29, 61–72.Google Scholar