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Influence of early life stress on later hypothalamic–pituitary–adrenal axis functioning and its covariation with mental health symptoms: A study of the allostatic process from childhood into adolescence

Published online by Cambridge University Press:  21 October 2011

Marilyn J. Essex ,
Elizabeth A. Shirtcliff ,
Linnea R. Burk ,
Paula L. Ruttle ,
Marjorie H. Klein ,
Marcia J. Slattery ,
Ned H. Kalin  and
Jeffrey M. Armstrong
Marilyn J. Essex*
Affiliation:
University of Wisconsin School of Medicine and Public Health
Elizabeth A. Shirtcliff
Affiliation:
University of New Orleans
Linnea R. Burk
Affiliation:
University of Wisconsin School of Medicine and Public Health University of Wisconsin–Madison
Paula L. Ruttle
Affiliation:
University of Wisconsin School of Medicine and Public Health
Marjorie H. Klein
Affiliation:
University of Wisconsin School of Medicine and Public Health
Marcia J. Slattery
Affiliation:
University of Wisconsin School of Medicine and Public Health
Ned H. Kalin
Affiliation:
University of Wisconsin School of Medicine and Public Health
Jeffrey M. Armstrong
Affiliation:
University of Wisconsin School of Medicine and Public Health
*
Address correspondence and reprint requests to: Marilyn J. Essex, Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, 6001 Research Park Boulevard, Madison, WI 53719-1176; E-mail: [email protected].
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Abstract

The hypothalamic–pituitary–adrenal (HPA) axis is a primary mechanism in the allostatic process through which early life stress (ELS) contributes to disease. Studies of the influence of ELS on children's HPA axis functioning have yielded inconsistent findings. To address this issue, the present study considers multiple types of ELS (maternal depression, paternal depression, and family expressed anger), mental health symptoms, and two components of HPA functioning (traitlike and epoch-specific activity) in a long-term prospective community study of 357 children. ELS was assessed during the infancy and preschool periods; mental health symptoms and cortisol were assessed at child ages 9, 11, 13, and 15 years. A three-level hierarchical linear model addressed questions regarding the influences of ELS on HPA functioning and its covariation with mental health symptoms. ELS influenced traitlike cortisol level and slope, with both hyper- and hypoarousal evident depending on type of ELS. Further, type(s) of ELS influenced covariation of epoch-specific HPA functioning and mental health symptoms, with a tighter coupling of HPA alterations with symptom severity among children exposed previously to ELS. Results highlight the importance of examining multiple types of ELS and dynamic HPA functioning in order to capture the allostatic process unfolding across the transition into adolescence.

Type
Articles
Information
Development and Psychopathology , Volume 23 , Issue 4: Allostatic Load: Part 2 , November 2011 , pp. 1039 - 1058
Copyright
Copyright © Cambridge University Press 2011

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References

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 ScholarPubMed
Barnett, R. C., & Marshall, N. L. (1989). Preliminary manual for the Role-Quality Scales. Wellesley, MA: Wellesley College Center for Research on Women.Google Scholar
Bernard, K., & Dozier, M. (2010). Examining infants' cortisol responses to laboratory tasks among children varying in attachment disorganization: Stress reactivity or return to baseline? Developmental Psychology, 46, 1771–1778.Google Scholar
Bjorklund, D. F., & Kipp, K. (1996). Parental investment theory and gender differences in the evolution of inhibition mechanisms. Psychological Bulletin, 120, 163–188.Google Scholar
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271–301.Google Scholar
Boyce, W. T., Essex, M. J., Alkon, A., Goldsmith, H. H., Kraemer, H. C., & Kupfer, D. J. (2006). Early father involvement moderates biobehavioral susceptibility to mental health problems in middle childhood. Journal of the American Academy of Child & Adolescent Psychiatry, 45, 1510–1520.CrossRefGoogle ScholarPubMed
Boyce, W. T., Essex, M. J., Goldstein, L. H., Armstrong, J. M., Kraemer, H. C., & Kupfer, D. J. (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood. I: Exploring the “headwaters” of early life morbidities. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 580–587.Google Scholar
Brennan, P. A., Pargas, R., Walker, E. F., Green, P., Newport, D. J., & Stowe, Z. N. (2008). Maternal depression and infant cortisol: Influences of timing, comorbidity and treatment. Journal of Child Psychology and Psychiatry, 49, 1099–1107.Google Scholar
Brownhill, S., Wilhelm, K., Barclay, L., & Schmied, V. (2005). “Big build”: Hidden depression in men. Australian and New Zealand Journal of Psychiatry, 39, 921–931.Google Scholar
Bureau, J.-F., Easterbrooks, M. A., & Lyons-Ruth, K. (2009). Maternal depressive symptoms in infancy: Unique contribution to children's depressive symptoms in childhood and adolescence? Development and Psychopathology, 21, 519–537.CrossRefGoogle ScholarPubMed
Calkins, S. D., & Hill, A. (2007). Caregiver influences on emerging emotion regulation: Biological and environmental transactions in early development. In Gross, J. J. (Ed.), Handbook of emotion regulation (pp. 229–248). New York: Guilford Press.Google Scholar
Cicchetti, D. (1990). A historical perspective on the discipline of developmental psychopathology. In Rolf, J., Masten, A. S., Cicchetti, D., Nuechterlein, K. H., & Weintraub, S. (Eds.), Risk and protective factors in the development of psychopathology (pp. 2–28). New York: Cambridge University Press.Google Scholar
Cicchetti, D., & Blender, J. A. (2004). A multiple-levels-of-analysis approach to the study of developmental processes in maltreated children. Proceedings of the National Academy of Sciences of the United States of America, 101, 17325–17326.CrossRefGoogle Scholar
Cicchetti, D., & Curtis, W. J. (2006). The developing brain and neural plasticity: Implications for normality, psychopathology, and resilience. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Vol. 2. Developmental neuroscience (2nd ed., pp. 1–64). Hoboken, NJ: Wiley.Google Scholar
Cicchetti, D., & Curtis, W. J. (2007). Multilevel perspectives on pathways to resilient functioning. Development and Psychopathology, 19, 627–629.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (2001). Diverse patterns of neuroendocrine activity in maltreated children. Development and Psychopathology, 13, 677–693.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2007). Personality, adrenal steroid hormones, and resilience in maltreated children: A multilevel perspective. Development and Psychopathology, 19, 787–809.Google Scholar
Cicchetti, D., Rogosch, F. A., Gunnar, M. R., & Toth, S. L. (2010). The differential impacts of early physical and sexual abuse and internalizing problems on daytime cortisol rhythm in school-aged children. Child Development, 81, 252–269.Google Scholar
Cicchetti, D., & Sroufe, L. A. (2000). The past as prologue to the future: The times they've been a changin'. Development and Psychopathology, 12, 255–264.CrossRefGoogle Scholar
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 16–25.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Valentino, K. (2006). An ecological–transactional perspective on child maltreatment: Failure of the average expectable environment and its influence on child development. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Vol. 3. Risk, disorder, and adaptation (2nd ed., pp. 129–201). Hoboken, NJ: Wiley.Google Scholar
Coe, C. L., Lubach, G. R., & Shirtcliff, E. A. (2007). Maternal stress during pregnancy predisposes for iron deficiency in infant monkeys impacting innate immunity. Pediatric Research, 61, 520–524.CrossRefGoogle ScholarPubMed
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, 746–773.Google Scholar
Crugnola, C. R., Tambelli, R., Spinelli, M., Gazzotti, S., Caprin, C., & Albizzati, A. (2011). Attachment patterns and emotion regulation strategies in the second year. Infant Behavior and Development, 34, 136–151.CrossRefGoogle Scholar
Cummings, E. M., & Davies, P. T. (2002). Effects of marital conflict on children: Recent advances and emerging themes in process-oriented research. Journal of Child Psychology and Psychiatry, 43, 31–63.CrossRefGoogle ScholarPubMed
Davies, P. T., Sturge-Apple, M. L., Cicchetti, D., & Cummings, E. M. (2007). The role of child adrenocortical functioning in pathways between interpersonal conflict and child maladjustment. Developmental Psychology, 43, 918–930.Google Scholar
Davies, P. T., Sturge-Apple, M. L., Cicchetti, D., Manning, L. G., & Zale, E. (2009). Children's patterns of emotional reactivity to conflict as explanatory mechanisms in links between interpartner aggression and child physiological functioning. Journal of Child Psychology and Psychiatry, 50, 1384–1391.Google Scholar
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience and Biobehavioral Reviews, 35, 1562–1592.Google Scholar
Ellis, B. J., Essex, M. J., & Boyce, W. T. (2005). Biological sensitivity to context: II. Empirical explorations of an evolutionary–developmental theory. Development and Psychopathology, 17, 303–328.Google Scholar
Ellis, B. J., Shirtcliff, E. A., Boyce, W. T., Deardorff, J., & Essex, M. J. (2011). Quality of early family relationships and the timing and tempo of puberty: Effects depend on biological sensitivity to context. Development and Psychopathology, 23, 85–99.CrossRefGoogle ScholarPubMed
Essex, M. J., Boyce, W. T., Goldstein, L. H., Armstrong, J. M., Kraemer, H. C., & Kupfer, D. J. (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood. II: Developing the MacArthur Health and Behavior Questionnaire. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 588–603.Google 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.Google Scholar
Essex, M. J., Klein, M. H., Cho, E., & Kraemer, H. C. (2003). Exposure to maternal depression and marital conflict: Gender differences in children's later mental health symptoms. Journal of the American Academy of Child & Adolescent Psychiatry, 42, 728–737.Google Scholar
Essex, M. J., Kraemer, H. C., Armstrong, J. M., Boyce, W. T., Goldsmith, H. H., Klein, M. H., et al. (2006). Exploring risk factors for the emergence of children's mental health problems. Archives of General Psychiatry, 63, 1246–1256.CrossRefGoogle ScholarPubMed
Essex, M. J., Kraemer, H. C., Slattery, M. J., Burk, L. R., Boyce, W. T., Woodward, H. R., et al. (2009). Screening for childhood mental health problems: Outcomes and early identification. Journal of Child Psychology and Psychiatry, 50, 562–570.CrossRefGoogle ScholarPubMed
Evans, G. W. (2003). A multimethodological analysis of cumulative risk and allostatic load among rural children. Developmental Psychology, 39, 924–933.CrossRefGoogle ScholarPubMed
Feng, X., Shaw, D. S., Skuban, E. M., & Lane, T. (2007). Emotional exchange in mother–child dyads: Stability, mutual influence, and associations with maternal depression and child problem behavior. Journal of Family Psychology, 21, 714–725.CrossRefGoogle ScholarPubMed
Fisher, P. A., & Stoolmiller, M. (2008). Intervention effects on foster parent stress: Associations with child cortisol levels. Development and Psychopathology, 20, 1003–1021.Google Scholar
Flinn, M. V., & England, B. G. (1995). Childhood stress and family environment. Current Anthropology, 36, 854–866.Google Scholar
Fox, N. A., & Calkins, S. D. (2003). The development of self-control of emotion: Intrinsic and extrinsic influences. Motivation and Emotion, 27, 7–26.Google Scholar
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, 984–992.Google Scholar
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, 458–490.Google Scholar
Gross, H. E., Shaw, D. S., Moilanen, K. L., Dishion, T. J., & Wilson, M. N. (2008). Reciprocal models of child behavior and depressive symptoms in mothers and fathers in a sample of children at risk for early conduct problems. Journal of Family Psychology, 22, 742–751.CrossRefGoogle Scholar
Grych, J. H., Fincham, F. D., Jouriles, E. N., & McDonald, R. (2000). Interparental conflict and child adjustment: Testing the mediational role of appraisals in the cognitive–contextual framework. Child Development, 71, 1648–1661.Google Scholar
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.CrossRefGoogle ScholarPubMed
Gunnar, M., & Vasquez, D. (2006). Stress neurobiology and developmental psychopathology. In Cicchetti, D. & Cohen, D. J. (Eds.) Developmental psychopathology: Vol. 2. Developmental neuroscience (2nd ed., pp. 533–577). Hoboken, NJ: Wiley.Google Scholar
Gunnar, M. R. (2001). The role of glucocorticoids in anxiety disorders: A critical analysis. In Vasey, M. W. & Dadds, M. R. (Eds.), Developmental psychopathology of anxiety (pp. 143–159). New York: Oxford University Press.Google 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.Google Scholar
Halberstadt, A. G. (1986). Family socialization of emotional expression and nonverbal communication styles and skills. Journal of Personality and Social Psychology, 51, 827–836.CrossRefGoogle Scholar
Halligan, S. L., Herbert, J., Goodyer, I. M., & Murray, L. (2007). Disturbances in morning cortisol secretion in association with maternal postnatal depression predict subsequent depressive symptomatology in adolescents. Biological Psychiatry, 62, 40–46.Google Scholar
Harkness, K. L., Stewart, J. G., & Wynne-Edwards, K. E. (2011). Cortisol reactivity to social stress in adolescents: Role of depression severity and child maltreatment. Psychoneuroendocrinology, 36, 173–181.Google Scholar
Hart, J., Gunnar, M., & Cicchetti, D. (1996). Altered neuroendocrine activity in maltreated children related to symptoms of depression. Development and Psychopathology, 8, 201–214.CrossRefGoogle Scholar
Hastings, P. D., Ruttle, P. L., Serbin, L. A., Mills, R. S. L., Stack, D. M., & Schwartzman, A. E. (2011). Adrenocortical responses to strangers in preschoolers: Relations with parenting, temperament, and psychopathology. Developmental Psychobiology. doi:10.1002/dev.20545Google Scholar
Hastings, P. D., Shirtcliff, E. A., Klimes-Dougan, B., Allison, A. L., DeRose, L., Usher, B., & Zahn-Waxler, C. (2011). Allostasis and the development of internalizing and externalizing problems: Changing relations with physiological systems across adolescence. Development and Psychopathology, 23, 1147–1163.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008). The link between childhood trauma and depression: Insights from HPA axis studies in humans. Psychoneuroendocrinology, 33, 693–710.CrossRefGoogle ScholarPubMed
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010). Neurobiological and psychiatric consequences of child abuse and neglect. Developmental Psychobiology, 52, 671–690.CrossRefGoogle ScholarPubMed
Hruschka, D. J., Kohrt, B. A., & Worthman, C. M. (2005). Estimating between- and within-individual variation in cortisol levels using multilevel models. Psychoneuroendocrinology, 30, 698–714.Google Scholar
Hwa-Froelich, D. A., Cook, C. A. L., & Flick, L. H. (2008). Maternal sensitivity and comunication styles: Mothers with depression. Journal of Early Intervention, 31, 44–66.CrossRefGoogle Scholar
Hyde, J. S., Klein, M. H., Essex, M. J., & Clark, R. (1995). Maternity leave and women's mental health. Psychology of Women Quarterly, 19, 257–285.CrossRefGoogle Scholar
Juster, R.-P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience and Biobehavioral Reviews, 35, 2–16.CrossRefGoogle ScholarPubMed
Kaufman, J. (1991). Depressive disorders in maltreated children. Journal of the American Academy of Child & Adolescent Psychiatry, 30, 257–265.Google Scholar
Kim, J., Cicchetti, D., Rogosch, F. A., & Manly, J. T. (2009). Child maltreatment and trajectories of personality and behavioral functioning: Implications for the development of personality disorder. Development and Psychopathology, 21, 889–912.Google 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
Kochanska, G., Philibert, R. A., & Barry, R. A. (2009). Interplay of genes and early mother–child relationship in the development of self-regulation from toddler to preschool age. Journal of Child Psychology and Psychiatry, 50, 1331–1338.Google Scholar
Koob, G. F., & Le Moal, M. (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology, 24, 97–129.Google Scholar
Koob, G. F., & Le Moal, M. (2008a). Addiction and the brain antireward system. Annual Review of Psychology, 59, 29–53.CrossRefGoogle ScholarPubMed
Koob, G. F., & Le Moal, M. (2008b). Review: Neurobiological mechanisms for opponent motivational processes in addiction. Philosophical Transactions of the Royal Society of London. Series B, Biologial Sciences, 363, 3113–3123.CrossRefGoogle ScholarPubMed
Koss, K. J., George, M. R. W., Bergman, K. N., Cummings, E. M., Davies, P. T., & Cicchetti, D. (2011). Understanding children's emotional processes and behavioral strategies in the context of marital conflict. Journal of Experimental Child Psychology, 109, 336–352.Google Scholar
Kraemer, H. C., Measelle, J. R., Ablow, J. C., Essex, M. J., Boyce, W. T., & Kupfer, D. J. (2003). A new approach to integrating data from multiple informants in psychiatric assessment and research: Mixing and matching contexts and perspectives. American Journal of Psychiatry, 160, 1566–1577.Google Scholar
Lindahl, K. M., & Malik, N. M. (2011). Marital conflict typology and children's appraisals: The moderating role of family cohesion. Journal of Family Psychology, 25, 194–201.Google Scholar
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, 976–980.Google Scholar
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
Lupien, S. J., Ouellet-Morin, I., Hupbach, A., Tu, M. T., Buss, C.,& Walker, D., et al. (2006). Beyond the stress concept: Allostatic load—A developmental biological and cognitive perspective. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology, Vol. 2: Developmental neuroscience (2nd ed., pp. 578–628). Hoboken, NJ: Wiley.Google Scholar
Marceau, K., Ram, N., Houts, R. M., Grimm, K. J., & Susman, E. J. (2011). Individual differences in boys' and girls' timing and tempo of puberty: Modeling development with nonlinear growth models. Developmental Psychology. doi:10.1037/a0023838CrossRefGoogle ScholarPubMed
Masharani, U., Shiboski, S., Eisner, M. D., Katz, P. P., Janson, S. L., Granger, D. A., & Blanc, P. D. (2005). Impact of exogenous glucocorticoid use on salivary cortisol measurements among adults with asthma and rhinitis. Psychoneuroendocrinology, 30, 744–752.CrossRefGoogle ScholarPubMed
McCrory, E., De Brito, S. A., & Viding, E. (2010). Research review: The neurobiology and genetics of maltreatment and adversity. Journal of Child Psychology and Psychiatry, 51, 1079–1095.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998). Protective and damaging effects of stress mediators. The New England Journal of Medicine, 338, 171–179.Google Scholar
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2–15.CrossRefGoogle ScholarPubMed
Meaney, M. J., & Szyf, M. (2005). Maternal care as a model for experience-dependent chromatin plasticity? Trends in Neurosciences, 28, 456–463.Google Scholar
Milan, S., Snow, S., & Belay, S. (2009). Depressive symptoms in mothers and children: Preschool attachment as a moderator of risk. Developmental Psychology, 45, 1019–1033.CrossRefGoogle ScholarPubMed
Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down? Chronic stress and the hypothalamic–pituitary–adrenocortical axis in humans. Psychological Bulletin, 133, 25–45.CrossRefGoogle ScholarPubMed
Mills-Koonce, W. R., Garrett-Peters, P., Barnett, M., Granger, D. A., Blair, C., & Cox, M. J. (2011). Father contributions to cortisol responses in infancy and toddlerhood. Developmental Psychology, 47, 388–395.Google Scholar
Murray, L., Fiori-Cowley, A., Hooper, R., & Cooper, P. (1996). The impact of postnatal depression and associated adversity on early mother–infant interactions and later infant outcome. Child Development, 67, 2512–2526.Google Scholar
Murray, L., Halligan, S. L., Goodyer, I. M., & Herbert, J. (2010). Disturbances in early parenting of depressed mothers and cortisol secretion in offspring: A preliminary study. Journal of Affective Disorders, 122, 218–223.Google Scholar
Pendry, P., & Adam, E. K. (2007). Associations between parents' marital functioning, maternal parenting quality, maternal emotion and child cortisol levels. International Journal of Behavioral Development, 31, 218–231.Google Scholar
Pollak, S. D., Messner, M., Kistler, D. J., & Cohn, J. F. (2009). Development of perceptual expertise in emotion recognition. Cognition, 110, 242–247.Google Scholar
Radloff, L. S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385–401.Google Scholar
Ramchandani, P., Stein, A., Evans, J., O'Connor, T. G., & The ALSPAC Study Team. (2005). Paternal depression in the postnatal period and child development: A prospective population study. Lancet, 365, 2201–2205.Google Scholar
Repetti, R. L., Taylor, S. E., & Seeman, T. E. (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128, 330–366.Google Scholar
Ruttle, P. L., Shirtcliff, E. A., Serbin, L. A., Ben-Dat Fisher, D., Stack, D. M., & Schwartzman, A. E. (2011). Disentangling psychobiological mechanisms underlying internalizing and externalizing behaviors in youth: Longitudinal and concurrent associations with cortisol. Hormones and Behavior, 59, 123–132.CrossRefGoogle ScholarPubMed
Sanchez, M. M. (2006). The impact of early adverse care on HPA axis development: Nonhuman primate models. Hormones and Behavior, 50, 623–631.Google Scholar
Schacht, P. M., Cummings, E. M., & Davies, P. T. (2009). Fathering in family context and child adjustment: A longitudinal analysis. Journal of Family Psychology, 23, 790–797.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
Schreiber, J. E., Shirtcliff, E. A., Van Hulle, C., Lemery-Chalfant, K., Klein, M. H., Kalin, N. H., et al. (2006). Environmental influences on family similarity in afternoon cortisol levels: Twin and parent–offspring designs. Psychoneuroendocrinology, 31, 1131–1137.Google Scholar
Shirtcliff, E. A., Allison, A. L., Armstrong, J. M., Slattery, M. J., Kalin, N. H., & Essex, M. J. (in press). Longitudinal stability and developmental properties of salivary cortisol levels and circadian rhythms from childhood to adolescence. Developmental Psychobiology.Google Scholar
Shirtcliff, E. A., & Essex, M. J. (2008). Concurrent and longitudinal associations of basal and diurnal cortisol with mental health symptoms in early adolescence. Developmental Psychobiology, 50, 690–703.Google Scholar
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. R. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17, 167–184.Google Scholar
Shirtcliff, E. A., Vitacco, M. J., Graf, A. R., Gostisha, A. J., Merz, J. L., & Zahn-Waxler, C. (2009). Neurobiology of empathy and callousness: Implications for the development of antisocial behavior. Behavioral Sciences and the Law, 27, 137–171.Google Scholar
Skinner, M. L., Shirtcliff, E. A., Haggerty, K. P., Coe, C. L., & Catalano, R. F. (2011). Allostasis model facilitates understanding race differences in the diurnal cortisol rhythm. Development and Psychopathology, 23, 1165–1184.CrossRefGoogle ScholarPubMed
Spielberger, C. D., Krasner, S. S., Solomon, E. P., & Janisse, M. P. (1988). The experience, expression, and control of anger. New York: Springer–Verlag.Google Scholar
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639.CrossRefGoogle ScholarPubMed
Toth, S. L., Rogosch, F. A., Sturge-Apple, M., & Cicchetti, D. (2009). Maternal depression, children's attachment security, and representational development: An organizational perspective. Child Development, 80, 192–208.Google Scholar
Trampolini, T., Ungerer, J. A., & McMahon, C. A. (2008). Maternal depression: Relations with maternal caregiving representations and emotional availability during the preschool years. Attachment and Human Development, 10, 73–90.CrossRefGoogle Scholar
Trickett, P. K., Negriff, S., Ji, J., & Peckins, M. (2011). Child maltreatment and adolescent development. Journal of Research on Adolescence, 21, 3–20.Google Scholar
Uvnäs-Moberg, K., Arn, I., & Magnusson, D. (2005). The psychobiology of emotion: The role of the oxytocinergic system. International Journal of Behavioral Medicine, 12, 59–65.Google Scholar
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.Google Scholar
Weems, C. F., & Carrion, V. G. (2007). The association between PTSD symptoms and salivary cortisol in youth: The role of time since the trauma. Journal of Traumatic Stress, 20, 903–907.Google Scholar
Weems, C. F., & Carrion, V. G. (2009). Brief report: Diurnal salivary cortisol in youth—Clarifying the nature of posttraumatic stress dysregulation. Journal of Pediatric Psychology, 34, 389–395.Google Scholar
Wilson, S., & Durbin, C. E. (2010). Effects of paternal depression on fathers' parenting behaviors: A meta-analytic review. Clinical Psychology Review, 30, 167–180.Google Scholar
Winkler, D., Pjrek, E., & Kasper, S. (2005). Anger attacks in depression: Evidence for a male depressive syndrome. Psychotherapy and Psychosomatics, 74, 303–307.Google Scholar
Wismer Fries, A. B., Shirtcliff, E. A., & Pollak, S. D. (2008). Neuroendocrine dysregulation following early social deprivation in children. Developmental Psychobiology, 50, 588–599.Google Scholar