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Adolescent internalizing symptoms and negative life events: The sensitizing effects of earlier life stress and cortisol

  • Paula L. Ruttle (a1), Jeffrey M. Armstrong (a1), Marjorie H. Klein (a1) and Marilyn J. Essex (a1)

Abstract

Although adolescence is marked by increased negative life events and internalizing problems, few studies investigate this association as an ongoing longitudinal process. Moreover, while there are considerable individual differences in the degree to which these phenomena are linked, little is known about the origins of these differences. The present study examines early life stress (ELS) exposure and early-adolescent longitudinal afternoon cortisol level as predictors of the covariation between internalizing symptoms and negative life events across high school. ELS was assessed by maternal report during infancy, and the measure of cortisol was derived from assessments at ages 11, 13, and 15 years. Life events and internalizing symptoms were assessed at ages 15, 17, and 18 years. A two-level hierarchical linear model revealed that ELS and cortisol were independent predictors of the covariation of internalizing symptoms and negative life events. Compared to those with lower levels of ELS, ELS-exposed adolescents displayed tighter covariation between internalizing symptoms and negative life events. Adolescents with lower longitudinal afternoon cortisol displayed tighter covariation between negative life events and internalizing symptoms, while those with higher cortisol demonstrated weaker covariation, partially due to increased levels of internalizing symptoms when faced with fewer negative life events.

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Corresponding author

Address correspondence and reprints requests to: Paula L. Ruttle, Department of Psychiatry, School of Medicine and Public Health, University of Wisconsin–Madison, 6001 Research Park Boulevard, Madison, WI 53719-1176; E-mail: ruttle@wisc.edu.

References

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Abidin, R. R. (1986). Parenting stress index (2nd ed.). Charlottesville, VA: Pediatric Psychology Press.
Arnett, J. J. (1999). Adolescent storm and stress, reconsidered. American Psychologist, 54, 317326.
Badanes, L. S., Watamura, S. E., & Hankin, B. L. (2011). Hypocortisolism as a potential marker of allostatic load in children: Associations with family risk and internalizing disorders. Development and Psychopathology, 23, 881896.
Bakshi, V. P., & Kalin, N. H. (2000). Corticotropin-releasing hormone and animal models of anxiety: Gene–environment interactions. Biological Psychiatry, 48, 11751198.
Barnett, R. C., & Marshall, N. L. (1989). Preliminary manual for the Role-Quality Scales. Unpublished manuscript, Wellesley College, Center for Research on Women.
Bartels, M., de Geus, E. J. C., Kirschbaum, C., Sluyter, F., & Boomsma, D. I. (2003). Heritability of daytime cortisol levels in children. Behavior Genetics, 33, 421433.
Block, J. H. (1965). The Child-Rearing Practices Report (CRPR): A set of Q items for the description of parental socialization attitudes and values. Berkeley, CA: Institute of Human Development.
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, 271301.
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, 580587.
Brand, S., Holsboer-Trachsler, E., Naranjo, J. R., & Schmidt, S. (2012). Influence of mindfulness practice on cortisol and sleep in long-term and short-term meditators. Neuropsychobiology, 65, 109118.
Brett, J. F., Brief, A. P., Burke, M. J., George, J. M., & Webster, J. (1990). Negative affectivity and the reporting of stressful life events. Health Psychology, 9, 5768.
Brown, G. W., Harris, T. O., & Hepworth, C. (1995). Loss, humiliation and entrapment among women developing depression: A patient and non-patient comparison. Psychological Medicine, 25, 721.
Brown, T. A., & Rosellini, A. J. (2011). The direct and interactive effects of neuroticism and life stress on the severity and longitudinal course of depressive symptoms. Journal of Abnormal Psychology, 120, 844856.
Bryk, A. S., & Raudenbush, S. W. (1992). Hierarchical linear models: Applications and data analysis methods, advanced qualitative techniques in the social sciences. Thousand Oaks, CA: Sage.
Burghy, C. A., Stodola, D. E., Ruttle, P. L., Molloy, E. K., Armstrong, J. M., Oler, J. A., et al. (2012). Developmental pathways to amygdala–prefrontal function and internalizing symptoms in adolescence. Nature Neuroscience, 15, 17361741.
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783804.
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, 252269.
Cisler, J. M., James, G. A., Tripathi, S., Mletzko, T., Heim, C., Hu, X. P., et al. (2013). Differential functional connectivity within an emotion regulation neural network among individuals resilient and susceptible to the depressogenic effects of early life stress. Psychological Medicine, 43, 507518.
Cole, D. A., Nolen-Hoeksema, S., Girgus, J., & Paul, G. (2006). Stress exposure and stress generation in child and adolescent depression: A latent trait–state–error approach to longitudinal analyses. Journal of Abnormal Psychology, 115, 4051.
Compas, B. E. (1987). Coping with stress during childhood and adolescence. Psychological Bulletin, 101, 393403.
Compas, B. E., Grant, K. E., & Ey, S. (1994). Psychosocial stress and child and adolescent depression: Can we be more specific? In Reynolds, W. M. & Johnston, H. F. (Eds.), Handbook of depression in children and adolescents (pp. 509523). New York: Plenum Press.
Costello, E. J., Mustillo, S., Erkanli, A., Keeler, G., & Angold, A. (2003). Prevalence and development of psychiatric disorders in childhood and adolescence. Archives of General Psychiatry, 60, 837844.
Deardorff, J., Gonzales, N. A., & Sandler, I. N. (2003). Control beliefs as a mediator of the relation between stress and depressive symptoms among inner-city adolescents. Journal of Abnormal Child Psychology, 31, 205217.
De Bellis, M. D., Dahl, R. E., Perel, J. M., Birmaher, B., Al-Shabbout, M., Williamson, D. E., et al. (1996). Nocturnal ACTH, cortisol, growth hormone, and prolactin secretion in prepubertal depression. Journal of the American Academy of Child & Adolescent Psychiatry, 35, 11301138.
Eiland, L., & McEwen, B. S. (2012). Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus, 22, 8291.
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, 303328.
Espejo, E. P., Hammen, C., & Brennan, P. A. (2012). Elevated appraisals of the negative impact of naturally occurring life events: A risk factor for depressive and anxiety disorders. Journal of Abnormal Child Psychology, 40, 303–15.
Espejo, E. P., Hammen, C. L., Connolly, N. P., Brennan, P. A., Najman, J. M., & Bor, W. (2006). Stress sensitization and adolescent depressive severity as a function of childhood adversity: A link to anxiety disorders. Journal of Abnormal Child Psychology, 35, 287299.
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, 588603.
Essex, M. J., Boyce, W. T., Hertzman, C., Lam, L. L., Armstrong, J. M., Neumann, S. M. A., et al. (2013). Epigenetic vestiges of early developmental adversity: Childhood stress exposure and DNA methylation in adolescence. Child Development, 84, 5875.
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, 776784.
Essex, M. J., Klein, M. H., Slattery, M. J., Goldsmith, H. H., & Kalin, N. H. (2010). Early risk factors and developmental pathways to chronic high inhibition and social anxiety disorder in adolescence. American Journal of Psychiatry, 167, 4046.
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, 12461256.
Essex, M. J., Shirtcliff, E. A., Burk, L. R., Ruttle, P. L., Klein, M. H., Slattery, M. J., et al. (2011). 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. Development and Psychopathology, 23, 1039–58.
Farmer, A. E., & McGuffin, P. (2003). Humiliation, loss and other types of life events and difficulties: A comparison of depressed subjects, healthy controls and their siblings. Psychological Medicine, 33, 11691175.
Fishbein, D., Warner, T., Krebs, C., Trevarthen, N., Flannery, B., & Hammond, J. (2009). Differential relationships between personal and community stressors and children's neurocognitive functioning. Child Maltreatment, 14, 299315.
Ge, X., Lorenz, F. O., Conger, R. D., Elder, G. H., & Simons, R. L. (1994). Trajectories of stressful life events and depressive symptoms during adolescence. Developmental Psychology, 30, 467483.
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. British Journal of Psychiatry, 177, 499504.
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, 351357.
Granger, D. A., Serbin, L. A., Schwartzman, A., Lehoux, P., Cooperman, J., & Ikeda, S. (1998). Children's salivary cortisol, internalising behaviour problems, and family environment: Results from the Condcordia Longitudinal Risk Project. International Journal of Behavioral Development, 22, 707728.
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. 143159). New York: Oxford University Press.
Halberstadt, A. G. (1986). Family socialization of emotional expression and nonverbal communication styles and skills. Journal of Personality and Social Psychology, 51, 827836.
Hale, W. W. III, Raaijmakers, Q., Muris, P., van Hoof, A., & Meeus, W. (2008). Developmental trajectories of adolescent anxiety disorder symptoms: A 5-year prospective community study. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 556564.
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, 4046.
Halligan, S. L., Murray, L., Martins, C., & Cooper, P. J. (2007). Maternal depression and psychiatric outcomes in adolescent offspring: A 13-year longitudinal study. Journal of Affective Disorders, 97, 145154.
Hammen, C., Henry, R., & Daley, S. E. (2000). Depression and sensitization to stressors among young women as a function of childhood adversity. Journal of Consulting and Clinical Psychology, 68, 782787.
Hankin, B. L. (2009). Development of sex differences in depressive and co-occurring anxious symptoms during adolescence: Descriptive trajectories and potential explanations in a multiwave prospective study. Journal of Clinical Child and Adolescent Psychology, 38, 460472.
Hankin, B. L., & Abramson, L. Y. (1999). Development of gender differences in depression: Description and possible explanations. Annals of Medicine, 31, 372379.
Hankin, B. L., & Abramson, L. Y. (2001). Development of gender differences in depression: An elaborated cognitive vulnerability-transactional stress theory. Psychological Bulletin, 127, 773796.
Hankin, B. L., Abramson, L. Y., Moffitt, T. E., Silva, P. A., McGee, R., & Angell, K. E. (1998). Development of depression from preadolescence to young adulthood: Emerging gender differences in a 10-year longitudinal study. Journal of Abnormal Psychology, 107, 128140.
Harkness, K. L., Bruce, A. E., & Lumley, M. N. (2006). The role of childhood abuse and neglect in the sensitization to stressful life events in adolescent depression. Journal of Abnormal Psychology, 115, 730741.
Honaker, J., King, G., & Blackwell, M. (2009). Amelia II: A program for missing data (Version 1.2-16) [Computer program]. Retrieved from http://gking.harvard.edu/amelia
Hruschka, D. J., Kohrt, B. A., & Worthman, C. M. (2005). Estimating between- and within-individual variation in cortisol levels using multilevel models. Psychoneuroendocrinology, 30, 698714.
Hyde, J. S., Klein, M. H., Essex, M. J., & Clark, R. (1995). Maternity leave and women's mental health. Psychology of Women Quarterly, 19, 257285.
Jacobs, T. L., Shaver, P. R., Epel, E. S., Zanesco, A. P., Aichele, S. R., Bridwell, D. A., et al. (2013). Self-reported mindfulness and cortisol during a Shamatha meditation retreat. Health Psychology, 32, 11041109.
Kendler, K. S., Gardner, C. O., & Lichtenstein, P. (2008). A developmental twin study of symptoms of anxiety and depression: Evidence for genetic innovation and attenuation. Psychological Medicine, 38, 15671575.
Kendler, K. S., Hettema, J. M., Butera, F., Gardner, C. O., & Prescott, C. A. (2003). Life event dimensions of loss, humiliation, entrapment, and danger in the prediction of onsets of major depression and generalized anxiety. Archives of General Psychiatry, 60, 789796.
Kendler, K. S., Kuhn, J. W., & Prescott, C. A. (2004). Childhood sexual abuse, stressful life events and risk for major depression in women. Psychological Medicine, 34, 14751482.
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, 889912.
Kovacs, M., & Devlin, B. (1998). Internalizing disorders in childhood. Journal of Child Psychology and Psychiatry, 39, 4763.
Kupper, N., de Geus, E. J. C., van den Berg, M., Kirschbaum, C., Boomsma, D. I., & Willemsen, G. (2005). Familial influences on basal salivary cortisol in an adult population. Psychoneuroendocrinology, 30, 857868.
Leve, L. D., Kim, H. K., & Pears, K. C. (2005). Childhood temperament and family environment as predictors of internalizing and externalizing trajectories from ages 5 to 17. Journal of Abnormal Child Psychology, 33, 505520.
Li, I., Chiou, H.-H., & Shen, P.-S. (2007). Correlations between cortisol level and internalizing disposition of young children are increased by selecting optimal sampling times and aggregating data. Developmental Psychobiology, 49, 633639.
Low, N. C. P., Dugas, E., O'Loughlin, E., Rodriguez, D., Contreras, G., Chaiton, M., et al. (2012). Common stressful life events and difficulties are associated with mental health symptoms and substance use in young adolescents. BMC Psychiatry, 12. doi:10.1186/1471-244X-12-116
Masharani, U., Shiboski, S., Eisner, M. D., Katz, P. P., Janson, S. L., Granger, D. A., et al. (2005). Impact of exogenous glucocorticoid use on salivary cortisol measurements among adults with asthma and rhinitis. Psychoneuroendocrinology, 30, 744752.
McLaughlin, K. A., Conron, K. J., Koenen, K. C., & Gilman, S. E. (2010). Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults. Psychological Medicine, 40, 16471658.
O'Connor, T. G., McGuire, S., Reiss, D., Hetherington, E. M., & Plomin, R. (1998). Co-occurrence of depressive symptoms and antisocial behavior in adolescence: A common genetic liability. Journal of Abnormal Psychology, 107, 2737.
Petersen, A. C., Compas, B. E., Brooks Gunn, J., Stemmler, M., Ey, S., & Grant, K. E. (1993). Depression in adolescence. American Psychologist, 48, 155168.
Radloff, L. S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385401.
Rudolph, K. D., & Flynn, M. (2007). Childhood adversity and youth depression: Influence of gender and pubertal status. Development and Psychopathology, 19, 497521.
Rudolph, K. D., Troop-Gordon, W., & Granger, D. A. (2011). Individual differences in biological stress responses moderate the contribution of early peer victimization to subsequent depressive symptoms. Psychopharmacology, 214, 209219.
Rutter, M. (2007). Psychopathological development across adolescence. Journal of Youth and Adolescence, 36, 101110.
Ruttle, P. L., Shirtcliff, E. A., Armstrong, J. M., Klein, M. H., & Essex, M. J. (2013). Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress. Developmental Psychobiology. Advance online publication. doi:10.1002/dev.21138
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, 123132.
Sanchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology, 13, 419449.
Sarason, I. G., Johnson, J. H., & Siegel, J. M. (1978). Assessing the impact of life changes: Development of the Life Experiences Survey. Journal of Consulting and Clinical Psychology, 46, 932946.
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, 11311137.
Shirtcliff, E. A., Allison, A. L., Armstrong, J. M., Slattery, M. J., Kalin, N. H., & Essex, M. J. (2012). Longitudinal stability and developmental properties of salivary cortisol levels and circadian rhythms from childhood to adolescence. Developmental Psychobiology, 54, 493502.
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, 690703.
Sliwinski, M. J., Smyth, J. M., Hofer, S. M., & Stawski, R. S. (2006). Intraindividual coupling of daily stress and cognition. Psychology and Aging, 21, 545557.
Smider, N. A., Essex, M. J., Kalin, N. H., Buss, K. A., Klein, M. H., Davidson, R. J., et al. (2002). Salivary cortisol as a predictor of socioemotional adjustment during kindergarten: A prospective study. Child Development, 73, 7592.
Spielberger, C. D., Krasner, S. S., Solomon, E. P., & Janisse, M. P. (1988). The experience, expression, and control of anger. New York: Springer Verlag.
Spratt, E. G., Friedenberg, S., LaRosa, A., Bellis, M. D. D., Macias, M. M., Summer, A. P., et al. (2012). The effects of early neglect on cognitive, language, and behavioral functioning in childhood. Psychology, 3, 175182.
Steinberg, L., & Morris, A. S. (2001). Adolescent development. Annual Review of Psychology, 52, 83110.
Trickett, P. K., Negriff, S., Ji, J., & Peckins, M. (2011). Child maltreatment and adolescent development. Journal of Research on Adolescence, 21, 320.
Van den Bergh, B. R. H., & Van Calster, B. (2009). Diurnal cortisol profiles and evening cortisol in post-pubertal adolescents scoring high on the Children's Depression Inventory. Psychoneuroendocrinology, 34, 791794.
Van Oort, F. V. A., Greaves-Lord, K., Verhulst, F. C., Ormel, J., & Huizink, A. C. (2009). The developmental course of anxiety symptoms during adolescence: The TRAILS study. Journal of Child Psychology and Psychiatry, 50, 12091217.
Wagner, B. M., & Compas, B. E. (1990). Gender, instrumentality, and expressivity: Moderators of the relation between stress and psychological symptoms during adolescence. American Journal of Community Psychology, 18, 383406.
Wichers, M., Maes, H. H., Jacobs, N., Derom, C., Thiery, E., & Kendler, K. S. (2012). Disentangling the causal inter-relationship between negative life events and depressive symptoms in women: A longitudinal twin study. Psychological Medicine, 42, 18011814.
Wust, S., Federenko, I., Hellhammer, D. H., & Kirschbaum, C. (2000). Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrinology, 25, 707720.
Young, E. A., Aggen, S. H., Prescott, C. A., & Kendler, K. S. (2000). Similarity in saliva cortisol measures in monozygotic twins and the influence of past major depression. Biological Psychiatry, 48, 7074.

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Adolescent internalizing symptoms and negative life events: The sensitizing effects of earlier life stress and cortisol

  • Paula L. Ruttle (a1), Jeffrey M. Armstrong (a1), Marjorie H. Klein (a1) and Marilyn J. Essex (a1)

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