Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-18T06:09:03.367Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  25 November 2014

Paula L. Ruttle*
Affiliation:
University of Wisconsin–Madison
Jeffrey M. Armstrong
Affiliation:
University of Wisconsin–Madison
Marjorie H. Klein
Affiliation:
University of Wisconsin–Madison
Marilyn J. Essex
Affiliation:
University of Wisconsin–Madison
*
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.

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.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2014 

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

Abidin, R. R. (1986). Parenting stress index (2nd ed.). Charlottesville, VA: Pediatric Psychology Press.Google Scholar
Arnett, J. J. (1999). Adolescent storm and stress, reconsidered. American Psychologist, 54, 317326.Google Scholar
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.Google Scholar
Bakshi, V. P., & Kalin, N. H. (2000). Corticotropin-releasing hormone and animal models of anxiety: Gene–environment interactions. Biological Psychiatry, 48, 11751198.Google Scholar
Barnett, R. C., & Marshall, N. L. (1989). Preliminary manual for the Role-Quality Scales. Unpublished manuscript, Wellesley College, Center for Research on Women.Google Scholar
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.Google Scholar
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.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, 271301.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, 580587.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783804.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
Compas, B. E. (1987). Coping with stress during childhood and adolescence. Psychological Bulletin, 101, 393403.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.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, 303328.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.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, 776784.Google Scholar
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.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, 12461256.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google 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, 351357.Google Scholar
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.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. 143159). New York: Oxford University Press.Google Scholar
Halberstadt, A. G. (1986). Family socialization of emotional expression and nonverbal communication styles and skills. Journal of Personality and Social Psychology, 51, 827836.CrossRefGoogle Scholar
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.Google 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, 4046.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Hankin, B. L., & Abramson, L. Y. (1999). Development of gender differences in depression: Description and possible explanations. Annals of Medicine, 31, 372379.CrossRefGoogle ScholarPubMed
Hankin, B. L., & Abramson, L. Y. (2001). Development of gender differences in depression: An elaborated cognitive vulnerability-transactional stress theory. Psychological Bulletin, 127, 773796.Google Scholar
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.Google Scholar
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.Google Scholar
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 Google Scholar
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.Google 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, 257285.CrossRefGoogle Scholar
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. Google Scholar
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.Google Scholar
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.Google Scholar
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.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, 889912.Google Scholar
Kovacs, M., & Devlin, B. (1998). Internalizing disorders in childhood. Journal of Child Psychology and Psychiatry, 39, 4763.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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 Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Petersen, A. C., Compas, B. E., Brooks Gunn, J., Stemmler, M., Ey, S., & Grant, K. E. (1993). Depression in adolescence. American Psychologist, 48, 155168.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, 385401.Google Scholar
Rudolph, K. D., & Flynn, M. (2007). Childhood adversity and youth depression: Influence of gender and pubertal status. Development and Psychopathology, 19, 497521.Google Scholar
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.Google Scholar
Rutter, M. (2007). Psychopathological development across adolescence. Journal of Youth and Adolescence, 36, 101110.Google Scholar
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 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, 123132.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.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, 11311137.Google Scholar
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.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, 690703.Google Scholar
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.Google Scholar
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.Google Scholar
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
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.Google Scholar
Steinberg, L., & Morris, A. S. (2001). Adolescent development. Annual Review of Psychology, 52, 83110.CrossRefGoogle ScholarPubMed
Trickett, P. K., Negriff, S., Ji, J., & Peckins, M. (2011). Child maltreatment and adolescent development. Journal of Research on Adolescence, 21, 320.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar