Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-18T01:16:19.421Z Has data issue: false hasContentIssue false

Homotypic and heterotypic continuity of internalizing and externalizing symptoms from ages 3 to 12: The moderating role of diurnal cortisol

Published online by Cambridge University Press:  25 September 2018

Allison Frost*
Affiliation:
Stony Brook University
Ellen Kessel
Affiliation:
Stony Brook University
Sarah Black
Affiliation:
The Ohio State University Wexner Medical Center
Brandon Goldstein
Affiliation:
Stony Brook University
Kristin Bernard
Affiliation:
Stony Brook University
Daniel N. Klein
Affiliation:
Stony Brook University
*
Address correspondence and reprint requests to Allison Frost, Department of Psychology, Stony Brook University, Stony Brook, NY 11794.

Abstract

Psychological symptoms that arise in early childhood can follow a multitude of patterns into adolescence, including homotypic continuity (i.e., similar symptoms over time) and heterotypic continuity (i.e., a shift in symptoms over time). However, we know very little about the factors that distinguish homotypic vs. heterotypic continuity of early internalizing and externalizing symptoms over development. In a separate line of research, diurnal cortisol has been shown to predict later internalizing and externalizing problems. In the current study, we tested whether diurnal cortisol patterns moderated the course of internalizing and externalizing symptoms from preschool to early adolescence. 554 children (54% male) and parents participated in a longitudinal study. Parents reported on their children’s internalizing and externalizing symptoms at ages 3 and 12, and children collected diurnal saliva samples at age 9. Results showed that a steeper cortisol decline at age 9 combined with high internalizing or externalizing problems at age 3 predicted higher internalizing problems at age 12. A more blunted cortisol decline combined with early internalizing or externalizing problems predicted higher externalizing problems in early adolescence. These results illustrate the moderating role of stress system functioning in homotypic and heterotypic patterns of psychopathology from preschool to early adolescence.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2018 

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.)

Footnotes

This work was supported by National Institute of Mental Health grant R01 MH069942 (to D.N.K.) and National Science Foundation Graduate Research Fellowship 1315232 (to A.F.).

References

Achenbach, T., & Rescorla, L. (2000). Child behavior checklist. ASEBA. Burlington, VT: University of Vermont.Google Scholar
Alink, L. R. A., Cicchetti, D., Kim, J., & Rogosch, F. A. (2012). Longitudinal associations among child maltreatment, social functioning, and cortisol regulation. Developmental Psychology, 48, 224236. http://doi.org/10.1037/a0024892Google Scholar
Alink, L. R. A., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Mesman, J., Juffer, F., & Koot, H. M. (2008). Cortisol and externalizing behavior in children and adolescents: Mixed meta-analytic evidence for the inverse relation of basal cortisol and cortisol reactivity with externalizing behavior. Developmental Psychobiology, 50, 427450. http://doi.org/10.1002/dev.20300Google 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. http://doi.org/10.1017/S095457941100037XGoogle Scholar
Bailey, S. L., & Heitkemper, M. M. (1991). Morningness-eveningness and early-morning salivary cortisol levels. Biological Psychology, 32, 181192. http://doi.org/10.1016/0301-0511(91)90009-6Google Scholar
Bauer, A., Quas, J., & Boyce, W. (2002). Associations between physiological reactivity and children's behavior: Advantages of a multisystem approach. Journal of Developmental & Behavioral Pediatrics, 23, 102113.Google Scholar
Beauchaine, T. P., & McNulty, T. (2013). Comorbidities and continuities as ontogenic processes: Toward a developmental spectrum model of externalizing psychopathology. Development and Psychopathology, 25, 15051528. http://doi.org/10.1017/S0954579413000746Google Scholar
Bernard, K., Butzin-Dozier, Z., Rittenhouse, J., & Dozier, M. (2010). Cortisol production patterns in young children living with birth parents vs children placed in foster care following involvement of child protective services. Archives of Pediatrics & Adolescent Medicine, 164. http://doi.org/10.1001/archpediatrics.2010.54Google Scholar
Bernard, K., Peloso, E., Laurenceau, J. P., Zhang, Z., & Dozier, M. (2015). Examining change in cortisol patterns during the 10-week transition to a new child-care setting. Child development, 86(2), 456471.Google Scholar
Bernard, K., Zwerling, J., & Dozier, M. (2015). Effects of early adversity on young children's diurnal cortisol rhythms and externalizing behavior. Developmental Psychobiology, 57, 935947.Google Scholar
Blair, C. (2010). Stress and the development of self-regulation in context. Child Development Perspectives, 4, 181188. http://doi.org/10.1111/j.1750-8606.2010.00145.xGoogle Scholar
Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. (2009). Morning cortisol levels in preschool-aged foster children: Differential effects of maltreatment type. Developmental Psychobiology, 51, 1423. http://doi.org/10.1002/dev.20333Google Scholar
Burt, K. B., & Obradovi, J. (2012). The construct of psychophysiological reactivity: Statistical and psychometric issues. Development Review. 33, 2957. http://doi.org/10.1016/j.dr.2012.10.002Google Scholar
Cham, H., Reshetnyak, E., Rosenfeld, B., & Breitbart, W. (2017). Full information maximum likelihood estimation for latent variable interactions with incomplete indicators. Multivariate Behavioral Research, 52, 1230.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2001). Diverse patterns of neuroendocrine activity in maltreated children. Development and Psychopathology, 13, 677693. http://doi.org/nullGoogle Scholar
Copeland, W. E., Adair, C. E., Smetanin, P., Stiff, D., Briante, C., Colman, I., … Angold, A. (2013). Diagnostic transitions from childhood to adolescence to early adulthood. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 54, 791799. http://doi.org/10.1111/jcpp.12062Google Scholar
DeSantis, A. S., Adam, E. K., Doane, L. D., Mineka, S., Zinbarg, R. E., & Craske, M. G. (2007). Racial/ethnic differences in cortisol diurnal rhythms in a community sample of adolescents. Journal of Adolescent Health, 41, 313. http://doi.org/10.1016/j.jadohealth.2007.03.006Google Scholar
Doane, L., Mineka, S., Zinbarg, R., & Craske, M. (2013). Are flatter diurnal cortisol rhythms associated with major depression and anxiety disorders in late adolescence? The role of life stress and daily negative emotion. Development and Psychopathology, 25, 629632.Google Scholar
Dozier, M., Manni, M., Gordon, M. K., Peloso, E., Gunnar, M. R., Stovall-McClough, K. C., … Levine, S. (2006). Foster children's diurnal production of cortisol: An exploratory study. Child Maltreatment, 11, 189197. http://doi.org/10.1177/1077559505285779Google Scholar
Ellenbogen, M., Hodgins, S., Linnen, A.-M., & Ostiguy, C. (2011). Elevated daytime cortisol levels: A biomarker of subsequent major affective disorder? Journal of Affective Disorders, 132, 265269. http://doi.org/10.1016/J.JAD.2011.01.007Google Scholar
El-Sheikh, M., Erath, S. A., Buckhalt, J. A., Granger, D. A., & Mize, J. (2008). Cortisol and children's adjustment: The moderating role of sympathetic nervous system activity. Journal of Abnormal Child Psychology, 36, 601611. http://doi.org/10.1007/s10802-007-9204-6Google Scholar
Enders, C. K., & Bandalos, D. L. (2001). The relative performance of full information maximum likelihood estimation for missing data in structural equation models. Structural Equation Modeling, 8, 430457.Google Scholar
Evans, G. W., & Kim, P. (2013). Childhood poverty, chronic stress, self-regulation, and coping. Child Development Perspectives, 7, 4348. http://doi.org/10.1111/cdep.12013Google Scholar
Fairchild, G., Goozen, S. van, Stollery, S., & Brown, J. (2008). Cortisol diurnal rhythm and stress reactivity in male adolescents with early-onset or adolescence-onset conduct disorder. Biological Psychiatry, 64, 599606.Google Scholar
Fisher, P. A., Gunnar, M. R., Dozier, M., Bruce, J., & Pears, K. C. (2006). Effects of therapeutic interventions for foster children on behavioral problems, caregiver attachment, and stress regulatory neural systems. Annals of the New York Academy of Sciences, 1094, 215225. http://doi.org/10.1196/annals.1376.023Google Scholar
Goldstein, B. L., Perlman, G., Kotov, R., Broderick, J. E., Liu, K., Ruggero, C., & Klein, D. N. (2017). Etiologic specificity of waking cortisol: Links with maternal history of depression and anxiety in adolescent girls. Journal of Affective Disorders, 208, 103109. http://doi.org/10.1016/j.jad.2016.08.079Google 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. The British Journal of Psychiatry, 177(6), 499504.Google Scholar
Gunnar, M., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199220. http://doi.org/10.1016/S0306-4530(01)00045-2Google Scholar
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 13, 515538.Google Scholar
Halligan, S. L., Herbert, J., Goodyer, I., & Murray, L. (2007). Disturbances in morning cortisol secretion in association with maternal postnatal depression predict subsequent depressive symptomatology in adolescents. Biological Psychiatry, 62, 4046. http://doi.org/10.1016/J.BIOPSYCH.2006.09.011Google Scholar
Harris, T. O., Borsanyi, S., Messari, S., Stanford, K., Brown, G. W., Cleary, S. E., … Herbert, J. (2000). Morning cortisol as a risk factor for subsequent major depressive disorder in adult women. The British Journal of Psychiatry, 177, 505510.Google Scholar
Hastings, P. D., Shirtcliff, E. A., Klimes-Dougan, B., Allison, A. L., Derose, L., Kendziora, K. T., … Zahn-Waxler, C. (2011). Allostasis and the development of internalizing and externalizing problems: Changing relations with physiological systems across adolescence. Development and Psychopathology, 23, 11491165. http://doi.org/10.1017/S0954579411000538Google Scholar
Hawes, D. J., Brennan, J., & Dadds, M. R. (2009). Cortisol, callous-unemotional traits, and pathways to antisocial behavior. Current Opinion in Psychiatry, 22, 357362. http://doi.org/10.1097/YCO.0b013e32832bfa6dGoogle Scholar
Kertes, D. A., Gunnar, M. R., Madsen, N. J., & Long, J. D. (2008). Early deprivation and home basal cortisol levels: A study of internationally adopted children. Development and psychopathology, 20, 473-491.Google Scholar
Kim-Cohen, J., Caspi, A., Moffitt, T. E., Harrington, H., Milne, B. J., Poulton, R., … J, P. (2003). Prior juvenile diagnoses in adults with mental disorder. Archives of General Psychiatry, 60, 709. http://doi.org/10.1001/archpsyc.60.7.709Google Scholar
King, D. W., King, L. A., McArdle, J. J., Grimm, K., Jones, R. T., & Ollendick, T. H. (2006). Characterizing time in longitudinal trauma research. Journal of Traumatic Stress, 19, 205215. http://doi.org/10.1002/jts.20112Google Scholar
Kohrt, B. A., Hruschka, D. J., Kohrt, H. E., Carrion, V. G., Waldman, I. D., & Worthman, C. M. (2015). Child abuse, disruptive behavior disorders, depression, and salivary cortisol levels among institutionalized and community-residing boys in Mongolia. Asia-Pacific Psychiatry, 7, 719. http://doi.org/10.1111/appy.12141Google Scholar
Koss, K. J., & Gunnar, M. R. (2017). Annual research review: Early adversity, the hypothalamic-pituitary-adrenocortical axis, and child psychopathology. Journal of Child Psychology and Psychiatry, 59, 327346. http://doi.org/10.1111/jcpp.12784Google Scholar
Koss, K. J., Hostinar, C. E., Donzella, B., & Gunnar, M. R. (2014). Social deprivation and the HPA axis in early development. Psychoneuroendocrinology, 50, 113. http://doi.org/10.1016/j.psyneuen.2014.07.028Google Scholar
Koss, K. J., Mliner, S. B., Donzella, B., & Gunnar, M. R. (2016). Early adversity, hypocortisolism, and behavior problems at school entry: A study of internationally adopted children. Psychoneuroendocrinology, 66, 3138. http://doi.org/10.1016/j.psyneuen.2015.12.018Google Scholar
Kuhlman, K. R., Geiss, E. G., Vargas, I., & Lopez-Duran, N. L. (2015). Differential associations between childhood trauma subtypes and adolescent HPA-axis functioning. Psychoneuroendocrinology, 54, 103114. http://doi.org/10.1016/j.psyneuen.2015.01.020Google Scholar
Lahey, B. B., Krueger, R. F., Rathouz, P. J., Waldman, I. D., & Zald, D. H. (2017). A hierarchical causal taxonomy of psychopathology across the life span. Psychological Bulletin, 143, 142186. http://doi.org/10.1037/bul0000069Google Scholar
LeMoult, J., Ordaz, S. J., Kircanski, K., Singh, M. K., & Gotlib, I. H. (2015). Predicting first onset of depression in young girls: Interaction of diurnal cortisol and negative life events. Journal of Abnormal Psychology, 124, 850859. http://doi.org/10.1037/abn0000087Google Scholar
Liu, K., Ruggero, C. J., Goldstein, B., Klein, D. N., Perlman, G., Broderick, J., & Kotov, R. (2016). Elevated cortisol in healthy female adolescent offspring of mothers with posttraumatic stress disorder. Journal of Anxiety Disorders, 40, 3743. http://doi.org/10.1016/j.janxdis.2016.04.003Google Scholar
Lok, A., Mocking, R. J. T., Ruhé, H. G., Visser, I., Koeter, M. W. J., Assies, J., … Schene, A. H. (2012). Longitudinal hypothalamic–pituitary–adrenal axis trait and state effects in recurrent depression. Psychoneuroendocrinology, 37, 892902. http://doi.org/10.1016/j.psyneuen.2011.10.005Google Scholar
Lopez-Duran, N. L., Kovacs, M., & George, C. J. (2009). Hypothalamic-pituitary-adrenal axis dysregulation in depressed children and adolescents: a meta-analysis. Psychoneuroendocrinology, 34, 1272–83. http://doi.org/10.1016/j.psyneuen.2009.03.016Google Scholar
Luby, J. L., Gaffrey, M. S., Tillman, R., April, L. M., & Belden, A. C. (2014). Trajectories of preschool disorders to full DSM depression at school age and early adolescence: Continuity of preschool depression. American Journal of Psychiatry, 171, 768776. http://doi.org/10.1176/appi.ajp.2014.13091198Google Scholar
McArdle, J. J. (2009). Latent variable modeling of differences and changes with longitudinal data. Annual Review of Psychology, 60, 577605.Google Scholar
McBurnett, K., Lahey, B., Rathouz, P., & Loeber, R. (2000). Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Archives of General Psychiatry, 57, 3843. http://doi.org/10.1001/archpsyc.57.1.38Google Scholar
Mesman, J., Bongers, I. L., & Koot, H. M. (2001). Preschool developmental pathways to preadolescent internalizing and externalizing problems. Journal of Child Psychology and Psychiatry, 42. http://doi.org/10.1017/S0021963001007351Google Scholar
Muthén, L. K., & Muthén, B. O. (2013). Mplus 7.11. Los Angeles, CA: Muthén & Muthén.Google Scholar
Olino, T. M., Klein, D. N., Dyson, M. W., Rose, S. A., & Durbin, C. E. (2010). Temperamental emotionality in preschool-aged children and depressive disorders in parents: Associations in a large community sample. Journal of Abnormal Psychology, 119, 468478. http://doi.org/10.1037/a0020112Google Scholar
Patalay, P., Moulton, V., Goodman, A., & Ploubidis, G. B. (2017). Cross-domain symptom development typologies and their antecedents: Results from the UK millennium cohort study. Journal of the American Academy of Child & Adolescent Psychiatry, 56, 765776. http://doi.org/10.1016/j.jaac.2017.06.009Google Scholar
Petersen, A. C., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Reliability, validity, and initial norms. Journal of youth and adolescence, 17(2), 117133.Google Scholar
Popma, A., Doreleijers, T., & Jansen, L. (2007). The diurnal cortisol cycle in delinquent male adolescents and normal controls. Neuropsychopharmacology, 32, 1622.Google Scholar
Roza, S. J., Hofstra, M. B., van der Ende, J., & Verhulst, F. C. (2003). Stable prediction of mood and anxiety disorders based on behavioral and emotional problems in childhood: A 14-year follow-up during childhood, adolescence, and young adulthood. American Journal of Psychiatry, 160, 21162121. http://doi.org/10.1176/appi.ajp.160.12.2116Google 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. http://doi.org/10.1007/s00213-010-1879-7Google Scholar
Salis, K. L., Bernard, K., Black, S. R., Dougherty, L. R., & Klein, D. (2016). Examining the concurrent and longitudinal relationship between diurnal cortisol rhythms and conduct problems during childhood. Psychoneuroendocrinology, 71, 147154. http://doi.org/10.1016/j.psyneuen.2016.05.021Google Scholar
Schumacher, S., Kirschbaum, C., Fydrich, T., & Ströhle, A. (2013). Is salivary alpha-amylase an indicator of autonomic nervous system dysregulations in mental disorders?—A review of preliminary findings and the interactions with cortisol. Psychoneuroendocrinology, 38, 729743. http://doi.org/10.1016/j.psyneuen.2013.02.003Google 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. http://doi.org/10.1002/dev.20336Google Scholar
Slemming, K., Sørensen, M. J., Thomsen, P. H., Obel, C., Henriksen, T. B., & Linnet, K. M. (2010). The association between preschool behavioural problems and internalizing difficulties at age 10–12 years. European Child & Adolescent Psychiatry, 19, 787795. http://doi.org/10.1007/s00787-010-0128-2Google Scholar
Tackett, J., Reardon, K., Herzhoff, K., Page-Gould, E., Harden, K. P., & Josephs, R. (2015). Estradiol and cortisol interactions in youth externalizing psychopathology. Psychoneuroendocrinology, 55, 146153. http://doi.org/10.1016/J.PSYNEUEN.2015.02.014Google Scholar
Tsigos, C., & Chrousos, G. P. (2002). Hypothalamic–pituitary–adrenal axis, neuroendocrine factors and stress. Journal of Psychosomatic Research, 53, 865871. http://doi.org/10.1016/S0022-3999(02)00429-4Google Scholar
Turan, B., Tackett, J., Lechtreck, M., & Browning, W. (2015). Coordination of the cortisol and testosterone responses: A dual axis approach to understanding the response to social status threats. Psychoneuroendocrinology, 62, 5968. http://doi.org/10.1016/J.PSYNEUEN.2015.07.166Google Scholar
Van Den Bergh, B., & 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 Goozen, S. H. M., Matthys, W., Cohen-Kettenis, P. T., Gispen-de Wied, C., Wiegant, V. M., & van Engeland, H. (1998). Salivary cortisol and cardiovascular activity during stress in oppositional-defiant disorder boys and normal controls. Biological Psychiatry, 43, 531539. http://doi.org/10.1016/S0006-3223(97)00253-9Google Scholar
Zalewski, M., Lengua, L., Kiff, C. J., & Fisher, P. A. (2012). Understanding the relation of low income to HPA-axis functioning in preschool children: Cumulative family risk and parenting as pathways to disruptions in cortisol. Child Psychiatry & Human Development, 43, 924942. http://doi.org/10.1007/s10578-012-0304-3Google Scholar
Supplementary material: File

Frost et al. supplementary material

Appendix A

Download Frost et al. supplementary material(File)
File 121.9 KB