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Developmental pathways from preschool irritability to multifinality in early adolescence: the role of diurnal cortisol

Published online by Cambridge University Press:  20 December 2019

Ellen M. Kessel Open the ORCID record for Ellen M. Kessel [Opens in a new window] ,
Allison Frost ,
Brandon L. Goldstein Open the ORCID record for Brandon L. Goldstein [Opens in a new window] ,
Sarah R. Black ,
Lea R. Dougherty ,
Gabrielle A. Carlson  and
Daniel N. Klein
Ellen M. Kessel*
Affiliation:
Division of Child and Adolescent Psychiatry, Columbia University and the New York State Psychiatric Institute, New York, NY
Allison Frost
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY
Brandon L. Goldstein
Affiliation:
Department of Psychiatry, University of Connecticut School of Medicine, Farmington, CT
Sarah R. Black
Affiliation:
Department of Psychology, The University of New Orleans, New Orleans, LA
Lea R. Dougherty
Affiliation:
Department of Psychology, University of Maryland, College Park, MD
Gabrielle A. Carlson
Affiliation:
Department of Psychiatry, Stony Brook University School of Medicine, Stony Brook, NY
Daniel N. Klein
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY
*
Author for correspondence: Ellen M. Kessel, E-mail: [email protected]
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Abstract

Background

Early irritability predicts a broad spectrum of psychopathology spanning both internalizing and externalizing disorders, rather than any particular disorder or group of disorders (i.e. multifinality). Very few studies, however, have examined the developmental mechanisms by which it leads to such phenotypically diverse outcomes. We examined whether variation in the diurnal pattern of cortisol moderates developmental pathways between preschool irritability and the subsequent emergence of internalizing and externalizing symptoms 9 years later.

Method

When children were 3 years old, mothers were interviewed about children's irritability and completed questionnaires about their children's psychopathology. Six years later, children collected saliva samples at wake-up and bedtime on three consecutive days. Diurnal cortisol patterns were modeled as latent difference scores between evening and morning samples. When children were approximately 12 years old, mothers again completed questionnaires about their children's psychopathology.

Results

Among children with higher levels of irritability at age 3, a steeper diurnal cortisol slope at age 9 predicted greater internalizing symptoms and irritability at age 12, whereas a blunted slope at age 9 predicted greater externalizing symptoms at age 12, adjusting for baseline and concurrent symptoms.

Conclusion

Our results suggest that variation in stress system functioning can predict and differentiate developmental trajectories of early irritability that are relatively more internalizing v. those in which externalizing symptoms dominate in pre-adolescence.

Keywords

Cortisolexternalizinginternalizingirritabilitymultifinality
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 5 , April 2021 , pp. 761 - 769
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Copyright
Copyright © Cambridge University Press 2019

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References

Achenbach, T. M., McConaughy, S. H., & Howell, C. T. (1987). Child/adolescent behavioral and emotional problems: Implications of cross-informant correlations for situational specificity. Psychological Bulletin, 101(2), 213–232.CrossRefGoogle ScholarPubMed
Achenbach, T. M., & Rescorla, L. (2000). Manual for the ASEBA preschool forms & profiles: An integrated system of multi-informant assessment. Burlington, VT: ASEBA.Google Scholar
Achenbach, T. M., & Rescorla, L. (2001). Manual for the ASEBA school-age forms & profiles: An integrated system of multi-informant assessment. Burlington, VT: ASEBA.Google Scholar
Aiken, L. S., West, S. G., & Reno, R. R. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, California: Sage.Google Scholar
Azar, R., Zoccolillo, M., Paquette, D., Quiros, E., Baltzer, F., & Tremblay, R. E. (2004). Cortisol levels and conduct disorder in adolescent mothers. Journal of the American Academy of Child and Adolescent Psychiatry, 43(4), 461–468; discussion 469–472. doi: 10.1097/00004583-200404000-00012.CrossRefGoogle ScholarPubMed
Beauchaine, T. P., & Constantino, J. N. (2017). Redefining the endophenotype concept to accommodate transdiagnostic vulnerabilities and etiological complexity. Biomarkers in Medicine 11(9): 769–780. doi: 10.2217/bmm-2017-0002.CrossRefGoogle ScholarPubMed
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), 456–471. doi: 10.1111/cdev.12304.CrossRefGoogle ScholarPubMed
Brennan, P. A., & Raine, A. (1997). Biosocial bases of antisocial behavior: Psychophysiological, neurological, and cognitive factors. Clinical Psychology Review, 17(6), 589–604.CrossRefGoogle ScholarPubMed
Burt, K. B., & Obradovic, J. (2013). The construct of psychophysiological reactivity: Statistical and psychometric issues. Developmental Review, 33(1), 29–57. doi: 10.1016/j.dr.2012.10.002.CrossRefGoogle Scholar
Caspi, A., Houts, R. M., Belsky, D. W., Goldman-Mellor, S. J., Harrington, H., Israel, S., … Moffitt, T. E. (2014). The p factor: One general psychopathology factor in the structure of psychiatric disorders? Clinical Psychological Science, 2(2), 119-137. doi: 10.1177/2167702613497473.CrossRefGoogle 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(1), 12–30. doi: 10.1080/00273171.2016.1245600.CrossRefGoogle ScholarPubMed
Copeland, W. E., Brotman, M. A., & Costello, E. J. (2015a). Normative irritability in youth: Developmental findings from the great smoky mountains study. Journal of the American Academy of Child and Adolescent Psychiatry, 54(8), 635–642. doi: 10.1016/j.jaac.2015.05.008.CrossRefGoogle Scholar
Copeland, W. E., Wolke, D., Shanahan, L., & Costello, E. J. (2015b). Adult functional outcomes of common childhood psychiatric problems: A prospective, longitudinal study. JAMA Psychiatry, 72(9), 892–899. doi: 10.1001/jamapsychiatry.2015.0730.CrossRefGoogle Scholar
Costello, E. J., Copeland, W., & Angold, A. (2011). Trends in psychopathology across the adolescent years: What changes when children become adolescents, and when adolescents become adults? Journal of Child Psychology and Psychiatry and Allied Disciplines, 52(10), 1015–1025. doi: 10.1111/j.1469-7610.2011.02446.x.CrossRefGoogle ScholarPubMed
De Bellis, M. D., Dahl, R. E., Perel, J. M., Birmaher, B., Al-Shabbout, M., Williamson, D. E., … (1996). Nocturnal ACTH, cortisol, growth hormone, and prolactin secretion in prepubertal depression. Journal of the American Academy of Child and Adolescent Psychiatry, 35(9), 1130–1138. doi: 10.1097/00004583-199609000-00010.CrossRefGoogle ScholarPubMed
Dougherty, L. R., Smith, V. C., Bufferd, S. J., Kessel, E., Carlson, G. A., & Klein, D. N. (2015). Preschool irritability predicts child psychopathology, functional impairment, and service use at age nine. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 56(9), 999–1007. doi: 10.1111/jcpp.12403.CrossRefGoogle ScholarPubMed
Dougherty, L. R., Smith, V. C., Bufferd, S. J., Stringaris, A., Leibenluft, E., Carlson, G. A., & Klein, D. N. (2013). Preschool irritability: Longitudinal associations with psychiatric disorders at age 6 and parental psychopathology. Journal of the American Academy of Child and Adolescent Psychiatry, 52(12), 1304–1313. doi: 10.1016/j.jaac.2013.09.007.CrossRefGoogle ScholarPubMed
Edwards, S., Clow, A., Evans, P., & Hucklebridge, F. (2001). Exploration of the awakening cortisol response in relation to diurnal cortisol secretory activity. Life Sciences, 68(18), 2093–2103.CrossRefGoogle ScholarPubMed
Egger, H. L., & Angold, A. (2006). Common emotional and behavioral disorders in preschool children: Presentation, nosology, and epidemiology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 47(3-4), 313–337. doi: 10.1111/j.1469-7610.2006.01618.x.CrossRefGoogle ScholarPubMed
Egger, H. L., Erkanli, A., Keeler, G., Potts, E., Walter, B. K., & Angold, A. (2006). Test-retest reliability of the Preschool Age Psychiatric Assessment (PAPA). Journal of the American Academy of Child and Adolescent Psychiatry, 45(5), 538–549. doi: 10.1097/01.chi.0000205705.71194.b8.CrossRefGoogle 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(3), 430–457. doi: 10.1207/S15328007sem0803_5.CrossRefGoogle Scholar
Garvey, M., Avenevoli, S., & Anderson, K. (2016). The national institute of mental health research domain criteria and clinical research in child and adolescent psychiatry. Journal of the American Academy of Child and Adolescent Psychiatry, 55(2), 93–98. doi: 10.1016/j.jaac.2015.11.002.CrossRefGoogle ScholarPubMed
Gerra, G., Zaimovic, A., Avanzini, P., Chittolini, B., Giucastro, G., Caccavari, R., … (1997). Neurotransmitter-neuroendocrine responses to experimentally induced aggression in humans: Influence of personality variable. Psychiatry Research, 66(1), 33–43.CrossRefGoogle ScholarPubMed
Goodyer, I. M., Herbert, J., Tamplin, A., & Altham, P. M. (2000). Recent life events, cortisol, dehydroepiandrosterone and the onset of major depression in high-risk adolescents. British Journal of Psychiatry, 177, 499–504.CrossRefGoogle ScholarPubMed
Granger, D. A., Fortunato, C. K., Beltzer, E. K., Virag, M., Bright, M. A., & Out, D. (2012). Focus on methodology: Salivary bioscience and research on adolescence: an integrated perspective. Journal of Adolescence, 35(4), 1081–1095.CrossRefGoogle 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(1), 40–46. doi: 10.1016/j.biopsych.2006.09.011.CrossRefGoogle ScholarPubMed
Hayes, A. F., & Matthes, J. (2009). Computational procedures for probing interactions in OLS and logistic regression: SPSS and SAS implementations. Behavior Research Methods, 41(3), 924–936. doi: 10.3758/BRM.41.3.924.CrossRefGoogle ScholarPubMed
Kariyawasam, S. H., Zaw, F., & Handley, S. L. (2002). Reduced salivary cortisol in children with comorbid attention deficit hyperactivity disorder and oppositional defiant disorder. Neuroendocrinology Letters, 23(1), 45–48.Google ScholarPubMed
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(2), 473–491. doi: 10.1017/S0954579408000230.CrossRefGoogle ScholarPubMed
Kessel, E. M., Meyer, A., Hajcak, G., Dougherty, L. R., Torpey-Newman, D. C., Carlson, G. A., & Klein, D. N. (2016). Transdiagnostic factors and pathways to multifinality: The error-related negativity predicts whether preschool irritability is associated with internalizing versus externalizing symptoms at age 9. Development and Psychopathology, 28(4pt1), 913–926. doi: 10.1017/S0954579416000626.CrossRefGoogle ScholarPubMed
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(2), 205–215. doi: 10.1002/jts.20112.CrossRefGoogle ScholarPubMed
Klimes-Dougan, B., Hastings, P. D., Granger, D. A., Usher, B. A., & Zahn-Waxler, C. (2001). Adrenocortical activity in at-risk and normally developing adolescents: Individual differences in salivary cortisol basal levels, diurnal variation, and responses to social challenges. Development and Psychopathology, 13(3), 695–719.CrossRefGoogle ScholarPubMed
Koss, K. J., & Gunnar, M. R. (2018). Annual research review: Early adversity, the hypothalamic-pituitary-adrenocortical axis, and child psychopathology. Journal of Child Psychology and Psychiatry, 59(4), 327–346. doi: 10.1111/jcpp.12784.CrossRefGoogle ScholarPubMed
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(2), 142–186. doi: 10.1037/bul0000069.CrossRefGoogle ScholarPubMed
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(4), 850–859. doi: 10.1037/abn0000087.CrossRefGoogle ScholarPubMed
Lok, A., Mocking, R. J., Ruhe, H. G., Visser, I., Koeter, M. W., Assies, J., … (2012). Longitudinal hypothalamic-pituitary-adrenal axis trait and state effects in recurrent depression. Psychoneuroendocrinology, 37(7), 892–902. doi: 10.1016/j.psyneuen.2011.10.005.CrossRefGoogle ScholarPubMed
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(9), 1272–1283. doi: 10.1016/j.psyneuen.2009.03.016.CrossRefGoogle ScholarPubMed
McArdle, J. J. (2009). Latent variable modeling of differences and changes with longitudinal data. Annual Review of Psychology, 60, 577–605. doi: 10.1146/annurev.psych.60.110707.163612.CrossRefGoogle ScholarPubMed
McBurnett, K., Raine, A., Stouthamer-Loeber, M., Loeber, R., Kumar, A. M., Kumar, M., & Lahey, B. B. (2005). Mood and hormone responses to psychological challenge in adolescent males with conduct problems. Biological Psychiatry, 57(10), 1109–1116. doi: 10.1016/j.biopsych.2005.01.041.CrossRefGoogle ScholarPubMed
Moss, H. B., Vanyukov, M. M., & Martin, C. S. (1995). Salivary cortisol responses and the risk for substance abuse in prepubertal boys. Biological Psychiatry, 38(8), 547–555. doi: 10.1016/0006-3223(94)00382-D.CrossRefGoogle ScholarPubMed
Mulraney, M., Melvin, G., & Tonge, B. (2014). Brief report: Can irritability act as a marker of psychopathology? Journal of Adolescence, 37(4), 419-423. doi: 10.1016/j.adolescence.2014.03.005.CrossRefGoogle ScholarPubMed
Nolen-Hoeksema, S., & Watkins, E. R. (2011). A heuristic for developing transdiagnostic models of psychopathology: Explaining multifinality and divergent trajectories. Perspectives on Psychological Science, 6(6), 589–609. doi: 10.1177/1745691611419672.CrossRefGoogle ScholarPubMed
Olino, T. M., Dougherty, L. R., Bufferd, S. J., Carlson, G. A., & Klein, D. N. (2014). Testing models of psychopathology in preschool-aged children using a structured interview-based assessment. Journal of Abnormal Child Psychology, 42(7), 1201–1211. doi: 10.1007/s10802-014-9865-x.CrossRefGoogle ScholarPubMed
Pajer, K., Gardner, W., Rubin, R. T., Perel, J., & Neal, S. (2001). Decreased cortisol levels in adolescent girls with conduct disorder. Archives of General Psychiatry, 58(3), 297–302.CrossRefGoogle ScholarPubMed
Platje, E., Jansen, L. M., Raine, A., Branje, S. J., Doreleijers, T. A., de Vries-Bouw, M., … Vermeiren, R. R. (2013). Longitudinal associations in adolescence between cortisol and persistent aggressive or rule-breaking behavior. Biological Psychology, 93(1), 132–137. doi: 10.1016/j.biopsycho.2013.01.002.CrossRefGoogle ScholarPubMed
Riglin, L., Eyre, O., Cooper, M., Collishaw, S., Martin, J., Langley, K., … Thapar, A. (2017). Investigating the genetic underpinnings of early-life irritability. Translational Psychiatry, 7(9), e1241. doi: 10.1038/tp.2017.212.CrossRefGoogle ScholarPubMed
Ruttle, P. L., Shirtcliff, E. A., Serbin, L. A., Fisher, D. B., 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(1), 123–132. doi: 10.1016/j.yhbeh.2010.10.015.CrossRefGoogle ScholarPubMed
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, 147–154. doi: 10.1016/j.psyneuen.2016.05.021.CrossRefGoogle ScholarPubMed
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(7), 690–703. doi: 10.1002/dev.20336.CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17(1), 167–184.CrossRefGoogle ScholarPubMed
Smyth, J. M., Ockenfels, M. C., Gorin, A. A., Catley, D., Porter, L. S., Kirschbaum, C., … Stone, A. A. (1997). Individual differences in the diurnal cycle of cortisol. Psychoneuroendocrinology, 22(2), 89–105.CrossRefGoogle ScholarPubMed
Stringaris, A., Goodman, R., Ferdinando, S., Razdan, V., Muhrer, E., Leibenluft, E., & Brotman, M. A. (2012). The affective reactivity Index: A concise irritability scale for clinical and research settings. Journal of Child Psychology and Psychiatry, 53(11), 1109–1117. doi: 10.1111/j.1469-7610.2012.02561.x.CrossRefGoogle ScholarPubMed
Stringaris, A., & Taylor, E. A. (2015). Disruptive mood: Irritability in children and adolescents. NY, New York: Oxford University Press.CrossRefGoogle Scholar
van Bokhoven, I., Van Goozen, S. H., van Engeland, H., Schaal, B., Arseneault, L., Seguin, J. R., … Tremblay, R. E. (2005). Salivary cortisol and aggression in a population-based longitudinal study of adolescent males. Journal of Neural Transmission, 112(8), 1083–1096. doi: 10.1007/s00702-004-0253-5.CrossRefGoogle Scholar
Vidal-Ribas, P., Brotman, M. A., Valdivieso, I., Leibenluft, E., & Stringaris, A. (2016). The status of irritability in psychiatry: a conceptual and quantitative review. Journal of the American Academy of Child & Adolescent Psychiatry, 55(7), 556–570.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., Choi, S. W., Carter, A. S., Hullsiek, H., Burns, J., McCarthy, K., … Briggs-Gowan, M. J. (2012). Defining the developmental parameters of temper loss in early childhood: Implications for developmental psychopathology. Journal of Child Psychology and Psychiatry, 53(11), 1099–1108. doi: 10.1111/j.1469-7610.2012.02595.x.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., Estabrook, R., Petitclerc, A., Henry, D., Burns, J. L., Perlman, S. B., … Briggs-Gowan, M. L. (2015). Clinical implications of a dimensional approach: The normal: Abnormal Spectrum of early irritability. Journal of the American Academy of Child and Adolescent Psychiatry, 54(8), 626–634. doi: 10.1016/j.jaac.2015.05.016.CrossRefGoogle ScholarPubMed
Wakschlag, L. S., Perlman, S. B., Blair, R. J., Leibenluft, E., Briggs-Gowan, M. J., & Pine, D. S. (2018). The neurodevelopmental basis of early childhood disruptive behavior: Irritable and callous phenotypes as exemplars. American Journal of Psychiatry, 175(2), 114–130. doi: 10.1176/appi.ajp.2017.17010045.CrossRefGoogle ScholarPubMed
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