Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-12-01T04:45:09.314Z Has data issue: false hasContentIssue false

How children's anxiety symptoms impact the functioning of the hypothalamus–pituitary–adrenal axis over time: A cross-lagged panel approach using hierarchical linear modeling

Published online by Cambridge University Press:  02 April 2018

Denise Ma*
Affiliation:
Concordia University
Lisa A. Serbin
Affiliation:
Concordia University
Dale M. Stack
Affiliation:
Concordia University
*
Address correspondence and reprint requests to: Denise Ma, Centre for Research in Human Development, Department of Psychology, PY-211, Concordia University, 7141 Sherbrooke Street West, Montreal, Quebec H4B 1R6, Canada; E-mail: [email protected].

Abstract

Anxiety symptoms in childhood and adolescence can have a long-term negative impact on mental and physical health. Although studies have shown dysregulation of the hypothalamus–pituitary–adrenal axis is associated with anxiety disorders, it is unclear how and in what direction children's experiences of anxiety symptoms, which include physiological and cognitive–emotional dimensions, impact the functioning of the hypothalamus–pituitary–adrenal axis over time. We hypothesized that higher physiological symptoms would be contemporaneously associated with hypercortisolism, whereas cognitive–emotional symptoms would be more chronic, reflecting traitlike stability, and would predict hypocortisolism over time. One hundred twenty children from the Concordia Longitudinal Risk Research Project were followed in successive data collection waves approximately 3 years apart from childhood through midadolescence. Between ages 10–12 and 13–15, children completed self-report questionnaires of anxiety symptoms and provided salivary cortisol samples at 2-hr intervals over 2 consecutive days. The results from hierarchical linear modeling showed that higher physiological symptoms were concurrently associated with hypercortisolism, involving cortisol levels that remained elevated over the day. In contrast, longitudinal results over the 3 years between data collection waves showed that chronic worry and social concerns predicted hypocortisolism, showing a low and blunted diurnal cortisol profile. These results have implications for broadening our understanding of the links between anxiety, the stress response system, and health across the course of development.

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

Denise Ma, Lisa A. Serbin, and Dale M. Stack conducted this research at the Centre for Research in Human Development in the Department of Psychology at Concordia University. The current research is an extension of the Concordia Longitudinal Risk Project, which was started by Drs. Jane Ledingham and Alex Schwartzman in 1976. The authors acknowledge the generous grant support for this research from the Fonds de Récherche du Quebec Société et Culture (2005-PS-103501) and the Social Sciences and Humanities Research Council (410-2002-1279 and 410-2005-1599). We are grateful to Claude Senneville and all members of the Concordia Project team for their assistance in data collection. Finally, this study would not be possible without the involvement of all of the participants and families over the years.

References

Adam, E. K. (2006). Transactions among adolescent trait and state emotion and diurnal and momentary cortisol activity in naturalistic settings. Psychoneuroendocrinology, 31, 664679. doi:10.1016/j.psyneuen.2006.01.010.Google Scholar
Aguilera, G. (2015). Stress adaptation and the hypothalamic–pituitary–adrenal axis. In Murphy, D. & Gainer, H. (Eds.), Molecular neuroendocrinology: From genome to physiology (pp. 375403). West Sussex: Wiley.Google Scholar
Angold, A., Costello, E. J., & Worthman, C. M. (1998). Puberty and depression: The roles of age, pubertal status and pubertal timing. Psychological Medicine, 28, 5161.Google Scholar
Asbrand, J., Blechert, J., Nitschke, K., Tuschen-Caffier, B., & Schmitz, J. (2016). Aroused at home: Basic autonomic regulation during orthostatic and physical activation is altered in children with social anxiety disorder. Journal of Abnormal Child Psychology. Advance online publication. doi:10.1007/s10802-016-0147-7.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. doi:10.1017/S095457941100037X.Google Scholar
Brosschot, J. F., Gerin, W., & Thayer, J. F. (2006). The perseverative cognition hypothesis: A review of worry, prolonged stress-related physiological activation, and health. Journal of Psychosomatic Research, 60, 113124.Google Scholar
Brosschot, J. F., Verkuil, B., & Thayer, J. F. (2010). Conscious and unconscious perseverative cognition: Is a large part of prolonged physiological activity due to unconscious stress? Journal of Psychosomatic Research, 69, 407416.Google Scholar
Bryk, A. S., & Raudenbush, S. W. (1992). Hierarchical linear models: Applications and data analysis. Newbury Park, CA: Sage.Google Scholar
Burdwood, E. N., Infantolino, Z. P., Crocker, L. D., Spielberg, J. M., Banich, M. T., Miller, G. A., & Heller, W. (2016). Resting-state functional connectivity differentiates anxious apprehension and anxious arousal. Psychophysiology, 53, 14511459. doi:10.1111/psyp.12696.Google Scholar
Campo, J. V. (2012). Annual Research Review: Functional somatic symptoms and associated anxiety and depression—Developmental psychopathology in pediatric practice: Functional somatic symptoms, anxiety, and depression. Journal of Child Psychology and Psychiatry, 53, 575592. doi:10.1111/j.1469-7610.2012.02535.x.Google Scholar
Chen, F. R., Raine, A., Soyfer, L., & Granger, D. A. (2015). Interaction of adrenocortical activity and autonomic arousal on children's externalizing and internalizing behavior problems. Journal of Abnormal Child Psychology, 43, 189202. doi:10.1007/s10802-014-9900-y.Google Scholar
Cole, D. A., & Martin, N. C. (2005). The longitudinal structure of the Children's Depression Inventory: Testing a latent trait-state model. Psychological Assessment, 17, 144155.Google Scholar
Costello, E. J., Egger, H. L., Copeland, W., Erkanli, A., & Angold, A. (2011). The developmental epidemiology of anxiety disorders: Phenomenology, prevalence, and comorbidity. In Silverman, W. K. & Field, A. P. (Eds.), Anxiety disorders in children and adolescents: Research, assessment and intervention (2nd ed., pp. 5675). Cambridge: Cambridge University Press.Google Scholar
de Kloet, E. R., Joels, M., & Holsboer, F. (2005). Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience, 6, 463475. doi:10.1038/nrn1683.Google Scholar
Dieleman, G. C., Huizink, A. C., Tulen, J. H., Utens, E. M., Creemers, H. E., van der Ende, J., & Verhulst, F. C. (2015). Alterations in HPA-axis and autonomic nervous system functioning in childhood anxiety disorders point to a chronic stress hypothesis. Psychoneuroendocrinology, 51, 135150.Google Scholar
Dietrich, A., Ormel, J., Buitelaar, J. K., Verhulst, F. C., Hoekstra, P. J., & Hartman, C. A. (2013). Cortisol in the morning and dimensions of anxiety, depression, and aggression in children from a general population and clinic-referred cohort: An integrated analysis. The TRAILS study. Psychoneuroendocrinology, 38, 12811298. doi:10.1016/j.psyneuen.2012.11.013.Google Scholar
Doane, L. D., Mineka, S., Zinbarg, R. E., Craske, M., Griffith, J. W., & Adam, E. K. (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, 629642. doi:10.1017/S0954579413000060.Google Scholar
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, 20932103.Google Scholar
Essex, M. J., Shirtcliff, E. A., Burk, L. R., Ruttle, P. L., Klein, M. H., Slattery, M. J., … Armstrong, J. M. (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, 10391058. doi:10.1017/S0954579411000484.Google Scholar
Eysenck, M. (1997). Anxiety and cognition: A unified theory. New York: Psychology Press.Google Scholar
Feder, A., Coplan, J. D., Goetz, R. R., Mathew, S. J., Pine, D. S., Dahl, R. E., … Weissman, M. M. (2004). Twenty-four-hour cortisol secretion patterns in prepubertal children with anxiety or depressive disorders. Biological Psychiatry, 56, 198204. doi:10.1016/j.biopsych.2004.05.005.Google Scholar
Forbes, E. E., Williamson, D. E., Ryan, N. D., Birmaher, B., Axelson, D. A., & Dahl, R. E. (2006). Peri-sleep-onset cortisol levels in children and adolescents with affective disorders. Biological Psychiatry, 59, 2430. doi:10.1016/j.biopsych.2005.06.002.Google Scholar
Forgays, D. G., Sosnowski, T., & Wrześniewski, K. (Eds.) (1992). Anxiety: Recent developments in cognitive, psychophysiological, and health research. Washington, DC: Hemisphere.Google Scholar
Fries, E., Hesse, J., Hellhammer, J., & Hellhammer, D. H. (2005). A new view on hypocortisolism. Psychoneuroendocrinology, 30, 10101016. doi:10.1016/j.psyneuen.2005.04.006.Google Scholar
Gerard, A. B., & Reynolds, C. R. (2004). Characteristics and applications of the Revised Children's Manifest Anxiety Scale (RCMAS). In Maruish, M. E. (Ed.), The use of psychological testing for treatment planning and outcomes assessment: Instruments for children and adolescents (3rd ed., Vol. 2, pp. 6381). Mahwah, NJ: Erlbaum.Google Scholar
Gullone, E., King, N. J., & Ollendick, T. H. (2001). Self-reported anxiety in children and adolescents: A three-year follow-up study. Journal of Genetic Psychology, 162, 519. doi:10.1080/00221320109597878.Google 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
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. doi:10.1017/S0954579411000538.Google Scholar
Hodges, W. F. (2015). The psychophysiology of anxiety. In Zuckerman, M. & Spielberger, C. D. (Eds.), Emotions and anxiety (PLE: emotion): New concepts, methods, and applications (Vol. 12, pp. 175197). New York: Psychology Press.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. doi:10.1016/j.psyneuen.2005.03.002.Google Scholar
Juster, R.-P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience & Biobehavioral Reviews, 35, 216. doi:10.1016/j.neubiorev.2009.10.002.Google Scholar
Keller, P. S., El-Sheikh, M., Vaughn, B., & Granger, D. A. (2010). Relations between mucosal immunity and children's mental health: The role of child sex. Physiology & Behavior, 101, 705712. doi:10.1016/j.physbeh.2010.08.012.Google Scholar
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry, 62, 593602.Google Scholar
Kirschbaum, C., & Hellhammer, D. H. (1994). Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinology, 19, 313333.Google Scholar
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, 695719.Google Scholar
Kovacs, M. (1985). The Children's Depression Inventory (CDI). Psychopharmacology Bulletin, 21, 995998.Google Scholar
Laurent, H. K., Gilliam, K. S., Wright, D. B., & Fisher, P. A. (2015). Child anxiety symptoms related to longitudinal cortisol trajectories and acute stress responses: Evidence of developmental stress sensitization. Journal of Abnormal Psychology, 124, 6879.Google Scholar
Lazarus, R. S. (1993). From psychological stress to the emotions: A history of changing outlooks. Annual Review of Psychology, 44, 121. doi:10.1146/annurev.ps.44.020193.000245.Google Scholar
Ledingham, J. E. (1981). Developmental patterns of aggressive and withdrawn behavior in childhood: A possible method for identifying preschizophrenics. Journal of Abnormal Child Psychology, 9, 122.Google Scholar
Lovallo, W. R. (2015). Stress and health: Biological and psychological interactions (3rd ed.). Thousand Oaks, CA: Sage.Google Scholar
Lupien, S. J., Ouellet-Morin, I., Trepanier, L., Juster, R. P., Marin, M. F., Francois, N., … Durand, N. (2013). The DeStress for success program: Effects of a stress education program on cortisol levels and depressive symptomatology in adolescents making the transition to high school. Neuroscience, 249, 7487.Google Scholar
Maas, C. J., & Hox, J. J. (2005). Sufficient sample sizes for multilevel modeling. Methodology, 1, 8692.Google Scholar
Mack, C., & Moor, L. (1982). Versions françaises d’échelles d’évaluation de la dépression: II. Les échelles DCI et ISC de Maria Kovacs/ French versions of the Evaluation of Depression Scale: II. CDI and ISC scales of Maria Kovacs. Neuropsychiatrie de l'Enfance et de l'Adolescence, 30, 627652.Google Scholar
Marceau, K., Ruttle, P. L., Shirtcliff, E. A., Hastings, P. D., Klimes-Dougan, B., & Zahn-Waxler, C. (2013). Within-person coupling of changes in cortisol, testosterone, and DHEA across the day in adolescents: Coupling of diurnal hormone changes. Developmental Psychobiology, 41, 3345. doi:10.1002/dev.21173.Google Scholar
Masip, A. F., Amador-Campos, J. A., Gómez-Benito, J., & del Barrio Gándara, V. (2010). Psychometric properties of the Children's Depression Inventory in community and clinical samples. Spanish Journal of Psychology, 13, 990999.Google Scholar
Matthey, S., & Petrovski, P. (2002). The Children's Depression Inventory: Error in cutoff scores for screening purposes. Psychological Assessment, 14, 146149.Google Scholar
McTeague, L. M., & Lang, P. J. (2012). The anxiety specturm and the reflex physiology of defense: From circumscribed fear to broad distress. Depression and Anxiety, 29, 264281. doi:10.1002/da.21891.Google Scholar
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, 2545. doi:10.1037/0033-2909.133.1.25.Google Scholar
Minelli, A., & Maffioletti, E. (2014). Genetics of anxiety disorders. In Roman, S. A. (Ed.), Anxiety disorders: Risk factors, genetic determinants and cognitive-behavioral treatment (pp. 6792). Hauppauge, NY: Nova Science.Google Scholar
Netherton, C., Goodyer, I., Tamplin, A., & Herbert, J. (2004). Salivary cortisol and dehydroepiandrosterone in relation to puberty and gender. Psychoneuroendocrinology, 29, 125140.Google Scholar
Newman, M. G., Llera, S. J., Erickson, T. M., Przeworski, A., & Castonguay, L. G. (2013). Worry and generalized anxiety disorder: A review and theoretical synthesis of evidence on nature, etiology, mechanisms, and treatment. Annual Review of Clinical Psychology, 9, 275297.Google Scholar
Rapee, R. M. (2012). Family factors in the development and management of anxiety disorders. Clinical Child and Family Psychology Review, 15, 6980.Google Scholar
Raudenbush, S. W., Bryk, A. S., & Congdon, R. (2004). HLM 6 for Windows [Computer software]. Lincolnwood, IL: Scientific Software International.Google Scholar
Reynolds, C. R., & Richmond, B. O. (1985). Revised Children's Manifest Anxiety Scale: Manual. Los Angeles: Western Psychological Services.Google Scholar
Roy-Byrne, P. P., Davidson, K. W., Kessler, R. C., Asmundson, G. J., Goodwin, R. D., Kubzansky, L., … Laden, S. K. (2008). Anxiety disorders and comorbid medical illness. General Hospital Psychiatry, 30, 208225.Google Scholar
Ruttle, P. L., Armstrong, J. M., Klein, M. H., & Essex, M. J. (2014). Adolescent internalizing symptoms and negative life events: The sensitizing effects of earlier life stress and cortisol. Development and Psychopathology, 26, 14111422.Google Scholar
Schleider, J., Krause, E., & Gillham, J. (2014). Sequential comorbidity of anxiety and depression in youth: Present knowledge and future directions. Current Psychiatry Reviews, 10, 7587.Google Scholar
Schultheiss, O. C., & Stanton, S. J. (2009). Assessment of salivary hormones. In Harmon-Jones, E. & Beer, J. S. (Eds.), Methods in social neuroscience (pp. 1744). New York: Guilford Press.Google Scholar
Schwartzman, A. E., Ledingham, J. E., & Serbin, L. A. (1985). Identification of children at risk for adult schizophrenia: A longitudinal study. Applied Psychology, 34, 363379.Google Scholar
Selye, H. (2013). Stress in health and disease. Boston: Butterworth.Google Scholar
Serbin, L. A., Cooperman, J. M., Peters, P. L., Lehoux, P. M., Stack, D. M., & Schwartzman, A. E. (1998). Intergenerational transfer of psychosocial risk in women with childhood histories of aggression, withdrawal, or aggression and withdrawal. Developmental Psychology, 34, 12461262.Google Scholar
Sharp, P. B., Miller, G. A., & Heller, W. (2015). Transdiagnostic dimensions of anxiety: Neural mechanisms, executive functions, and new directions. International Journal of Psychophysiology, 98, 365377. doi:10.1016/j.ijpsycho.2015.07.001.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. doi:10.1002/dev.20336.Google Scholar
Stallard, P., Velleman, R., Langsford, J., & Baldwin, S. (2001). Coping and psychological distress in children involved in road traffic accidents. British Journal of Clinical Psychology, 40, 197208.Google Scholar
Statistics Canada. (2013). Table 111-0009—Family characteristics, summary, annual (number unless otherwise noted). Retrieved from http://www5.statcan.gc.ca/cansim/a26?lang=eng&id=1110009Google Scholar
Stroud, C. B., Chen, F. R., Doane, L. D., & Granger, D. A. (2016). Individual differences in early adolescents’ latent trait cortisol (LTC): Relation to early adversity. Developmental Psychobiology, 58, 700713.Google Scholar
Stroud, L. R., Foster, E., Papandonatos, G. D., Handwerger, K., Granger, D. A., Kivlighan, K. T., & Niaura, R. (2009). Stress response and the adolescent transition: Performance versus peer rejection stressors. Development and Psychopathology, 21, 4768.Google Scholar
Timbremont, B., Braet, C., & Dreessen, L. (2004). Assessing depression in youth: Relation between the Children's Depression Inventory and a structured interview. Journal of Clinical Child and Adolescent Psychology, 33, 149157.Google Scholar
Turgeon, L., & Chartrand, É. (2003). Reliability and validity of the Revised Children's Manifest Anxiety Scale in a French-Canadian sample. Psychological Assessment, 15, 378383.Google Scholar
Turner-Cobb, J. M., Rixon, L., & Jessop, D. S. (2011). Hypothalamic–pituitary–adrenal axis activity and upper respiratory tract infection in young children transitioning to primary school. Psychopharmacology, 214, 309317.Google Scholar
Varela, R. E., & Biggs, B. K. (2006). Reliability and validity of the Revised Children's Manifest Anxiety Scale (RCMAS) across samples of Mexican, Mexican American, and European American children: A preliminary investigation. Anxiety, Stress and Coping, 19, 6780. doi:10.1080/10615800500499727.Google Scholar
Vliegenthart, J., Noppe, G., van Rossum, E. F. C., Koper, J. W., Raat, H., & van den Akker, E. L. T. (2016). Socioeconomic status in children is associated with hair cortisol levels as a biological measure of chronic stress. Psychoneuroendocrinology, 65, 914.Google Scholar
Zeiders, K. H., Doane, L. D., & Adam, E. K. (2011). Reciprocal relations between objectively measured sleep patterns and diurnal cortisol rhythms in late adolescence. Journal of Adolescent Health, 48, 566571.Google Scholar