Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T15:38:20.896Z Has data issue: false hasContentIssue false

Predicting mental disorders from hypothalamic-pituitary-adrenal axis functioning: a 3-year follow-up in the TRAILS study

Published online by Cambridge University Press:  19 March 2015

E. Nederhof*
Affiliation:
University of Groningen, University Medical Center Groningen, University Center for Psychiatry, Interdisciplinary Center Psychopathology and Emotion regulation, Groningen, The Netherlands
F. V. A. van Oort
Affiliation:
Department of Child and Adolescent Psychiatry, Erasmus University Medical Center, Rotterdam, The Netherlands
E. M. C. Bouma
Affiliation:
University of Groningen, University Medical Center Groningen, University Center for Psychiatry, Interdisciplinary Center Psychopathology and Emotion regulation, Groningen, The Netherlands
O. M. Laceulle
Affiliation:
University of Groningen, University Medical Center Groningen, University Center for Psychiatry, Interdisciplinary Center Psychopathology and Emotion regulation, Groningen, The Netherlands
A. J. Oldehinkel
Affiliation:
University of Groningen, University Medical Center Groningen, University Center for Psychiatry, Interdisciplinary Center Psychopathology and Emotion regulation, Groningen, The Netherlands
J. Ormel
Affiliation:
University of Groningen, University Medical Center Groningen, University Center for Psychiatry, Interdisciplinary Center Psychopathology and Emotion regulation, Groningen, The Netherlands
*
* Address for correspondence: Dr E. Nederhof, Ph.D., Interdisciplinary Center Psychopathology and Emotion Regulation, University Center for Psychiatry, University Medical Center Groningen, University of Groningen, CC72, PO Box 30001, 9700RB Groningen, The Netherlands. (Email: [email protected])

Abstract

Background

Hypothalamic-pituitary-adrenal axis functioning, with cortisol as its major output hormone, has been presumed to play a key role in the development of psychopathology. Predicting affective disorders from diurnal cortisol levels has been inconclusive, whereas the predictive value of stress-induced cortisol concentrations has not been studied before. The aim of this study was to predict mental disorders over a 3-year follow-up from awakening and stress-induced cortisol concentrations.

Method

Data were used from 561 TRAILS (TRacking Adolescents’ Individual Lives Survey) participants, a prospective cohort study of Dutch adolescents. Saliva samples were collected at awakening and half an hour later and during a social stress test at age 16. Mental disorders were assessed 3 years later with the Composite International Diagnostic Interview (CIDI).

Results

A lower cortisol awakening response (CAR) marginally significantly predicted new disorders [odds ratio (OR) 0.77, p = 0.06]. A flat recovery slope predicted disorders with a first onset after the experimental session (OR 1.27, p = 0.04). Recovery revealed smaller, non-significant ORs when predicting new onset affective or anxiety disorders, major depressive disorder, or dependence disorders in three separate models, corrected for all other new onsets.

Conclusions

Our results suggest that delayed recovery and possibly reduced CAR are indicators of a more general risk status and may be part of a common pathway to psychopathology. Delayed recovery suggests that individuals at risk for mental disorders perceived the social stress test as less controllable and less predictable.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2015 

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

Adam, EK, Doane, LD, Zinbarg, RE, Mineka, S, Craske, MG, Griffith, JW (2010). Prospective prediction of major depressive disorder from cortisol awakening responses in adolescence. Psychoneuroendocrinology 35, 921931.CrossRefGoogle ScholarPubMed
Adam, EK, Vrshek-Schallhorn, S, Kendall, AD, Mineka, S, Zinbarg, RE, Craske, MG (2014). Prospective associations between the cortisol awakening response and first onsets of anxiety disorders over a six-year follow-up-2013 Curt Richter Award Winner. Psychoneuroendocrinology 44, 4759.CrossRefGoogle Scholar
Allen, AP, Kennedy, PJ, Cryan, JF, Dinan, TG, Clarke, G (2014). Biological and psychological markers of stress in humans: focus on the trier social stress test. Neuroscience and Biobehavioral Reviews 38, 94124.CrossRefGoogle ScholarPubMed
APA (2000). Diagnostic and Statistican Manual of Mental Disorders: DSM-IV-TR. APA: Arlington, VA.Google Scholar
Barnard, J, Rubin, D (1999). Small-sample degrees of freedom with multiple imputation. Biometrika 86, 948955.CrossRefGoogle Scholar
Benschop, R, Geenen, R, Mills, P, Naliboff, B, Kiecolt-Glaser, J, Herbert, T, van der Pompe, G, Miller, G, Matthews, K, Godaert, G, Gilmore, S, Glaser, R, Heijnen, C, Dopp, J, Bijlsma, J, Solomon, G, Cacioppo, J (1998). Cardiovascular and immune responses to acute psychological stress in young and old women: a meta-analysis. Psychosomatic Medicine 60, 290296.CrossRefGoogle Scholar
Booij, SH, Bouma, EMC, de Jonge, P, Ormel, J, Oldehinkel, AJ (2013). Chronicity of depressive problems and the cortisol response to psychosocial stress in adolescents: The TRAILS study. Psychoneuroendocrinology 38, 659666.CrossRefGoogle ScholarPubMed
Bouma, EMC, Riese, H, Ormel, J, Verhulst, FC, Oldehinkel, AJ (2009). Adolescents’ cortisol responses to awakening and social stress; Effects of gender, menstrual phase and oral contraceptives. The TRAILS study. Psychoneuroendocrinology 34, 884893.CrossRefGoogle ScholarPubMed
Caspi, A, Houts, RM, Belsky, DW, Goldman-Mellor, SJ, Harrington, H, Israel, S, Meier, MH, Ramrakha, S, Shalev, I, Poulton, R, Moffitt, TE (2014). The p factor: one general psychopathology factor in the structure of psychiatric disorders? Clinical Psychological Science 2, 119137.CrossRefGoogle Scholar
Cole, T, Bellizzi, M, Flegal, K, Dietz, W (2000). Establishing a standard definition for child overweight and obesity worldwide: international survey. British Medical Journal 320, 12401243.CrossRefGoogle ScholarPubMed
De Winter, AF, Oldehinkel, AJ, Veenstra, R, Brunnekreef, JA, Verhulst, FC, Ormel, J (2005). Evaluation of non-response bias in mental health determinants and outcomes in a large sample of pre-adolescents. European Journal of Epidemiology 20, 173181.CrossRefGoogle Scholar
Dickerson, S, Kemeny, M (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin 130, 355391.CrossRefGoogle ScholarPubMed
Dietrich, A, Ormel, J, Buitelaar, JK, Verhulst, FC, Hoekstra, PJ, Hartman, CA (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.CrossRefGoogle ScholarPubMed
Donders, ART, van der Heijden, GJMG, Stijnen, T, Moons, KGM (2006). Review: a gentle introduction to imputation of missing values. Journal of Clinical Epidemiology 59, 10871091.CrossRefGoogle ScholarPubMed
Ellenbogen, MA, Hodgins, S, Linnen, AM, Ostiguy, CS (2011). Elevated daytime cortisol levels: a biomarker of subsequent major affective disorder? Journal of Affective Disorders 132, 265269.CrossRefGoogle Scholar
Fries, E, Dettenborn, L, Kirschbaum, C (2009). The cortisol awakening response (CAR): facts and future directions. International Journal of Psychophysiology 72, 6773.CrossRefGoogle ScholarPubMed
Goodyer, IM, Bacon, A, Ban, M, Croudace, T, Herbert, J (2009). Serotonin transporter genotype, morning cortisol and subsequent depression in adolescents. British Journal of Psychiatry 195, 3945.CrossRefGoogle ScholarPubMed
Goodyer, IM, Herbert, J, Tamplin, A (2003). Psychoendocrine antecedents of persistent first-episode major depression in adolescents: a community-based longitudinal enquiry. Psychological Medicine 33, 601610.CrossRefGoogle ScholarPubMed
Goodyer, IM, Herbert, J, Tamplin, A, Altham, PM (2000 a). Recent life events, cortisol, dehydroepiandrosterone and the onset of major depression in high-risk adolescents. British Journal of Psychiatry 177, 499504.CrossRefGoogle ScholarPubMed
Goodyer, IM, Herbert, J, Tamplin, A, Altham, PME (2000 b). First-episode major depression in adolescents – affective, cognitive and endocrine characteristics of risk status and predictors of onset. British Journal of Psychiatry 176, 142149.CrossRefGoogle ScholarPubMed
Gruenewald, T, Kemeny, M, Aziz, N, Fahey, J (2004). Acute threat to the social self: shame, social self-esteem, and cortisol activity. Psychosomatic Medicine 66, 915924.CrossRefGoogle Scholar
Haro, JM, Arbabzadeh-Bouchez, S, Brugha, TS, de Girolamo, G, Guyer, ME, Jin, R, Lepine, JP, Mazzi, F, Reneses, B, Vilagut, G, Sampson, NA, Kessler, RC (2006). Concordance of the Composite International Diagnostic Interview Version 3.0 (CIDI 3.0) with standardized clinical assessments in the WHO World Mental Health surveys. International Journal of Methods in Psychiatric Research 15, 167180.CrossRefGoogle ScholarPubMed
Harris, TO, Borsanyi, S, Messari, S, Stanford, K, Cleary, SE, Shiers, HM, Brown, GW, Herbert, J (2000). Morning cortisol as a risk factor for subsequent major depressive disorder in adult women. British Journal of Psychiatry 177, 505510.CrossRefGoogle ScholarPubMed
Hellhammer, J, Fries, E, Schweisthal, OW, Schlotz, W, Stone, AA, Hagemann, D (2007). Several daily measurements are necessary to reliably assess the cortisol rise after awakening: state- and trait components. Psychoneuroendocrinology 32, 8086.CrossRefGoogle ScholarPubMed
Kertes, DA, van Dulmen, M (2012). Latent state trait modeling of children's cortisol at two points of the diurnal cycle. Psychoneuroendocrinology 37, 249255.CrossRefGoogle ScholarPubMed
Kessler, R, Ustun, T (2004). The World Mental Health (WMH) Survey Initiative version of the World Health Organization (WHO) Composite International Diagnostic Interview (CIDI). International Journal of Methods in Psychiatric Research 13, 93121.CrossRefGoogle ScholarPubMed
Kessler, RC, Avenevoli, S, Green, J, Gruber, MJ, Guyer, M, He, Y, Jin, R, Kaufman, J, Sampson, NA, Zaslavsky, AM, Merikangas, KR (2009). National comorbidity survey replication adolescent supplement (NCS-A): III. Concordance of DSM-IV/CIDI diagnoses with clinical reassessments. Journal of the American Academy of Child and Adolescent Psychiatry 48, 386399.CrossRefGoogle ScholarPubMed
Kim, KJ, Conger, RD, Elder, GH, Lorenz, FO (2003). Reciprocal influences between stressful life events and adolescent internalizing and externalizing problems. Child Development 74, 127143.CrossRefGoogle ScholarPubMed
Kirschbaum, C, Hellhammer, DH (1994). Salivary cortisol in psychoneuroendocrine research – recent developments and applications. Psychoneuroendocrinology 19, 313333.CrossRefGoogle ScholarPubMed
Kirschbaum, C, Pirke, KM, Hellhammer, DH (1993). The trier social stress test – a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 7681.CrossRefGoogle Scholar
Koolhaas, JM (2008). Coping style and immunity in animals: making sense of individual variation. Brain Behavior and Immunity 22, 662667.CrossRefGoogle ScholarPubMed
Koolhaas, JM, Bartolomucci, A, Buwalda, B, Boer, SFd, Flugge, G, Korte, SM, Meerlo, P, Murison, R, Olivier, B, Palanza, P, Richter-Levin, G, Sgoifo, A, Steimer, T, Stiedl, O, Dijk, Gv, Wohr, M, Fuchs, E (2011). Stress revisited: a critical evaluation of the stress concept. Neuroscience and Biobehavioral Reviews 35, 12911301.CrossRefGoogle ScholarPubMed
Kudielka, B, Schommer, N, Hellhammer, D, Kirschbaum, C (2004). Acute HPA axis responses, heart rate, and mood changes to psychosocial stress (TSST) in humans at different times of day. Psychoneuroendocrinology 29, 983992.CrossRefGoogle ScholarPubMed
Laceulle, OM, Nederhof, E, van Aken, MAG, Ormel, J (2014). Adolescent personality: associations with basal, awakening, and stress-induced cortisol responses. Journal of Personality. Published online: 26 05 2014 . doi:10.1111/jopy.12101.Google ScholarPubMed
Laceulle, OM, Vollebergh, WAM, Ormel, J (2015). The structure of psychopathology in adolescence: replication of a general psychopathology factor in the TRAILS study. Psychological Science. Published online: Published online 23 02 2015 . doi:10.1177/2167702614560750.Google Scholar
Lahey, BB, Van Hulle, CA, Singh, AL, Waldman, ID, Rathouz, PJ (2011). Higher-order genetic and environmental structure of prevalent forms of child and adolescent psychopathology. Archives of General Psychiatry 68, 181189.CrossRefGoogle ScholarPubMed
Law, R, Hucklebridge, F, Thorn, L, Evans, P, Clow, A (2013). State variation in the cortisol awakening response. Stress 16, 483492.CrossRefGoogle ScholarPubMed
Meeusen, R, Nederhof, E, Buyse, L, Roelands, B, de Schutter, G, Piacentini, MF (2010). Diagnosing overtraining in athletes using the two-bout exercise protocol. British Journal of Sports Medicine 44, 642648.CrossRefGoogle ScholarPubMed
Mikolajczak, M, Roy, E, Luminet, O, De Timary, P (2008). Resilience and hypothalamic-pituitary-adrenal axis reactivity under acute stress in young men. Stress 11, 477482.CrossRefGoogle ScholarPubMed
Nederhof, E, Jorg, F, Raven, D, Veenstra, R, Verhulst, FC, Ormel, J, Oldehinkel, AJ (2012). Benefits of extensive recruitment effort persist during follow-ups and are consistent across age group and survey method. The TRAILS study. BMC Medical Research Methodology 12, 93.CrossRefGoogle ScholarPubMed
Nederhof, E, Lemmink, KAPM, Visscher, C, Meeusen, R, Mulder, T (2006). Psychomotor speed – possibly a new marker for overtraining syndrome. Sports Medicine 36, 817828.CrossRefGoogle ScholarPubMed
Raghunathan, TE, Solenberger, PW, Van Hoewyk, J (2002). IVEware: Imputation and Variance Estimation Software, User Guide. Survey Research Center, Institute for Social Research, University of Michigan, Ann Arbor, MI.Google Scholar
Rao, U, Hammen, C, Ortiz, LR, Chen, LA, Poland, RE (2008). Effects of early and recent adverse experiences on adrenal response to psychosocial stress in depressed adolescents. Biological Psychiatry 64, 521526.CrossRefGoogle ScholarPubMed
Rao, U, Hammen, CL, Poland, RE (2009). Risk markers for depression in adolescents: sleep and HPA measures. Neuropsychopharmacology 34, 19361945.CrossRefGoogle ScholarPubMed
Rosmalen, JGM, Oldehinkel, AJ (2011). The role of group dynamics in scientific inconsistencies: a case study of a research consortium. PLoS Medicine 8, e1001143.CrossRefGoogle ScholarPubMed
Sapolsky, R, Romero, L, Munck, A (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 5589.Google ScholarPubMed
Scheurink, A, Ammar, A, Benthem, B, van Dijk, G, Sodersten, P (1999). Exercise and the regulation of energy intake. International Journal of Obesity 23, S1S6.CrossRefGoogle ScholarPubMed
Sondeijker, FEPL, Ferdinand, RF, Oldehinkel, AJ, Tiemeier, H, Ormel, J, Verhulst, FC (2008). HPA-axis activity as a predictor of future disruptive behaviors in young adolescents. Psychophysiology 45, 398404.CrossRefGoogle ScholarPubMed
Timmermans, M, van Lier, PAC, Koot, HM (2010). The role of stressful events in the development of behavioural and emotional problems from early childhood to late adolescence. Psychological Medicine 40, 16591668.CrossRefGoogle ScholarPubMed
Vrshek-Schallhorn, S, Doane, LD, Mineka, S, Zinbarg, RE, Craske, MG, Adam, EK (2013). The cortisol awakening response predicts major depression: predictive stability over a 4-year follow-up and effect of depression history. Psychological Medicine 43, 483493.CrossRefGoogle Scholar
Young, E, Abelson, J, Cameron, O (2004). Effect of comorbid anxiety disorders on the hypothalamic-pituitary-adrenal axis response to a social stressor in major depression. Biological Psychiatry 56, 113120.CrossRefGoogle ScholarPubMed