Skip to main content

Advertisement

Log in

Neuroendocrine Response to School Load in Prepubertal Children: Focus on Trait Anxiety

  • Original Research
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

At the time of school-age, the most frequent stress stimuli are related to school environment and educational process. Anxiety may play a big role in coping with stressful situations associated with school load. To approach this issue, we performed a real-life study at school during the classwork. The sample consisted of 36 healthy children aged 10 years, which were divided to low and high trait anxiety group based on the median value of the anxiety score. The investigations were carried out in the classroom during a stress condition (final exams) and non-stress condition (without any exam). In the whole sample, the condition with exam was associated with higher cortisol and lower testosterone concentrations in saliva compared to the condition without exam. The activity of salivary alpha-amylase increased at the end of the exam. Anxious children showed higher concentrations of aldosterone and lower activity of alpha-amylase compared to children with low trait anxiety. Cortisol levels were higher in anxious children in the first morning samples before starting the lessons. Children with high and low trait anxiety did not differ in extraversion, neuroticism, as well as non-verbal intelligence and school success. Thus, the anxious children at school showed a more rapid decrease of anticipatory stress-induced cortisol concentrations, higher aldosterone levels, and lower alpha-amylase activities compared to non-anxious children. These changes, particularly high concentrations of aldosterone in children with high trait anxiety, may have an impact on their psychophysiological development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abelson JL, Khan S, Liberzon I, Young EA (2007) HPA axis activity in patients with panic disorder: review and synthesis of four studies. Depress Anxiety 24:66–76

    Article  PubMed  Google Scholar 

  • Ali N, Pruessner JC (2012) The salivary alpha amylase over cortisol ratio as a marker to assess dysregulations of the stress systems. Physiol Behav 106:65–72

    Article  CAS  PubMed  Google Scholar 

  • Benjamin CL, Harrison JP, Settipani CA, Brodman DM, Kendall PC (2013) Anxiety and related outcomes in young adults 7 to 19 years after receiving treatment for child anxiety. J Consult Clin Psychol 81:865–876

    Article  PubMed  Google Scholar 

  • Bittner A, Goodwin RD, Wittchen HU, Beesdo K, Höfler M, Lieb R (2014) What characteristics of primary anxiety disorders predict subsequent major depressive disorder? J Clin Psychiatry 65:618–626

    Article  Google Scholar 

  • Brosschot JF, Gerin W, Thayer JF (2006) The perseverative cognition hypothesis: a review of worry, prolonged stress-related physiological activation, and health. J Psychosom Res 60:113–124

    Article  PubMed  Google Scholar 

  • Büttner M, Jezova D, Greene B, Konrad C, Kircher T, Murck H (2015) Target-based biomarker selection—mineralocorticoid receptor-related biomarkers and treatment outcome in major depression. J Psych Res 66–67:24–37

    Article  Google Scholar 

  • Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381

    Article  CAS  PubMed  Google Scholar 

  • Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267:1244–1252

    Article  CAS  PubMed  Google Scholar 

  • Costello EJ, Mustillo S, Erkanli A, Keeler G, Angold A (2003) Prevalence and development of psychiatric disorders in childhood and adolescence. Arch Gen Psychiatry 60:837–844

    Article  PubMed  Google Scholar 

  • Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130:355–391

    Article  PubMed  Google Scholar 

  • 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 38:1281–1298

    Article  CAS  PubMed  Google Scholar 

  • Eysenck HJ, Eysenck SBG (1994) Eysenck personality questionnaire for children (Slovak version). Psychodiagnostika, Bratislava

    Google Scholar 

  • Feder A, Coplan JD, Goetz RR, Mathew SJ, Pine DS, Dahl RE, Ryan ND, Greenwald S, Weissman MM (2004) Twenty-four-hour cortisol secretion patterns in prepubertal children with anxiety or depressive disorders. Biol Psychiatry 56:198–204

    Article  CAS  PubMed  Google Scholar 

  • Ferjencik J (1985) Raven’s Coloured Progressive matrices (Slovak version). Manual. Psychodiagnostic and didactic tests, Bratislava

    Google Scholar 

  • Forbes EE, Williamson DE, Ryan ND, Birmaher B, Axelson DA, Dahl RE (2006) Peri-sleep-onset cortisol levels in chil-dren and adolescents with affective disorders. Biol Psychiatry 59:24–30

    Article  CAS  PubMed  Google Scholar 

  • Gerra G, Zaimovic A, Zambelli U, Timpano M, Reali N, Bernasconi S, Brambilla FC (2000) Neuroendocrine responses to psychological stress in adolescents with anxiety disorder. Neuropsychobiology 42:82–92

    Article  CAS  PubMed  Google Scholar 

  • Granger DA, Kivlighan KT, El-Sheikh M, Bordis EB, Stroud LR (2007) Salivary alpha-amylase in bio-behavioral research. Recent developments and applications. Ann NY Acad Sci 1098:122–144

    Article  CAS  PubMed  Google Scholar 

  • Greaves-Lord K, Ferdinand RF, Oldehinkel AJ, Sondeijker FE, Ormel J, Verhulst FC (2007) Higher cortisol awakening response in young adolescents with persistent anxiety problems. Acta Psychiatr Scand 116:137–144

    Article  CAS  PubMed  Google Scholar 

  • Häfner S, Baumert J, Emeny RT, Lacruz ME, Bidlingmaier M, Reincke M, Kuenzel H, Holle R, Rupprecht R, Ladwig KH, MONICA/KORA Study Investigators (2012) To live alone and to be depressed, an alarming combination for the renin-angiotensin-aldosterone system (RAAS). Psychoneuroendocrinology 37:230–237

    Article  PubMed  Google Scholar 

  • Harl B, Weisshuhn S, Kerschbaum HH (2006) Cortisol titre increases with novelty of academic oral examinations. Neuro Endocrinol Lett 27:669–674

    CAS  PubMed  Google Scholar 

  • Heim C, Nemeroff CB (2002) Neurobiology of early life stress: clinical studies. Semin Clin Neuropsychiatry 7:147–159

    Article  PubMed  Google Scholar 

  • Hlavacova N, Jezova D (2008a) Chronic treatment with the mineralocorticoid hormone aldosterone results in increased anxiety-like behavior. Horm Behav 54:90–97

    Article  CAS  PubMed  Google Scholar 

  • Hlavacova N, Jezova D (2008b) Effect of single treatment with the antihypertensive drug eplerenone on hormone levels and anxiety-like behaviour in rats. Endocr Regul 42:147–153

    CAS  PubMed  Google Scholar 

  • Hlavacova N, Bakos J, Jezova D (2010) Eplerenone, a selective mineralocorticoid receptor blocker, exerts anxiolytic effects accompanied by changes in stress hormone release. J Psychopharmacol 24:779–786

    Article  CAS  PubMed  Google Scholar 

  • Hlavacova N, Wes PD, Ondrejcakova M, Flynn ME, Poundstone PK, Babic S, Murck H, Jezova D (2012) Subchronic treatment with aldosterone induces depression-like behaviours and gene expression changes relevant to major depressive disorder. Int J Neuropsychopharmacol 15:247–265

    Article  CAS  PubMed  Google Scholar 

  • Hlavacova N, Kerlik J, Radikova Z, Izakova L, Jezova D (2013) Measurement of salivary aldosterone: validation by low-dose ACTH test and gender differences. Endocr Regul 47:201–204

    Article  CAS  PubMed  Google Scholar 

  • Hlavacova N, Solarikova P, Marko M, Brezina I, Jezova D (2017) Blunted cortisol response to psychosocial stress in atopic patients is associated with decrease in salivary alpha-amylase and aldosterone: focus on sex and menstrual cycle phase. Psychoneuroendocrinology 78:31–38

    Article  CAS  PubMed  Google Scholar 

  • Jezova D, Hlavacova N (2008) Endocrine factors in stress and psychiatric disorders: focus on anxiety and salivary steroids. Ann NY Acad Sci 1148:495–503

    Article  CAS  PubMed  Google Scholar 

  • Jezova D, Vigas M (1988) Apomorphine injection stimulates beta-endorphin, adrenocorticotropin, and cortisol release in healthy man. Psychoneuroendocrinology 13:479–485

    Article  CAS  PubMed  Google Scholar 

  • Jezova D, Vigas M, Tatar P, Kvetnansky R, Nazar K, Kaciuba-Uścilko H, Kozlowski S (1985) Plasma testosterone and catecholamine responses to physical exercise of different intensities in men. Eur J Appl Physiol 54:62–66

    Article  CAS  Google Scholar 

  • Jezova D, Jurankova E, Mosnarova A, Kriska M, Skultetyova I (1996) Neuroendocrino response during stress with relation to gender differences. Acta Neurobiol Exp 56:779–785

    CAS  Google Scholar 

  • Jezova D, Hlavacova N, Dicko I, Solarikova P, Brezina I (2016) Psychosocial stress based on public speech in humans: is there a real life/laboratory setting cross-adaptation? Stress 19:429–433

    Article  CAS  PubMed  Google Scholar 

  • Kallen VL, Tulen JH, Utens EM, Treffers PD, De Jong FH, Ferdinand RF (2008) Associations between HPA axis functioning and level of anxiety in children and adolescents with an anxiety disorder. Depress Anxiety 25:131–141

    Article  CAS  PubMed  Google Scholar 

  • Kendall PC, Safford S, Flannery-Schroeder E, Webb A (2004) Child anxiety treatment: outcomes in adolescence and impact on substance use and depression at 7.4 year follow-up. J Consult Clin Psychol 72:276–287

    Article  PubMed  Google Scholar 

  • Kondas O (1973) KSAT—Scale of classic fear, social-situational anxiety and stage-fright (in Slovak). Psychodiagnostic and didactic tests, Bratislava

    Google Scholar 

  • Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kirschbaum C (2004) Differential heart rate reactivity and recovery after psychosocial stress (TSST) in healthy children, younger adults, and elderly adults: the impact of age and gender. Int J Behav Med 11:116–121

    Article  PubMed  Google Scholar 

  • Mogotsi M, Kaminer D, Stein DJ (2000) Quality of life in anxiety disorders. Harv Rev Psychiatry 8:273–282

    Article  CAS  PubMed  Google Scholar 

  • Nater UM, Rohleder N, Gaab J, Berger S, Jud A, Kirschbaum C, Ehlert U (2005) Human salivary alphaamylase reactivity in a psychosocial stress paradigm. Int J Psychophysiol 55:333–342

    Article  PubMed  Google Scholar 

  • Nater UM, La Marca R, Florin L, Moses A, Langhans W, Koller MM, Ehlert U (2006) Stress-induced changes in human salivary alpha-amylase activity-associations with adrenergic activity. Psychoneuroendocrinology 31:49–58

    Article  CAS  PubMed  Google Scholar 

  • Nelemans SA, Hale WW, Branje SJT, Jansen L, Platje E (2014) Persistent heightened cortisol awakening response and adolescent internalizing symptoms: a 3 year Longitudinal Community Study. J Abnorm Child Psychol 42:767–777

    Article  PubMed  Google Scholar 

  • Ostatnikova D, Celec P, Putz Z, Hodosy J, Schmidt F, Laznibatova J, Kudela M (2007) Intelligence and salivary testosterone levels in prepubertal children. Neuropsychologia 45:378–385

    Article  Google Scholar 

  • Payne LA, Hibel LC, Granger DA, Tsao JCI, Zeltzer LK (2014) Relationship of salivary alpha amylase and cortisol to social anxiety in healthy children undergoing laboratory pain tasks. J Child Adolesc Psychopharmacol. doi:10.4172/2375-4494.1000129

    Google Scholar 

  • Quaiser-Pohl C, Jansen P, Lehmann J, Kudielka BM (2016) Is there a relationship between the performance in a chronometric mental-rotations test and salivary testosterone and estradiol levels in children aged 9–14 years? Dev Psychobiol 58:120–128

    Article  CAS  PubMed  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. Biol Psychiatry 64:521–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Repcekova D, Mikulaj L (1977) Plasma testosterone of rats subjected to immobilization stress and/or HCG administration. Horm Res 8:51–57

    Article  CAS  PubMed  Google Scholar 

  • Sevcikova L, Liska J, Arochova O (1984) Response of pupils to a mental load at school in relation to their personality characteristics (in Slovak). Ceskoslovenska Hygiene 29:527–534

    Google Scholar 

  • Skoluda N, Strahler J, Schlotz W, Niederberger L, Marques S, Fischer S, Thma MW, Spoerri C, Ehlert U, Nater UM (2015) Intra-individual psychological and physiological responses to acute laboratory stressors of different intensity. Psychoneuroendocrinology 51:227–236

    Article  PubMed  Google Scholar 

  • Stein MB, Walker JR, Forde DR (1996) Public speaking fears in a community sample: prevalence, impact on functioning, and diagnostic classification. Arch Gen Psychiatry 53:169–174

    Article  CAS  PubMed  Google Scholar 

  • Tauler P, Martinez S, Moreno C, Martínez P, Aguilo A (2014) Changes in salivary hormones, immunoglobulin A, and C-reactive protein in response to ultra-endurance exercises. Appl Physiol Nutr Metab 39:560–565

    Article  CAS  PubMed  Google Scholar 

  • Van Ameringen M, Mancini C, Farvolden P (2003) The impact of anxiety disorders on educational achievement. J Anxiety Disord 17:561–571

    Article  PubMed  Google Scholar 

  • Varga J, Ferenczi S, Kovács KJ, Garafova A, Jezova D, Zelena D (2013) Comparison of stress-induced changes in adults and pups: is aldosterone the main adrenocortical stress hormone during the perinatal period in rats? PLoS One 8:e72313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf JM, Nicholls E, Chen E (2008) Chronic stress, salivary cortisol, and alpha-amylase in children with asthma and healthy children. Biol Psychol 78:20–28

    Article  PubMed  Google Scholar 

  • Yim IS, Granger DA, Quas JA (2010) Children’s and adults’ salivary alpha-amylaseresponses to a laboratory stressor and to verbal recall of the stressor. Dev Psychobiol 52:598–602

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by grants of Slovak Research and Development Agency under the Contract Nos. APVV-14-0840 and APVV-15-0063.

Author information

Authors and Affiliations

Authors

Contributions

D. K. performed the examinations of the subjects, completed psychological analyses and wrote the draft of the manuscript. N. H. undertook the statistical analysis, participated on biochemical analyses and wrote the draft of the manuscript. D. V. and L. A. performed the examinations of the subjects. L. S. designed the study and wrote the protocol. D. J. performed general supervision, interpreted the results and wrote the manuscript. All authors have approved the final manuscript.

Corresponding author

Correspondence to Daniela Jezova.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kapsdorfer, D., Hlavacova, N., Vondrova, D. et al. Neuroendocrine Response to School Load in Prepubertal Children: Focus on Trait Anxiety. Cell Mol Neurobiol 38, 155–162 (2018). https://doi.org/10.1007/s10571-017-0544-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-017-0544-7

Keywords

Navigation