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European Child & Adolescent Psychiatry

, Volume 26, Issue 12, pp 1501–1510 | Cite as

Impaired cardiac profile in adolescents with an increasing trajectory of anxiety when confronting an acute stressor

  • Alejandro de la Torre-Luque
  • Aina Fiol-Veny
  • Xavier Bornas
  • Maria Balle
  • Jordi Llabres
Original Contribution

Abstract

Maladaptive patterns of cardiac adjustment to stress in adolescents may reveal their vulnerability to anxiety disorders (ADs). Traditional research in this field has focused on anxiety levels, whereas the time course of anxiety has rarely been considered. Nevertheless, since overall anxiety decreases as adolescence progresses, increasing time courses are clinically relevant and can be associated with maladaptive contextual adjustment. In this study, the cardiac pattern of adjustment to stress in adolescents with increasing anxiety was analysed. A sample of 44 adolescents (M = 14.88 years, SD = 0.53, 45.45% boys) were exposed to a socially relevant stress induction protocol, and their cardiac functioning was recorded. Participants with a trajectory of increasing anxious symptomatology over a 12-month period (n = 24) showed attenuated heart rate levels in the stage of maximum stress in comparison to their non-increasing anxious counterparts (p < 0.05), as well as a heightened pattern of sample entropy throughout the stress induction (p < 0.05). These findings suggest a loss of cardiac flexibility in those adolescents at risk of ADs when confronting an acute stressor.

Keywords

Anxiety Trajectory Stress Heart rate variability Adolescence 

Notes

Compliance with ethical standards

Funding

This study was supported by the Spanish Ministry of Economy and Competitiveness Grant Ref. PSI2012-34780.

Conflict of interest

The authors of this manuscript declare that they have no conflict of interest.

References

  1. 1.
    Gunnar MR, Wewerka S, Frenn K, Long JD, Griggs C (2009) Developmental changes in hypothalamus–pituitary–adrenal activity over the transition to adolescence: normative changes and associations with puberty. Dev Psychopathol 21:69–85. doi: 10.1017/S0954579409000054 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Skinner EA, Zimmer-Gembeck MJ (2007) The development of coping. Ann Rev Psychol 58:119–144. doi: 10.1146/annurev.psych.58.110405.085705 CrossRefGoogle Scholar
  3. 3.
    Hollenstein T, Lougheed JP (2013) Beyond storm and stress: typicality, transactions, timing, and temperament to account for adolescent change. Am Psychol 68:444–454. doi: 10.1037/a0033586 CrossRefPubMedGoogle Scholar
  4. 4.
    Essau CA, Gabbidon J (2013) Epidemiology, comorbidity and mental health services utilization. In: Essau CA, Ollendick TH (eds) The treatment of childhood and adolescent anxiety. Wiley, Oxford, pp 23–42Google Scholar
  5. 5.
    Essau CA, Lewinsohn PM, Olaya B, Seeley JR (2014) Anxiety disorders in adolescents and psychosocial outcomes at age 30. J Affect Disord 163:125–132. doi: 10.1016/j.jad.2013.12.033 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Gustafsson PE, Gustafsson PA, Ivarsson T, Nelson N (2008) Diurnal cortisol levels and cortisol response in youths with obsessive-compulsive disorder. Neuropsychobiology 57:14–21. doi: 10.1159/000123117 CrossRefPubMedGoogle Scholar
  7. 7.
    Schmitz J, Kramer M, Tuschen-Caffier B, Heinrichs N, Blechert J (2011) Restricted autonomic flexibility in children with social phobia. J Child Psychol Psychiatry 52:1203–1211. doi: 10.1111/j.1469-7610.2011.02417.x CrossRefPubMedGoogle Scholar
  8. 8.
    Lyons MD, Huebner ES, Hills KJ (2016) Relations among personality characteristics, environmental events, coping behavior and adolescents’ life satisfaction. J Happiness Stud 17:1033–1050. doi: 10.1007/s10902-015-9630-z CrossRefGoogle Scholar
  9. 9.
    Valiente C, Eisenberg N, Fabes RA, Spinrad TL, Sulik MJ (2014) Coping across the transition to adolescence: evidence of interindividual consistency and mean-level change. J Early Adolesc 35:947–965. doi: 10.1177/0272431614548068 CrossRefGoogle Scholar
  10. 10.
    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. Neurosci Biobehav Rev 38:94–124. doi: 10.1016/j.neubiorev.2013.11.005 CrossRefPubMedGoogle Scholar
  11. 11.
    Mateo M, Blasco-Lafarga C, Martinez-Navarro I, Guzman JF, Zabala M (2012) Heart rate variability and pre-competitive anxiety in BMX discipline. Eur J Appl Physiol 112:113–123. doi: 10.1007/s00421-011-1962-8 CrossRefPubMedGoogle Scholar
  12. 12.
    Vuksanovic V, Gal V (2007) Heart rate variability in mental stress aloud. Med Eng Phys 29:344–349. doi: 10.1016/j.medengphy.2006.05.011 CrossRefPubMedGoogle Scholar
  13. 13.
    Kramer M, Seefeldt WL, Heinrichs N, Tuschen-Caffier B, Schmitz J, Wolf OT, Blechert J (2012) Subjective, autonomic, and endocrine reactivity during social stress in children with social phobia. J Abnorm Child Psychol 40:95–104. doi: 10.1007/s10802-011-9548-9 CrossRefPubMedGoogle Scholar
  14. 14.
    Klumbies E, Braeuer D, Hoyer J, Kirschbaum C (2014) The reaction to social stress in social phobia: discordance between physiological and subjective parameters. PLoS One 9:e105670. doi: 10.1371/journal.pone.0105670 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bornas X, Riera A, Tortella-Feliu M, Llabres J (2012) Heart rate variability profiles and exposure therapy treatment outcome in flight phobia. Appl Psychophysiol Bioofeedback 37:53–62. doi: 10.1007/s10484-011-9179-5 CrossRefGoogle Scholar
  16. 16.
    Siess J, Blechert J, Schmitz J (2013) Psychophysiological arousal and biased perception of bodily anxiety symptoms in socially anxious children and adolescents: a systematic review. Eur Child Adolesc Psychiatry 23:127–142. doi: 10.1007/s00787-013-0443-5 CrossRefPubMedGoogle Scholar
  17. 17.
    Chatkoff DK, Maier KJ, Klein C (2010) Nonlinear associations between chronic stress and cardiovascular reactivity and recovery. Int J Psychophysiol 77:150–156. doi: 10.1016/j.ijpsycho.2010.05.008 CrossRefPubMedGoogle Scholar
  18. 18.
    Chida Y, Hamer M (2008) Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: a quantitative review of 30 years of investigations. Psychol Bull 134:829–885. doi: 10.1037/a0013342 CrossRefPubMedGoogle Scholar
  19. 19.
    Duncko R, Makatsori A, Fickova E, Selko D, Jezova D (2006) Altered coordination of the neuroendocrine response during psychosocial stress in subjects with high trait anxiety. Prog Neuropsychopharmacol Biol Psychiatry 30:1058–1066. doi: 10.1016/j.pnpbp.2006.04.002 CrossRefPubMedGoogle Scholar
  20. 20.
    Schmitz J, Ruschen-Caffier B, Wilhelm FH, Blechert J (2013) Taking a closer look: autonomic dysregulation in socially anxious children. Eur Child Adolesc Psychiatry 22:631–640. doi: 10.1007/s00787-013-0405-y CrossRefPubMedGoogle Scholar
  21. 21.
    Beauchaine TP, Thayer JF (2015) Heart rate variability as a transdiagnostic biomarker of psychopathology. Int J Psychophysiol 98:338–350. doi: 10.1016/j.ijpsycho.2015.08.004 CrossRefPubMedGoogle Scholar
  22. 22.
    Cavanagh JF, Allen JJB (2008) Multiple aspects of the stress response under social evaluative threat: an electrophysiological investigation. Psychoneuroendocrinol 33:41–53CrossRefGoogle Scholar
  23. 23.
    Gunnar M, Quevedo K (2007) The neurobiology of stress and development. Ann Rev Psychol 58:145–173. doi: 10.1146/annurev.psych.58.110405.085605 CrossRefGoogle Scholar
  24. 24.
    Talge NN, Donzella B, Gunnar MR (2008) Fearful temperament and stress reactivity among preschool-aged children. Infant Child Dev 17:427–445. doi: 10.1002/icd.585 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Miers AC, Blote AW, de Rooij M, Bolhorst CL, Westenberg PM (2013) Trajectories of social anxiety during adolescence and relations with cognition, social competence, and temperament. J Abnorm Child Psychol 41:97–110. doi: 10.1007/s10802-012-9651-6 CrossRefPubMedGoogle Scholar
  26. 26.
    Insel T (2014) The NIMH Research Domain Criteria (RDoC) project: precision medicine for psychiatry. Am J Psychiatry 171:395–397. doi: 10.1176/appi.ajp.2014.14020138 CrossRefPubMedGoogle Scholar
  27. 27.
    Insel T, Cuthbert B, Heinssen R et al (2010) Research Domain Criteria (RDoC): toward a new classification framework for research on m ental disorders. Am J Psychiatry 167:748–751. doi: 10.1176/appi.ajp.2010.09091379 CrossRefPubMedGoogle Scholar
  28. 28.
    Okasha A (2009) Would the use of dimensions instead of categories remove problems related to subthreshold disorders? Eur Arch Psychiatry Clin Neurosci 259:S129–S133. doi: 10.1007/s00406-009-0052-y CrossRefPubMedGoogle Scholar
  29. 29.
    Shankman SA, Klein DN, Lewinsohn PM, Seeley JR, Small JW (2008) Family study of subthreshold psychopathology in a community sample. Psychol Med 38:187–198. doi: 10.1111/j.1469-7610.2009.02117.x CrossRefPubMedGoogle Scholar
  30. 30.
    Hale WW III, Raaijmakers Q, Muris P, van Hoof A, Meeus W (2008) Developmental trajectories of adolescent anxiety disorder symptoms: a 5-year prospective community study. J Am Acad Child Adolesc Psychiatry 47:556–564. doi: 10.1097/CHI.0b013e3181676583 CrossRefPubMedGoogle Scholar
  31. 31.
    Sportel BE, Nauta MH, de Hullu E, de Jong PJ, Hartman CA (2011) Behavioral inhibition and attentional control in adolescents: robust relationships with anxiety and depression. J Child Fam Stud 20:149–156. doi: 10.1007/s10826-010-9435-y CrossRefPubMedGoogle Scholar
  32. 32.
    McLaughlin KA, King K (2015) Developmental trajectories of anxiety and depression in early adolescence. J Abnorm Child Psychol 43:311–323. doi: 10.1007/s10802-014-9898-1 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Morin AJS, Maiano C, Nagensgast B, Marsh HW, Morizot J, Janosz M (2011) General growth mixture analysis of adolescents’ developmental trajectories of anxiety: the impact of untested invariance assumptions on substantive interpretations. Struct Equ Modeling 18:613–648. doi: 10.1080/10705511.2011.607714 CrossRefGoogle Scholar
  34. 34.
    Shankman SA, Lewinsohn PM, Klein DN, Small JW, Seeley JR, Altman SE (2009) Subthreshold conditions as precursors for full syndrome disorders: a 15-year longitudinal study of multiple diagnostic classes. J Child Psychol Psychiatry 50:1485–1494. doi: 10.1111/j.1469-7610.2009.02117.x CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191. doi: 10.3758/BF03193146 CrossRefPubMedGoogle Scholar
  36. 36.
    Bornas X, Llabres J, Balle M, de la Torre-Luque A, Fiol-Veny A (2014) The use of a secure social network for the study of anxiety in adolescence. Revista Psicopatologia Psicologia Clinica 19:171–184. doi: 10.5944/rppc.vol.19.num.3.2014.13899 CrossRefGoogle Scholar
  37. 37.
    Ellis LK, Rothbart MK (2001) Revision of the Early Adolescent Temperament Questionnaire. Poster session presented at the Biennial Meeting of the Society for Research in Child Development, MinneapolisGoogle Scholar
  38. 38.
    Rothbart MK (2007) Temperament, development, and personality. Curr Dir Psychol Sci 16:207–212. doi: 10.1111/j.1467-8721.2007.00505.x CrossRefGoogle Scholar
  39. 39.
    Rapee RM, Coplan RJ (2010) Conceptual relations between anxiety disorder and fearful temperament. New Dir Child Adolesc Dev 127:17–31. doi: 10.1002/cd.260 CrossRefGoogle Scholar
  40. 40.
    Chorpita BF, Yim L, Moffitt C, Umemoto LA, Francis SE (2000) Assessment of symptoms of DSM-IV anxiety and depression in children: a revised child anxiety and depression scale. Behav Res Ther 38:835–855. doi: 10.1016/S0005-7967(99)00130-8 CrossRefPubMedGoogle Scholar
  41. 41.
    Sheehan DV, Lecrubier Y, Harnett-Sheehan K et al (1998) The mini international neuropsychiatric interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview. J Clin Psychiatry 59:22–33PubMedGoogle Scholar
  42. 42.
    Camm AJ, Malik M, Bigger JT Jr et al (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17:354–381CrossRefGoogle Scholar
  43. 43.
    Peng CK, Havlin S, Stanley HE, Goldberger AL (1995) Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82–87CrossRefPubMedGoogle Scholar
  44. 44.
    Richman JA, Moorman JR (2000) Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol 278:H2039–H2049PubMedGoogle Scholar
  45. 45.
    Von Dawans B, Kirschbaum C, Heinrichs M (2011) The Trier Social Stress Test for Groups (TSST-G): a new research tool for controlled simultaneous social stress exposure in a group format. Psychoneuroendocrinol 36:514–522. doi: 10.1016/j.psyneuen.2010.08.004 CrossRefGoogle Scholar
  46. 46.
    Kirschbaum C (2010) Trier social stress test. In: Stolerman IP (ed) Encyclopedia of Psychopharmacology (chapter ID: 0001093214). Springer-Verlag, BerlinGoogle Scholar
  47. 47.
    Tarvainen M, Niskanen J, Lipponen JA, Ranta-aho PO, Karjalainen PA (2014) Kubios HRV-heart rate variability analysis software. Comput Methods Programs Biomed 113:210–220CrossRefPubMedGoogle Scholar
  48. 48.
    Young H, Benton D (2015) We should be using nonlinear indices when relating heart-rate dynamics to cognition and mood. Sci Rep 5:16619. doi: 10.1038/srep16619 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Billman GE (2013) The effect of heart rate on the heart rate variability response to autonomic interventions. Front Physiol 4:222. doi: 10.3389/fphys.2013.00222 PubMedPubMedCentralGoogle Scholar
  50. 50.
    Sacha J (2013) Why should one normalize heart rate variability with respect to average heart rate. Front Physiol 4:306. doi: 10.3389/fphys.2013.00306 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Senn S (2006) Change from baseline and analysis of covariance revisited. Stat Med 25:4334–4344. doi: 10.1002/sim.2682 CrossRefPubMedGoogle Scholar
  52. 52.
    Hollenstein T, Lichtwarck-Aschoff A, Potworowski G (2013) A model of socioemotional flexibility at three time scales. Emot Rev 5:397–405. doi: 10.1177/1754073913484181 CrossRefGoogle Scholar
  53. 53.
    Thayer JF, Ahs F, Fredrikson M, Sollers JJ III, Wager TD (2012) A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 36:747–756. doi: 10.1016/j.neubiorev.2011.11.009 CrossRefPubMedGoogle Scholar
  54. 54.
    Anderson ER, Hope DA (2009) The relationship among social phobia, objective and perceived physiological reactivity, and anxiety sensitivity in an adolescent population. J Anxiety Disord 23:18–26. doi: 10.1016/j.janxdis.2008.03.011 CrossRefPubMedGoogle Scholar
  55. 55.
    Bornas X (2016) Mesures quantitatives de la complexitat (quantitative measures of complexity). Psicopatologia i caos (Psychopatology and chaos), 2nd edn. Bubok, Madrid, pp 127–152Google Scholar
  56. 56.
    Friedman BH (2007) An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biol Psychol 74:185–199. doi: 10.1016/j.biopsycho.2005.08.009 CrossRefPubMedGoogle Scholar
  57. 57.
    De la Torre-Luque A, Caparros-Gonzalez RA, Bastard T, Vico FJ, Buela-Casal G (2016) Acute stress recovery through listening to Melomics relaxing music: a randomized controlled trial. Nord J Music Ther. doi: 10.1080/08098131.2015.1131186 Google Scholar
  58. 58.
    Williamon A, Aufegger L, Wasley D, Looney D, Mandic DP (2013) Complexity of physiological responses decreases in high-stress musical performance. J R Soc Interface 10:20130719. doi: 10.1098/rsif.2013.0719 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Porta A, Gnecchi-Ruscone T, Tobaldini E, Guzzetti S, Furlan R, Montano N (2007) Progressive decrease of heart period variability entropy-based complexity during graded head-up tilt. J Appl Physiol 103:1143–1149. doi: 10.1152/japplphysiol.00293.2007 CrossRefPubMedGoogle Scholar
  60. 60.
    Porta A, Guzzetti S, Furlan R, Gnecchi-Ruscone T, Montano N, Malliani A (2007) Complexity and non linearity in short-term heart period variability: comparison of methods based on local non linear prediction. IEEE Trans Biomed Eng 54:94–106. doi: 10.1109/TBME.2006.883789 CrossRefPubMedGoogle Scholar
  61. 61.
    De la Torre-Luque A, Fiol-Veny A, Balle M, Bornas X (2016) Heartbeat scaling in early adolescents: its association with anxiety symptoms and sensitivity to punishment. Int J Clin Health Psychol 16:287–294. doi: 10.1016/j.ijchp.2016.04.002 CrossRefGoogle Scholar
  62. 62.
    De la Torre-Luque A, Bornas X, Balle M, Fiol-Veny A (2016) Complexity and nonlinear biomarkers in emotional disorders: a meta-analytic study. Neurosci Biobehav Rev 68:410–422. doi: 10.1016/j.neubiorev.2016.05.023 CrossRefPubMedGoogle Scholar
  63. 63.
    Chu BC (2012) Translating transdiagnostic approaches to children and adolescents. Cogn Behav Pract 19:1–4. doi: 10.1016/j.cbpra.2011.06.003 CrossRefGoogle Scholar
  64. 64.
    Essau CA, Olaya B, Sasagawa S, Pithia J, Bray D, Ollendick TH (2014) Integrating video-feedback and cognitive preparation, social skills training and behavioural activation in a cognitive behavioural therapy in the treatment of childhood anxiety. J Affect Disord 167:261–267. doi: 10.1016/j.jad.2014.05.056 CrossRefPubMedGoogle Scholar
  65. 65.
    Lehrer PM, Gevirtz R (2014) Heart rate variability biofeedback: how and why does it work? Front Psychol 5:PMC4104929. doi: 10.3389/fpsyg.2014.00756 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Research Institute of Health Sciences, Scientific-Technical Services and University Research InstitutesUniversity of Balearic IslandsPalmaSpain

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