Top

Published in:

01-12-2017 | Original Contribution

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

Authors: Alejandro de la Torre-Luque, Aina Fiol-Veny, Xavier Bornas, Maria Balle, Jordi Llabres

Published in: European Child & Adolescent Psychiatry | Issue 12/2017

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.

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 CrossRefPubMedPubMedCentral

Skinner EA, Zimmer-Gembeck MJ (2007) The development of coping. Ann Rev Psychol 58:119–144. doi:10.1146/annurev.psych.58.110405.085705 CrossRef

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 CrossRefPubMed

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 23–42

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRef

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

22.

Cavanagh JF, Allen JJB (2008) Multiple aspects of the stress response under social evaluative threat: an electrophysiological investigation. Psychoneuroendocrinol 33:41–53CrossRef

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 CrossRef

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRef

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRef

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, Minneapolis

38.

Rothbart MK (2007) Temperament, development, and personality. Curr Dir Psychol Sci 16:207–212. doi:10.1111/j.1467-8721.2007.00505.x CrossRef

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 CrossRef

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 CrossRefPubMed

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 59:22–33PubMed

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 17:354–381CrossRef

43.

Peng CK, Havlin S, Stanley HE, Goldberger AL (1995) Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82–87CrossRefPubMed

44.

Richman JA, Moorman JR (2000) Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol 278:H2039–H2049PubMed

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 CrossRef

46.

Kirschbaum C (2010) Trier social stress test. In: Stolerman IP (ed) Encyclopedia of Psychopharmacology (chapter ID: 0001093214). Springer-Verlag, Berlin

47.

Tarvainen M, Niskanen J, Lipponen JA, Ranta-aho PO, Karjalainen PA (2014) Kubios HRV-heart rate variability analysis software. Comput Methods Programs Biomed 113:210–220CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 PubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

51.

Senn S (2006) Change from baseline and analysis of covariance revisited. Stat Med 25:4334–4344. doi:10.1002/sim.2682 CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

55.

Bornas X (2016) Mesures quantitatives de la complexitat (quantitative measures of complexity). Psicopatologia i caos (Psychopatology and chaos), 2nd edn. Bubok, Madrid, pp 127–152

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 CrossRefPubMed

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

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRef

Title: Impaired cardiac profile in adolescents with an increasing trajectory of anxiety when confronting an acute stressor
Authors: Alejandro de la Torre-Luque
Aina Fiol-Veny
Xavier Bornas
Maria Balle
Jordi Llabres
Publication date: 01-12-2017
Publisher: Springer Berlin Heidelberg
Published in: European Child & Adolescent Psychiatry / Issue 12/2017
Print ISSN: 1018-8827
Electronic ISSN: 1435-165X
DOI: https://doi.org/10.1007/s00787-017-1009-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

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

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 12/2017

Mental health assessed by the Strengths and Difficulties Questionnaire for children born extremely preterm without severe disabilities at 11 years of age: a Norwegian, national population-based study

ECAP Editorial

NEET adolescents grown up: eight-year longitudinal follow-up of education, employment and mental health from adolescence to early adulthood in Mexico City

Stressful life events during adolescence and risk for externalizing and internalizing psychopathology: a meta-analysis

Comorbidity prevalence and treatment outcome in children and adolescents with ADHD

Changes in serum levels of kynurenine metabolites in paediatric patients affected by ADHD