Association of salivary steroid hormones and their ratios with time-domain heart rate variability indices in healthy individuals

Eglė Mazgelytė; Gintaras Chomentauskas; Edita Dereškevičiūtė; Virginija Rekienė; Audronė Jakaitienė; Tomas Petrėnas; Jurgita Songailienė; Algirdas Utkus; Zita Aušrelė Kučinskienė; Dovilė Karčiauskaitė

doi:10.5937/jomb0-26045

Eglė Mazgelytė Department of Physiology, Biochemistry, Microbiology, and Laboratory Medicine, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
Gintaras Chomentauskas Human Study Center, Vilnius, Lithuania
Edita Dereškevičiūtė Human Study Center, Vilnius, Lithuania
Virginija Rekienė Human Study Center, Vilnius, Lithuania
Audronė Jakaitienė Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
Tomas Petrėnas Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
Jurgita Songailienė Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
Algirdas Utkus Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
Zita Aušrelė Kučinskienė Department of Physiology, Biochemistry, Microbiology, and Laboratory Medicine, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania
Dovilė Karčiauskaitė Department of Physiology, Biochemistry, Microbiology, and Laboratory Medicine, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, Vilnius, Lithuania

DOI: https://doi.org/10.5937/jomb0-26045

Keywords: autonomic nervous system; heart rate variability; hypothalamic-pituitary-adrenal axis; steroid hormones; stress biomarkers.

Abstract

Backgound: Stress system consists of the hypothalamic-pituitary-adrenal (HPA) axis and the locus caeruleus/norepinephrine-autonomic nervous system (ANS). Traditionally, HPA axis activity is evaluated by measuring its end-product cortisol while the activity of ANS is assessed using heart rate variability (HRV) indices. Alterations in cortisol levels and HRV measures during laboratory-based stress tasks were extensively studied in previous research. However, scarce data exist on the associations of HRV measures with the levels of other adrenal steroid hormones under baseline conditions. Thus, we aimed to evaluate the activity of HPA axis by measuring salivary cortisol, cortisone, dehydroepiandrosterone (DHEA) levels and their ratios and to examine its association with HRV measures in a sample of healthy young and middle-aged adults.

Methods: For each participant (n=40), three data collection sessions taking place at the same time of the day were scheduled within five working days. Participants completed a self-reported questionnaire on sociodemographic and lifestyle characteristics, filled out Perceived Stress Scale and State-Trait Anxiety Inventory. Also, saliva samples were collected and physiological measures including resting HR and HRV were recorded during three data collection sessions.

Results: Statistically significant associations between diminished parasympathetic vagal tone evaluated by time-domain HRV measures and higher salivary cortisol, lower DHEA levels, as well as increased DHEA to cortisol ratio were found. Also, physiological stress indicators (i.e. HRV) showed greater intrindividual stability compared with biochemical biomarkers (i. e. salivary steroid hormones) within the period of five days.

Conclusions: Our findings suggest that both cortisol and DHEA mediate the link between two stress-sensitive homeostatic systems.

References

Pereira VH, Campos I, Sousa N. The role of autonomic nervous system in susceptibility and resilience to stress. Curr Opin Behav Sci. 2017;14:102–7. Available from: http://dx.doi.org/10.1016/j.cobeha.2017.01.003

Michels N, Sioen I, Clays E, de Buyzere M, Ahrens W, Huybrechts I, et al. Children’s heart rate variability as stress indicator: Association with reported stress and cortisol. Biol Psychol. 2013;94(2):433–40. Available from: http://dx.doi.org/10.1016/j.biopsycho.2013.08.005

Cool J, Zappetti D. The physiology of stress. In: Medical Student Well-Being. Springer, Cham; 2019.

Agorastos A, Heinig A, Stiedl O, Hager T, Sommer A, Müller JC, et al. Vagal effects of endocrine HPA axis challenges on resting autonomic activity assessed by heart rate variability measures in healthy humans. Psychoneuroendocrinology. 2019;102:196–203. Available from: https://doi.org/10.1016/j.psyneuen.2018.12.017

Lennartsson A-K, Kushnir MM, Bergquist J, Jonsdottir IH. DHEA and DHEA-S response to acute psychosocial stress in healthy men and women. Biol Psychol. 2012;90(2):143–9. Available from: http://dx.doi.org/10.1016/j.biopsycho.2012.03.003

Pulopulos MM, Vanderhasselt M-A, De Raedt R. Association between changes in heart rate variability during the anticipation of a stressful situation and the stress-induced cortisol response. Psychoneuroendocrinology. 2018;94:63–71. Available from: https://doi.org/10.1016/j.psyneuen.2018.05.004

Tripod L, Marca RLA, Waldvogel P, Tho H, Wirtz PH, Pruessner JC, et al. Association between cold face test-induced vagal inhibition and cortisol response to acute stress. Psychophysiology. 2011;48:420–9.

Heilman KJ, Bazhenova O V, Perlman SB, Hanley MC, Porges SW. Physiological responses to social and physical challenges in children: quantifying mechanisms supporting social engagement and mobilization behaviors. Dev Psychobiol. 2008;50(2):171–82.

Spielberger CD, Gorsuch R, Lushene R, Vagg P, Jacobs G. State-Trait Anxiety Inventory for Adults Manual. In Redwood City, CA: Mind Garden; 1983.

Adlan AM, van Zanten JJCSV, Lip GYH, Paton JFR, Kitas GD, Fisher JP. Acute hydrocortisone administration reduces cardiovagal baroreflex sensitivity and heart rate variability in young men. J Physiol. 2018;596(20):4847–61.

Pellissier S, Dantzer C, Mondillon L, Trocme C, Gauchez A-S, Ducros V, et al. Relationship between vagal tone, cortisol , TNF-alpha, epinephrine and negative affects in Crohn’s disease and irritable bowel syndrome. PLoS One. 2014;9(9):1–9.

Perna G, Riva A, Defillo A, Sangiorgio E, Nobile M, Caldirola D. Heart rate variability: Can it serve as a marker of mental health resilience? Special Section on “ Translational and Neuroscience Studies in Affective Disorders ” Section Editor, Maria Nobile. J Affect Disord. 2019; Available from: https://doi.org/10.1016/j.jad.2019.10.017

Thayer JF, Sternberg E. Beyond Heart Rate Variability. Vagal Regulation of Allostatic Systems. In: Neuroendocrine and Immune Crosstalk. 2006. p. 361–72.

Lemos MDP, Miranda MT, Marocolo M, Aparecida E, Rodrigues M, Chriguer S, et al. Low levels of dehydroepiandrosterone sulfate are associated with the risk of developing cardiac autonomic dysfunction in elderly subjects. Arch Endocrinol Metab. 2019;63(1):62–9.

Rydlewska A, Maj J, Katkowski B, Biel B, Ponikowska B, Banasiak W, et al. Circulating testosterone and estradiol, autonomic balance and baroreflex sensitivity in middle-aged and elderly men with heart failure. Aging Male. 2013;16(2):58–66.

Doğru TM, Başar MM, Yuvanç E, Şimşek V, Şahin Ö. The relationship between serum sex steroid levels and heart rate variability parameters in males and the effect of age. Arch Turk Soc Cardiol. 2010;38(7):459–65.

Kamin HS, Kertes DA. Hormones and Behavior Cortisol and DHEA in development and psychopathology. Horm Behav. 2017;89:69–85. Available from: http://dx.doi.org/10.1016/j.yhbeh.2016.11.018

Wranicz JK, Rosiak M, Cygankiewicz I, Kula P, Kula K, Zareba W. Sex steroids and heart rate variability in patients after myocardial Infarction. Ann Noninvasive Electrocardiol. 2004;9(2):156–61.

Wood P. Salivary steroid assays – research or routine ? Ann Clin Biochem. 2009;46(3):183–96.

La Marca-Ghaemmaghami P, La Marca R, Dainese SM, Haller M, Zimmermann R, Ehlert U. The association between perceived emotional support, maternal mood, salivary cortisol, salivary cortisone, and the ratio between the two compounds in response to acute stress in second trimester pregnant women. J Psychosom Res. 2013;75(4):314–20. Available from: http://dx.doi.org/10.1016/j.jpsychores.2013.08.010

Bakusic J, Nys S De, Creta M, Godderis L, Duca RC. Study of temporal variability of salivary cortisol and cortisone by LC-MS/MS using a new atmospheric pressure ionization source. Sci Rep. 2019;9(19313):1–12.

Hautaniemi EJ, Tahvanainen AM, Koskela JK, Tikkakoski AJ, Kähönen M, Uitto M, et al. Voluntary liquorice ingestion increases blood pressure via increased volume load , elevated peripheral arterial resistance , and decreased aortic compliance. Sci Rep. 2017;10947(7):1–11.

Zhang Q, Chen Z, Chen S, Xu Y, Deng H. Intraindividual stability of cortisol and cortisone and the ratio of cortisol to cortisone in saliva, urine and hair. Steroids. 2017;118:61–7. Available from: http://dx.doi.org/10.1016/j.steroids.2016.12.008

Ryan K, Robles TF, Dickenson L, Reynolds B, Repetti RL. Stability of diurnal cortisol measures across days, weeks, and years across middle childhood and early adolescence: Exploring the role of age, pubertal development, and sex. Psychoneuroendocrinology. 2019;100:67–74. Available from: https://doi.org/10.1016/j.psyneuen.2018.09.033

Kobayashi H, Park B, Miyazaki Y. Normative references of heart rate variability and salivary alpha-amylase in a healthy young male population. J Physiol Anthropol. 2012;31(9):1–8.

Bertsch K, Hagemann D, Naumann E, Schächinger H. Stability of heart rate variability indices reflecting parasympathetic activity. Psychophysiology. 2012;49:672–82.