Low vagal tone is associated with impaired post stress recovery of cardiovascular, endocrine, and immune markers

European Journal of Applied Physiology

Volumn 109, Issue 2, 2010, Pages 201-211

  Weber, Cora Stefanie ^a   Thayer, Julian F ^b,c   Rudat, Miriam ^a   Wirtz, Petra H ^d   Zimmermann Viehoff, Frank ^a   Thomas, Alexander ^a   Perschel, Frank H ^a   Arck, Petra C ^a   Deter, Hans C ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Blood pressure; Cortisol; Heart rate variability; Recovery; Stress; TNF alpha

Indexed keywords

HYDROCORTISONE; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; BLOOD; BLOOD PRESSURE; HEART RATE; HUMAN; MALE; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; VAGUS NERVE;

ADULT; BLOOD PRESSURE; HEART RATE; HUMANS; HYDROCORTISONE; INTERLEUKIN-6; MALE; STRESS, PSYCHOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA; VAGUS NERVE; YOUNG ADULT;

EID: 77953545241     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-009-1341-x     Document Type: Article

References (67)

1. Akselrod S, Gordon D, Ubel FA, Shannon DC, Berger AC, Cohen RJ (1981) Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 213:220-222
2. al'Absi M, Arnett DK (2000) Adrenocortical responses to psychological stress and risk for hypertension. Biomed Pharmacother 54:234-244
3. al'Absi M, Lovallo WR, McKey BS, Pincomb GA (1994) Borderline hypertensives produce exaggerated adrenocortical responses to mental stress. Psychosom Med 56:245-250
4. Altemus M, Rao B, Dhabhar FS, Ding W, Granstein RD (2001) Stress-induced changes in skin barrier function in healthy women. J Invest Dermatol 117 (2):309-317
5. Bernik TR, Friedman SG, Ochani M, DiRaimo R, Ulloa L, Yang H, Sudan S, Czura CJ, Ivanova SM, Tracey KJ (2002) Pharmacological stimulation of the cholinergic antiinflammatory pathway. J Exp Med 195 (6):781-788
6. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Wang H, Abumrad N, Eaton JW, Tracey KJ (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405 (6785):458-462
7. Brook RD, Julius S (2003) Autonomic imbalance, hypertension, and cardiovascular risk. Am J Hypertens 13 (6 Pt 2):112S-122S
8. Brosschot JF, Pieper S, Thayer JF (2005) Expanding stress theory: prolonged activation and perseverative cognition. Psychoneuroendocrinology 30 (10):1043-1049
9. Brydon L, Edwards S, Jia H, Mohamed-Ali V, Zachary I, Martin JF, Steptoe A (2005) Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain Behav Immun 19 (6):540-546
10. Buchholz K, Schachinger H, Wagner M, Sharma AM, Deter HC (2003) Reduced vagal activity in salt-sensitive subjects during mental challenge. Am J Hypertens 16:531-536
11. Deter HC, Buchholz K, Schorr U, Mathiak K, Sharma AM (2001) Salt-sensitivity and other predictors of stress-related cardiovascular reactivity in healthy young males. Clin Exp Hypertens 23:213-225
12. Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130 (3):355-391
13. Dugué B, Leppänen EA, Teppo AM, Fyhrquist F, Gräsbeck R (1993) Effects of psychological stress on plasma interleukins-1 beta and 6, C-reactive protein, tumour necrosis factor alpha, anti-diuretic hormone and serum cortisol. Scand J Clin Lab Invest 53 (6):555-561
14. Edwards KM, Burns VE, Ring C, Carroll D (2006) Sex differences in the interleukin-6 response to acute psychological stress. Biol Psychol 71 (3):236-239
15. Elenkov IJ, Chrousos GP (2006) Stress system-organization, physiology and immunoregulation. Neuroimmunomodulation 13 (5-6): 257-267
16. Ellins E, Halcox J, Donald A, Field B, Brydon L, Deanfield J, Steptoe A (2008) Arterial stiffness and inflammatory response to psychophysiological stress. Brain Behav Immun Mar. 1 [Epub ahead of print]
17. Fliege H, Rose M, Arck P, Walter OB, Kocalevent RD, Weber CS, Klapp BF (2005) The Perceived Stress Questionnaire (PSQ) reconsidered: validation and reference values from different clinical and healthy adult samples. Psychosom Med 67:78-88
18. Heesen C, Schulz H, Schmidt M, Gold S, Tessmer W, Schulz KH (2002) Endocrine and cytokine responses to acute psychological stress in multiple sclerosis. Brain Behav Immun 16 (3):282-287
19. Heinz A, Hermann D, Smolka MN, Rieks M, Gräf KJ, Pöhlau D, Kuhn W, Bauer M (2003) Effects of acute psychological stress on adhesion molecules, interleukins and sex hormones: implications for coronary heart disease. Psychopharmacology (Berl) 165 (2):111-117
20. Huikuri HV, Jokinen V, Syvänne M, Nieminen MS, Airaksinen KE, Ikäheimo MJ, Koistinen JM, Kauma H, Kesäniemi AY, Majahalme S, Niemelä KO, Frick MH (1999) Heart rate variability and progression of coronary atherosclerosis. Arterioscler Thromb Vasc Biol 19 (8):1979-1985
21. Imholz BP, Langewouters GJ, van Montfrans GA, Parati G, van Goudoever J, Wesseling KH, Wieling W, Mancia G (1993) Feasibility of ambulatory, continuous 24 h finger arterial pressure recording. Hypertension 21:65-73
22. Janszky I, Ericson M, Lekander M, Blom M, Buhlin K, Georgiades A, Ahnve S (2004) Inflammatory markers and heart rate variability in women with coronary heart disease. J Intern Med 256:421-428
23. Kop WJ (2003) The integration of cardiovascular behavioral medicine and psychoneuroimmunology: new developments based on converging research fields. Brain Behav Immun 17 (4):233-237
24. Kop WJ, Weissman NJ, Zhu J, Bonsall RW, Doyle M, Stretch MR, Glaes SB, Krantz DS, Gottdiener JS, Tracy RP (2008) Effects of acute mental stress and exercise on inflammatory markers in patients with coronary artery disease and healthy controls. Am J Cardiol 101 (6):767-773
25. Kraemer HC, Stice E, Kazdin A, Offord D, Kupfer D (2001) How do risk factors work together? Mediators, moderators, and independent, overlapping, and proxy risk factors. Am J Psychiatry 158 (6):848-856
26. Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) STAI State-Trait-Angstinventar. Beltz, Weinheim
27. Levenstein S, Prantera C, Varvo V, Scribano ML, Berto E, Luzi C, Andreoli A (1993) Development of the Perceived Stress Questionnaire-A new tool for psychosomatic research. J Psychosom Res 37:19-32
28. Liao D, Cai J, Barnes RW, Tyroler HA, Rautaharju P, Holme I et al (1996) Association of cardiac autonomic function and the development of hypertension: the ARIC study. Am J Hypertens 9:1147-1156
29. Lutgendorf SK, Logan H, Costanzo E, Lubaroff D (2004) Effects of acute stress, relaxation, and a neurogenic inflammatory stimulus on interleukin-6 in humans. Brain Behav Immun 18 (1):55-64
30. Marsland AL, Gianaros PJ, Prather AA, Jennings JR, Neumann SA, Manuck SB (2007) Stimulated production of proinflammatory cytokines covaries inversely with heart rate variability. Psychosom Med 69 (8):709-716
31. McEwen BS (1998) Stress, adaptation, and disease Allostasis and allostatic load. Ann N Y Acad Sci 840:33-44
32. Melzig CA, Weike AI, Hamm AO, Thayer JF (2009) Individual differences in fear-potentiated startle as a function of resting heart rate variability: implications for panic disorder. Int J Psychophysiol 71 (2):109-117
33. Miller GE, Rohleder N, Stetler C, Kirschbaum C (2005) Clinical depression and regulation of the inflammatory response during acute stress. Psychosom Med 67 (5):679-687
34. Packard RR, Libby P (2008) Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin Chem 54 (1):24-38
35. Ridker PM, Rifai N, Pfeffer M, Sacks F, Lepage S, Braunwald E (2000a) Elevation of tumor necrosis factor-alpha and increased risk of recurrent coronary events after myocardial infarction. Circulation 101 (18):2149-2153
36. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH (2000b) Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 101 (15):1767-1772
37. Ross R (1999) Atherosclerosis is an inflammatory disease. Am Heart J 138 (5 Pt 2): S419-S420
38. Schwenkmezger P, Hodapp V (1991) The state-trait anger expression inventory. Zeitschrift Fur Klinische Psychologie Psychiatrie und Psychotherapie 39:63-68
39. Sloan RP, McCreath H, Tracey KJ, Sidney S, Liu K, Seeman T (2007) RR interval variability is inversely related to inflammatory markers: the CARDIA study. Mol Med 13 (3-4): 178-184
40. Spielberger CD (1983) Manual for the state-trait anxiety inventory. Consulting Psychologist Press, Palo Alto, CA
41. Spielberger CD (1999) Manual for the state-trait anger inventory, STAXI-2. Psychological Assessment Resources, Odessa, FL
42. Steptoe A, Marmot M (2005) Impaired cardiovascular recovery following stress predicts 3-year increases in blood pressure. J Hypertens 23 (3):529-536
43. Steptoe A, Marmot M (2006) Psychosocial, hemostatic, and inflammatory correlates of delayed poststress blood pressure recovery. Psychosom Med 68 (4):531-537
44. Steptoe A, Willemsen G, Owen N, Flower L, Mohamed-Ali V (2001) Acute mental stress elicits delayed increases in circulating inflammatory cytokine levels. Clin Sci (Lond) 101 (2):185-192
45. Steptoe A, Hamer M, Chida Y (2007) The effects of acute psychological stress on circulating inflammatory factors in humans: A review and meta-analysis. Brain Behav Immun 21 (7):901-912
46. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur Heart J 17:354-381
47. Thayer JF (2006) On the importance of inhibition: central and peripheral manifestations of nonlinear inhibitory processes in neural systems. Dose Response 4:2-21
48. Thayer JF, Brosschot JF (2005) Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology 30:1050-1058
49. Thayer JF, Fischer JE (2009) Heart rate variability, overnight urinary norepinephrine, and C-reactive protein: evidence for the cholinergic anti-inflammatory pathway in healthy human adults. J Intern Med 265:439-447
50. Thayer JF, Lane RD (2007) The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol 74:224-242
51. Thayer JF, Lane RD (2009) Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev 33:81-88
52. Thayer JF, Sternberg E (2006) Beyond heart rate variability: vagal regulation of allostatic systems. Ann N Y Acad Sci 1088:361-372
53. Thayer JF, Hall M, Sollers JJ, Fischer JE (2006) Alcohol use, urinary cortisol, and heart rate variability in apparently healthy men: evidence for impaired inhibitory control of the HPA axis in heavy drinkers. Int J Psychophysiol 59:244-250
54. Thayer JF, Yamamoto SS, Brosschot JF (2009) The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int J Cardiol. doi:10.1016/j.icard.2009. 09.543
55. Tracey KJ (2002) The inflammatory reflex. Nature 420:853-859
56. Tsuji H, Larson MG, Venditti FJ Jr, Manders ES, Evans JC, Feldman CL, Levy D (1996) Impact of reduced heart rate variability on risk for cardiac events. The Framingham Heart Study. Circulation 94 (11):2850-2855
57. Vasey MW, Thayer JF (1987) The continuing problem of false positives in repeated measures ANOVA in psychophysiology: a multivariate solution. Psychophysiololgy 24:479-486
58. von Känel R, Kudielka BM, Preckel D, Hanebuth D, Fischer JE (2006) Delayed response and lack of habituation in plasma interleukin-6 to acute mental stress in men. Brain Behav Immun 20 (1):40-48
59. Walker BR, Phillips DI, Noon JP, Panarelli M, Andrew R, Edwards HV, Holton DW, Skl JR, Webb DJ, Watt GC (1998) Increased glucocorticoid activity in men with cardiovascular risk factors. Hypertension 31 (4):891-895
60. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421 (6921):384-388
61. Watt GC, Harrap SB, Foy CJ, Holton DW, Edwards HV, Davidson HR, Connor JM, Lever AF, Fraser R (1992) Abnormalities of glucocorticoid metabolism and the renin-angiotensin system: a four-corners approach to the identification of genetic determinants of blood pressure. J Hypertens 10 (5):473-482
62. Weber C, Arck P, Mazurek B, Klapp BF (2002) Impact of a relaxation training on psychometric and immunologic parameters in tinnitus sufferers. J Psychosom Res 52 (1):29-33
63. Weber CS, Thayer JF, Rudat M, Perschel HF, Buchholz K, Deter HC (2007) Emotional irritation before mental stress is associated with enhanced peripheral norepinephrine. Scand J Psychol 48 (6):459-466
64. Weber CS, Thayer JF, Rudat M, Sharma AM, Perschel FH, Buchholz K, Deter HC (2008) Salt sensitive males show reduced heart rate variability, lower norepinpehrine and enhanced cortisol during mental stress. J Hum Hypertens 22 (6):423-431
65. Yang S, Zhang L (2004) Glucocorticoids and vascular reactivity. Curr Vasc Pharmacol 2 (1):1-12
66. Ziegler D, Laude D, Akila F, Elghozi JL (2001) Time and frequency domain estimation of early diabetic cardiovascular autonomic neuropathy. Clin Auton Res 11:369-376
67. Zimmermann-Viehoff F, Weber CS, Merswolken M, Rudat M, Deter HC (2008) Low anxiety males display higher degree of salt sensitivity, increased autonomic reactivity, and higher defensiveness. Am J Hypertens 21 (12):1292-1297