Anger Is Associated with Increased IL-6 Stress Reactivity in Women, But Only Among Those Low in Social Support

International Journal of Behavioral Medicine - Tập 21 - Trang 936-945 - 2013
Eli Puterman1, Elissa S. Epel1, Aoife O’Donovan1,2, Aric A. Prather1, Kirstin Aschbacher1, Firdaus S. Dhabhar3,4
1Department of Psychiatry, School of Medicine, University of California, San Francisco, USA
2SF Veteran’s Affairs Medical Center, San Francisco, USA
3Stanford Cancer Institute, Stanford University, Stanford, USA
4Department of Psychiatry and Behavioral Sciences, Institute for Immunity, Transplantation, and Infection, Stanford University School of Medicine, Stanford, USA

Tóm tắt

Social connections moderate the effects of high negative affect on health. Affective states (anger, fear, and anxiety) predict interleukin-6 (IL-6) reactivity to acute stress; in turn, this reactivity predicts risk of cardiovascular disease progression. Here, we examined whether perceived social support mitigates the relationship between negative affect and IL-6 stress reactivity. Forty-eight postmenopausal women completed a standardized mental lab stressor with four blood draws at baseline and 30, 50, and 90 min after the onset of the stressor and anger, anxiety, and fear were assessed 10 min after task completion. Participants self-rated levels of social support within a week prior to the stressor. Only anger was related to IL-6 stress reactivity—those experiencing high anger after the stressor had significant increases in IL-6. IL-6 reactivity was marginally associated with perceived support, but more strikingly, perceived support mitigated anger associations with IL-6 stress reactivity. Supportive ties can dampen the relationship of anger to pro-inflammatory reactivity to acute stress. Implications to cardiovascular disease are discussed.

Tài liệu tham khảo

House JS, Landis KR, Umberson D. Social relationships and health. Science. 1988;241:540–5. Berkman LF, Glass T, Brissette I, Seeman TE. From social integration to health: Durkheim in the new millennium. Soc Sci Med. 2000;51:843–57. Cohen S. Social relationships and health. Am Psychol. 2004;59:676–84. Uchino BN, Cacioppo JT, Kiecolt-Glaser JK. The relationship between social support and physiological processes: a review with emphasis on underlying mechanisms and implications for health. Psychol Bull. 1996;119:488–531. Cohen S, Wills TS. Stress, social support, and the buffering hypothesis. Psychol Bull. 1985;98:310–57. Uchino BN. Social support and health: a review of physiological processes potentially underlying links to disease outcomes. J Behav Med. 2006;29:377–87. Packard RRS, Libby P. Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin Chem. 2008;54:24–38. Ferrucci L et al. Serum IL-6 level and the development of disability in older persons. J Am Geriatr Soc. 1999;47:639–46. Baune BT, Rothermundt M, Ladwig KH, Meisinger C, Berger K. Systemic inflammation (interleukin 6) predicts all-cause mortality in men: results from a 9-year follow-up of the MEMO Study. Age. 2011;33:209–17. Lim HS, Blann AD, Lip GYH. Soluble CD40 ligand, soluble P-selectin, interleukin-6, and tissue factor in diabetes mellitus—relationships to cardiovascular disease and risk factor intervention. Circulation. 2004;109:2524–8. Honda H et al. Serum albumin, C-reactive protein, interleukin 6, and fetuin A as predictors of malnutrition, cardiovascular disease, and mortality in patients with ESRD. Am J Kidney Dis. 2006;47:139–48. Lindmark E, Diderholm E, Wallentin L, Siegbahn A. Relationship between interleukin 6 and mortality in patients with unstable coronary artery disease: effects of an early invasive or noninvasive strategy. JAMA 2001; 286:2107–13. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 2000;101:1767–72. Ershler WB, Keller ET. Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu Rev Med. 2000;51:245–70. Harris TB et al. Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am J Med. 1999;106:506–12. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868–74. Brydon L, Steptoe A. Stress-induced increases in interleukin-6 and fibrinogen predict ambulatory blood pressure at 3-year follow-up. J Hypertens. 2005;23:1001–7. Steptoe A, Hamer M, Chida Y. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav Immun. 2007;21:901–12. Friedman EM et al. Social relationships, sleep quality, and interleukin-6 in aging women. Proc Natl Acad Sci U S A. 2005;102:18757–62. Kiecolt-Glaser JK, Gouin J-P, Hantsoo L. Close relationships, inflammation, and health. Neurosci Biobehav Rev. 2010;35:33–8. Mezuk B, Roux AVD, Seeman TE. Evaluating the buffering vs. direct effects hypotheses of emotional social support on inflammatory markers: the Multi-Ethnic Study of Atherosclerosis. Brain Behav Immun. 2010;24:1294–300. Steptoe A. Stress, social support and cardiovascular activity over the working day. Int J Psychophysiol. 2000;37:299–308. Eisenberger NI, Taylor SE, Gable SL, Hilmert CJ, Lieberman MD. Neural pathways link social support to attenuated neuroendocrine stress responses. NeuroImage. 2007;35:1601–12. Chida Y, Hamer M. Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: a quantitative review of 30 years of investigations. Psychol Bull. 2008;134:829–85. Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull. 2004;130:355–91. Carroll JE et al. Negative affective responses to a speech task predict changes in interleukin (IL)-6. Brain Behav Immun. 2011;25:232–8. Moons WG, Eisenberger NI, Taylor SE. Anger and fear responses to stress have different biological profiles. Brain Behav Immun. 2010;24:215–9. Kirschbaum C, Pirke KM, Hellhammer DH. The Trier Social Stress Test—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology. 1993;28:76–81. Cohen S, Memelstein R, Kamarck T, Hoberman H. In: Sarason IG, Sarason, B, editors. Social support: theory, research and application. The Hague: Martinus Nijhoff; 1985. pp. 73–94. Cohen J, Cohen P, West SG, Aiken LS. Applied multiple regression/correlation analysis for the behavioral sciences, 3rd edn. Mahwah, NJ: Lawrence Erlbaum; 2003. Raudenbush SW, Bryk AS. Hierarchical linear models: applications and data analysis methods (second edition). Newbury Park: Sage; 2002. Singer JD, Willett JB. Applied longitudinal data analysis: modeling change and event occurrence. New York: Oxford University Press; 2003. http://books.google.com/books?id=PpnA1M8VwR8C. Woodward M, Rumley A, Tunstall-Pedoe H, Lowe GDO. Associations of blood rheology and interleukin-6 with cardiovascular risk factors and prevalent cardiovascular disease. Br J Haematol. 1999;104:246–57. Kiecolt-Glaser JK et al. Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci. 2003;100:9090–5. Mausbach BT et al. Self-efficacy buffers the relationship between dementia caregiving stress and circulating concentrations of the proinflammatory cytokine interleukin-6. Am J Geriatr Psychiatr. 2011;19:64–71. Mills PJ et al. Effects of gender and dementia severity on Alzheimer’s disease caregivers’ sleep and biomarkers of coagulation and inflammation. Brain Behav Immun. 2009;23:605–10. Pace TWW et al. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am J Psychiatr. 2006;163:1630-U1. Von Känel R et al. Effect of Alzheimer caregiving stress and age on frailty markers interleukin-6, C-reactive protein, and D-dimer. J Gerontol A: Biol Med Sci. 2006;61:963–9. Carver CS, Harmon-Jones E. Anger is an approach-related affect: evidence and implications. Psychol Bull. 2009;135:183–204. Gray JR, Braver TS, Raichle ME. Integration of emotion and cognition in the lateral prefrontal cortex. Proc Natl Acad Sci. 2002;99:4115–20. Lerner JS, Keltner D. Fear, anger, and risk. J Pers Soc Psychol. 2001;81:146–59. McNaughton N, Corr PJ. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev. 2004;28:285–305. Stemmler G, Aue T, Wacker J. Anger and fear: separable effects of emotion and motivational direction on somatovisceral responses. Int J Psychophysiol. 2007;66:141–53. Mendes WB, Major B, McCoy S, Blascovich J. How attributional ambiguity shapes physiological and emotional responses to social rejection and acceptance. J Pers Soc Psychol. 2008;94:278–91. Lerner JS, Dahl RE, Hariri AR, Taylor SE. Facial expressions of emotion reveal neuroendocrine and cardiovascular stress responses. Biol Psychiatry. 2007;61:253–60. Dhabhar FS, McEwen BS. Stress-induced enhancement of antigen-specific cell-mediated immunity. J Immunol. 1996;156:2608–15. Dhabhar FS, McEwen BS. Enhancing versus suppressive effects of stress hormones on skin immune function. Proc Natl Acad Sci U S A. 1999;96:1059–64. Dhabhar FS, Viswanathan K. Short-term stress experienced at time of immunization induces a long-lasting increase in immunologic memory. Am J Physiol Regul Integr Comp Physiol. 2005;289:R738–R44. Viswanathan K, Daugherty C, Dhabhar FS. Stress as an endogenous adjuvant: augmentation of the immunization phase of cell-mediated immunity. Int Immunol. 2005;17:1059–69. Edwards KM et al. Meningococcal A vaccination response is enhanced by acute stress in men. Psychosom Med. 2008;70:147–51. Edwards KM et al. Acute stress exposure prior to influenza vaccination enhances antibody response in women. Brain Behav Immun. 2006;20:159–68. Rosenberger PH et al. Surgical stress-induced immune cell redistribution profiles predict short-term and long-term postsurgical recovery: a prospective study. J Bone Joint Surg. 2009;91:2783–94. Ridker PM. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation. 2003;107:363–9. Carroll D et al. Increased blood pressure reactions to acute mental stress are associated with 16-year cardiovascular disease mortality. Psychophysiology. 2012;49:1444–8. Georgiades A, Lemne C, De Faire U, Lindvall K, Fredrikson M. Stress-induced blood pressure measurements predict left ventricular mass over three years among borderline hypertensive men. Eur J Clin Investig. 1997;27:733–9. Matthews KA et al. Stress-induced pulse pressure change predicts women’s carotid atherosclerosis. Stroke. 1998;29:1525–30. Hamer M, O’Donnell K, Lahiri A, Steptoe A. Salivary cortisol responses to mental stress are associated with coronary artery calcification in healthy men and women. Eur Heart J. 2010;31:424–9. Chida Y, Steptoe A. The association of anger and hostility with future coronary heart disease: a meta-analytic review of prospective evidence. J Am Coll Cardiol. 2009;53:936–46. Siegman AW. Cardiovascular consequences of expressing, experiencing, and repressing anger. J Behav Med. 1993;16:539–69. Mittleman MA et al. Triggering of acute myocardial infarction onset by episodes of anger. Circulation. 1995;92:1720–5. Lipovetzky N et al. Emotional events and anger at the workplace as triggers for a first event of the acute coronary syndrome: a case–crossover study. Israel Med Assoc J. 2007;9:310–5. Nawrot TS, Perez L, Kunzli N, Munters E, Nemery B. Public health importance of triggers of myocardial infarction: a comparative risk assessment. Lancet. 2011;377:732–40. Steptoe A, Brydon L. Emotional triggering of cardiac events. Neurosci Biobehav Rev. 2009;33:63–70. Strike PC, Perkins-Porras L, Whitehead DL, McEwan J, Steptoe A. Triggering of acute coronary syndromes by physical exertion and anger: clinical and sociodemographic characteristics. Heart. 2006;92:1035–40. Fernandez AB et al. Tendency to angry rumination predicts stress-provoked endothelin-1 increase in patients with coronary artery disease. Psychosom Med. 2010;72:348–53. Liu H et al. Correlation between endothelin-1 and atherosclerosis in chronic hemodialysis patients. J Nephrol. 2010;23:593–602. Han JH, Lee MY, Myung SC. The effect of endothelin-1 on the production of interleukin-6 in cultured human detrusor smooth muscle cells, and the effect of interleukin-6 on the contractile response of bladder smooth muscle strips from rats. BJU Int. 2009;104:707–12. Keltikangas-Jarvinen L, Ravaja N. Relationships between hostility and physiological coronary heart disease risk factors in young adults: moderating influence of perceived social support and sociability. Psychol Health. 2002;17:173–90. Schwerdtfeger A, Friedrich-Mai P. Social interaction moderates the relationship between depressive mood and heart rate variability: evidence from an ambulatory monitoring study. Health Psychol. 2009;28:501–9. Puterman E, DeLongis A, Pomaki G. Protecting us from ourselves: social support as a buffer of trait and state rumination. J Soc Clin Psychol. 2010;29:797–820. Denson TF, Pedersen WC, Ronquillo J, Nandy AS. The angry brain: neural correlates of anger, angry rumination, and aggressive personality. J Cogn Neurosci. 2009;21:734–44. Slavich GM, Way BM, Eisenberger NI, Taylor SE. Neural sensitivity to social rejection is associated with inflammatory responses to social stress. Proc Natl Acad Sci U S A. 2010;107:14817–22. Eisenberger NI et al. Attachment figures activate a safety signal-related neural region and reduce pain experience. Proc Natl Acad Sci U S A. 2011;108:11721–6. Phillips AC, Carroll D, Hunt K, Der G. The effects of the spontaneous presence of a spouse/partner and others on cardiovascular reactions to an acute psychological challenge. Psychophysiology. 2006;43:633–40. Aspinwall LG, Taylor SE. A stitch in time: self-regulation and proactive coping. Psychol Bull. 1997;121:417–36. Uchino, BN, Birmingham W. In: Contrada RJ, Baum A, editors. The handbook of stress science: biology, psychology, and health. New York: Springer; 2011. pp. 111–121. Uchino BN, Carlisle M, Birmingham W, Vaughn AA. Social support and the reactivity hypothesis: conceptual issues in examining the efficacy of received support during acute psychological stress. Biol Psychol. 2011;86:137–42. Kiecolt-Glaser JK, McGuire L, Robles TF, Glaser R. Psychoneuroimmunology: psychological influences on immune function and health. J Consult Clin Psychol. 2002;70:537–47. Heritier S, Cantoni E, Copt S, Victoria-Feser, M.-P. Robust methods in biostatistics. New York: Wiley; 2009. Lampert R et al. Anger-induced T-Wave alternans predicts future ventricular arrhythmias in patients with implantable cardioverter-defibrillators. J Am Coll Cardiol. 2009;53:774–8. Shimbo D et al. Hostility and platelet reactivity in individuals without a history of cardiovascular disease events. Psychosom Med. 2009;71:741–7. Cole SW et al. Computational identification of gene-social environment interaction at the human IL6 locus. Proc Natl Acad Sci U S A. 2010;107:5681–6.