Stress and inflammation – The need to address the gap in the transition between acute and chronic stress effects

Psychoneuroendocrinology

Volumn 105, Issue , 2019, Pages 164-171

  Rohleder, Nicolas ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Acute stress; Chronic stress; Habituation; HPA axis; Inflammation; Repeated acute stress

Indexed keywords

INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ACUTE STRESS; AMPLITUDE MODULATION; CHRONIC STRESS; DEPRESSION; EXPERIENCE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFLAMMATION; JOB STRESS; KNOWLEDGE; LIFE STRESS; LONG TERM EXPOSURE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; STRESS; TASK PERFORMANCE; ACUTE DISEASE; CHRONIC DISEASE; HABITUATION; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOLOGY; MENTAL STRESS; METABOLISM; PHYSIOLOGY;

ACUTE DISEASE; CHRONIC DISEASE; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFLAMMATION; STRESS, PSYCHOLOGICAL;

EID: 85062042221     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2019.02.021     Document Type: Review

References (111)

1. Allen, A.P., Curran, E.A., Duggan, Á., Cryan, J.F., Chorcoráin, A.N., Dinan, T.G., Molloy, D.W., Kearney, P.M., Clarke, G., A systematic review of the psychobiological burden of informal caregiving for patients with dementia: focus on cognitive and biological markers of chronic stress. Neurosci. Biobehav. Rev. 73 (2017), 123–164.
2. Aschbacher, K., Epel, E., Wolkowitz, O.M., Prather, A.A., Puterman, E., Dhabhar, F.S., Maintenance of a positive outlook during acute stress protects against pro-inflammatory reactivity and future depressive symptoms. Brain Behav. Immun. 26 (2012), 346–352.
3. Bauer, M.E., Chronic stress and immunosenescence: a review. Neuroimmunomodulation 15 (2008), 241–250.
4. Baumeister, D., Akhtar, R., Ciufolini, S., Pariante, C.M., Mondelli, V., Childhood trauma and adulthood inflammation: a meta-analysis of peripheral C-reactive protein, interleukin-6 and tumour necrosis factor-α. Molecular Psychiatry 21:5 (2016), 642–649.
5. Benson, S., Arck, P.C., Blois, S., Schedlowski, M., Elsenbruch, S., Subclinical depressive symptoms affect responses to acute psychosocial stress in healthy premenopausal women. Stress 14 (2011), 88–92.
6. Bernstein, D.P., Fink, L., Handelsman, L., Foote, J., Lovejoy, M., Wenzel, K., Sapareto, E., Ruggiero, J., Initial reliability and validity of a new retrospective measure of child abuse and neglect. Am. J. Psychiatry 151 (1994), 1132–1136.
7. Black, P.H., Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav. Immun. 16 (2002), 622–653.
8. Black, D.S., Cole, S.W., Irwin, M.R., Breen, E., St Cyr, N.M., Nazarian, N., Khalsa, D.S., Lavretsky, H., Yogic meditation reverses NF-κB and IRF-related transcriptome dynamics in leukocytes of family dementia caregivers in a randomized controlled trial. Psychoneuroendocrinology 38 (2013), 348–355.
9. Böbel, T.S., Hackl, S.B., Langgartner, D., Jarczok, M.N., Rohleder, N., Rook, G.A., Lowry, C.A., Gündel, H., Waller, C., Reber, S.O., Less immune activation following social stress in rural vs. urban participants raised with regular or no animal contact, respectively. Proc. Natl. Acad. Sci. U. S. A. 115 (2018), 5259–5264.
10. Breines, J.G., Thoma, M.V., Gianferante, D., Hanlin, L., Chen, X., Rohleder, N., Self-compassion as a predictor of interleukin-6 response to acute psychosocial stress. Brain Behav. Immun. 37 (2014), 109–114.
11. Brydon, L., Steptoe, A., Stress-induced increases in interleukin-6 and fibrinogen predict ambulatory blood pressure at 3-year follow-up. J. Hypertens. 23 (2005), 1001–1007.
12. Brydon, L., Edwards, S., Mohamed-Ali, V., Steptoe, A., Socioeconomic status and stress-induced increases in interleukin-6. Brain Behav. Immun. 18 (2004), 281–290.
13. Brydon, L., Strike, P.C., Bhattacharyya, M.R., Whitehead, D.L., McEwan, J., Zachary, I., Steptoe, A., Hostility and physiological responses to laboratory stress in acute coronary syndrome patients. J. Psychosom. Res. 68 (2010), 109–116.
14. Carpenter, L.L., Gawuga, C.E., Tyrka, A.R., Lee, J.K., Anderson, G.M., Price, L.H., Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults. Neuropsychopharmacology 35 (2010), 2617–2623.
15. Carroll, J.E., Low, C.A., Prather, A.A., Cohen, S., Fury, J.M., Ross, D.C., Marsland, A.L., Negative affective responses to a speech task predict changes in interleukin (IL)-6. Brain Behav. Immun. 25 (2011), 232–238.
16. Chen, X., Gianferante, D., Hanlin, L., Fiksdal, A., Breines, J.G., Thoma, M.V., Rohleder, N., HPA-axis and inflammatory reactivity to acute stress is related with basal HPA-axis activity. Psychoneuroendocrinology 78 (2017), 168–176.
17. Christian, L.M., Glaser, R., Porter, K., Iams, J.D., Stress-induced inflammatory responses in women: effects of race and pregnancy. Psychosom. Med. 75 (2013), 658–669.
18. Cohen, S., Janicki-Deverts, D., Miller, G.E., Psychological stress and disease. JAMA 298 (2007), 1685–1687.
19. Cohen, S., Janicki-Deverts, D., Doyle, W.J., Miller, G.E., Frank, E., Rabin, B.S., Turner, R.B., Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 5995–5999.
20. Couzin-Frankel, J., Inflammation bares a dark side. Science, 330, 2010, 1621.
21. Derry, H.M., Fagundes, C.P., Andridge, R., Glaser, R., Malarkey, W.B., Kiecolt-Glaser, J.K., Lower subjective social status exaggerates interleukin-6 responses to a laboratory stressor. Psychoneuroendocrinology 38:11 (2013), 2676–2685.
22. Ellins, E., Halcox, J., Donald, A., Field, B., Brydon, L., Deanfield, J., Steptoe, A., Arterial stiffness and inflammatory response to psychophysiological stress. Brain Behav. Immun. 22 (2008), 941–948.
23. Elliot, G.G., Eisdorfer, C., Stress and Human Health: Analysis and Implications of Research. 1982, Springer, New York.
24. Epel, E.S., Blackburn, E.H., Lin, J., Dhabhar, F.S., Adler, N.E., Morrow, J.D., Cawthon, R.M., Accelerated telomere shortening in response to life stress. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 17312–17315.
25. Fagundes, C.P., Glaser, R., Hwang, B.S., Malarkey, W.B., Kiecolt-Glaser, J.K., Depressive symptoms enhance stress-induced inflammatory responses. Brain Behav. Immun. 31 (2013), 172–176.
26. Ford, E.S., Loucks, E.B., Berkman, L.F., Social integration and concentrations of C-reactive protein among US adults. Ann. Epidemiol. 16 (2006), 78–84.
27. Giletta, M., Slavich, G.M., Rudolph, K.D., Hastings, P.D., Nock, M.K., Prinstein, M.J., Peer victimization predicts heightened inflammatory reactivity to social stress in cognitively vulnerable adolescents. J. Child Psychol. Psychiatry 59:2 (2017), 129–139, 10.1111/jcpp.12804.
28. Glaser, R., Kiecolt-Glaser, J.K., Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5 (2005), 243–251.
29. Gouin, J.-P., Hantsoo, L., Kiecolt-Glaser, J.K., Immune dysregulation and chronic stress among older adults: a review. Neuroimmunomodulation 15 (2008), 251–259.
30. Gouin, J.-P., Glaser, R., Malarkey, W.B., Beversdorf, D., Kiecolt-Glaser, J., Chronic stress, daily stressors, and circulating inflammatory markers. Health Psychol. 31 (2012), 264–268.
31. Grossi, G., Perski, A., Evengård, B., Blomkvist, V., Orth-Gomér, K., Physiological correlates of burnout among women. J. Psychosom. Res. 55 (2003), 309–316.
32. Hackett, R.A., Hamer, M., Endrighi, R., Brydon, L., Steptoe, A., Loneliness and stress-related inflammatory and neuroendocrine responses in older men and women. Psychoneuroendocrinology 37 (2012), 1801–1809.
33. Häfner, S., Emeny, R.T., Lacruz, M.E., Baumert, J., Herder, C., Koenig, W., Thorand, B., Ladwig, K.H., KORA Study Investigators, Association between social isolation and inflammatory markers in depressed and non-depressed individuals: results from the MONICA/KORA study. Brain Behav. Immun. 25 (2011), 1701–1707.
34. Haley, W.E., Roth, D.L., Howard, G., Safford, M.M., Caregiving strain and estimated risk for stroke and coronary heart disease among spouse caregivers: differential effects by race and sex. Stroke 41 (2010), 331–336.
35. Hamer, M., Steptoe, A., Association between physical fitness, parasympathetic control, and proinflammatory responses to mental stress. Psychosom. Med. 69 (2007), 660–666.
36. Hamer, M., Williams, E., Vuonovirta, R., Giacobazzi, P., Gibson, E.L., Steptoe, A., The effects of effort-reward imbalance on inflammatory and cardiovascular responses to mental stress. Psychosom. Med. 68 (2006), 408–413.
37. Hänsel, A., Hong, S., Cámara, R.J.A., von Känel, R., Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci. Biobehav. Rev. 35 (2010), 115–121.
38. Heffner, K.L., Ng, H.M., Suhr, J.A., France, C.R., Marshall, G.D., Pigeon, W.R., Moynihan, J.A., Sleep disturbance and older adults’ inflammatory responses to acute stress. Am. J. Geriatr. Psychiatry 20 (2012), 744–752.
39. Hintikka, J., Lehto, S.M., Niskanen, L., Huotari, A., Herzig, K.-H., Koivumaa-Honkanen, H., Honkalampi, K., Sinikallio, S., Viinamäki, H., Unemployment and ill health: a connection through inflammation?. BMC Public Health, 9, 2009, 410.
40. Janusek, L.W., Tell, D., Gaylord-Harden, N., Mathews, H.L., Relationship of childhood adversity and neighborhood violence to a proinflammatory phenotype in emerging adult African American men: an epigenetic link. Brain Behav. Immun. 60 (2017), 126–135.
41. Kiecolt-Glaser, J.K., Preacher, K.J., MacCallum, R.C., Atkinson, C., Malarkey, W.B., Glaser, R., Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 9090–9095.
42. Kiecolt-Glaser, J.K., Gouin, J.-P., Weng, N.-P., Malarkey, W.B., Beversdorf, D.Q., Glaser, R., Childhood adversity heightens the impact of later-life caregiving stress on telomere length and inflammation. Psychosom. Med. 73 (2011), 16–22.
43. Kirschbaum, C., Prüssner, J.C., Stone, A.A., Federenko, I., Gaab, J., Lintz, D., Schommer, N., Hellhammer, D.H., Persistent high cortisol responses to repeated psychological stress in a subpopulation of healthy men. Psychosom. Med. 57 (1995), 468–474.
44. Kivimäki, M., Virtanen, M., Elovainio, M., Kouvonen, A., Väänänen, A., Vahtera, J., Work stress in the etiology of coronary heart disease—a meta-analysis. Scand. J. Work Environ. Health 32 (2006), 431–442.
45. Kuebler, U., Zuccarella-Hackl, C., Arpagaus, A., Wolf, J.M., Farahmand, F., von Känel, R., Ehlert, U., Wirtz, P.H., Stress-induced modulation of NF-κB activation, inflammation-associated gene expression, and cytokine levels in blood of healthy men. Brain Behav. Immun. 46 (2015), 87–95.
46. Laudenslager, M.L., Simoneau, T.L., Philips, S., Benitez, P., Natvig, C., Cole, S., A randomized controlled pilot study of inflammatory gene expression in response to a stress management intervention for stem cell transplant caregivers. J. Behav. Med. 39 (2016), 346–354.
47. Lockwood, K.G., John-Henderson, N.A., Marsland, A.L., Early life socioeconomic status associates with interleukin-6 responses to acute laboratory stress in adulthood. Physiol. Behav. 188 (2018), 212–220, 10.1016/j.physbeh.2018.02.016.
48. Loucks, E.B., Berkman, L.F., Gruenewald, T.L., Seeman, T.E., Social integration is associated with fibrinogen concentration in elderly men. Psychosom. Med. 67 (2005), 353–358.
49. Loucks, E.B., Sullivan, L.M., D'Agostino, R.B. Sr, Larson, M.G., Berkman, L.F., Benjamin, E.J., Social networks and inflammatory markers in the Framingham Heart Study. J. Biosoc. Sci. 38 (2006), 835–842.
50. Lovell, B., Moss, M., Wetherell, M., The psychosocial, endocrine and immune consequences of caring for a child with autism or ADHD. Psychoneuroendocrinology 37 (2012), 534–542.
51. Lutgendorf, S.K., Garand, L., Buckwalter, K.C., Reimer, T.T., Hong, S.Y., Lubaroff, D.M., Life stress, mood disturbance, and elevated interleukin-6 in healthy older women. J. Gerontol. A Biol. Sci. Med. Sci. 54 (1999), M434–9.
52. Marsland, A.L., Bachen, E.A., Cohen, S., Rabin, B., Manuck, S.B., Stress, immune reactivity and susceptibility to infectious disease. Physiol. Behav. 77 (2002), 711–716.
53. Marsland, A.L., Walsh, C., Lockwood, K., John-Henderson, N.A., The effects of acute psychological stress on circulating and stimulated inflammatory markers: a systematic review and meta-analysis. Brain Behav. Immun. 64 (2017), 208–219.
54. Mausbach, B.T., von Känel, R., Roepke, S.K., Moore, R., Patterson, T.L., Mills, P.J., Dimsdale, J.E., Ziegler, M.G., Ancoli-Israel, S., Allison, M., Grant, I., Self-efficacy buffers the relationship between dementia caregiving stress and circulating concentrations of the proinflammatory cytokine interleukin-6. Am. J. Geriatr. Psychiatry 19 (2011), 64–71.
55. McDade, T.W., Hawkley, L.C., Cacioppo, J.T., Psychosocial and behavioral predictors of inflammation in middle-aged and older adults: the Chicago health, aging, and social relations study. Psychosom. Med. 68 (2006), 376–381.
56. McEwen, B.S., Protective and damaging effects of stress mediators. N. Engl. J. Med. 338 (1998), 171–179.
57. McEwen, B.S., Stellar, E., Stress and the individual. Mechanisms leading to disease. Arch. Intern. Med. 153 (1993), 2093–2101.
58. McInnis, C.M., Thoma, M.V., Gianferante, D., Hanlin, L., Chen, X., Breines, J.G., Hong, S., Rohleder, N., Measures of adiposity predict interleukin-6 responses to repeated psychosocial stress. Brain Behav. Immun. 42 (2014), 33–40.
59. McInnis, C.M., Wang, D., Gianferante, D., Hanlin, L., Chen, X., Thoma, M.V., Rohleder, N., Response and habituation of pro- and anti-inflammatory gene expression to repeated acute stress. Brain Behav. Immun. 46 (2015), 237–248.
60. Miller, G.E., Cohen, S., Ritchey, A.K., Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Health Psychol. 21 (2002), 531–541.
61. Miller, G.E., Chen, E., Zhou, E.S., If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol. Bull. 133 (2007), 25–45.
62. Miller, G.E., Chen, E., Fok, A.K., Walker, H., Lim, A., Nicholls, E.F., Cole, S., Kobor, M.S., Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 14716–14721.
63. Miller, G.E., Murphy, M.L.M., Cashman, R., Ma, R., Ma, J., Arevalo, J.M.G., Kobor, M.S., Cole, S.W., Greater inflammatory activity and blunted glucocorticoid signaling in monocytes of chronically stressed caregivers. Brain Behav. Immun. 41 (2014), 191–199.
64. Mommersteeg, P.M.C., Heijnen, C.J., Kavelaars, A., van Doornen, L.J.P., Immune and endocrine function in burnout syndrome. Psychosom. Med. 68 (2006), 879–886.
65. O'Donnell, K., Brydon, L., Wright, C.E., Steptoe, A., Self-esteem levels and cardiovascular and inflammatory responses to acute stress. Brain Behav. Immun. 22 (2008), 1241–1247.
66. Pace, T.W.W., Mletzko, T.C., Alagbe, O., Musselman, D.L., Nemeroff, C.B., Miller, A.H., Heim, C.M., Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am. J. Psychiatry 163 (2006), 1630–1633.
67. Pace, T.W.W., Negi, L.T., Adame, D.D., Cole, S.P., Sivilli, T.I., Brown, T.D., Issa, M.J., Raison, C.L., Effect of compassion meditation on neuroendocrine, innate immune and behavioral responses to psychosocial stress. Psychoneuroendocrinology 34 (2009), 87–98.
68. Packard, C.J., Bezlyak, V., McLean, J.S., Batty, G.D., Ford, I., Burns, H., Cavanagh, J., Deans, K.A., Henderson, M., McGinty, A., Millar, K., Sattar, N., Shiels, P.G., Velupillai, Y.N., Tannahill, C., Early life socioeconomic adversity is associated in adult life with chronic inflammation, carotid atherosclerosis, poorer lung function and decreased cognitive performance: a cross-sectional, population-based study. BMC Public Health, 11, 2011, 42.
69. Penz, M., Kirschbaum, C., Buske-Kirschbaum, A., Wekenborg, M.K., Miller, R., Stressful life events predict one-year change of leukocyte composition in peripheral blood. Psychoneuroendocrinology 94 (2018), 17–24.
70. Petrowski, K., Wintermann, G.-B., Siepmann, M., Cortisol response to repeated psychosocial stress. Appl. Psychophysiol. Biofeedback 37 (2012), 103–107.
71. Petrowski, K., Wintermann, G.-B., Kirschbaum, C., Strahler, J., Salivary alpha-amylase response following repeated psychosocial stress in patients with panic disorder. J. Anxiety Disord. 37 (2016), 54–63.
72. Picard, M., McEwen, B.S., Psychological stress and mitochondria: a conceptual framework. Psychosom. Med. 80 (2018), 126–140.
73. Pinquart, M., Sörensen, S., Differences between caregivers and noncaregivers in psychological health and physical health: a meta-analysis. Psychol. Aging 18 (2003), 250–267.
74. Potier, F., Degryse, J.-M., de Saint-Hubert, M., Impact of caregiving for older people and pro-inflammatory biomarkers among caregivers: a systematic review. Aging Clin. Exp. Res. 30 (2018), 119–132.
75. Puterman, E., Epel, E.S., O'Donovan, A., Prather, A.A., Aschbacher, K., Dhabhar, F.S., Anger is associated with increased IL-6 stress reactivity in women, but only among those low in social support. Int. J. Behav. Med. 21 (2014), 936–945.
76. Ranjit, N., Diez-Roux, A.V., Shea, S., Cushman, M., Seeman, T., Jackson, S.A., Ni, H., Psychosocial factors and inflammation in the multi-ethnic study of atherosclerosis. Arch. Intern. Med. 167 (2007), 174–181.
77. Rohleder, N., Acute and chronic stress induced changes in sensitivity of peripheral inflammatory pathways to the signals of multiple stress systems –2011 curt Richter Award Winner. Psychoneuroendocrinology 37 (2012), 307–316.
78. Rohleder, N., Stimulation of systemic low-grade inflammation by psychosocial stress. Psychosom. Med. 76 (2014), 181–189.
79. Rohleder, N., Beulen, S.E., Chen, E., Wolf, J.M., Kirschbaum, C., Stress on the dance floor: the cortisol stress response to social-evaluative threat in competitive ballroom dancers. Pers. Soc. Psychol. Bull. 33 (2007), 69–84.
80. Rohleder, N., Marin, T.J., Ma, R., Miller, G.E., Biologic cost of caring for a cancer patient: dysregulation of pro- and anti-inflammatory signaling pathways. J. Clin. Oncol. 27 (2009), 2909–2915.
81. Rohleder, N., Wolf, J.M., Wolf, O.T., Glucocorticoid sensitivity of cognitive and inflammatory processes in depression and posttraumatic stress disorder. Neurosci. Biobehav. Rev. 35 (2010), 104–114.
82. Saban, K.L., Mathews, H.L., Collins, E.G., Hogan, N.S., Tell, D., Bryant, F.B., Pape, T.L.B., Griffin, J.M., Janusek, L.W., The man i once knew: grief and inflammation in female partners of veterans with traumatic brain injury. Biol. Res. Nurs. 18:1 (2016), 50–59.
83. Saban, K.L., Mathews, H.L., Bryant, F.B., Tell, D., Joyce, C., DeVon, H.A., Witek Janusek, L., Perceived discrimination is associated with the inflammatory response to acute laboratory stress in women at risk for cardiovascular disease. Brain Behav. Immun., 2018, 10.1016/j.bbi.2018.07.010.
84. Sapolsky, R.M., Romero, L.M., Munck, A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21 (2000), 55–89.
85. Schommer, N.C., Hellhammer, D.H., Kirschbaum, C., Dissociation between reactivity of the hypothalamus-pituitary-adrenal axis and the sympathetic-adrenal-medullary system to repeated psychosocial stress. Psychosom. Med. 65 (2003), 450–460.
86. Schulz, R., Beach, S.R., Caregiving as a risk factor for mortality: the Caregiver Health Effects Study. JAMA 282 (1999), 2215–2219.
87. Segerstrom, S.C., Miller, G.E., Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol. Bull. 130 (2004), 601–630.
88. Segerstrom, S.C., Schipper, L.J., Greenberg, R.N., Caregiving, repetitive thought, and immune response to vaccination in older adults. Brain Behav. Immun. 22 (2008), 744–752.
89. Sephton, S.E., Sapolsky, R.M., Kraemer, H.C., Spiegel, D., Diurnal cortisol rhythm as a predictor of breast cancer survival. J. Natl. Cancer Inst. 92 (2000), 994–1000.
90. Sephton, S.E., Lush, E., Dedert, E.A., Floyd, A.R., Rebholz, W.N., Dhabhar, F.S., Spiegel, D., Salmon, P., Diurnal cortisol rhythm as a predictor of lung cancer survival. Brain Behav. Immun. 30:Suppl (2013), S163–70.
91. Sherwood, P.R., Price, T.J., Weimer, J., Ren, D., Donovan, H.S., Given, C.W., Given, B.A., Schulz, R., Prince, J., Bender, C., Boele, F.W., Marsland, A.L., Neuro-oncology family caregivers are at risk for systemic inflammation. J. Neurooncol. 128 (2016), 109–118.
92. Shields, G.S., Kuchenbecker, S.Y., Pressman, S.D., Sumida, K.D., Slavich, G.M., Better cognitive control of emotional information is associated with reduced pro-inflammatory cytokine reactivity to emotional stress. Stress 19 (2016), 63–68.
93. Slavich, G.M., Understanding inflammation, its regulation, and relevance for health: a top scientific and public priority. Brain Behav. Immun. 45 (2015), 13–14.
94. Slavich, G.M., Cole, S.W., The emerging field of human social genomics. Clin. Psychol. Sci. 1 (2013), 331–348.
95. Slavich, G.M., Irwin, M.R., From stress to inflammation and major depressive disorder: a social signal transduction theory of depression. Psychol. Bull. 140 (2014), 774–815.
96. Slavish, D.C., Graham-Engeland, J.E., Smyth, J.M., Engeland, C.G., Salivary markers of inflammation in response to acute stress. Brain Behav. Immun. 44 (2015), 253–269.
97. Steptoe, A., Owen, N., Kunz-Ebrecht, S., Mohamed-Ali, V., Inflammatory cytokines, socioeconomic status, and acute stress responsivity. Brain Behav. Immun. 16 (2002), 774–784.
98. 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. 21 (2007), 901–912.
99. Suarez, E.C., C-reactive protein is associated with psychological risk factors of cardiovascular disease in apparently healthy adults. Psychosom. Med. 66 (2004), 684–691.
100. Thoma, M.V., Gianferante, D., Hanlin, L., Fiksdal, A., Chen, X., Rohleder, N., Stronger hypothalamus-pituitary-adrenal axis habituation predicts lesser sensitization of inflammatory response to repeated acute stress exposures in healthy young adults. Brain Behav. Immun. 61 (2017), 228–235.
101. Toker, S., Shirom, A., Shapira, I., Berliner, S., Melamed, S., The association between burnout, depression, anxiety, and inflammation biomarkers: C-reactive protein and fibrinogen in men and women. J. Occup. Health Psychol. 10 (2005), 344–362.
102. von Känel, R., Dimsdale, J.E., Mills, P.J., Ancoli-Israel, S., Patterson, T.L., Mausbach, B.T., Grant, I., Effect of Alzheimer caregiving stress and age on frailty markers interleukin-6, C-reactive protein, and D-dimer. J. Gerontol. A Biol. Sci. Med. Sci. 61 (2006), 963–969.
103. von Känel, R., Kudielka, B.M., Preckel, D., Hanebuth, D., Fischer, J.E., Delayed response and lack of habituation in plasma interleukin-6 to acute mental stress in men. Brain Behav. Immun. 20 (2006), 40–48.
104. von Känel, R., Bellingrath, S., Kudielka, B.M., Association between burnout and circulating levels of pro- and anti-inflammatory cytokines in schoolteachers. J. Psychosom. Res. 65 (2008), 51–59.
105. von Känel, R., Mills, P.J., Mausbach, B.T., Dimsdale, J.E., Patterson, T.L., Ziegler, M.G., Ancoli-Israel, S., Allison, M., Chattillion, E.A., Grant, I., Effect of Alzheimer caregiving on circulating levels of C-reactive protein and other biomarkers relevant to cardiovascular disease risk: a longitudinal study. Gerontology 58 (2012), 354–365.
106. von Känel, R., Mausbach, B.T., Mills, P.J., Dimsdale, J.E., Patterson, T.L., Ancoli-Israel, S., Ziegler, M.G., Allison, M., Chattillion, E.A., Grant, I., Longitudinal relationship of low leisure satisfaction but not depressive symptoms with systemic low-grade inflammation in dementia caregivers. J. Gerontol. B Psychol. Sci. Soc. Sci. 69 (2014), 397–407.
107. Weinstein, A.A., Deuster, P.A., Francis, J.L., Bonsall, R.W., Tracy, R.P., Kop, W.J., Neurohormonal and inflammatory hyper-responsiveness to acute mental stress in depression. Biol. Psychol. 84 (2010), 228–234.
108. Wirtz, P.H., von Känel, R., Psychological stress, inflammation, and coronary heart disease. Curr. Cardiol. Rep., 19, 2017, 111.
109. Woody, A., Figueroa, W.S., Benencia, F., Zoccola, P.M., Trait reflection predicts interleukin-6 response to a social-evaluative stressor. Brain Behav. Immun. 52 (2016), 27–31.
110. Wüst, S., Federenko, I.S., van Rossum, E.F.C., Koper, J.W., Hellhammer, D.H., Habituation of cortisol responses to repeated psychosocial stress-further characterization and impact of genetic factors. Psychoneuroendocrinology 30 (2005), 199–211.
111. Yamakawa, K., Matsunaga, M., Isowa, T., Kimura, K., Kasugai, K., Yoneda, M., Kaneko, H., Ohira, H., Transient responses of inflammatory cytokines in acute stress. Biol. Psychol. 82 (2009), 25–32.