Greater lifetime stress exposure predicts blunted cortisol but heightened DHEA responses to acute stress

Stress and Health

Volumn 35, Issue 1, 2019, Pages 15-26

  Lam, Jovian C W ^a   Shields, Grant S ^b   Trainor, Brian C ^b   Slavich, George M ^c   Yonelinas, Andrew P ^b  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

allostatic load; cortisol; cumulative life stress; DHEA; disease; health

Indexed keywords

HYDROCORTISONE; PRASTERONE; BIOLOGICAL MARKER;

ACUTE STRESS; ADULT; ADULTHOOD; ARTICLE; FEMALE; HORMONE RESPONSE; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIFE EVENT; LIFE STRESS; LIFESPAN; MALE; MARRIAGE; NORMAL HUMAN; SALIVA LEVEL; SOCIAL STRESS; YOUNG ADULT; ADOLESCENT; ALLOSTASIS; CHEMISTRY; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; METABOLISM; SALIVA;

ADOLESCENT; ADULT; ALLOSTASIS; BIOMARKERS; DEHYDROEPIANDROSTERONE; FEMALE; HEALTHY VOLUNTEERS; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PITUITARY-ADRENAL SYSTEM; SALIVA; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 85053554653     PISSN: 15323005     EISSN: 15322998     Source Type: Journal    
DOI: 10.1002/smi.2835     Document Type: Article

References (58)

1. Aguilera, G. (2011). HPA axis responsiveness to stress: Implications for healthy aging. Experimental Gerontology, 46, 90–95. https://doi.org/10.1016/j.exger.2010.08.023
2. Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561–571. https://doi.org/10.1001/archpsyc.1961.01710120031004
3. Bower, J. E., Crosswell, A. D., & Slavich, G. M. (2014). Childhood adversity and cumulative life stress: Risk factors for cancer-related fatigue. Clinical Psychological, 2, 108–115. https://doi.org/10.1177/2167702613496243
4. Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271–301. https://doi.org/10.1017/S0954579405050145
5. Buford, T. W., & Willoughby, D. S. (2008). Impact of DHEA (S) and cortisol on immune function in aging: A brief review. Applied Physiology, Nutrition, and Metabolism, 33, 429–433. https://doi.org/10.1139/H08-013
6. Bunea, I. M., Szentágotai-Tătar, A., & Miu, A. C. (2017). Early-life adversity and cortisol response to social stress: A meta-analysis. Translational Psychiatry, 7:1274. https://doi.org/10.1038/s41398-017-0032-3
7. Buske-Kirschbaum, A., Ebrecht, M., & Hellhammer, D. H. (2010). Blunted HPA axis responsiveness to stress in atopic patients is associated with the acuity and severeness of allergic inflammation. Brain, Behavior, and Immunity, 24, 1347–1353. https://doi.org/10.1016/j.bbi.2010.06.013
8. Carpenter, L. L., Carvalho, J. P., Tyrka, A. R., Wier, L. M., Mello, A. F., Mello, M. F., … Price, L. H. (2007). Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biological Psychiatry, 62, 1080–1087. https://doi.org/10.1016/j.biopsych.2007.05.002
9. Carroll, D., Ginty, A. T., Whittaker, A. C., Lovallo, W. R., & de Rooij, S. R. (2017). The behavioural, cognitive, and neural corollaries of blunted cardiovascular and cortisol reactions to acute psychological stress. Neuroscience & Biobehavioral Reviews, 77, 74–86. https://doi.org/10.1016/j.neubiorev.2017.02.025
10. Charney, D. S. (2004). Psychobiological mechanisms of resilience and vulnerability. American Journal of Psychiatry, 161, 195–216. https://doi.org/10.1176/foc.2.3.368
11. Cuneo, M. G., Schrepf, A., Slavich, G. M., Thaker, P. H., Goodheart, M., Bender, D., … Lutgendorf, S. K. (2017). Diurnal cortisol rhythms, fatigue and psychosocial factors in five-year survivors of ovarian cancer. Psychoneuroendocrinology, 84, 139–142. https://doi.org/10.1016/j.psyneuen.2017.06.019
12. Epel, E. S., Blackburn, E. H., Lin, J., Dhabhar, F. S., Adler, N. E., Morrow, J. D., & Cawthon, R. M. (2004). Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences of the United States of America, 101, 17312-17315. https://doi.org/10.1073/pnas.0407162101
13. Epel, E. S., Crosswell, A. D., Mayer, S. E., Prather, A. A., Slavich, G. M., Puterman, E., & Mendes, W. B. (2018). More than a feeling: A unified view of stress measurement for population science. Frontiers in Neuroendocrinology, 49, 146–169. https://doi.org/10.1016/j.yfrne.2018.03.001
14. Feder, A., Nestler, E. J., & Charney, D. S. (2009). Psychobiology and molecular genetics of resilience. Nature Reviews Neuroscience, 10, 446–457. https://doi.org/10.1038/nrn2649
15. Gill, J., Vythilingam, M., & Page, G. G. (2008). Low cortisol, high DHEA, and high levels of stimulated TNF-α, and IL-6 in women with PTSD. Journal of Traumatic Stress, 21, 530–539. https://doi.org/10.1002/jts.20372
16. Goldfarb, E. V., Shields, G. S., Daw, N. D., Slavich, G. M., & Phelps, E. A. (2017). Low lifetime stress exposure is associated with reduced stimulus–response memory. Learning & Memory, 24, 162–168. https://doi.org/10.1101/lm.045179.117
17. Hammen, C., Adrian, C., Gordon, D., Burge, D., Jaenicke, C., & Hiroto, D. (1987). Children of depressed mothers: Maternal strain and symptom predictors of dysfunction. Journal of Abnormal Psychology, 96, 190–198. https://doi.org/10.1037/0021-843X.96.3.190
18. Hu, Y., Cardounel, A., Gursoy, E., Anderson, P., & Kalimi, M. (2000). Anti-stress effects of dehydroepiandrosterone: Protection of rats against repeated immobilization stress-induced weight loss, glucocorticoid receptor production, and lipid peroxidation. Biochemical Pharmacology, 59, 753–762. https://doi.org/10.1016/S0006-2952(99)00385-8
19. Jiang, X., Zhong, W., An, H., Fu, M., Chen, Y., Zhang, Z., & Xiao, Z. (2017). Attenuated DHEA and DHEA-S response to acute psychosocial stress in individuals with depressive disorders. Journal of Affective Disorders, 215, 118–124. https://doi.org/10.1016/j.jad.2017.03.013
20. Kajantie, E., & Phillips, D. I. (2006). The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology, 31, 151–178. https://doi.org/10.1016/j.psyneuen.2005.07.002
21. Kalimi, M., Shafagoj, Y., Loria, R., Padgett, D., & Regelson, W. (1994). Anti-glucocorticoid effects of dehydroepiandrosterone (DHEA). Molecular and Cellular Biochemistry, 131, 99–104. https://doi.org/10.1007/BF00925945
22. Kamin, H. S., & Kertes, D. A. (2017). Cortisol and DHEA in development and psychopathology. Hormones and Behavior, 89, 69–85. https://doi.org/10.1016/j.yhbeh.2016.11.018
23. Lennartsson, A. K., Sjörs, A., & Jonsdottir, I. H. (2015). Indication of attenuated DHEA-S response during acute psychosocial stress in patients with clinical burnout. Journal of Psychosomatic Research, 79, 107–111. https://doi.org/10.1016/j.jpsychores.2015.05.011
24. Lennartsson, A. K., Theorell, T., Kushnir, M. M., Bergquist, J., & Jonsdottir, I. H. (2013). Perceived stress at work is associated with attenuated DHEA-S response during acute psychosocial stress. Psychoneuroendocrinology, 38, 1650–1657. https://doi.org/10.1016/j.psyneuen.2013.01.010
25. Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445. https://doi.org/10.1038/nrn2639
26. Maninger, N., Capitanio, J. P., Mason, W. A., Ruys, J. D., & Mendoza, S. P. (2010). Acute and chronic stress increase DHEAS concentrations in rhesus monkeys. Psychoneuroendocrinology, 35, 1055–1062. https://doi.org/10.1016/j.psyneuen.2010.01.006
27. Maninger, N., Wolkowitz, O. M., Reus, V. I., Epel, E. S., & Mellon, S. H. (2009). Neurobiological and neuropsychiatric effects of dehydroepiandrosterone (DHEA) and DHEA sulfate (DHEAS). Frontiers in Neuroendocrinology, 30, 65–91. https://doi.org/10.1016/j.yfrne.2008.11.002
28. Matthews, K. A., Gump, B. B., & Owens, J. F. (2001). Chronic stress influences cardiovascular and neuroendocrine responses during acute stress and recovery, especially in men. Health Psychology, 20, 403–410. https://doi.org/10.1037/0278-6133.20.6.403
29. McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44. https://doi.org/10.1111/j.1749-6632.1998.tb09546.x
30. McEwen, B. S., & Gianaros, P. J. (2011). Stress- and allostasis-induced brain plasticity. Annual Review of Medicine, 62, 431–445. https://doi.org/10.1146/annurev-med-052209-100430
31. Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin, 133, 25–45. https://doi.org/10.1037/0033-2909.133.1.25
32. O'Connor, M. F., Bower, J. E., Cho, H. J., Creswell, J. D., Dimitrov, S., Hamby, M. E., … Thomas, K. S. (2009). To assess, to control, to exclude: Effects of biobehavioral factors on circulating inflammatory markers. Brain, Behavior, and Immunity, 23, 887–897. https://doi.org/10.1016/j.bbi.2009.04.005
33. Pfau, M. L., & Russo, S. J. (2015). Peripheral and central mechanisms of stress resilience. Neurobiology of Stress, 1, 66–79. https://doi.org/10.1016/j.ynstr.2014.09.004
34. Prall, S. P., Larson, E. E., & Muehlenbein, M. P. (2017). The role of dehydroepiandrosterone on functional innate immune responses to acute stress. Stress and Health, 33, 656–664. https://doi.org/10.1002/smi.2752
35. Ritsner, M., Maayan, R., Gibel, A., Strous, R. D., Modai, I., & Weizman, A. (2004). Elevation of the cortisol/dehydroepiandrosterone ratio in schizophrenia patients. European Neuropsychopharmacology, 14, 267–273. https://doi.org/10.1016/j.euroneuro.2003.09.003
36. Rohleder, N., Wolf, J. M., Maldonado, E. F., & Kirschbaum, C. (2006). The psychosocial stress-induced increase in salivary alpha-amylase is independent of saliva flow rate. Psychophysiology, 43, 645–652. https://doi.org/10.1111/j.1469-8986.2006.00457.x
37. Seo, D., Tsou, K. A., Ansell, E. B., Potenza, M. N., & Sinha, R. (2014). Cumulative adversity sensitizes neural response to acute stress: Association with health symptoms. Neuropsychopharmacology, 39, 670–680. https://doi.org/10.1038/npp.2013.250
38. Shields, G. S., Doty, D., Shields, R. H., Gower, G., Slavich, G. M., & Yonelinas, A. P. (2017). Recent life stress exposure is associated with poorer long-term memory, working memory, and self-reported memory. Stress, 20, 598–607. https://doi.org/10.1080/10253890.2017.1380620
39. Shields, G. S., Lam, J. C. W., Trainor, B. C., & Yonelinas, A. P. (2016). Exposure to acute stress enhances decision-making competence: Evidence for the role of DHEA. Psychoneuroendocrinology, 67, 51–60. https://doi.org/10.1016/j.psyneuen.2016.01.031
40. Shields, G. S., Moons, W. G., & Slavich, G. M. (2017). Better executive function under stress mitigates the effects of recent life stress exposure on health in young adults. Stress, 20, 92–102. https://doi.org/10.1080/10253890.2017.1286322
41. Shields, G. S., & Slavich, G. M. (2017). Lifetime stress exposure and health: A review of contemporary assessment methods and biological mechanisms. Social and Personality Psychology Compass, 11:8. https://doi.org/10.1111/spc3.12335
42. Siegrist, J., Klein, D., & Voigt, K. H. (1997). Linking sociological with physiological data: The model of effort-reward imbalance at work. Acta Physiologica Scandinavica. Supplementum, 640, 112–116.
43. Silverman, M. N., & Sternberg, E. M. (2012). Glucocorticoid regulation of inflammation and its functional correlates: From HPA axis to glucocorticoid receptor dysfunction. Annals of the New York Academy of Sciences, 1261, 55–63. https://doi.org/10.1111/j.1749-6632.2012.06633.x
44. Slavich, G. M. (2016). Life stress and health: A review of conceptual issues and recent findings. Teaching of Psychology, 43, 346–355. https://doi.org/10.1177/0098628316662768
45. Slavich, G. M., & Irwin, M. R. (2014). From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. Psychological Bulletin, 140, 774–815. https://doi.org/10.1037/a0035302
46. Slavich, G. M., O'Donovan, A., Epel, E. S., & Kemeny, M. E. (2010). Black sheep get the blues: A psychobiological model of social rejection and depression. Neuroscience and Biobehavioral Reviews, 35, 39–45. https://doi.org/10.1016/j.neubiorev.2010.01.003
47. Slavich, G. M., & Shields, G. S. (2018). Assessing lifetime stress exposure using the Stress and Adversity Inventory for Adults (Adult STRAIN): An overview and initial validation. Psychosomatic Medicine, 80, 17–27. https://doi.org/10.1097/PSY.0000000000000534
48. Slavich, G. M., Thornton, T., Torres, L. D., Monroe, S. M., & Gotlib, I. H. (2009). Targeted rejection predicts hastened onset of major depression. Journal of Social and Clinical Psychology, 28, 223–243. https://doi.org/10.1521/jscp.2009.28.2.223
49. Starr, L. R., Dienes, K., Stroud, C. B., Shaw, Z. A., Li, Y. I., Mlawer, F., & Huang, M. (2017). Childhood adversity moderates the influence of proximal episodic stress on the cortisol awakening response and depressive symptoms in adolescents. Development and Psychopathology, 29, 1877–1893. https://doi.org/10.1017/S0954579417001468
50. Tomiyama, A. J., Dallman, M. F., & Epel, E. S. (2011). Comfort food is comforting to those most stressed: Evidence of the chronic stress response network in high stress women. Psychoneuroendocrinology, 36, 1513–1519. https://doi.org/10.1016/j.psyneuen.2011.04.005
51. Tomiyama, A. J., O'Donovan, A., Lin, J., Puterman, E., Lazaro, A., Chan, J., … Epel, E. (2012). Does cellular aging relate to patterns of allostasis? An examination of basal and stress reactive HPA axis activity and telomere length. Physiology & Behavior, 106, 40–45. https://doi.org/10.1016/j.physbeh.2011.11.016
52. Turner, R. J., & Lloyd, D. A. (1995). Lifetime traumas and mental health: The significance of cumulative adversity. Journal of Health and Social Behavior, 36, 360–376. https://doi.org/10.2307/2137325
53. Vining, R. F., & McGinley, R. A. (1987). The measurement of hormones in saliva: Possibilities and pitfalls. Journal of Steroid Biochemistry, 27, 81–94. https://doi.org/10.1016/0022-4731(87)90297-4
54. 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. Psychoneuroendocrinology, 36, 514–522. https://doi.org/10.1016/j.psyneuen.2010.08.004
55. Walker, F. R., Pfingst, K., Carnevali, L., Sgoifo, A., & Nalivaiko, E. (2017). In the search for integrative biomarker of resilience to psychological stress. Neuroscience & Biobehavioral Reviews, 74, 310–320. https://doi.org/10.1016/j.neubiorev.2016.05.003
56. Wolf, O. T., Köster, B., Kirschbaum, C., Pietrowsky, R., Kern, W., Hellhammer, D. H., … Fehm, H. L. (1997). A single administration of dehydroepiandrosterone does not enhance memory performance in young healthy adults, but immediately reduces cortisol levels. Biological Psychiatry, 42, 845–848. https://doi.org/10.1016/S0006-3223(97)00323-5
57. Yehuda, R., Brand, S. R., Golier, J. A., & Yang, R. K. (2006). Clinical correlates of DHEA associated with post-traumatic stress disorder. Acta Psychiatrica Scandinavica, 114, 187–193. https://doi.org/10.1111/j.1600-0447.2006.00801.x
58. Young, A. H., Gallagher, P., & Porter, R. J. (2002). Elevation of the cortisol-dehydroepiandrosterone ratio in drug-free depressed patients. American Journal of Psychiatry, 159, 1237–1239. https://doi.org/10.1176/appi.ajp.159.7.1237