Current posttraumatic stress disorder and exaggerated threat sensitivity associated with elevated inflammation in the Mind Your Heart Study

Brain, Behavior, and Immunity

Volumn 60, Issue , 2017, Pages 198-205

  O'Donovan, Aoife ^a,b   Ahmadian, Ashkan J ^a,b   Neylan, Thomas C ^a,b   Pacult, Mark A ^a,b   Edmondson, Donald ^c   Cohen, Beth E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Department of Medicine   (United States)

Author keywords

Avoidance; C reactive protein; Fibrinogen; Inflammation; Posttraumatic stress disorder; Threat reactivity; Threat sensitivity; Trauma; Veterans; White blood cell count

Indexed keywords

FIBRINOGEN; BIOLOGICAL MARKER; C REACTIVE PROTEIN;

ADULT; AGE DISTRIBUTION; ALCOHOL CONSUMPTION; ARTICLE; BODY MASS; DISEASE SEVERITY; EDUCATIONAL STATUS; ETHNICITY; FEMALE; FIBRINOGEN BLOOD LEVEL; GENDER; HUMAN; INFLAMMATION; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; PHYSICAL ACTIVITY; PHYSICAL INACTIVITY; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PSYCHOLOGICAL RATING SCALE; SMOKING; SOCIAL STATUS; SYMPTOM ASSESSMENT; AGED; BIOSYNTHESIS; BLOOD; COMORBIDITY; METABOLISM; MIDDLE AGED; PSYCHOLOGY; VETERAN;

ADULT; AGED; BIOMARKERS; C-REACTIVE PROTEIN; COMORBIDITY; FEMALE; FIBRINOGEN; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; STRESS DISORDERS, POST-TRAUMATIC; VETERANS;

EID: 85005873059     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.10.014     Document Type: Article

References (66)

1. Aadahl, M., Kjaer, M., Kristensen, J.H., Mollerup, B., Jorgensen, T., Self-reported physical activity compared with maximal oxygen uptake in adults. Eur. J. Cardiovasc. Prev. Rehabil. 14 (2007), 422–428.
2. Abraham, G., Sundaram, V., Sundaram, V., Mathew, M., Leslie, N., Sathiah, V., C-Reactive protein, a valuable predictive marker in chronic kidney disease. Saudi J. Kidney Dis. Transpl. 20 (2009), 811–815.
3. Ainsworth, B.E., Jacobs, D.R. Jr., Leon, A.S., Validity and reliability of self-reported physical activity status: the Lipid Research Clinics questionnaire. Med. Sci. Sports Exerc. 25 (1993), 92–98.
4. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders (4th Edition, Text Revision). 2000, American Psychiatric Association, Washington, DC.
5. Black, P.H., Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav. Immun. 16 (2002), 622–653.
6. Blanchard, E.B., Hickling, E.J., Taylor, A.E., Loos, W.R., Gerardi, R.J., Psychological morbidity associated with motor vehicle accidents. Behav. Res. Ther. 32 (1994), 283–290.
7. Boscarino, J.A., Posttraumatic stress disorder and physical illness: results from clinical and epidemiologic studies. Ann. N. Y. Acad. Sci. 1032 (2004), 141–153.
8. Boscarino, J.A., Posttraumatic stress disorder and mortality among U.S. Army veterans 30 years after military service. Ann. Epidemiol. 16 (2006), 248–256.
9. Boscarino, J.A., Chang, J., Electrocardiogram abnormalities among men with stress-related psychiatric disorders: implications for coronary heart disease and clinical research. Ann. Behav. Med. 21 (1999), 227–234.
10. Boscarino, J.A., Forsberg, C.W., Goldberg, J., A twin study of the association between PTSD symptoms and rheumatoid arthritis. Psychosom. Med. 72 (2010), 481–486.
11. Bowles, H.R., FitzGerald, S.J., Morrow, J.R. Jr., Jackson, A.W., Blair, S.N., Construct validity of self-reported historical physical activity. Am. J. Epidemiol. 160 (2004), 279–286.
12. Bradley, K.A., Bush, K.R., McDonell, M.B., Malone, T., Fihn, S.D., Screening for problem drinking: Comparison of CAGE and AUDIT. J. Gen. Intern. Med. 13 (1998), 379–388.
13. Bush, K., Kivlahan, D.R., McDonell, M.B., Fihn, S.D., Bradley, K.A., The AUDIT alcohol consumption questions (AUDIT-C): an effective brief screening test for problem drinking. Ambulatory Care Quality Improvement Project (ACQUIP). Alcohol Use Disorders Identification Test. Arch. Intern. Med. 158 (1998), 1789–1795.
14. Chen, J., Song, Y., Yang, J., Zhang, Y., Zhao, P., Zhu, X.J., Su, H.C., The contribution of TNF-alpha in the amygdala to anxiety in mice with persistent inflammatory pain. Neurosci. Lett. 541 (2013), 275–280.
15. Cohen, B.E., Marmar, C., Ren, L., Bertenthal, D., Seal, K.H., Association of cardiovascular risk factors with mental health diagnoses in Iraq and Afghanistan war veterans using VA health care. JAMA 302 (2009), 489–492.
16. Cohen, B.E., Marmar, C.R., Neylan, T.C., Schiller, N.B., Ali, S., Whooley, M.A., Posttraumatic stress disorder and health-related quality of life in patients with coronary heart disease: findings from the Heart and Soul Study. Arch. Gen. Psychiatry 66 (2009), 1214–1220.
17. Cohen, B.E., Neylan, T.C., Yaffe, K., Samuelson, K.W., Li, Y., Barnes, D.E., Posttraumatic stress disorder and cognitive function: findings from the mind your heart study. J. Clin. Psychiatry 74 (2013), 1063–1070.
18. Cohen, S., Janicki-Deverts, D., Miller, G.E., Psychological stress and disease. JAMA 298 (2007), 1685–1687.
19. Danese, A., Pariante, C.M., Caspi, A., Taylor, A., Poulton, R., Childhood maltreatment predicts adult inflammation in a life-course study. Proc. Natl. Acad. Sci. USA 104 (2007), 1319–1324.
20. Dantzer, R., O'Connor, J.C., Freund, G.G., Johnson, R.W., Kelley, K.W., From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9 (2008), 46–56.
21. Dekaris, D., Sabioncello, A., Mazuran, R., Rabatic, S., Svoboda-Beusan, I., Racunica, N.L., Tomasic, J., Multiple changes of immunologic parameters in prisoners of war. Assessments after release from a camp in Manjaca. Bosnia. JAMA 270 (1993), 595–599.
22. Dohrenwend, B.P., Turner, J.B., Turse, N.A., Adams, B.G., Koenen, K.C., Marshall, R., Continuing controversy over the psychological risks of Vietnam for U.S. veterans. J. Trauma. Stress 20 (2007), 449–465.
23. Du Clos, T.W., Function of C-reactive protein. Ann. Med. 32 (2000), 274–278.
24. Engler, H., Doenlen, R., Engler, A., Riether, C., Prager, G., Niemi, M.B., Pacheco-Lopez, G., Krugel, U., Schedlowski, M., Acute amygdaloid response to systemic inflammation. Brain Behav. Immun. 25 (2011), 1384–1392.
25. Eraly, S.A., Nievergelt, C.M., Maihofer, A.X., Barkauskas, D.A., Biswas, N., Agorastos, A., O'Connor, D.T., Baker, D.G., Assessment of plasma C-reactive protein as a biomarker of posttraumatic stress disorder risk. JAMA psychiat. 71:4 (2014), 423–431.
26. Gill, J.M., Saligan, L., Lee, H., Rotolo, S., Szanton, S., Women in recovery from PTSD have similar inflammation and quality of life as non-traumatized controls. J. Psychosom. Res. 74 (2013), 301–306.
27. Heath, N.M., Chesney, S.A., Gerhart, J.I., Goldsmith, R.E., Luborsky, J.L., Stevens, N.R., Hobfoll, S.E., Interpersonal violence, PTSD, and inflammation: potential psychogenic pathways to higher C-reactive protein levels. Cytokine 63 (2013), 172–178.
28. Hoge, E.A., Brandstetter, K., Moshier, S., Pollack, M.H., Wong, K.K., Simon, N.M., Broad spectrum of cytokine abnormalities in panic disorder and posttraumatic stress disorder. Depress Anxiety 26 (2009), 447–455.
29. Inagaki, T.K., Muscatell, K.A., Irwin, M.R., Cole, S.W., Eisenberger, N.I., Inflammation selectively enhances amygdala activity to socially threatening images. Neuroimage 59 (2012), 3222–3226.
30. Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D.S., Quinn, K., Sanislow, C., Wang, P., Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167 (2010), 748–751.
31. Ironson, G., Wynings, C., Schneiderman, N., Baum, A., Rodriguez, M., Greenwood, D., Benight, C., Antoni, M., LaPerriere, A., Huang, H.S., Klimas, N., Fletcher, M.A., Posttraumatic stress symptoms, intrusive thoughts, loss, and immune function after Hurricane Andrew. Psychosom. Med. 59 (1997), 128–141.
32. Ix, J.H., Shlipak, M.G., Liu, H.H., Schiller, N.B., Whooley, M.A., Association between renal insufficiency and inducible ischemia in patients with coronary artery disease: the heart and soul study. J. Am. Soc. Nephrol. 14 (2003), 3233–3238.
33. Jackson, A.W., Morrow, J.R. Jr., Bowles, H.R., FitzGerald, S.J., Blair, S.N., Construct validity evidence for single-response items to estimate physical activity levels in large sample studies. Res. Q. Exerc. Sport 78 (2007), 24–31.
34. Kawamura, N., Kim, Y., Asukai, N., Suppression of cellular immunity in men with a past history of posttraumatic stress disorder. Am. J. Psychiatry 158 (2001), 484–486.
35. Kurtze, N., Rangul, V., Hustvedt, B.E., Flanders, W.D., Reliability and validity of self-reported physical activity in the Nord-Trondelag Health Study: HUNT 1. Scand. J. Public Health 36 (2008), 52–61.
36. Marshall, R.D., Olfson, M., Hellman, F., Blanco, C., Guardino, M., Struening, E.L., Comorbidity, impairment, and suicidality in subthreshold PTSD. Am. J. Psychiatry 158 (2001), 1467–1473.
37. Michopoulos, V., Rothbaum, A.O., Jovanovic, T., Almli, L.M., Bradley, B., Rothbaum, B.O., Gillespie, C.F., Ressler, K.J., Association of CRP genetic variation and CRP level with elevated PTSD symptoms and physiological responses in a civilian population with high levels of trauma. Am. J. Psychiatry 172 (2015), 353–362.
38. O'Connor, M.F., Irwin, M.R., Links between behavioral factors and inflammation. Clin. Pharmacol. Ther. 87 (2010), 479–482.
39. O'Donovan, A., Chao, L.L., Paulson, J., Samuelson, K.W., Shigenaga, J.K., Grunfeld, C., Weiner, M.W., Neylan, T.C., Altered inflammatory activity associated with reduced hippocampal volume and more severe posttraumatic stress symptoms in Gulf War veterans. Psychoneuroendocrinology 51 (2015), 557–566.
40. O'Donovan, A., Cohen, B.E., Seal, K.H., Bertenthal, D., Margaretten, M., Nishimi, K., Neylan, T.C., Elevated risk for autoimmune disorders in Iraq and Afghanistan veterans with posttraumatic stress disorder. Biol. Psychiatry 77 (2015), 365–374.
41. O'Donovan, A., Neylan, T.C., Metzler, T., Cohen, B.E., Lifetime exposure to traumatic psychological stress is associated with elevated inflammation in the Heart and Soul Study. Brain Behav. Immun. 26 (2012), 642–649.
42. O'Donovan, A., Slavich, G.M., Epel, E.S., Neylan, T.C., Exaggerated neurobiological sensitivity to threat as a mechanism linking anxiety with increased risk for diseases of aging. Neurosci. Biobehav. Rev. 37 (2013), 96–108.
43. O'Donovan, A., Sun, B., Cole, S., Rempel, H., Lenoci, M., Pulliam, L., Neylan, T., Transcriptional control of monocyte gene expression in post-traumatic stress disorder. Dis. Markers 30 (2011), 123–132.
44. Plantinga, L., Bremner, J.D., Miller, A.H., Jones, D.P., Veledar, E., Goldberg, J., Vaccarino, V., Association between posttraumatic stress disorder and inflammation: a twin study. Brain Behav. Immun. 30 (2013), 125–132.
45. Raison, C.L., Rutherford, R.E., Woolwine, B.J., Shuo, C., Schettler, P., Drake, D.F., Haroon, E., Miller, A.H., A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: the role of baseline inflammatory biomarkers. JAMA Psychiatry 70 (2013), 31–41.
46. Sayer, N.A., Noorbaloochi, S., Frazier, P., Carlson, K., Gravely, A., Murdoch, M., Reintegration problems and treatment interests among Iraq and Afghanistan combat veterans receiving VA medical care. Psychiatr. Serv. 61 (2010), 589–597.
47. Seal, K.H., Metzler, T., Gima, K., Bertenthal, D., Maguen, S., Marmar, C.R., 2008. Growing burden of mental disorders among Iraq and Afghanistan Veterans: Trends and risk factors for mental health diagnoses in new users of VA healthcare, 2002–2008. Under Review.
48. 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.
49. Sondergaard, H.P., Hansson, L.O., Theorell, T., The inflammatory markers C-reactive protein and serum amyloid A in refugees with and without posttraumatic stress disorder. Clin. Chim. Acta 342 (2004), 93–98.
50. Spitzer, C., Barnow, S., Volzke, H., Wallaschofski, H., John, U., Freyberger, H.J., Lowe, B., Grabe, H.J., Association of posttraumatic stress disorder with low-grade elevation of C-reactive protein: evidence from the general population. J. Psychiatr. Res. 44 (2010), 15–21.
51. Spoormaker, V.I., Montgomery, P., Disturbed sleep in post-traumatic stress disorder: secondary symptom or core feature?. Sleep Med. Rev. 12 (2008), 169–184.
52. 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.
53. Stuveling, E.M., Hillege, H.L., Bakker, S.J., Gans, R.O., De Jong, P.E., De Zeeuw, D., C-reactive protein is associated with renal function abnormalities in a non-diabetic population. Kidney Int. 63 (2003), 654–661.
54. Talbot, L.S., Maguen, S., Epel, E.S., Metzler, T.J., Neylan, T.C., Posttraumatic stress disorder is associated with emotional eating. J. Trauma. Stress 26 (2013), 521–525.
55. Turner, J.H., Neylan, T.C., Schiller, N.B., Li, Y., Cohen, B.E., Objective evidence of myocardial ischemia in patients with posttraumatic stress disorder. Biol. Psychiatry 74 (2013), 861–866.
56. Vaccarino, V., Bremner, J.D., Afzal, N., Veledar, E., Goldberg, J., Posttraumatic stress disorder is associated with higher C-reactive protein levels. J. Am. Coll. Cardiol., 55, 2010 A176.E1656–A1176.E1656.
57. Vidovic, A., Grubisic-Ilic, M., Kozaric-Kovacic, D., Gotovac, K., Rakos, I., Markotic, A., Rabatic, S., Dekaris, D., Sabioncello, A., Exaggerated platelet reactivity to physiological agonists in war veterans with posttraumatic stress disorder. Psychoneuroendocrinology 36 (2010), 161–172.
58. Vidovic, M., Hisheh, S., Schmitt, L.H., Cortisol and testosterone levels on a weekend and a work day in three mountain villages in the Selska Valley of northwest Slovenia. Ann. Hum. Biol. 34 (2007), 26–33.
59. von Kanel, R., Begre, S., Abbas, C.C., Saner, H., Gander, M.L., Schmid, J.P., Inflammatory biomarkers in patients with posttraumatic stress disorder caused by myocardial infarction and the role of depressive symptoms. Neuroimmunomodulation 17 (2010), 39–46.
60. von Kanel, R., Hepp, U., Buddeberg, C., Keel, M., Mica, L., Aschbacher, K., Schnyder, U., Altered blood coagulation in patients with posttraumatic stress disorder. Psychosom. Med. 68 (2006), 598–604.
61. von Kanel, R., Hepp, U., Kraemer, B., Traber, R., Keel, M., Mica, L., Schnyder, U., Evidence for low-grade systemic proinflammatory activity in patients with posttraumatic stress disorder. J. Psychiatr. Res. 41 (2007), 744–752.
62. Weathers, F.W., Keane, T.M., Davidson, J.R., Clinician-administered PTSD scale: a review of the first ten years of research. Depress Anxiety 13 (2001), 132–156.
63. Whooley, M.A., de Jonge, P., Vittinghoff, E., Otte, C., Moos, R., Carney, R.M., Ali, S., Dowray, S., Na, B., Feldman, M.D., Schiller, N.B., Browner, W.S., Depressive symptoms, health behaviors, and risk of cardiovascular events in patients with coronary heart disease. JAMA 300 (2008), 2379–2388.
64. Wingenfeld, K., Whooley, M.A., Neylan, T.C., Otte, C., Cohen, B.E., Effect of current and lifetime posttraumatic stress disorder on 24-h urinary catecholamines and cortisol: results from the Mind Your Heart Study. Psychoneuroendocrinology 52 (2015), 83–91.
65. Yaffe, K., Vittinghoff, E., Lindquist, K., Barnes, D., Covinsky, K.E., Neylan, T., Kluse, M., Marmar, C., Posttraumatic stress disorder and risk of dementia among US veterans. Arch. Gen. Psychiatry 67 (2010), 608–613.
66. Zen, A.L., Whooley, M.A., Zhao, S., Cohen, B.E., Post-traumatic stress disorder is associated with poor health behaviors: Findings from the Heart and Soul Study. Health Psychol. 31 (2012), 194–201.