Autonomic and inflammatory consequences of posttraumatic stress disorder and the link to cardiovascular disease

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 309, Issue 4, 2015, Pages R315-R321

  Brudey, Chevelle ^a   Park, Jeanie ^b,c   Wiaderkiewicz, Jan ^e   Kobayashi, Ihori ^d   Mellman, Thomas ^d   Marvar, Paul J ^e  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Department of Veterans Affairs Medical Center ^*  (Georgia)

^d HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Cardiovascular disease; Posttraumatic stress disorder; Renin angiotensin system

Indexed keywords

ARTICLE; AUTONOMIC DYSFUNCTION; BLOOD PRESSURE REGULATION; CARDIOVASCULAR DISEASE; CLINICAL STUDY; FEAR; HUMAN; INFLAMMATION; MEMORY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; ANIMAL; AUTONOMIC NERVOUS SYSTEM; AUTONOMIC NERVOUS SYSTEM DISEASES; CARDIOVASCULAR DISEASES; COMPLICATION; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; PROGNOSIS; RISK FACTOR;

AUTACOID;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; AUTONOMIC NERVOUS SYSTEM DISEASES; CARDIOVASCULAR DISEASES; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; PROGNOSIS; RENIN-ANGIOTENSIN SYSTEM; RISK FACTORS; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84939520886     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00343.2014     Document Type: Article

References (119)

1. Abouzeid M, Kelsall HL, Forbes AB, Sim MR, Creamer MC. Posttraumatic stress disorder and hypertension in Australian veterans of the 1991 Gulf War. J Psychosom Res 72: 33–38, 2012.
2. Aguilera G, Young WS, Kiss A, Bathia A. Direct regulation of hypothalamic corticotropin-releasing-hormone neurons by angiotensin II. Neuroendocrinology 61: 437–444, 1995.
3. Ahmadi N, Hajsadeghi F, Mirshkarlo HB, Budoff M, Yehuda R, Ebrahimi R. Post-traumatic stress disorder, coronary atherosclerosis, and mortality. Am J Cardiol 108: 29–33, 2011.
4. Andero R, Heldt SA, Ye K, Liu X, Armario A, Ressler KJ. Effect of 7,8 dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. Am J Psychiatry 168: 163–172, 2011.
5. Anderson C. More indirect evidence of potential neuroprotective benefits of angiotensin receptor blockers. J Hypertens 28: 429, 2010.
6. Armando I, Volpi S, Aguilera G, Saavedra JM. Angiotensin II AT1 receptor blockade prevents the hypothalamic corticotropin-releasing factor response to isolation stress. Brain Res 1142: 92–99, 2007.
7. Baumert J, Lukaschek K, Kruse J, Emeny RT, Koenig W, Känel von R, Ladwig KH, KORA Investigators. No evidence for an association of posttraumatic stress disorder with circulating levels of CRP and IL-18 in a population-based study. Cytokine 63: 201–208, 2013.
8. Beckham JC, Feldman ME, Barefoot JC, Fairbank JA, Helms MJ, Haney TL, Hertzberg MA, Moore SD, Davidson JR. Ambulatory cardiovascular activity in Vietnam combat veterans with and without posttraumatic stress disorder. J Consult Clin Psychol 68: 269–276, 2000.
9. Bedi US, Arora R. Cardiovascular manifestations of posttraumatic stress disorder. J Natl Med Assoc 99: 642–649, 2007.
10. Benicky J, Sanchez-Lemus E, Honda M, Pang T, Orecna M, Wang J, Leng Y, Chuang DM, Saavedra JM. Angiotensin II AT1 receptor blockade ameliorates brain inflammation. Neuropsychopharmacology 36: 857–870, 2011.
11. Benigni A, Cassis P, Remuzzi G. Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med 2: 247–257, 2010.
12. Blechert J, Michael T, Vriends N, Margraf J, Wilhelm FH. Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav Res Ther 45: 2019–2033, 2007.
13. Boscarino JA. Diseases among men 20 years after exposure to severe stress: implications for clinical research and medical care. Psychosom Med 59: 605–614, 1997.
14. Boscarino JA. External-cause mortality after psychologic trauma: the effects of stress exposure and predisposition. Compr Psychiatry 47: 503–514, 2006.
15. Boscarino JA. A prospective study of PTSD and early-age heart disease mortality among Vietnam veterans: implications for surveillance and prevention. Psychosom Med 70: 668–676, 2008.
16. Buckley TC, Kaloupek DG. A meta-analytic examination of basal cardiovascular activity in posttraumatic stress disorder. Psychosom Med 63: 585–594, 2001.
17. Castren E, Saavedra JM. Repeated stress increases the density of angiotensin II binding sites in rat paraventricular nucleus and subfornical organ. Endocrinology 122: 370–372, 1988.
18. Chung IM, Kim YM, Yoo MH, Shin MK, Kim CK, Suh SH. Immobilization stress induces endothelial dysfunction by oxidative stress via the activation of the angiotensin II/its type I receptor pathway. Atherosclerosis 213: 109–114, 2010.
19. Cohen BE, Marmar C, Ren L, Bertenthal D, Seal KH. Association of cardiovascular risk factors with mental health diagnoses in Iraq and Afghanistan war veterans using VA health care. JAMA 302: 489–492, 2009.
20. Coughlin SS. Post-traumatic stress disorder and cardiovascular disease. Open Cardiovasc Med J 5: 164–170, 2011.
21. Crum-Cianflone NF, Bagnell ME, Schaller E, Boyko EJ, Smith B, Maynard C, Ulmer CS, Vernalis M, Smith TC. Impact of combat deployment and posttraumatic stress disorder on newly reported coronary heart disease among US active duty and reserve forces. Circulation 129: 1813–1820, 2014.
22. Dedert EA, Calhoun PS, Watkins LL, Sherwood A, Beckham JC. Posttraumatic stress disorder, cardiovascular, and metabolic disease: a review of the evidence. Ann Behav Med 39: 61–78, 2010.
23. Edmondson D, Cohen BE. Posttraumatic stress disorder and cardiovascular disease. Prog Cardiovasc Dis 55: 548–556, 2013.
24. Edmondson D, Richardson S, Falzon L, Davidson KW, Mills MA, Neria Y. Posttraumatic stress disorder prevalence and risk of recurrence in acute coronary syndrome patients: a meta-analytic review. PLoS One 7: e38915, 2012.
25. Eguchi K, Shimizu M, Hoshide S, Shimada K, Kario K. A bedtime dose of ARB was better than a morning dose in improving baroreflex sensitivity and urinary albumin excretion—the J-TOP study. Clin Exp Hypertens 34: 488–492, 2012.
26. Fagundes CP, Glaser R, Kiecolt-Glaser JK. Stressful early life experiences and immune dysregulation across the lifespan. Brain Behav Immun 27: 8–12, 2013.
27. Gill J, Luckenbaugh D, Charney D, Vythilingam M. Sustained elevation of serum interleukin-6 and relative insensitivity to hydrocortisone differentiates posttraumatic stress disorder with and without depression. Biol Psychiatry 68: 999–1006, 2010.
28. Gill J, Vythilingam M, Page GG. Low cortisol, high DHEA, and high levels of stimulated TNF-α, and IL-6 in women with PTSD. J Traum Stress 21: 530–539, 2008.
29. Gill JM, Saligan L, Woods S, Page G. PTSD is associated with an excess of inflammatory immune activities. Perspect Psychiatr Care 45: 262–277, 2009.
30. Goetz M, Shah A, Goldberg J, Cheema F, Shallenberger L, Murrah NV, Bremner JD, Vaccarino V. Posttraumatic stress disorder, combat exposure, and carotid intima-media thickness in male twins. Am J Epidemiol 180: 989–996, 2014.
31. Gola H, Engler H, Sommershof A, Adenauer H, Kolassa S, Schedlowski M, Groettrup M, Elbert T, Kolassa IT. Posttraumatic stress disorder is associated with an enhanced spontaneous production of pro-inflammatory cytokines by peripheral blood mononuclear cells. BMC Psychiatry 13: 40, 2013.
32. Grassi G, Seravalle G, Cattaneo BM, Lanfranchi A, Vailati S, Giannattasio C, Del Bo A, Sala C, Bolla GB, Pozzi M. Sympathetic activation and loss of reflex sympathetic control in mild congestive heart failure. Circulation 92: 3206–3211, 1995.
33. Grassi G, Seravalle G, Colombo M, Bolla G, Cattaneo BM, Cavagnini F, Mancia G. Body weight reduction, sympathetic nerve traffic, and arterial baroreflex in obese normotensive humans. Circulation 97: 2037–2042, 1998.
34. Grassi G, Seravalle G, Dell’Oro R, Trevano FQ, Bombelli M, Scopelliti F, Facchini A, Mancia G. Comparative effects of candesartan and hydrochlorothiazide on blood pressure, insulin sensitivity, and sympathetic drive in obese hypertensive individuals: results of the CROSS study. J Hypertens 21: 1761–1769, 2003.
35. Guo M, Liu T, Guo JC, Jiang XL, Chen F, Gao YS. Study on serum cytokine levels in posttraumatic stress disorder patients. Asian Pac J Trop Med 5: 323–325, 2012.
36. Heath NM, Chesney SA, Gerhart JI, Goldsmith RE, Luborsky JL, Stevens NR, Hobfoll SE. Interpersonal violence, PTSD, and inflammation: potential psychogenic pathways to higher C-reactive protein levels. Cytokine 63: 172–178, 2013.
37. Hoge EA, Brandstetter K, Moshier S, Pollack MH, Wong KK, Simon NM. Broad spectrum of cytokine abnormalities in panic disorder and posttraumatic stress disorder. Depress Anxiety 26: 447–455, 2009.
38. Hughes JW, Dennis MF, Beckham JC. Baroreceptor sensitivity at rest and during stress in women with posttraumatic stress disorder or major depressive disorder. J Traum Stress 20: 667–676, 2007.
39. Hurt RC, Garrett JC, Keifer OP, Linarea A, Couling L, Speth RC, Milner T, Ressler KJ, Marvar PJ. Angiotensin II receptor type 1 knockout from corticotropin-releasing factor neurons reduces conditioned fear expression in mice FASEB J. 29: Suppl. 840.5, 2015.
40. Jin H, Folsom D, Sasaki A, Mudaliar S, Henry R, Torres M, Golshan S, Glorioso DK, Jeste D. Increased Framingham 10-year risk of coronary heart disease in middle-aged and older patients with psychotic symptoms. Schizophr Res 125: 295–299, 2011.
41. Johansen JP, Tarpley JW, LeDoux JE, Blair HT. Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray. Nat Neurosci 13: 979–986, 2010.
42. Johnson AK, Grippo AJ. Sadness and broken hearts: neurohumoral mechanisms and co-morbidity of ischemic heart disease and psychological depression. J Physiol Pharmacol 57 Suppl 11: 5–29, 2006.
43. Johnson PL, Sajdyk TJ, Fitz SD, Hale MW, Lowry CA, Hay- Schmidt A, Shekhar A. Angiotensin II’s role in sodium lactate-induced panic-like responses in rats with repeated urocortin 1 injections into the basolateral amygdala: amygdalar angiotensin receptors and panic. Prog Neuro-Psychopharmacol Biol Psychiatry 44: 248–256, 2013.
44. Jordan HT, Miller-Archie SA, Cone JE, Morabia A, Stellman SD. Heart disease among adults exposed to the September 11, 2001 World Trade Center disaster: results from the World Trade Center Health Registry. Prev Med 53: 370–376, 2011.
45. Jordan HT, Stellman SD, Morabia A, Miller-Archie SA, Alper H, Laskaris Z, Brackbill RM, Cone JE. Cardiovascular disease hospitalizations in relation to exposure to the September 11, 2001 World Trade Center disaster and posttraumatic stress disorder. J Am Heart Assoc 2: e000431–e000431, 2013.
46. Joseph AM, McFall M, Saxon AJ, Chow BK, Leskela J, Dieperink ME, Carmody TP, Beckham JC. Smoking intensity and severity of specific symptom clusters in posttraumatic stress disorder. J Traum Stress 25: 10–16, 2012.
47. Jovanovic T, Ressler KJ. How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am J Psychiatry 167: 648–662, 2010.
48. Kanel von 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: 744–752, 2007.
49. Kang H, Bullman T, Taylor J. Risk of selected cardiovascular diseases and posttraumatic stress disorder among former World War II prisoners of war. Annals of Epidemiology 16: 381–386, 2006.
50. Khoury NM, Marvar PJ, Gillespie CF, Wingo A, Schwartz A, Bradley B, Kramer M, Ressler KJ. The renin-angiotensin pathway in posttraumatic stress disorder: angiotensin-converting enzyme inhibitors and angiotensin receptor blockers are associated with fewer traumatic stress symptoms. J Clin Psychiatry 73: 849–855, 2012.
51. Kibler JL, Joshi K, Ma M. Hypertension in relation to posttraumatic stress disorder and depression in the US National Comorbidity Survey. Behav Med 34: 125–132, 2009.
52. Kibler JL. Metabolic, autonomic and immune markers for cardiovascular disease in posttraumatic stress disorder. World J Cardiol 6: 455, 2014.
53. Klein IH, Ligtenberg G, Oey PL, Koomans HA, Blankestijn PJ. Enalapril and losartan reduce sympathetic hyperactivity in patients with chronic renal failure. J Am Soc Nephrol 14: 425–430, 2003.
54. Kobayashi I, Lavela J, Mellman TA. Nocturnal autonomic balance and sleep in PTSD and resilience. J Traum Stress 27: 712–716, 2014.
55. Krause EG, de Kloet AD, Scott KA, Flak JN, Jones K, Smeltzer MD, Ulrich-Lai YM, Woods SC, Wilson SP, Reagan LP, Herman JP, Sakai RR. Blood-borne angiotensin II acts in the brain to influence behavioral and endocrine responses to psychogenic stress. J Neurosci 31: 15,009–15,015, 2011.
56. Kubzansky LD, Adler GK. Aldosterone: a forgotten mediator of the relationship between psychological stress and heart disease. Neurosci Biobehav Rev 34: 80–86, 2010.
57. Kubzansky LD, Koenen KC, Jones C, Eaton WW. A prospective study of posttraumatic stress disorder symptoms and coronary heart disease in women. Health Psychol 28: 125–130, 2009.
58. Kubzansky LD, Koenen KC, Spiro A3, Vokonas PS, Sparrow D. Prospective study of posttraumatic stress disorder symptoms and coronary heart disease in the Normative Aging Study. Arch Gen Psychiatry 64: 109–116, 2007.
59. Ladwig KH, Baumert J, Marten-Mittag B, Kolb C, Zrenner B, Schmitt C. Posttraumatic stress symptoms and predicted mortality in patients with implantable cardioverter-defibrillators: results from the prospective living with an implanted cardioverter-defibrillator study. Arch Gen Psychiatry 65: 1324–1330, 2008.
60. LeDoux J. The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23: 727–738, 2003.
61. Lemieux A, Coe CL, Carnes M. Symptom severity predicts degree of T-cell activation in adult women following childhood maltreatment. Brain Behav Immun 22: 994–1003, 2008.
62. Leong DS, Terrón JA, Falcón-Neri A, Armando I, Ito T, Jöhren O, Tonelli LH, Hoe KL, Saavedra JM. Restraint stress modulates brain, pituitary and adrenal expression of angiotensin II AT(1A), AT(1B), and AT(2) receptors. Neuroendocrinology 75: 227–240, 2002.
63. Levine AB, Levine LM, Levine TB. Posttraumatic stress disorder and cardiometabolic disease. Cardiology 127: 1–19, 2014.
64. Likhtik E, Pelletier JG, Paz R, Paré D. Prefrontal control of the amygdala. J Neurosci 25: 7429–7437, 2005.
65. Likhtik E, Popa D, Apergis-Schoute J, Fidacaro GA, Paré D. Amygdala intercalated neurons are required for expression of fear extinction. Nature 454: 642–645, 2008.
66. Maes M, Lin AH, Delmeire L, Van Gastel A, Kenis G, De Jongh R, Bosmans E. Elevated serum interleukin-6 (IL-6) and IL-6 receptor concentrations in posttraumatic stress disorder following accidental manmade traumatic events. Biol Psychiatry 45: 833–839, 1999.
67. Marinzalda M de los A, Pérez PA, Gargiulo PA, Casarsa BS, Bregonzio C, Baiardi G. Fear-potentiated behaviour is modulated by central amygdala angiotensin II AT1 receptors stimulation. Biomed Res Int 2014: 183248, 2014.
68. Marvar PJ, Goodman J, Fuchs S, Choi DC, Banerjee S, Ressler KJ. Angiotensin type 1 receptor inhibition enhances the extinction of fear memory. Biol Psychiatry 75: 864–872, 2014.
69. Matsukawa T, Gotoh E, Uneda S, Miyajima E, Shionoiri H, Tochikubo O, Ishii M. Augmented sympathetic nerve activity in response to stressors in young borderline hypertensive men. Acta Physiol Scand 141: 157–165, 1991.
70. Matsukawa T, Gotoh E, Uneda S, Miyajima E, Shionoiri H, Tochikubo O, Ishii M. Augmented sympathetic nerve activity in response to stressors in young borderline hypertensive men. Acta Physiol Scand 141: 157–165, 1991.
71. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292: C82–C97, 2007.
72. Mellman TA, Brown DD, Jenifer ES, Hipolito MM, Randall OS. Posttraumatic stress disorder and nocturnal blood pressure dipping in young adult African Americans. Psychosom Med 71: 627–630, 2009.
73. Mellman TA, Brown TSH, Kobayashi I, Abu-Bader SH, Lavela J, Altaee D, McLaughlin L, Randall OS. Blood pressure dipping and urban stressors in young adult African Americans. Ann Behav Med (January 27, 2015). doi: 10.1007/s12160-014-9684-x.
74. Michopoulos V, Rothbaum AO, Jovanovic T, Almli LM, Bradley B, Rothbaum BO, Gillespie CF, Ressler KJ. 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: 353–362, 2015.
75. Miller AH, Haroon E, Raison CL, Felger JC. Cytokine targets in the brain: impact on neurotransmitters and neurocircuits. Depress Anxiety 30: 297–306, 2013.
76. Morris MC, Compas BE, Garber J. Relations among posttraumatic stress disorder, comorbid major depression, and HPA function: a systematic review and meta-analysis. Clin Psychol Rev 32: 301–315, 2012.
77. Muraoka MY, Carlson JG, Chemtob CM. Twenty-four-hour ambulatory blood pressure and heart rate monitoring in combat-related posttraumatic stress disorder. J Traum Stress 11: 473–484, 1998.
78. Nance DM, Sanders VM. Autonomic innervation and regulation of the immune system (1987–2007). Brain Behav Immun 21: 736–745, 2007.
79. Nicholls JG, Paton JFR. Brainstem: neural networks vital for life. Philos Trans R Soc B Biol Sci 364: 2447–2451, 2009.
80. Nylocks KM, Michopoulos V, Rothbaum AO, Almli L, Gillespie CF, Wingo A, Schwartz AC, Habib L, Gamwell KL, Marvar PJ, Bradley B, Ressler KJ. An angiotensin-converting enzyme (ACE) polymorphism may mitigate the effects of angiotensin-pathway medications on posttraumatic stress symptoms. Am J Med Genet B Neuropsychiatr Genet 168B: 307–315, 2015.
81. Ohayon MM, Shapiro CM. Sleep disturbances and psychiatric disorders associated with posttraumatic stress disorder in the general population. Compr Psychiatry 41: 469–478, 2000.
82. Onose T, Nochioka K, Sakata Y, Miura M, Tadaki S, Ushigome R, Yamauchi T, Sato K, Tsuji K, Abe R, Miyata S, Takahashi J, Shimokawa H, CHART2 Investigators. Predictors and prognostic impact of post-traumatic stress disorder after the great East Japan earthquake in patients with cardiovascular disease. Circ J 79: 664–667, 2015.
83. Oosthuizen F, Wegener G, Harvey BH. Nitric oxide as inflammatory mediator in post-traumatic stress disorder (PTSD): evidence from an animal model. Neuropsychiatr Dis Treat 1: 109–123, 2005.
84. Pavlatou MG, Mastorakos G, Lekakis I, Liatis S, Vamvakou G, Zoumakis E, Papassotiriou I, Rabavilas AD, Katsilambros N, Chrousos GP. Chronic administration of an angiotensin II receptor antagonist resets the hypothalamic-pituitary-adrenal (HPA) axis and improves the affect of patients with diabetes mellitus type 2: Preliminary results. Stress 11: 62–72, 2008.
85. Peckerman A, Dahl K, Chemitiganti R, LaManca JJ, Ottenweller JE, Natelson BH. Effects of posttraumatic stress disorder on cardiovascular stress responses in Gulf War veterans with fatiguing illness. Auton Neurosci Basic Clin 108: 63–72, 2003.
86. Porter JP. Effect of stress on the control of renin release in spontaneously hypertensive rats. Hypertension 15: 310–317, 1990.
87. Reid IA. Interactions between ANG II, sympathetic nervous system, and baroreceptor reflexes in regulation of blood pressure. Am J Physiol Endocrinol Metab 262: E763–E778, 1992.
88. Ridker PM. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 107: 363–369, 2003.
89. Roberts AL, Agnew-Blais JC, Spiegelman D, Kubzansky LD, Mason SM, Galea S, Hu FB, Rich-Edwards JW, Koenen KC. Posttraumatic stress disorder and incidence of type 2 diabetes mellitus in a sample of women: a 22-year longitudinal study. JAMA Psychiatry 72: 203–210, 2015.
90. Roszell DK, McFall ME, Malas KL. Frequency of symptoms and concurrent psychiatric disorder in Vietnam veterans with chronic PTSD. Hosp Community Psychiatry 42: 293–296, 1991.
91. Roy SS, Foraker RE, Girton RA, Mansfield AJ. Posttraumatic stress disorder and incident heart failure among a community-based sample of US veterans. Am J Public Health 105: 757–763, 2015.
92. Saavedra JM, Ando H, Armando I, Baiardi G, Bregonzio C, Juorio A, Macova M. Anti-stress and anti-anxiety effects of centrally acting angiotensin II AT1 receptor antagonists. Regul Pept 128: 227–238, 2005.
93. Saavedra JM, Ando H, Armando I, Baiardi G, Bregonzio C, Juorio A, Macova M. Anti-stress and anti-anxiety effects of centrally acting angiotensin II AT1 receptor antagonists. Regul Pept 128: 227–238, 2005.
94. Saavedra JM, Benicky J. Brain and peripheral angiotensin II play a major role in stress. Stress 10: 185–193, 2007.
95. Saavedra JM. Angiotensin II AT1 receptor blockers ameliorate inflammatory stress: a beneficial effect for the treatment of brain disorders. Cell Mol Neurobiol 32: 667–681, 2012.
96. Scherrer JF, Chrusciel T, Zeringue A, Garfield LD, Hauptman PJ, Lustman PJ, Freedland KE, Carney RM, Bucholz KK, Owen R, True WR. Anxiety disorders increase risk for incident myocardial infarction in depressed and nondepressed Veterans Administration patients. Am Heart J 159: 772–779, 2010.
97. Shekhar A. Angiotensin type 1 receptor antagonists-a novel approach to augmenting posttraumatic stress disorder and phobia therapies? Biol Psychiatry 75: 836–837, 2014.
98. Smith AK, Conneely KN, Kilaru V, Mercer KB, Weiss TE, Bradley B, Tang Y, Gillespie CF, Cubells JF, Ressler KJ. Differential immune system DNA methylation and cytokine regulation in post-traumatic stress disorder. Am J Med Genet 156: 700–708, 2011.
99. Sommershof A, Aichinger H, Engler H, Adenauer H, Catani C, Boneberg EM, Elbert T, Groettrup M, Kolassa IT. Substantial reduction of naïve and regulatory T cells following traumatic stress. Brain Behav Immun 23: 1117–1124, 2009.
100. Song C, Phillips AG, Leonard B. Interleukin 1β enhances conditioned fear memory in rats: possible involvement of glucocorticoids. Eur J Neurosci 18: 1739–1743, 2003.
101. Söndergaard HP, Hansson LO, Theorell T. The inflammatory markers C-reactive protein and serum amyloid A in refugees with and without posttraumatic stress disorder. Clin Chim Acta 342: 93–98, 2004.
102. Speth RC, Giese MJ. Update on the renin-angiotensin system. J Pharmacol Clin Toxicol 1: 1004, 2013.
103. Spitzer C, Barnow S, Völzke H, Wallaschofski H, John U, Freyberger HJ, Löwe B, Grabe HJ. Association of posttraumatic stress disorder with low-grade elevation of C-reactive protein: evidence from the general population. J Psychiatr Res 44: 15–21, 2010.
104. Spivak B, Shohat B, Mester R, Avraham S, Gil-Ad I, Bleich A, Valevski A, Weizman A. Elevated levels of serum interleukin-1β in combat-related posttraumatic stress disorder. Biol Psychiatry 42: 345–348, 1997.
105. Sueta D, Koibuchi N, Hasegawa Y, Toyama K, Uekawa K, Katayama T, Ma M, Nakagawa T, Ogawa H, Kim-Mitsuyama S. Telmisartan exerts sustained blood pressure control and reduces blood pressure variability in metabolic syndrome by inhibiting sympathetic activity. Am J Hypertension 27: 1464–1471, 2014.
106. Vaccarino V, Goldberg J, Rooks C, Shah AJ, Veledar E, Faber TL, Votaw JR, Forsberg CW, Bremner JD. Post-traumatic stress disorder and incidence of coronary heart disease: a twin study. J Am Coll Cardiol 62: 970–978, 2013.
107. Vidović A, Vilibić M, Sabioncello A, Gotovac K, Rabatić S, Folnegović-Smalc V, Dekaris D. Circulating lymphocyte subsets, natural killer cell cytotoxicity, and components of hypothalamic-pituitary-adrenal axis in Croatian war veterans with posttraumatic stress disorder: cross-sectional study. Croat Med J 48: 198–206, 2007.
108. Villapol S, Yaszemski AK, Logan TT, Sánchez-Lemus E, Saavedra JM, Symes AJ. Candesartan, an angiotensin II AT1-receptor blocker and PPAR-γ agonist, reduces lesion volume and improves motor and memory function after traumatic brain injury in mice. Neuropsychopharmacology 37: 2817–2829, 2012.
109. Walczewska J, Rutkowski K, Wizner B, Cwynar M, Grodzicki T. Stiffness of large arteries and cardiovascular risk in patients with posttraumatic stress disorder. Eur Heart J 32: 730–736, 2011.
110. Wang Y, Seto SW, Golledge J. Angiotensin II, sympathetic nerve activity and chronic heart failure. Heart Fail Rev 19: 187–198, 2014.
111. Weiss T, Skelton K, Phifer J, Jovanovic T, Gillespie CF, Smith A, Umpierrez G, Bradley B, Ressler KJ. Posttraumatic stress disorder is a risk factor for metabolic syndrome in an impoverished urban population. Gen Hosp Psychiatry 33: 135–142, 2011.
112. Wentworth BA, Stein MB, Redwine LS, Xue Y, Taub PR, Clopton P, Nayak KR, Maisel AS. Post-traumatic stress disorder: a fast track to premature cardiovascular disease? Cardiol Rev 21: 16–22, 2013.
113. Wessa M, Flor H. Failure of extinction of fear responses in posttraumatic stress disorder: evidence from second-order conditioning. Am J Psychiatry 164: 1684–1692, 2007.
114. Wohleb ES, Patterson JM, Sharma V, Quan N, Godbout JP, Sheridan JF. Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior. J Neurosci 34: 2583–2591, 2014.
115. Woodward SH, Arsenault NJ, Voelker K, Nguyen T, Lynch J, Skultety K, Mozer E, Leskin GA, Sheikh JI. Autonomic activation during sleep in posttraumatic stress disorder and panic: a mattress actigraphic study. Biol Psychiatry 66: 41–46, 2009.
116. Wright JW, Harding JW. Brain angiotensin receptor subtypes AT1, AT2, and AT4 and their functions. Regul Pept 59: 269–295, 1995.
117. Wu CY, Zha H, Xia QQ, Yuan Y, Liang XY, Li JH, Guo ZY, Li JJ. Expression of angiotensin II and its receptors in activated microglia in experimentally induced cerebral ischemia in the adult rats. Mol Cell Biochem 382: 47–58, 2013.
118. Xia H, Feng Y, Obr TD, Hickman PJ, Lazartigues E. Angiotensin II type 1 receptor-mediated reduction of angiotensin-converting enzyme 2 activity in the brain impairs baroreflex function in hypertensive mice. Hypertension 53: 210–216, 2009.
119. Zen AL, Whooley MA, Zhao S, Cohen BE. Post-traumatic stress disorder is associated with poor health behaviors: findings from the heart and soul study. Health Psychol 31: 194–201, 2012.