Catecholamines, steroids and immune alterations in ischemic stroke and other acute diseases

Aging and Disease

Volumn 5, Issue 5, 2014, Pages 327-339

  Schulze, Juliane ^a   Vogelgesang, Antje ^a   Dressel, Alexander ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

Aging; Catecholamines; Immune; Ischemic stroke; Steroids

Indexed keywords

EID: 84916892283     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: 10.14336/AD.2014.0500327     Document Type: Review

References (133)

1. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ (2006). Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet, 367: 1747-1757
2. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, et al. (2010). Executive summary: heart disease and stroke statistics--2010 update: a report from the American Heart Association. Circulation, 121: 948-954
3. Murray CJ, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, et al. (2012). Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet, 380: 2197-2223
4. Harms H, Reimnitz P, Bohner G, Werich T, Klingebiel R, Meisel C, et al. (2011). Influence of stroke localization on autonomic activation, immunodepression, and post-stroke infection. Cerebrovasc Dis, 32: 552-560
5. Vermeij FH, Scholte op Reimer WJ, de Man P, van Oostenbrugge RJ, Franke CL, de Jong G, et al. (2009). Stroke-associated infection is an independent risk factor for poor outcome after acute ischemic stroke: data from the Netherlands Stroke Survey. Cerebrovasc Dis, 27: 465-471
6. Dirnagl U, Klehmet J, Braun JS, Harms H, Meisel C, Ziemssen T, et al. (2007). Stroke-induced immunodepression: experimental evidence and clinical relevance. Stroke, 38: 770-773
7. Vogelgesang A, Grunwald U, Langner S, Jack R, Broker BM, Kessler C, et al. (2008). Analysis of lymphocyte subsets in patients with stroke and their influence on infection after stroke. Stroke, 39: 237-241
8. Urra X, Obach V, Chamorro A (2009). Stroke induced immunodepression syndrome: from bench to bedside. Curr Mol Med, 9: 195-202
9. Meisel C, Schwab JM, Prass K, Meisel A, Dirnagl U (2005). Central nervous system injury-induced immune deficiency syndrome. Nat Rev Neurosci, 6: 775-786
10. Straub RH, Westermann J, Scholmerich J, Falk W (1998). Dialogue between the CNS and the immune system in lymphoid organs. Immunol Today, 19: 409-413
11. Kohm AP, Sanders VM (1999). Suppression of antigen-specific Th2 cell-dependent IgM and IgG1 production following norepinephrine depletion in vivo. J Immunol, 162: 5299-5308
12. Sanders VM, Baker RA, Ramer-Quinn DS, Kasprowicz DJ, Fuchs BA, Street NE (1997). Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J Immunol, 158: 4200-4210
13. Ramer-Quinn DS, Baker RA, Sanders VM (1997). Activated T helper 1 and T helper 2 cells differentially express the beta-2-adrenergic receptor: a mechanism for selective modulation of T helper 1 cell cytokine production. J Immunol, 159: 4857-4867
14. Charlene A. McQueen, editor. Comprehensive Toxicology, Kidlington: Elsevier Science & Technology; 2010
15. Dunn AJ (1995). Interactions Between the Nervous System and the Immune System: Implications for Psychopharmacology. In: Bloom FE, Kupfer DJ, editors. Psychopharmacology: The Fourth Generation of Progress, Lippincott Williams and Wilkins.
16. Musso NR, Brenci S, Setti M, Indiveri F, Lotti G (1996). Catecholamine content and in vitro catecholamine synthesis in peripheral human lymphocytes. J Clin Endocrinol Metab, 81: 3553-3557
17. Josefsson E, Bergquist J, Ekman R, Tarkowski A (1996). Catecholamines are synthesized by mouse lymphocytes and regulate function of these cells by induction of apoptosis. Immunology, 88: 140-146
18. Bergquist J, Tarkowski A, Ekman R, Ewing A (1994). Discovery of endogenous catecholamines in lymphocytes and evidence for catecholamine regulation of lymphocyte function via an autocrine loop. Proc Natl Acad Sci U S A, 91: 12912-12916
19. Flierl MA, Rittirsch D, Huber-Lang M, Sarma JV, Ward PA (2008). Catecholamines-crafty weapons in the inflammatory arsenal of immune/inflammatory cells or opening pandora's box? Mol Med, 14: 195-204
20. Benschop RJ, Rodriguez-Feuerhahn M, Schedlowski M (1996). Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain, behavior, and immunity, 10: 77-91
21. Sanders VM (2012). The beta2-adrenergic receptor on T and B lymphocytes: do we understand it yet? Brain, behavior, and immunity, 26: 195-200
22. Kin NW, Sanders VM (2006). It takes nerve to tell T and B cells what to do. Journal of leukocyte biology, 79: 1093-1104
23. Straub RH (2004). Complexity of the bi-directional neuroimmune junction in the spleen. Trends Pharmacol Sci, 25: 640-646
24. Pratt WB, Toft DO (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood), 228: 111-133
25. Zhou J, Cidlowski JA (2005). The human glucocorticoid receptor: one gene, multiple proteins and diverse responses. Steroids, 70: 407-417
26. Lowenberg M, Stahn C, Hommes DW, Buttgereit F (2008). Novel insights into mechanisms of glucocorticoid action and the development of new glucocorticoid receptor ligands. Steroids, 73: 1025-1029
27. De Bosscher K, Haegeman G (2009). Minireview: latest perspectives on antiinflammatory actions of glucocorticoids. Mol Endocrinol, 23: 281-291
28. Baschant U, Tuckermann J (2010). The role of the glucocorticoid receptor in inflammation and immunity. J Steroid Biochem Mol Biol, 120: 69-75
29. Moser M, De Smedt T, Sornasse T, Tielemans F, Chentoufi AA, Muraille E, et al. (1995). Glucocorticoids down-regulate dendritic cell function in vitro and in vivo. European journal of immunology, 25: 2818-2824
30. Kitajima T, Ariizumi K, Bergstresser PR, Takashima A (1996). A novel mechanism of glucocorticoid-induced immune suppression: the inhibiton of T cell-mediated terminal maturation of a murine dendritic cell line. The Journal of clinical investigation, 98: 142-147
31. Matyszak MK, Citterio S, Rescigno M, Ricciardi-Castagnoli P (2000). Differential effects of corticosteroids during different stages of dendritic cell maturation. European journal of immunology, 30: 1233-1242
32. Tuckermann JP, Kleiman A, Moriggl R, Spanbroek R, Neumann A, Illing A, et al. (2007). Macrophages and neutrophils are the targets for immune suppression by glucocorticoids in contact allergy. The Journal of clinical investigation, 117: 1381-1390
33. Cumberbatch M, Dearman RJ, Kimber I (1999). Inhibition by dexamethasone of Langerhans cell migration: influence of epidermal cytokine signals. Immunopharmacology, 41: 235-243
34. Vizzardelli C, Pavelka N, Luchini A, Zanoni I, Bendickson L, Pelizzola M, et al. (2006). Effects of dexamethazone on LPS-induced activationand migration of mouse dendritic cells revealed by a genome-wide transcriptional analysis. European journal of immunology, 36: 1504-1515
35. Rutella S, Danese S, Leone G (2006). Tolerogenic dendritic cells: cytokine modulation comes of age. Blood, 108: 1435-1440
36. Kim BJ, Jones HP (2010). Epinephrine-primed murine bone marrow-derived dendritic cells facilitate production of IL-17A and IL-4 but not IFN-gamma by CD4+ T cells. Brain, behavior, and immunity, 24: 1126-1136
37. Maestroni GJ (2000). Dendritic cell migration controlled by alpha 1b-adrenergic receptors. J Immunol, 165: 6743-6747
38. Maestroni GJ (2002). Short exposure of maturing, bone marrow-derived dendritic cells to norepinephrine: impact on kinetics of cytokine production and Th development. Journal of neuroimmunology, 129: 106-114
39. Yanagawa Y, Matsumoto M, Togashi H (2011). Adrenoceptor-mediated enhancement of interleukin-33 production by dendritic cells. Brain, behavior, and immunity, 25: 1427-1433
40. Goyarts E, Matsui M, Mammone T, Bender AM, Wagner JA, Maes D, et al. (2008). Norepinephrine modulates human dendritic cell activation by altering cytokine release. Experimental dermatology, 17: 188-196
41. Ehrchen J, Steinmuller L, Barczyk K, Tenbrock K, Nacken W, Eisenacher M, et al. (2007). Glucocorticoids induce differentiation of a specifically activated, anti-inflammatory subtype of human monocytes. Blood, 109: 1265-1274
42. Varga G, Ehrchen J, Tsianakas A, Tenbrock K, Rattenholl A, Seeliger S, et al. (2008). Glucocorticoids induce an activated, anti-inflammatory monocyte subset in mice that resembles myeloid-derived suppressor cells. Journal of leukocyte biology, 84: 644-650
43. Platzer C, Docke W, Volk H, Prosch S (2000). Catecholamines trigger IL-10 release in acute systemic stress reaction by direct stimulation of its promoter/enhancer activity in monocytic cells. Journal of neuroimmunology, 105: 31-38
44. Rainer TH, Lam N, Cocks RA (1999). Adrenaline upregulates monocyte L-selectin in vitro. Resuscitation, 43: 47-55
45. Straub RH, Herrmann M, Berkmiller G, Frauenholz T, Lang B, Scholmerich J, et al. (1997). Neuronal regulation of interleukin 6 secretion in murine spleen: adrenergic and opioidergic control. Journal of neurochemistry, 68: 1633-1639
46. Straub RH, Dorner M, Riedel J, Kubitza M, Van Rooijen N, Lang B, et al. (1998). Tonic neurogenic inhibition of interleukin-6 secretion from murine spleen caused by opioidergic transmission. The American journal of physiology, 274: R997-1003
47. Pitzalis C, Pipitone N, Perretti M (2002). Regulation of leukocyte-endothelial interactions by glucocorticoids. Annals of the New York Academy of Sciences, 966: 108-118
48. Stroncek DF, Yau YY, Oblitas J, Leitman SF (2001). Administration of G--CSF plus dexamethasone produces greater granulocyte concentrate yields while causing no more donor toxicity than G--CSF alone. Transfusion, 41: 1037-1044
49. Heasman SJ, Giles KM, Ward C, Rossi AG, Haslett C, Dransfield I (2003). Glucocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation. The Journal of endocrinology, 178: 29-36
50. Parks KR, Davis JM (2012). Epinephrine, cortisol, endotoxin, nutrition, and the neutrophil. Surgical infections, 13: 300-306
51. Giraldo E, Multhoff G, Ortega E (2010). Noradrenaline increases the expression and release of Hsp72 by human neutrophils. Brain, behavior, and immunity, 24: 672-677
52. Trabold B, Gruber M, Frohlich D (2007). Functional and phenotypic changes in polymorphonuclear neutrophils induced by catecholamines. Scandinavian cardiovascular journal: SCJ, 41: 59-64
53. Kaufmann I, Eisner C, Richter P, Huge V, Beyer A, Chouker A, et al. (2007). Psychoneuroendocrine stress response may impair neutrophil function in complex regional pain syndrome. Clin Immunol, 125: 103-111
54. Cupps TR, Edgar LC, Thomas CA, Fauci AS (1984). Multiple mechanisms of B cell immunoregulation in man after administration of in vivo corticosteroids. J Immunol, 132: 170-175
55. Cupps TR, Gerrard TL, Falkoff RJ, Whalen G, Fauci AS (1985). Effects of in vitro corticosteroids on B cell activation, proliferation, and differentiation. The Journal of clinical investigation, 75: 754-761
56. Kasprowicz DJ, Kohm AP, Berton MT, Chruscinski AJ, Sharpe A, Sanders VM (2000). Stimulation of the B cell receptor, CD86 (B7-2), and the beta 2-adrenergic receptor intrinsically modulates the level of IgG1 and IgE produced per B cell. J Immunol, 165: 680-690
57. Kohm AP, Mozaffarian A, Sanders VM (2002). B cell receptor- and beta 2-adrenergic receptor-induced regulation of B7-2 (CD86) expression in B cells. J Immunol, 168: 6314-6322
58. Pongratz G, McAlees JW, Conrad DH, Erbe RS, Haas KM, Sanders VM (2006). The level of IgE produced by a B cell is regulated by norepinephrine in a p38 MAPK- and CD23-dependent manner. J Immunol, 177: 2926-2938
59. Wang D, Muller N, McPherson KG, Reichardt HM (2006). Glucocorticoids engage different signal transduction pathways to induce apoptosis in thymocytes and mature T cells. J Immunol, 176: 1695-1702
60. Chen X, Murakami T, Oppenheim JJ, Howard OM (2004). Differential response of murine CD4+CD25+ and CD4+CD25- T cells to dexamethasone-induced cell death. European journal of immunology, 34: 859-869
61. Ramirez F, Fowell DJ, Puklavec M, Simmonds S, Mason D (1996). Glucocorticoids promote a TH2 cytokine response by CD4+ T cells in vitro. J Immunol, 156: 2406-2412
62. Momcilovic M, Miljkovic Z, Popadic D, Markovic M, Savic E, Ramic Z, et al. (2008). Methylprednisolone inhibits interleukin-17 and interferon-gamma expression by both naive and primed T cells. BMC immunology, 9: 47
63. Franchimont D, Galon J, Gadina M, Visconti R, Zhou Y, Aringer M, et al. (2000). Inhibition of Th1 immune response by glucocorticoids: dexamethasone selectively inhibits IL-12-induced Stat4 phosphorylation in T lymphocytes. J Immunol, 164: 1768-1774
64. Liberman AC, Druker J, Refojo D, Holsboer F, Arzt E (2009). Glucocorticoids inhibit GATA-3 phosphorylation and activity in T cells. FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 23: 1558-1571
65. Maneechotesuwan K, Yao X, Ito K, Jazrawi E, Usmani OS, Adcock IM, et al. (2009). Suppression of GATA-3 nuclear import and phosphorylation: a novel mechanism of corticosteroid action in allergic disease. PLoS medicine, 6: e1000076
66. Biola A, Andreau K, David M, Sturm M, Haake M, Bertoglio J, et al. (2000). The glucocorticoid receptor and STAT6 physically and functionally interact in T-lymphocytes. FEBS letters, 487: 229-233
67. Swanson MA, Lee WT, Sanders VM (2001). IFN-gamma production by Th1 cells generated from naive CD4+ T cells exposed to norepinephrine. J Immunol, 166: 232-240
68. Bush KA, Krukowski K, Eddy JL, Janusek LW, Mathews HL (2012). Glucocorticoid receptor mediated suppression of natural killer cell activity: identification of associated deacetylase and corepressor molecules. Cellular immunology, 275: 80-89
69. Gan X, Zhang L, Solomon GF, Bonavida B (2002). Mechanism of norepinephrine-mediated inhibition of human NK cytotoxic functions: inhibition of cytokine secretion, target binding, and programming for cytotoxicity. Brain, behavior, and immunity, 16: 227-246
70. Brait VH, Arumugam TV, Drummond GR, Sobey CG (2012). Importance of T lymphocytes in brain injury, immunodeficiency, and recovery after cerebral ischemia. J Cereb Blood Flow Metab, 32: 598-611
71. Morganti-Kossmann MC, Satgunaseelan L, Bye N, Kossmann T (2007). Modulation of immune response by head injury. Injury, 38: 1392-1400
72. Morganti-Kossmann MC, Rancan M, Stahel PF, Kossmann T (2002). Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr Opin Crit Care, 8: 101-105
73. Kamel H, Iadecola C (2012). Brain-immune interactions and ischemic stroke: clinical implications. Arch Neurol, 69: 576-581
74. Whiting MJ, Doogue MP (2009). Advances in biochemical screening for phaeochromocytoma using biogenic amines. Clin Biochem Rev, 30: 3-17
75. Chamorro A, Amaro S, Vargas M, Obach V, Cervera A, Gomez-Choco M, et al. (2007). Catecholamines, infection, and death in acute ischemic stroke. J Neurol Sci, 252: 29-35
76. Vogelgesang A, May VE, Grunwald U, Bakkeboe M, Langner S, Wallaschofski H, et al. (2010). Functional status of peripheral blood T-cells in ischemic stroke patients. PLoS One, 5: e8718
77. Prass K, Meisel C, Hoflich C, Braun J, Halle E, Wolf T, et al. (2003). Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med, 198: 725-736
78. Mracsko E, Liesz A, Karcher S, Zorn M, Bari F, Veltkamp R (2014). Differential effects of sympathetic nervous system and hypothalamic-pituitary-adrenal axis on systemic immune cells after severe experimental stroke. Brain, behavior, and immunity
79. Wong CH, Jenne CN, Lee WY, Leger C, Kubes P (2011). Functional innervation of hepatic iNKT cells is immunosuppressive following stroke. Science, 334: 101-105
80. Ajmo CT, Jr., Collier LA, Leonardo CC, Hall AA, Green SM, Womble TA, et al. (2009). Blockade of adrenoreceptors inhibits the splenic response to stroke. Exp Neurol, 218: 47-55
81. Fassbender K, Schmidt R, Mossner R, Daffertshofer M, Hennerici M (1994). Pattern of activation of the hypothalamic-pituitary-adrenal axis in acute stroke. Relation to acute confusional state, extent of brain damage, and clinical outcome. Stroke, 25: 1105-1108
82. Franceschini R, Gandolfo C, Cataldi A, Del Sette M, Cianciosi P, Finocchi C, et al. (1994). Twenty-four-hour beta-endorphin secretory pattern in stroke patients. Stroke, 25: 2142-2145
83. Olsson T (1990). Urinary free cortisol excretion shortly after ischaemic stroke. J Intern Med, 228: 177-181
84. Emsley H (2003). An early and sustained peripheral inflammatory response in acute ischaemic stroke: relationships with infection and atherosclerosis. Journal of neuroimmunology, 139: 93-101
85. Marklund N, Peltonen M, Nilsson TK, Olsson T (2004). Low and high circulating cortisol levels predict mortality and cognitive dysfunction early after stroke. J Intern Med, 256: 15-21
86. Neidert S, Katan M, Schuetz P, Fluri F, Ernst A, Bingisser R, et al. (2011). Anterior pituitary axis hormones and outcome in acute ischaemic stroke. J Intern Med, 269: 420-432
87. Christensen H, Boysen G, Johannesen HH (2004). Serum-cortisol reflects severity and mortality in acute stroke. J Neurol Sci, 217: 175-180
88. O'Neill PA, Davies I, Fullerton KJ, Bennett D (1991). Stress hormone and blood glucose response following acute stroke in the elderly. Stroke, 22: 842-847
89. Murros K, Fogelholm R, Kettunen S, Vuorela AL (1993). Serum cortisol and outcome of ischemic brain infarction. J Neurol Sci, 116: 12-17
90. Anne M, Juha K, Timo M, Mikko T, Olli V, Kyosti S, et al. (2007). Neurohormonal activation in ischemic stroke: effects of acute phase disturbances on long-term mortality. Curr Neurovasc Res, 4: 170-175
91. Szczudlik A, Dziedzic T, Bartus S, Slowik A, Kieltyka A (2004). Serum interleukin-6 predicts cortisol release in acute stroke patients. J Endocrinol Invest, 27: 37-41
92. Weidenfeld J, Leker RR, Gai N, Teichner A, Bener D, Ovadia H (2011). The function of the adrenocortical axis in permanent middle cerebral artery occlusion: effect of glucocorticoids on the neurological outcome. Brain Res, 1407: 90-96
93. Torres KC, Antonelli LR, Souza AL, Teixeira MM, Dutra WO, Gollob KJ (2005). Norepinephrine, dopamine and dexamethasone modulate discrete leukocyte subpopulations and cytokine profiles from human PBMC. Journal of neuroimmunology, 166: 144-157
94. Woiciechowsky C, Asadullah K, Nestler D, Eberhardt B, Platzer C, Schoning B, et al. (1998). Sympathetic activation triggers systemic interleukin-10 release in immunodepression induced by brain injury. Nat Med, 4: 808-813
95. Johansson PI, Stensballe J, Rasmussen LS, Ostrowski SR (2012). High circulating adrenaline levels at admission predict increased mortality after trauma. The journal of trauma and acute care surgery, 72: 428-436
96. Ostrowski SR, Pedersen SH, Jensen JS, Mogelvang R, Johansson PI (2013). Acute myocardial infarction is associated with endothelial glycocalyx and cell damage and a parallel increase in circulating catecholamines. Crit Care, 17: R32
97. Christensen NJ, Videbaek J (1974). Plasma catecholamines and carbohydrate metabolism in patients with acute myocardial infarction. The Journal of clinical investigation, 54: 278-286
98. Haeusler KG, Schmidt WU, Foehring F, Meisel C, Guenther C, Brunecker P, et al. (2012). Immune responses after acute ischemic stroke or myocardial infarction. Int J Cardiol, 155: 372-377
99. Goldstein RS, Gallowitsch-Puerta M, Yang L, Rosas-Ballina M, Huston JM, Czura CJ, et al. (2006). Elevated high-mobility group box 1 levels in patients with cerebral and myocardial ischemia. Shock, 25: 571-574
100. Haeusler KG, Schmidt WU, Fohring F, Meisel C, Helms T, Jungehulsing GJ, et al. (2008). Cellular immunodepression preceding infectious complications after acute ischemic stroke in humans. Cerebrovasc Dis, 25: 50-58
101. Kossmann T, Hans VH, Imhof HG, Stocker R, Grob P, Trentz O, et al. (1995). Intrathecal and serum interleukin-6 and the acute-phase response in patients with severe traumatic brain injuries. Shock, 4: 311-317
102. Ruparelia N, Digby JE, Jefferson A, Medway DJ, Neubauer S, Lygate CA, et al. (2013). Myocardial infarction causes inflammation and leukocyte recruitment at remote sites in the myocardium and in the renal glomerulus. Inflammation research: official journal of the European Histamine Research Society . [et al.], 62: 515-525
103. Fukui D, Yasukawa H, Sugi Y, Oba T, Nagata T, Kyogoku S, et al. (2012). Transient reduction and activation of circulating dendritic cells in patients with acute myocardial infarction. Int J Cardiol, 160: 216-219
104. Urra X, Cervera A, Obach V, Climent N, Planas AM, Chamorro A (2009). Monocytes are major players in the prognosis and risk of infection after acute stroke. Stroke, 40: 1262-1268
105. Riegger T, Conrad S, Liu K, Schluesener HJ, Adibzahdeh M, Schwab JM (2007). Spinal cord injury-induced immune depression syndrome (SCI-IDS). The European journal of neuroscience, 25: 1743-1747
106. Menges P, Kessler W, Kloecker C, Feuerherd M, Gaubert S, Diedrich S, et al. (2012). Surgical trauma and postoperative immune dysfunction. Eur Surg Res, 48: 180-186
107. Riegger T, Conrad S, Schluesener HJ, Kaps HP, Badke A, Baron C, et al. (2009). Immune depression syndrome following human spinal cord injury (SCI): a pilot study. Neuroscience, 158: 1194-1199
108. Kirchhoff C, Biberthaler P, Mutschler WE, Faist E, Jochum M, Zedler S (2009). Early down-regulation of the pro-inflammatory potential of monocytes is correlated to organ dysfunction in patients after severe multiple injury: a cohort study. Crit Care, 13: R88
109. Klehmet J, Harms H, Richter M, Prass K, Volk HD, Dirnagl U, et al. (2009). Stroke-induced immunodepression and post-stroke infections: lessons from the preventive antibacterial therapy in stroke trial. Neuroscience, 158: 1184-1193
110. Li M, Li F, Luo C, Shan Y, Zhang L, Qian Z, et al. (2011). Immediate splenectomy decreases mortality and improves cognitive function of rats after severe traumatic brain injury. J Trauma, 71: 141-147
111. Silveira FP, Nicoluzzi JE, Saucedo Junior NS, Silveira F, Nicollelli GM, Maranhao BS (2012). Evaluation of serum levels of interleukin-6 and interleukin-10 in patients undergoing laparoscopic versus conventional cholecystectomy. Rev Col Bras Cir, 39: 33-40
112. Chu W, Li M, Li F, Hu R, Chen Z, Lin J, et al. (2013). Immediate splenectomy down-regulates the MAPK-NF-kappaB signaling pathway in rat brain after severe traumatic brain injury. The journal of trauma and acute care surgery, 74: 1446-1453
113. Dziedzic T, Slowik A, Szczudlik A (2004). Nosocomial infections and immunity: lesson from brain-injured patients. Crit Care, 8: 266-270
114. Wang KY, Yu GF, Zhang ZY, Huang Q, Dong XQ (2012). Plasma high-mobility group box 1 levels and prediction of outcome in patients with traumatic brain injury. Clinica chimica acta; international journal of clinical chemistry, 413: 1737-1741
115. Peltz ED, Moore EE, Eckels PC, Damle SS, Tsuruta Y, Johnson JL, et al. (2009). HMGB1 is markedly elevated within 6 hours of mechanical trauma in humans. Shock, 32: 17-22
116. Urra X, Cervera A, Villamor N, Planas AM, Chamorro A (2009). Harms and benefits of lymphocyte subpopulations in patients with acute stroke. Neuroscience, 158: 1174-1183
117. Czlonkowska A, Korlak J (1979). [Humoral immune response in patients with stroke]. Pol Tyg Lek, 34: 485-487
118. Cheng X, Liao YH, Ge H, Li B, Zhang J, Yuan J, et al. (2005). TH1/TH2 functional imbalance after acute myocardial infarction: coronary arterial inflammation or myocardial inflammation. Journal of clinical immunology, 25: 246-253
119. Griffin GD (2011). The injured brain: TBI, mTBI, the immune system, and infection: connecting the dots. Mil Med, 176: 364-368
120. Wolach B, Sazbon L, Gavrieli R, Broda A, Schlesinger M (2001). Early immunological defects in comatose patients after acute brain injury. J Neurosurg, 94: 706-711
121. Schulze J, Zierath D, Tanzi P, Cain K, Shibata D, Dressel A, et al. (2013). Severe stroke induces long-lasting alterations of high-mobility group box 1. Stroke, 44: 246-248
122. Kawabata H, Setoguchi T, Yone K, Souda M, Yoshida H, Kawahara K, et al. (2010). High mobility group box 1 is upregulated after spinal cord injury and is associated with neuronal cell apoptosis. Spine (Phila Pa 1976), 35: 1109-1115
123. Angele MK, Chaudry IH (2005). Surgical trauma and immunosuppression: pathophysiology and potential immunomodulatory approaches. Langenbecks Arch Surg, 390: 333-341
124. Castillo L, Velasco N, Wainstein C, Bugedo G, Hernandez G, Klaassen J, et al. (1999). [Transcranial cytokine gradient and intestinal permeability in acute severe brain injury]. Rev Med Chil, 127: 639-646
125. Hernandez G, Hasbun P, Velasco N, Wainstein C, Bugedo G, Bruhn A, et al. (2007). Splanchnic ischemia and gut permeability after acute brain injury secondary to intracranial hemorrhage. Neurocrit Care, 7: 40-44
126. Jiang XH, Li N, Li JS (2003). Intestinal permeability in patients after surgical trauma and effect of enteral nutrition versus parenteral nutrition. World J Gastroenterol, 9: 1878-1880
127. O'Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC (1998). Microbiology of bacterial translocation in humans. Gut, 42: 29-35
128. MacFie J (1997). Bacterial translocation in surgical patients. Ann R Coll Surg Engl, 79: 183-189
129. Bansal V, Costantini T, Ryu SY, Peterson C, Loomis W, Putnam J, et al. (2010). Stimulating the central nervous system to prevent intestinal dysfunction after traumatic brain injury. J Trauma, 68: 1059-1064
130. Heffernan DS, Inaba K, Arbabi S, Cotton BA (2010). Sympathetic hyperactivity after traumatic brain injury and the role of beta-blocker therapy. J Trauma, 69: 1602-1609
131. Salehpoor F, Bazzazi AM, Estakhri R, Zaheri M, Asghari B (2010). Correlation between catecholamine levels and outcome in patients with severe head trauma. Pak J Biol Sci, 13: 738-742
132. Woolf PD, Hamill RW, Lee LA, Cox C, McDonald JV (1987). The predictive value of catecholamines in assessing outcome in traumatic brain injury. J Neurosurg, 66: 875-882
133. Ruhnau J, Schulze K, Gaida B, Langner S, Kessler C, Broker B, et al. (2014). Stroke alters respiratory burst in neutrophils and monocytes. Stroke, 45: 794-800