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Published in: Journal of Neuroinflammation 1/2014

Open Access 01-12-2014 | Review

Cross-talk between the inflammatory response, sympathetic activation and pulmonary infection in the ischemic stroke

Authors: Pawel J Winklewski, Marek Radkowski, Urszula Demkow

Published in: Journal of Neuroinflammation | Issue 1/2014

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Abstract

The immune system response and inflammation play a key role in brain injury during and after a stroke. The acute immune response is responsible for secondary brain tissue damage immediately after the stroke, followed by immunosuppression due to sympathetic nervous system activation. The latter increases risk of infection complications, such as pneumonia. The pneumonia-related inflammatory state can release a bystander autoimmune response against central nervous system antigens, thereby initiating a vicious circle. The aim of this review is to summarize the relationship between ischemic stroke, sympathetic nervous system activation and pulmonary infection.
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Literature
1.
go back to reference Davenport RJ, Dennis MS, Wellwood I, Warlow CP: Complications after acute stroke. Stroke. 1996, 27: 415-420. 10.1161/01.STR.27.3.415.CrossRefPubMed Davenport RJ, Dennis MS, Wellwood I, Warlow CP: Complications after acute stroke. Stroke. 1996, 27: 415-420. 10.1161/01.STR.27.3.415.CrossRefPubMed
2.
go back to reference Langhorne P, Stott DJ, Robertson L, MacDonald J, Jones L, McAlpine C, Dick F, Taylor GS, Murray G: Medical complications after stroke: a multicenter study. Stroke. 2000, 31: 1223-1229. 10.1161/01.STR.31.6.1223.CrossRefPubMed Langhorne P, Stott DJ, Robertson L, MacDonald J, Jones L, McAlpine C, Dick F, Taylor GS, Murray G: Medical complications after stroke: a multicenter study. Stroke. 2000, 31: 1223-1229. 10.1161/01.STR.31.6.1223.CrossRefPubMed
3.
go back to reference Emsley HC, Hopkins SJ: Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol. 2008, 7: 341-353. 10.1016/S1474-4422(08)70061-9.CrossRefPubMed Emsley HC, Hopkins SJ: Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol. 2008, 7: 341-353. 10.1016/S1474-4422(08)70061-9.CrossRefPubMed
4.
go back to reference Katzan IL, Cebul RD, Husak SH, Dawson NV, Baker DW: The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology. 2003, 60: 620-625. 10.1212/01.WNL.0000046586.38284.60.CrossRefPubMed Katzan IL, Cebul RD, Husak SH, Dawson NV, Baker DW: The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology. 2003, 60: 620-625. 10.1212/01.WNL.0000046586.38284.60.CrossRefPubMed
5.
go back to reference Hannawi Y, Hannawi B, Rao CP, Suarez JI, Bershad EM: Stroke-associated pneumonia: major advances and obstacles. Cerebrovasc Dis. 2013, 35: 430-443. 10.1159/000350199.CrossRefPubMed Hannawi Y, Hannawi B, Rao CP, Suarez JI, Bershad EM: Stroke-associated pneumonia: major advances and obstacles. Cerebrovasc Dis. 2013, 35: 430-443. 10.1159/000350199.CrossRefPubMed
6.
go back to reference Teramoto S: Novel preventive and therapeutic strategy for post-stroke pneumonia. Expert Rev Neurother. 2009, 9: 1187-1200. 10.1586/ern.09.72.CrossRefPubMed Teramoto S: Novel preventive and therapeutic strategy for post-stroke pneumonia. Expert Rev Neurother. 2009, 9: 1187-1200. 10.1586/ern.09.72.CrossRefPubMed
7.
go back to reference Dziewas R, Ritter M, Schilling M, Konrad C, Oelenberg S, Nabavi DG, Stögbauer F, Ringelstein EB, Lüdemann P: Pneumonia in acute stroke patients fed by nasogastric tube. J Neurol Neurosurg Psychiatry. 2004, 75: 852-856. 10.1136/jnnp.2003.019075.PubMedCentralCrossRefPubMed Dziewas R, Ritter M, Schilling M, Konrad C, Oelenberg S, Nabavi DG, Stögbauer F, Ringelstein EB, Lüdemann P: Pneumonia in acute stroke patients fed by nasogastric tube. J Neurol Neurosurg Psychiatry. 2004, 75: 852-856. 10.1136/jnnp.2003.019075.PubMedCentralCrossRefPubMed
8.
go back to reference Riquelme R, Torres A, El-Ebiary M, de la Bellacasa JP, Estruch R, Mensa J, Fernández-Solá J, Hernández C, Rodriguez-Roisin R: Community-acquired pneumonia in the elderly: a multivariate analysis of risk and prognostic factors. Am J Respir Crit Care Med. 1996, 154: 1450-1455. 10.1164/ajrccm.154.5.8912763.CrossRefPubMed Riquelme R, Torres A, El-Ebiary M, de la Bellacasa JP, Estruch R, Mensa J, Fernández-Solá J, Hernández C, Rodriguez-Roisin R: Community-acquired pneumonia in the elderly: a multivariate analysis of risk and prognostic factors. Am J Respir Crit Care Med. 1996, 154: 1450-1455. 10.1164/ajrccm.154.5.8912763.CrossRefPubMed
9.
go back to reference Prass K, Braun JS, Dirnagl U, Meisel C, Meisel A: Stroke propagates bacterial aspiration to pneumonia in a model of cerebral ischemia. Stroke. 2006, 37: 2607-2612. 10.1161/01.STR.0000240409.68739.2b.CrossRefPubMed Prass K, Braun JS, Dirnagl U, Meisel C, Meisel A: Stroke propagates bacterial aspiration to pneumonia in a model of cerebral ischemia. Stroke. 2006, 37: 2607-2612. 10.1161/01.STR.0000240409.68739.2b.CrossRefPubMed
10.
go back to reference Prass K, Meisel C, Höflich C, Braun J, Halle E, Wolf T, Ruscher K, Victorov IV, Priller J, Dirnagl U, Volk HD, Meisel A, Priller J, Dirnagl U, Volk HD, Meisel A: 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. 2003, 198: 725-736. 10.1084/jem.20021098.PubMedCentralCrossRefPubMed Prass K, Meisel C, Höflich C, Braun J, Halle E, Wolf T, Ruscher K, Victorov IV, Priller J, Dirnagl U, Volk HD, Meisel A, Priller J, Dirnagl U, Volk HD, Meisel A: 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. 2003, 198: 725-736. 10.1084/jem.20021098.PubMedCentralCrossRefPubMed
11.
go back to reference Walter U, Kolbaske S, Patejdl R, Steinhagen V, Abu-Mugheisib M, Grossmann A, Zingler C, Benecke R: Insular stroke is associated with acute sympathetic hyperactivation and immunodepression. Eur J Neurol. 2013, 20: 153-159. 10.1111/j.1468-1331.2012.03818.x.CrossRefPubMed Walter U, Kolbaske S, Patejdl R, Steinhagen V, Abu-Mugheisib M, Grossmann A, Zingler C, Benecke R: Insular stroke is associated with acute sympathetic hyperactivation and immunodepression. Eur J Neurol. 2013, 20: 153-159. 10.1111/j.1468-1331.2012.03818.x.CrossRefPubMed
13.
go back to reference Macrez R, Ali C, Toutirais O, Le Mauff B, Defer G, Dirnagl U, Vivien D: Stroke and the immune system: from pathophysiology to new therapeutic strategies. Lancet Neurol. 2011, 10: 471-480. 10.1016/S1474-4422(11)70066-7.CrossRefPubMed Macrez R, Ali C, Toutirais O, Le Mauff B, Defer G, Dirnagl U, Vivien D: Stroke and the immune system: from pathophysiology to new therapeutic strategies. Lancet Neurol. 2011, 10: 471-480. 10.1016/S1474-4422(11)70066-7.CrossRefPubMed
14.
go back to reference Chamorro A, Urra X, Planas AM: Infection after acute ischemic stroke: a manifestation of brain-induced immunodepression. Stroke. 2007, 38: 1097-1103. 10.1161/01.STR.0000258346.68966.9d.CrossRefPubMed Chamorro A, Urra X, Planas AM: Infection after acute ischemic stroke: a manifestation of brain-induced immunodepression. Stroke. 2007, 38: 1097-1103. 10.1161/01.STR.0000258346.68966.9d.CrossRefPubMed
15.
go back to reference Bellinger DL, Millar BA, Perez S, Carter J, Wood C, ThyagaRajan S, Molinaro C, Lubahn C, Lorton D: Sympathetic modulation of immunity: relevance to disease. Cell Immunol. 2008, 252: 27-56. 10.1016/j.cellimm.2007.09.005.PubMedCentralCrossRefPubMed Bellinger DL, Millar BA, Perez S, Carter J, Wood C, ThyagaRajan S, Molinaro C, Lubahn C, Lorton D: Sympathetic modulation of immunity: relevance to disease. Cell Immunol. 2008, 252: 27-56. 10.1016/j.cellimm.2007.09.005.PubMedCentralCrossRefPubMed
16.
go back to reference Dziedzic T, Slowik A, Pera J, Szczudlik A: Beta-blockers reduce the risk of early death in ischemic stroke. J Neurol Sci. 2007, 252: 53-56. 10.1016/j.jns.2006.10.007.CrossRefPubMed Dziedzic T, Slowik A, Pera J, Szczudlik A: Beta-blockers reduce the risk of early death in ischemic stroke. J Neurol Sci. 2007, 252: 53-56. 10.1016/j.jns.2006.10.007.CrossRefPubMed
17.
go back to reference Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD: Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab. 2006, 26: 654-665. 10.1038/sj.jcbfm.9600217.CrossRefPubMed Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD: Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab. 2006, 26: 654-665. 10.1038/sj.jcbfm.9600217.CrossRefPubMed
18.
go back to reference Chang L, Chen Y, Li J, Liu Z, Wang Z, Chen J, Cao W, Xu Y: Cocaine-and amphetamine-regulated transcript modulates peripheral immunity and protects against brain injury in experimental stroke. Brain Behav Immun. 2011, 25: 260-269. 10.1016/j.bbi.2010.09.017.CrossRefPubMed Chang L, Chen Y, Li J, Liu Z, Wang Z, Chen J, Cao W, Xu Y: Cocaine-and amphetamine-regulated transcript modulates peripheral immunity and protects against brain injury in experimental stroke. Brain Behav Immun. 2011, 25: 260-269. 10.1016/j.bbi.2010.09.017.CrossRefPubMed
19.
go back to reference Woiciechowsky C, Schöning B, Daberkow N, Asche K, Stoltenburg G, Lanksch WR, Volk HD: Brain-IL-1beta induces local inflammation but systemic anti-inflammatory response through stimulation of both hypothalamic-pituitary-adrenal axis and sympathetic nervous system. Brain Res. 1999, 816: 563-571. 10.1016/S0006-8993(98)01238-4.CrossRefPubMed Woiciechowsky C, Schöning B, Daberkow N, Asche K, Stoltenburg G, Lanksch WR, Volk HD: Brain-IL-1beta induces local inflammation but systemic anti-inflammatory response through stimulation of both hypothalamic-pituitary-adrenal axis and sympathetic nervous system. Brain Res. 1999, 816: 563-571. 10.1016/S0006-8993(98)01238-4.CrossRefPubMed
20.
go back to reference Hardy J, Bednarski RM, Biller DS: Effect of phenylephrine on hemodynamics and splenic dimensions in horses. Am J Vet Res. 1994, 55: 1570-1578.PubMed Hardy J, Bednarski RM, Biller DS: Effect of phenylephrine on hemodynamics and splenic dimensions in horses. Am J Vet Res. 1994, 55: 1570-1578.PubMed
21.
go back to reference Ajmo CT, Collier LA, Leonardo CC, Hall AA, Green SM, Womble TA, Cuevas J, Willing AE, Pennypacker KR: Blockade of adrenoreceptors inhibits the splenic response to stroke. Exp Neurol. 2009, 218: 47-55. 10.1016/j.expneurol.2009.03.044.PubMedCentralCrossRefPubMed Ajmo CT, Collier LA, Leonardo CC, Hall AA, Green SM, Womble TA, Cuevas J, Willing AE, Pennypacker KR: Blockade of adrenoreceptors inhibits the splenic response to stroke. Exp Neurol. 2009, 218: 47-55. 10.1016/j.expneurol.2009.03.044.PubMedCentralCrossRefPubMed
22.
go back to reference Offner H, Subramanian S, Parker SM, Wang C, Afentoulis ME, Lewis A, Vandenbark AA, Hurn PD: Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol. 2006, 176: 6523-6531. 10.4049/jimmunol.176.11.6523.CrossRefPubMed Offner H, Subramanian S, Parker SM, Wang C, Afentoulis ME, Lewis A, Vandenbark AA, Hurn PD: Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol. 2006, 176: 6523-6531. 10.4049/jimmunol.176.11.6523.CrossRefPubMed
23.
go back to reference Bakovic D, Pivac N, Eterovic D, Breskovic T, Zubin P, Obad A, Dujic Z: The effects of low-dose epinephrine infusion on spleen size, central and hepatic circulation and circulating platelets. Clin Physiol Funct Imaging. 2013, 33: 30-37. 10.1111/j.1475-097X.2012.01156.x.CrossRefPubMed Bakovic D, Pivac N, Eterovic D, Breskovic T, Zubin P, Obad A, Dujic Z: The effects of low-dose epinephrine infusion on spleen size, central and hepatic circulation and circulating platelets. Clin Physiol Funct Imaging. 2013, 33: 30-37. 10.1111/j.1475-097X.2012.01156.x.CrossRefPubMed
24.
go back to reference Wong CH, Jenne CN, Lee WY, Léger C, Kubes P: Functional innervation of hepatic iNKT cells is immunosuppressive following stroke. Science. 2011, 334: 101-105. 10.1126/science.1210301.CrossRefPubMed Wong CH, Jenne CN, Lee WY, Léger C, Kubes P: Functional innervation of hepatic iNKT cells is immunosuppressive following stroke. Science. 2011, 334: 101-105. 10.1126/science.1210301.CrossRefPubMed
25.
go back to reference Meisel C, Meisel A: Suppressing immunosuppression after stroke. N Engl J Med. 2011, 365: 2134-2136. 10.1056/NEJMcibr1112454.CrossRefPubMed Meisel C, Meisel A: Suppressing immunosuppression after stroke. N Engl J Med. 2011, 365: 2134-2136. 10.1056/NEJMcibr1112454.CrossRefPubMed
26.
go back to reference Maddahi A, Edvinsson L: Cerebral ischemia induces microvascular pro-inflammatory cytokine expression via the MEK/ERK pathway. J Neuroinflammation 2010, 7:14.. Maddahi A, Edvinsson L: Cerebral ischemia induces microvascular pro-inflammatory cytokine expression via the MEK/ERK pathway. J Neuroinflammation 2010, 7:14..
27.
go back to reference Maddahi A, Kruse LS, Chen QW, Edvinsson L: The role of tumor necrosis factor-α and TNF-α receptors in cerebral arteries following cerebral ischemia in rat. J Neuroinflammation 2011, 8:107.. Maddahi A, Kruse LS, Chen QW, Edvinsson L: The role of tumor necrosis factor-α and TNF-α receptors in cerebral arteries following cerebral ischemia in rat. J Neuroinflammation 2011, 8:107..
28.
go back to reference Ahnstedt H, Stenman E, Cao L, Henriksson M, Edvinsson L: Cytokines and growth factors modify the upregulation of contractile endothelin ET(A) and ET(B) receptors in rat cerebral arteries after organ culture. Acta Physiol (Oxf). 2012, 205: 266-278. 10.1111/j.1748-1716.2011.02392.x.CrossRef Ahnstedt H, Stenman E, Cao L, Henriksson M, Edvinsson L: Cytokines and growth factors modify the upregulation of contractile endothelin ET(A) and ET(B) receptors in rat cerebral arteries after organ culture. Acta Physiol (Oxf). 2012, 205: 266-278. 10.1111/j.1748-1716.2011.02392.x.CrossRef
29.
go back to reference Faraco G, Moraga A, Moore J, Anrather J, Pickel VM, Iadecola C: Circulating endothelin-1 alters critical mechanisms regulating cerebral microcirculation. Hypertension. 2013, 62: 759-766. 10.1161/HYPERTENSIONAHA.113.01761.CrossRefPubMed Faraco G, Moraga A, Moore J, Anrather J, Pickel VM, Iadecola C: Circulating endothelin-1 alters critical mechanisms regulating cerebral microcirculation. Hypertension. 2013, 62: 759-766. 10.1161/HYPERTENSIONAHA.113.01761.CrossRefPubMed
30.
go back to reference Winklewski PJ, Frydrychowski AF: Cerebral blood flow, sympathetic nerve activity and stroke risk in obstructive sleep apnoea. Is there a direct link?. Blood Press. 2013, 22: 27-33. 10.3109/08037051.2012.701407.CrossRefPubMed Winklewski PJ, Frydrychowski AF: Cerebral blood flow, sympathetic nerve activity and stroke risk in obstructive sleep apnoea. Is there a direct link?. Blood Press. 2013, 22: 27-33. 10.3109/08037051.2012.701407.CrossRefPubMed
31.
go back to reference Ainslie PN, Brassard P: Why is the neural control of cerebral autoregulation so controversial? F1000Prime Rep 2014, 6:14.. Ainslie PN, Brassard P: Why is the neural control of cerebral autoregulation so controversial? F1000Prime Rep 2014, 6:14..
32.
go back to reference Ter Laan M, van Dijk JM, Elting JW, Staal MJ, Absalom AR: Sympathetic regulation of cerebral blood flow in humans: a review. Br J Anaesth. 2013, 111: 361-367. 10.1093/bja/aet122.CrossRefPubMed Ter Laan M, van Dijk JM, Elting JW, Staal MJ, Absalom AR: Sympathetic regulation of cerebral blood flow in humans: a review. Br J Anaesth. 2013, 111: 361-367. 10.1093/bja/aet122.CrossRefPubMed
33.
go back to reference Cassaglia PA, Griffiths RI, Walker AM: Sympathetic nerve activity in the superior cervical ganglia increases in response to imposed increases in arterial pressure. Am J Physiol Regul Integr Comp Physiol. 2008, 294: R1255-R1261. 10.1152/ajpregu.00332.2007.CrossRefPubMed Cassaglia PA, Griffiths RI, Walker AM: Sympathetic nerve activity in the superior cervical ganglia increases in response to imposed increases in arterial pressure. Am J Physiol Regul Integr Comp Physiol. 2008, 294: R1255-R1261. 10.1152/ajpregu.00332.2007.CrossRefPubMed
34.
go back to reference Hamner JW, Tan CO, Lee K, Cohen MA, Taylor JA: Sympathetic control of the cerebral vasculature in humans. Stroke. 2010, 41: 102-109. 10.1161/STROKEAHA.109.557132.PubMedCentralCrossRefPubMed Hamner JW, Tan CO, Lee K, Cohen MA, Taylor JA: Sympathetic control of the cerebral vasculature in humans. Stroke. 2010, 41: 102-109. 10.1161/STROKEAHA.109.557132.PubMedCentralCrossRefPubMed
35.
go back to reference Immink RV, van Montfrans GA, Stam J, Karemaker JM, Diamant M, van Lieshout JJ: Dynamic cerebral autoregulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke. 2005, 36: 2595-2600. 10.1161/01.STR.0000189624.06836.03.CrossRefPubMed Immink RV, van Montfrans GA, Stam J, Karemaker JM, Diamant M, van Lieshout JJ: Dynamic cerebral autoregulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke. 2005, 36: 2595-2600. 10.1161/01.STR.0000189624.06836.03.CrossRefPubMed
36.
go back to reference Gur AY, Gücüyener D, Uzüner N, Gilutz Y, Ozdemir G, Korczyn AD, Bornstein NM: Cerebral vasomotor reactivity of patients with acute ischemic stroke: cortical versus subcortical infarcts: an Israeli-Turkish collaborative study. J Neurol Sci. 2007, 257: 121-125. 10.1016/j.jns.2007.01.024.CrossRefPubMed Gur AY, Gücüyener D, Uzüner N, Gilutz Y, Ozdemir G, Korczyn AD, Bornstein NM: Cerebral vasomotor reactivity of patients with acute ischemic stroke: cortical versus subcortical infarcts: an Israeli-Turkish collaborative study. J Neurol Sci. 2007, 257: 121-125. 10.1016/j.jns.2007.01.024.CrossRefPubMed
37.
go back to reference Kamel H, Iadecola C: Brain-immune interactions and ischemic stroke: clinical implications. Arch Neurol. 2012, 69: 576-581. 10.1001/archneurol.2011.3590.PubMedCentralCrossRefPubMed Kamel H, Iadecola C: Brain-immune interactions and ischemic stroke: clinical implications. Arch Neurol. 2012, 69: 576-581. 10.1001/archneurol.2011.3590.PubMedCentralCrossRefPubMed
38.
go back to reference Armstead WM, Bohman LE, Riley J, Yarovoi S, Higazi AA, Cines DB: tPA-S (481) A prevents impairment of cerebrovascular autoregulation by endogenous tPA after traumatic brain injury by upregulating p38 MAPK and inhibiting ET-1. J Neurotrauma. 2013, 30: 1898-1907. 10.1089/neu.2013.2962.PubMedCentralCrossRefPubMed Armstead WM, Bohman LE, Riley J, Yarovoi S, Higazi AA, Cines DB: tPA-S (481) A prevents impairment of cerebrovascular autoregulation by endogenous tPA after traumatic brain injury by upregulating p38 MAPK and inhibiting ET-1. J Neurotrauma. 2013, 30: 1898-1907. 10.1089/neu.2013.2962.PubMedCentralCrossRefPubMed
39.
go back to reference Ishikawa M, Cooper D, Russell J, Salter JW, Zhang JH, Nanda A, Granger DN: Molecular determinants of the prothrombogenic and inflammatory phenotype assumed by the postischemic cerebral microcirculation. Stroke. 2003, 34: 1777-1782. 10.1161/01.STR.0000074921.17767.F2.CrossRefPubMed Ishikawa M, Cooper D, Russell J, Salter JW, Zhang JH, Nanda A, Granger DN: Molecular determinants of the prothrombogenic and inflammatory phenotype assumed by the postischemic cerebral microcirculation. Stroke. 2003, 34: 1777-1782. 10.1161/01.STR.0000074921.17767.F2.CrossRefPubMed
40.
go back to reference Nieswandt B, Kleinschnitz C, Stoll G: Ischaemic stroke: a thrombo-inflammatory disease?. J Physiol. 2011, 589: 4115-4123. 10.1113/jphysiol.2011.212886.PubMedCentralCrossRefPubMed Nieswandt B, Kleinschnitz C, Stoll G: Ischaemic stroke: a thrombo-inflammatory disease?. J Physiol. 2011, 589: 4115-4123. 10.1113/jphysiol.2011.212886.PubMedCentralCrossRefPubMed
41.
go back to reference Stoll G, Kleinschnitz C, Nieswandt B: Combating innate inflammation: a new paradigm for acute treatment of stroke?. Ann N Y Acad Sci. 2010, 1207: 149-154. 10.1111/j.1749-6632.2010.05730.x.CrossRefPubMed Stoll G, Kleinschnitz C, Nieswandt B: Combating innate inflammation: a new paradigm for acute treatment of stroke?. Ann N Y Acad Sci. 2010, 1207: 149-154. 10.1111/j.1749-6632.2010.05730.x.CrossRefPubMed
43.
go back to reference Nakajima K, Kohsaka S: Microglia: activation and their significance in the central nervous system. J Biochem. 2001, 130: 169-175. 10.1093/oxfordjournals.jbchem.a002969.CrossRefPubMed Nakajima K, Kohsaka S: Microglia: activation and their significance in the central nervous system. J Biochem. 2001, 130: 169-175. 10.1093/oxfordjournals.jbchem.a002969.CrossRefPubMed
44.
go back to reference Banati RB, Gehrmann J, Schubert P, Kreutzberg GW: Cytotoxicity of microglia. Glia. 1993, 7: 111-118. 10.1002/glia.440070117.CrossRefPubMed Banati RB, Gehrmann J, Schubert P, Kreutzberg GW: Cytotoxicity of microglia. Glia. 1993, 7: 111-118. 10.1002/glia.440070117.CrossRefPubMed
45.
go back to reference Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG: Microglia potentiate damage to blood–brain barrier constituents: improvement by minocycline in vivo and in vitro . Stroke. 2006, 37: 1087-1093. 10.1161/01.STR.0000206281.77178.ac.CrossRefPubMed Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG: Microglia potentiate damage to blood–brain barrier constituents: improvement by minocycline in vivo and in vitro . Stroke. 2006, 37: 1087-1093. 10.1161/01.STR.0000206281.77178.ac.CrossRefPubMed
46.
go back to reference Pun PB, Lu J, Moochhala S: Involvement of ROS in BBB dysfunction. Free Radic Res. 2009, 43: 348-364. 10.1080/10715760902751902.CrossRefPubMed Pun PB, Lu J, Moochhala S: Involvement of ROS in BBB dysfunction. Free Radic Res. 2009, 43: 348-364. 10.1080/10715760902751902.CrossRefPubMed
47.
go back to reference Denes A, Vidyasagar R, Feng J, Narvainen J, McColl BW, Kauppinen RA, Allan SM: Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab. 2007, 27: 1941-1953. 10.1038/sj.jcbfm.9600495.CrossRefPubMed Denes A, Vidyasagar R, Feng J, Narvainen J, McColl BW, Kauppinen RA, Allan SM: Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab. 2007, 27: 1941-1953. 10.1038/sj.jcbfm.9600495.CrossRefPubMed
48.
go back to reference Lalancette-Hébert M, Gowing G, Simard A, Weng YC, Kriz J: Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci. 2007, 27: 2596-2605. 10.1523/JNEUROSCI.5360-06.2007.CrossRefPubMed Lalancette-Hébert M, Gowing G, Simard A, Weng YC, Kriz J: Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci. 2007, 27: 2596-2605. 10.1523/JNEUROSCI.5360-06.2007.CrossRefPubMed
49.
go back to reference Kriz J: Inflammation in ischemic brain injury: timing is important. Crit Rev Neurobiol. 2006, 18: 145-157. 10.1615/CritRevNeurobiol.v18.i1-2.150.CrossRefPubMed Kriz J: Inflammation in ischemic brain injury: timing is important. Crit Rev Neurobiol. 2006, 18: 145-157. 10.1615/CritRevNeurobiol.v18.i1-2.150.CrossRefPubMed
51.
go back to reference Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, Siler DA, Arumugam TV, Orthey E, Gerloff C, Tolosa E, Magnus T: Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke. 2009, 40: 1849-1857. 10.1161/STROKEAHA.108.534503.CrossRefPubMed Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, Siler DA, Arumugam TV, Orthey E, Gerloff C, Tolosa E, Magnus T: Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke. 2009, 40: 1849-1857. 10.1161/STROKEAHA.108.534503.CrossRefPubMed
52.
go back to reference Chao HJ, Hsu YC, Yuan HP, Jiang HS, Hsueh CM: The conditioned enhancement of neutrophil activity is catecholamine dependent. J Neuroimmunol. 2005, 158: 159-169. 10.1016/j.jneuroim.2004.09.008.CrossRefPubMed Chao HJ, Hsu YC, Yuan HP, Jiang HS, Hsueh CM: The conditioned enhancement of neutrophil activity is catecholamine dependent. J Neuroimmunol. 2005, 158: 159-169. 10.1016/j.jneuroim.2004.09.008.CrossRefPubMed
53.
go back to reference Brait VH, Jackman KA, Walduck AK, Selemidis S, Diep H, Mast AE, Guida E, Broughton BR, Drummond GR, Sobey CG: Mechanisms contributing to cerebral infarct size after stroke: gender, reperfusion, T lymphocytes, and Nox2-derived superoxide. J Cereb Blood Flow Metab. 2010, 30: 1306-1317. 10.1038/jcbfm.2010.14.PubMedCentralCrossRefPubMed Brait VH, Jackman KA, Walduck AK, Selemidis S, Diep H, Mast AE, Guida E, Broughton BR, Drummond GR, Sobey CG: Mechanisms contributing to cerebral infarct size after stroke: gender, reperfusion, T lymphocytes, and Nox2-derived superoxide. J Cereb Blood Flow Metab. 2010, 30: 1306-1317. 10.1038/jcbfm.2010.14.PubMedCentralCrossRefPubMed
54.
go back to reference Jander S, Kraemer M, Schroeter M, Witte OW, Stoll G: Lymphocytic infiltration and expression of intercellular adhesion molecule-1 in photochemically induced ischemia of the rat cortex. J Cereb Blood Flow Metab. 1995, 15: 42-51. 10.1038/jcbfm.1995.5.CrossRefPubMed Jander S, Kraemer M, Schroeter M, Witte OW, Stoll G: Lymphocytic infiltration and expression of intercellular adhesion molecule-1 in photochemically induced ischemia of the rat cortex. J Cereb Blood Flow Metab. 1995, 15: 42-51. 10.1038/jcbfm.1995.5.CrossRefPubMed
55.
go back to reference Konoeda F, Shichita T, Yoshida H, Sugiyama Y, Muto G, Hasegawa E, Morita R, Suzuki N, Yoshimura A: Therapeutic effect of IL-12/23 and their signaling pathway blockade on brain ischemia model. Biochem Biophys Res Commun. 2010, 402: 500-506. 10.1016/j.bbrc.2010.10.058.CrossRefPubMed Konoeda F, Shichita T, Yoshida H, Sugiyama Y, Muto G, Hasegawa E, Morita R, Suzuki N, Yoshimura A: Therapeutic effect of IL-12/23 and their signaling pathway blockade on brain ischemia model. Biochem Biophys Res Commun. 2010, 402: 500-506. 10.1016/j.bbrc.2010.10.058.CrossRefPubMed
56.
go back to reference Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, Takada I, Iwaki T, Okada Y, Iida M, Cua DJ, Iwakura Y, Yoshimura A: Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med. 2009, 15: 946-950. 10.1038/nm.1999.CrossRefPubMed Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, Takada I, Iwaki T, Okada Y, Iida M, Cua DJ, Iwakura Y, Yoshimura A: Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med. 2009, 15: 946-950. 10.1038/nm.1999.CrossRefPubMed
57.
go back to reference Arumugam TV, Granger DN, Mattson MP: Stroke and T-cells. Neuromolecular Med. 2005, 7: 229-242. 10.1385/NMM:7:3:229.CrossRefPubMed Arumugam TV, Granger DN, Mattson MP: Stroke and T-cells. Neuromolecular Med. 2005, 7: 229-242. 10.1385/NMM:7:3:229.CrossRefPubMed
58.
go back to reference Liesz A, Zhou W, Mracskó É, Karcher S, Bauer H, Schwarting S, Sun L, Bruder D, Stegemann S, Cerwenka A, Sommer C, Dalpke AH, Veltkamp R: Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke. Brain. 2011, 134: 704-720. 10.1093/brain/awr008.CrossRefPubMed Liesz A, Zhou W, Mracskó É, Karcher S, Bauer H, Schwarting S, Sun L, Bruder D, Stegemann S, Cerwenka A, Sommer C, Dalpke AH, Veltkamp R: Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke. Brain. 2011, 134: 704-720. 10.1093/brain/awr008.CrossRefPubMed
59.
go back to reference Barry M, Bleackley RC: Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol. 2002, 2: 401-409.PubMed Barry M, Bleackley RC: Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol. 2002, 2: 401-409.PubMed
60.
go back to reference Brait VH, Arumugam TV, Drummond GR, Sobey CG: Importance of T lymphocytes in brain injury, immunodeficiency, and recovery after cerebral ischemia. J Cereb Blood Flow Metab. 2012, 32: 598-611. 10.1038/jcbfm.2012.6.PubMedCentralCrossRefPubMed Brait VH, Arumugam TV, Drummond GR, Sobey CG: Importance of T lymphocytes in brain injury, immunodeficiency, and recovery after cerebral ischemia. J Cereb Blood Flow Metab. 2012, 32: 598-611. 10.1038/jcbfm.2012.6.PubMedCentralCrossRefPubMed
61.
go back to reference Martin A, Aguirre J, Sarasa-Renedo A, Tsoukatou D, Garofalakis A, Meyer H, Mamalaki C, Ripoll J, Planas AM: Imaging changes in lymphoid organs in vivo after brain ischemia with three-dimensional fluorescence molecular tomography in transgenic mice expressing green fluorescent protein in T lymphocytes. Mol Imaging. 2008, 7: 157-167.PubMed Martin A, Aguirre J, Sarasa-Renedo A, Tsoukatou D, Garofalakis A, Meyer H, Mamalaki C, Ripoll J, Planas AM: Imaging changes in lymphoid organs in vivo after brain ischemia with three-dimensional fluorescence molecular tomography in transgenic mice expressing green fluorescent protein in T lymphocytes. Mol Imaging. 2008, 7: 157-167.PubMed
62.
go back to reference Gendron A, Teitelbaum J, Cossette C, Nuara S, Dumont M, Geadah D, du Souich P, Kouassi E: Temporal effects of left versus right middle cerebral artery occlusion on spleen lymphocyte subsets and mitogenic response in Wistar rats. Brain Res. 2002, 955: 85-97. 10.1016/S0006-8993(02)03368-1.CrossRefPubMed Gendron A, Teitelbaum J, Cossette C, Nuara S, Dumont M, Geadah D, du Souich P, Kouassi E: Temporal effects of left versus right middle cerebral artery occlusion on spleen lymphocyte subsets and mitogenic response in Wistar rats. Brain Res. 2002, 955: 85-97. 10.1016/S0006-8993(02)03368-1.CrossRefPubMed
63.
go back to reference Mracsko E, Liesz A, Karcher S, Zorn M, Bari F, Veltkamp R: Differential effects of sympathetic nervous system and hypothalamic-pituitary-adrenal axis on systemic immune cells after severe experimental stroke. Brain Behav Immun. 2014, 41: 200-209. 10.1016/j.bbi.2014.05.015.CrossRefPubMed Mracsko E, Liesz A, Karcher S, Zorn M, Bari F, Veltkamp R: Differential effects of sympathetic nervous system and hypothalamic-pituitary-adrenal axis on systemic immune cells after severe experimental stroke. Brain Behav Immun. 2014, 41: 200-209. 10.1016/j.bbi.2014.05.015.CrossRefPubMed
64.
go back to reference Wang J, Yu L, Jiang C, Fu X, Liu X, Wang M, Ou C, Cui X, Zhou C, Wang J: Cerebral ischemia increases bone marrow CD4 + CD25 + FoxP3+ regulatory T cells in mice via signals from sympathetic nervous system. Brain Behav Immun 2015, 43:172-83. doi:10.1016/j.bbi.2014.07.022. Wang J, Yu L, Jiang C, Fu X, Liu X, Wang M, Ou C, Cui X, Zhou C, Wang J: Cerebral ischemia increases bone marrow CD4 + CD25 + FoxP3+ regulatory T cells in mice via signals from sympathetic nervous system. Brain Behav Immun 2015, 43:172-83. doi:10.1016/j.bbi.2014.07.022.
65.
go back to reference Demling R, Riessen R: Pulmonary dysfunction after cerebral injury. Crit Care Med. 1990, 18: 768-774. 10.1097/00003246-199007000-00019.CrossRefPubMed Demling R, Riessen R: Pulmonary dysfunction after cerebral injury. Crit Care Med. 1990, 18: 768-774. 10.1097/00003246-199007000-00019.CrossRefPubMed
66.
go back to reference Davison DL, Terek M, Chawla LS: Neurogenic pulmonary edema. Crit Care 2012, 16:212.. Davison DL, Terek M, Chawla LS: Neurogenic pulmonary edema. Crit Care 2012, 16:212..
67.
go back to reference Pelosi P, Severgnini P, Chiaranda M: An integrated approach to prevent and treat respiratory failure in brain-injured patients. Curr Opin Crit Care. 2005, 11: 37-42. 10.1097/00075198-200502000-00006.CrossRefPubMed Pelosi P, Severgnini P, Chiaranda M: An integrated approach to prevent and treat respiratory failure in brain-injured patients. Curr Opin Crit Care. 2005, 11: 37-42. 10.1097/00075198-200502000-00006.CrossRefPubMed
68.
go back to reference Holland MC, Mackersie RC, Morabito D, Campbell AR, Kivett VA, Patel R, Erickson VR, Pittet JF: The development of acute lung injury is associated with worse neurologic outcome in patients with severe traumatic brain injury. J Trauma. 2003, 55: 106-111. 10.1097/01.TA.0000071620.27375.BE.CrossRefPubMed Holland MC, Mackersie RC, Morabito D, Campbell AR, Kivett VA, Patel R, Erickson VR, Pittet JF: The development of acute lung injury is associated with worse neurologic outcome in patients with severe traumatic brain injury. J Trauma. 2003, 55: 106-111. 10.1097/01.TA.0000071620.27375.BE.CrossRefPubMed
69.
go back to reference Kahn JM, Caldwell EC, Deem S, Newell DW, Heckbert SR, Rubenfeld GD: Acute lung injury in patients with subarachnoid hemorrhage: incidence, risk factors, and outcome. Crit Care Med. 2006, 34: 196-202. 10.1097/01.CCM.0000194540.44020.8E.CrossRefPubMed Kahn JM, Caldwell EC, Deem S, Newell DW, Heckbert SR, Rubenfeld GD: Acute lung injury in patients with subarachnoid hemorrhage: incidence, risk factors, and outcome. Crit Care Med. 2006, 34: 196-202. 10.1097/01.CCM.0000194540.44020.8E.CrossRefPubMed
70.
go back to reference López-Aguilar J, Villagrá A, Bernabé F, Murias G, Piacentini E, Real J, Fernández-Segoviano P, Romero PV, Hotchkiss JR, Blanch L: Massive brain injury enhances lung damage in an isolated lung model of ventilator-induced lung injury. Crit Care Med. 2005, 33: 1077-1083. 10.1097/01.CCM.0000162913.72479.F7.CrossRefPubMed López-Aguilar J, Villagrá A, Bernabé F, Murias G, Piacentini E, Real J, Fernández-Segoviano P, Romero PV, Hotchkiss JR, Blanch L: Massive brain injury enhances lung damage in an isolated lung model of ventilator-induced lung injury. Crit Care Med. 2005, 33: 1077-1083. 10.1097/01.CCM.0000162913.72479.F7.CrossRefPubMed
71.
go back to reference Colice GL: Neurogenic pulmonary edema. Clin Chest Med. 1985, 6: 473-489.PubMed Colice GL: Neurogenic pulmonary edema. Clin Chest Med. 1985, 6: 473-489.PubMed
72.
go back to reference Theodore J, Robin E: Pathogenesis of neurogenic pulmonary oedema. Lancet. 1975, 2: 749-751. 10.1016/S0140-6736(75)90729-1.CrossRefPubMed Theodore J, Robin E: Pathogenesis of neurogenic pulmonary oedema. Lancet. 1975, 2: 749-751. 10.1016/S0140-6736(75)90729-1.CrossRefPubMed
73.
go back to reference Rassler B: Contribution of α - and β-adrenergic mechanisms to the development of pulmonary edema. Scientifica (Cairo) 2012, 2012:829504.. Rassler B: Contribution of α - and β-adrenergic mechanisms to the development of pulmonary edema. Scientifica (Cairo) 2012, 2012:829504..
74.
go back to reference Kalsotra A, Zhao J, Anakk S, Dash PK, Strobel HW: Brain trauma leads to enhanced lung inflammation and injury: evidence for role of P4504Fs in resolution. J Cereb Blood Flow Metab. 2007, 27: 963-974.PubMed Kalsotra A, Zhao J, Anakk S, Dash PK, Strobel HW: Brain trauma leads to enhanced lung inflammation and injury: evidence for role of P4504Fs in resolution. J Cereb Blood Flow Metab. 2007, 27: 963-974.PubMed
75.
go back to reference Mascia L: Acute lung injury in patients with severe brain injury: a double hit model. Neurocrit Care. 2009, 11: 417-426. 10.1007/s12028-009-9242-8.CrossRefPubMed Mascia L: Acute lung injury in patients with severe brain injury: a double hit model. Neurocrit Care. 2009, 11: 417-426. 10.1007/s12028-009-9242-8.CrossRefPubMed
76.
go back to reference Cobelens PM, Tiebosch IA, Dijkhuizen RM, van der Meide PH, Zwartbol R, Heijnen CJ, Kesecioglu J, van den Bergh WM: Interferon-β attenuates lung inflammation following experimental subarachnoid hemorrhage. Crit Care 2010, 14:R157.. Cobelens PM, Tiebosch IA, Dijkhuizen RM, van der Meide PH, Zwartbol R, Heijnen CJ, Kesecioglu J, van den Bergh WM: Interferon-β attenuates lung inflammation following experimental subarachnoid hemorrhage. Crit Care 2010, 14:R157..
77.
go back to reference Wu S, Fang CX, Kim J, Ren J: Enhanced pulmonary inflammation following experimental intracerebral hemorrhage. Exp Neurol. 2006, 200: 245-249. 10.1016/j.expneurol.2006.01.027.CrossRefPubMed Wu S, Fang CX, Kim J, Ren J: Enhanced pulmonary inflammation following experimental intracerebral hemorrhage. Exp Neurol. 2006, 200: 245-249. 10.1016/j.expneurol.2006.01.027.CrossRefPubMed
78.
go back to reference Flierl MA, Rittirsch D, Nadeau BA, Sarma JV, Day DE, Lentsch AB, Huber-Lang MS, Ward PA: Upregulation of phagocyte-derived catecholamines augments the acute inflammatory response. PLoS One 2009, 4:e4414.. Flierl MA, Rittirsch D, Nadeau BA, Sarma JV, Day DE, Lentsch AB, Huber-Lang MS, Ward PA: Upregulation of phagocyte-derived catecholamines augments the acute inflammatory response. PLoS One 2009, 4:e4414..
79.
go back to reference Avlonitis VS, Wigfield CH, Kirby JA, Dark JH: The hemodynamic mechanisms of lung injury and systemic inflammatory response following brain death in the transplant donor. Am J Transplant. 2005, 5: 684-693. 10.1111/j.1600-6143.2005.00755.x.CrossRefPubMed Avlonitis VS, Wigfield CH, Kirby JA, Dark JH: The hemodynamic mechanisms of lung injury and systemic inflammatory response following brain death in the transplant donor. Am J Transplant. 2005, 5: 684-693. 10.1111/j.1600-6143.2005.00755.x.CrossRefPubMed
80.
go back to reference Sammani S, Park KS, Zaidi SR, Mathew B, Wang T, Huang Y, Zhou T, Lussier YA, Husain AN, Moreno-Vinasco L, Vigneswaran WT, Garcia JG: A sphingosine 1-phosphate 1 receptor agonist modulates brain death-induced neurogenic pulmonary injury. Am J Respir Cell Mol Biol. 2011, 45: 1022-1027. 10.1165/rcmb.2010-0267OC.PubMedCentralCrossRefPubMed Sammani S, Park KS, Zaidi SR, Mathew B, Wang T, Huang Y, Zhou T, Lussier YA, Husain AN, Moreno-Vinasco L, Vigneswaran WT, Garcia JG: A sphingosine 1-phosphate 1 receptor agonist modulates brain death-induced neurogenic pulmonary injury. Am J Respir Cell Mol Biol. 2011, 45: 1022-1027. 10.1165/rcmb.2010-0267OC.PubMedCentralCrossRefPubMed
81.
go back to reference Chiarella SE, Soberanes S, Urich D, Morales-Nebreda L, Nigdelioglu R, Green D, Young JB, Gonzalez A, Rosario C, Misharin AV, Ghio AJ, Wunderink RG, Donnelly HK, Radigan KA, Perlman H, Chandel NS, Budinger GR, Mutlu GM: Β2-adrenergic agonists augment air pollution-induced IL-6 release and thrombosis. J Clin Invest. 2014, 124: 2935-2946. 10.1172/JCI75157.PubMedCentralCrossRefPubMed Chiarella SE, Soberanes S, Urich D, Morales-Nebreda L, Nigdelioglu R, Green D, Young JB, Gonzalez A, Rosario C, Misharin AV, Ghio AJ, Wunderink RG, Donnelly HK, Radigan KA, Perlman H, Chandel NS, Budinger GR, Mutlu GM: Β2-adrenergic agonists augment air pollution-induced IL-6 release and thrombosis. J Clin Invest. 2014, 124: 2935-2946. 10.1172/JCI75157.PubMedCentralCrossRefPubMed
82.
go back to reference Toung TJ, Chang Y, Lin J, Bhardwaj A: Increases in lung and brain water following experimental stroke: effect of mannitol and hypertonic saline. Crit Care Med. 2005, 33: 203-208. 10.1097/01.CCM.0000150659.15558.23.CrossRefPubMed Toung TJ, Chang Y, Lin J, Bhardwaj A: Increases in lung and brain water following experimental stroke: effect of mannitol and hypertonic saline. Crit Care Med. 2005, 33: 203-208. 10.1097/01.CCM.0000150659.15558.23.CrossRefPubMed
83.
go back to reference Marrie TJ: Community-acquired pneumonia. Clin Infect Dis. 1994, 18: 501-513. 10.1093/clinids/18.4.501.CrossRefPubMed Marrie TJ: Community-acquired pneumonia. Clin Infect Dis. 1994, 18: 501-513. 10.1093/clinids/18.4.501.CrossRefPubMed
84.
go back to reference Planas AM, Gómez-Choco M, Urra X, Gorina R, Caballero M, Chamorro Á: Brain-derived antigens in lymphoid tissue of patients with acute stroke. J Immunol. 2012, 188: 2156-2163. 10.4049/jimmunol.1102289.CrossRefPubMed Planas AM, Gómez-Choco M, Urra X, Gorina R, Caballero M, Chamorro Á: Brain-derived antigens in lymphoid tissue of patients with acute stroke. J Immunol. 2012, 188: 2156-2163. 10.4049/jimmunol.1102289.CrossRefPubMed
85.
go back to reference Becker KJ, Kindrick DL, Lester MP, Shea C, Ye ZC: Sensitization to brain antigens after stroke is augmented by lipopolysaccharide. J Cereb Blood Flow Metab. 2005, 25: 1634-1644. 10.1038/sj.jcbfm.9600160.PubMedCentralCrossRefPubMed Becker KJ, Kindrick DL, Lester MP, Shea C, Ye ZC: Sensitization to brain antigens after stroke is augmented by lipopolysaccharide. J Cereb Blood Flow Metab. 2005, 25: 1634-1644. 10.1038/sj.jcbfm.9600160.PubMedCentralCrossRefPubMed
86.
go back to reference Zierath D, Thullbery M, Hadwin J, Gee JM, Savos A, Kalil A, Becker KJ: CNS immune responses following experimental stroke. Neurocrit Care. 2010, 12: 274-284. 10.1007/s12028-009-9270-4.PubMedCentralCrossRefPubMed Zierath D, Thullbery M, Hadwin J, Gee JM, Savos A, Kalil A, Becker KJ: CNS immune responses following experimental stroke. Neurocrit Care. 2010, 12: 274-284. 10.1007/s12028-009-9270-4.PubMedCentralCrossRefPubMed
87.
go back to reference Becker KJ, Kalil AJ, Tanzi P, Zierath DK, Savos AV, Gee JM, Hadwin J, Carter KT, Shibata D, Cain KC: Autoimmune responses to the brain after stroke are associated with worse outcome. Stroke. 2011, 42: 2763-2769. 10.1161/STROKEAHA.111.619593.PubMedCentralCrossRefPubMed Becker KJ, Kalil AJ, Tanzi P, Zierath DK, Savos AV, Gee JM, Hadwin J, Carter KT, Shibata D, Cain KC: Autoimmune responses to the brain after stroke are associated with worse outcome. Stroke. 2011, 42: 2763-2769. 10.1161/STROKEAHA.111.619593.PubMedCentralCrossRefPubMed
88.
go back to reference Tanzi P, Cain K, Kalil A, Zierath D, Savos A, Gee JM, Shibata D, Hadwin J, Carter K, Becker K: Post-stroke infection: a role for IL-1ra?. Neurocrit Care. 2011, 14: 244-252. 10.1007/s12028-010-9490-7.PubMedCentralCrossRefPubMed Tanzi P, Cain K, Kalil A, Zierath D, Savos A, Gee JM, Shibata D, Hadwin J, Carter K, Becker K: Post-stroke infection: a role for IL-1ra?. Neurocrit Care. 2011, 14: 244-252. 10.1007/s12028-010-9490-7.PubMedCentralCrossRefPubMed
Metadata
Title
Cross-talk between the inflammatory response, sympathetic activation and pulmonary infection in the ischemic stroke
Authors
Pawel J Winklewski
Marek Radkowski
Urszula Demkow
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2014
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-014-0213-4

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