Neutrophil extracellular traps are increased in patients with acute ischemic stroke: Prognostic significance

Thrombosis and Haemostasis

Volumn 117, Issue 10, 2017, Pages 1919-1929

  Vallés, Juana ^a   Lago, Aida ^b   Santos, María Teresa ^a   Latorre, Ana María ^a   Tembl, José I ^b   Salom, Juan B ^a,c   Nieves, Candela ^b   Moscardó, Antonio ^a  

^a HEALTH RESEARCH INSTITUTE LA FE   (Spain)

^b HOSPITAL UNIVERSITARIO LA FE   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Atrial fibrillation; Extracellular traps; Glucose; Immunity; Stroke

Indexed keywords

ADULT; ARTERY THROMBOSIS; ARTICLE; BRAIN ISCHEMIA; CARDIOEMBOLIC STROKE; CLINICAL OUTCOME; COMPUTER ASSISTED TOMOGRAPHY; ECHOGRAPHY; EXTRACELLULAR TRAP; FEMALE; FOLLOW UP; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOSOME; PERIPHERAL VASCULAR DISEASE; PRIORITY JOURNAL; RISK FACTOR; AGED; BLOOD; CASE CONTROL STUDY; CAUSE OF DEATH; CEREBROVASCULAR ACCIDENT; CHI SQUARE DISTRIBUTION; METABOLISM; MIDDLE AGED; MORTALITY; MULTIVARIATE ANALYSIS; ODDS RATIO; PROGNOSIS; SEVERITY OF ILLNESS INDEX; STATISTICAL MODEL; TIME FACTOR; UPREGULATION; VERY ELDERLY;

BIOLOGICAL MARKER; CITRULLINE; HISTONE;

AGED; AGED, 80 AND OVER; BIOMARKERS; BRAIN ISCHEMIA; CASE-CONTROL STUDIES; CAUSE OF DEATH; CHI-SQUARE DISTRIBUTION; CITRULLINE; EXTRACELLULAR TRAPS; FEMALE; HISTONES; HUMANS; LOGISTIC MODELS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; ODDS RATIO; PROGNOSIS; RISK FACTORS; SEVERITY OF ILLNESS INDEX; STROKE; TIME FACTORS; UP-REGULATION;

EID: 85031094067     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH17-02-0130     Document Type: Article

References (54)

1. Krishnamurthi RV, Feigin VL, Forouzanfar MH, et al. Global and regional burden of first-ever ischaemic and haemorrhagic stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet Glob Health 2013; 1: 259-281.
2. Chamorro A, Dirnagl U, Urra X, et al. Neuroprotection in acute stroke: targeting excitotoxicity, oxidative and nitrosative stress, and inflammation. Lancet Neurol 2016; 15: 869-881.
3. Kehrel BE, Fender AC. Resolving Thromboinflammation in the Brain After Ischemic Stroke? Circulation 2016; 133: 2128-2131.
4. Moscardo A, Latorre A, Santos MT,et al. Platelet function in malignant hematological disorders. Curr Opin Oncol 2015; 27: 522-531.
5. Valles J, Santos MT, Aznar J, et al. Platelet-erythrocyte interactions enhance alpha(IIb)beta(3) integrin receptor activation and P-selectin expression during platelet recruitment: down-regulation by aspirin ex vivo. Blood 2002; 99: 3978-3984.
6. Santos MT, Valles J, Marcus AJ, et al. Enhancement of platelet reactivity and modulation of eicosanoid production by intact erythrocytes. A new approach to platelet activation and recruitment. J Clin Invest 1991; 87: 571-580.
7. Valles J, Lago A, Moscardo A, et al. TXA2 synthesis and COX1-independent platelet reactivity in aspirin-treated patients soon after acute cerebral stroke or transient ischaemic attack. Thromb Res 2013; 132: 211-216.
8. Lago A, Parkhutik V, Tembl JI, et al. Assessment of platelet function in acute ischemic stroke patients previously treated with aspirin. J Stroke Cerebrovasc Dis 2014; 23: 2794-2799.
9. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535.
10. Fuchs TA, Brill A, Wagner DD. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler Thromb Vasc Biol 2012; 32: 1777-1783.
11. Li P, Li M, Lindberg MR, et al. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 2010; 207: 1853-1862.
12. Martinod K, Demers M, Fuchs TA, et al. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proc Natl Acad Sci USA 2013; 110: 8674-8679.
13. Etulain J, Martinod K, Wong SL, et al. P-selectin promotes neutrophil extracellular trap formation in mice. Blood 2015; 126: 242-246.
14. Adams HP, Jr, del Zoppo G, Alberts MJ, et al. Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/ American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: The American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists. Circulation 2007; 115: 478-534.
15. Banks JL, Marotta CA. Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke 2007; 38: 1091-1096.
16. Borissoff JI, Joosen IA, Versteylen MO, et al. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol 2013; 33: 2032-2040.
17. Wong SL, Demers M, Martinod K, et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med 2015; 21: 815-819.
18. Adams HP, Jr, Davis PH, Leira EC, et al. Baseline NIH Stroke Scale score strongly predicts outcome after stroke: A report of the Trial of Org 10172 in Acute Stroke Treatment (TOAST). Neurology 1999; 53: 126-131.
19. Fuchs TA, Brill A, Duerschmied D, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 107: 15880-15885.
20. Mangold A, Alias S, Scherz T, et al. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res 2015; 116: 1182-1192.
21. Savchenko AS, Martinod K, Seidman MA, et al. Neutrophil extracellular traps form predominantly during the organizing stage of human venous thromboembolism development. J Thromb Haemost 2014; 12: 860-870.
22. van Montfoort ML, Stephan F, Lauw MN, et al. Circulating nucleosomes and neutrophil activation as risk factors for deep vein thrombosis. Arterioscler Thromb Vasc Biol 2013; 33: 147-151.
23. Diaz JA, Fuchs TA, Jackson TO, et al. Plasma DNA is Elevated in Patients with Deep Vein Thrombosis. J Vasc Surg Venous Lymphat Disord 2013; 1: 10.1016.
24. Geiger S, Holdenrieder S, Stieber P, et al. Nucleosomes in serum of patients with early cerebral stroke. Cerebrovasc Dis 2006; 21: 32-37.
25. Lam NY, Rainer TH, Wong LK, et al. Plasma DNA as a prognostic marker for stroke patients with negative neuroimaging within the first 24 h of symptom onset. Resuscitation 2006; 68: 71-78.
26. Tsai NW, Lin TK, Chen SD, et al. The value of serial plasma nuclear and mitochondrial DNA levels in patients with acute ischemic stroke. Clin Chim Acta 2011; 412: 476-479.
27. Rainer TH, Wong LK, Lam W, et al. Prognostic use of circulating plasma nucleic acid concentrations in patients with acute stroke. Clin Chem 2003; 49: 562-569.
28. Perez-de-Puig I, Miro-Mur F, Ferrer-Ferrer M, et al. Neutrophil recruitment to the brain in mouse and human ischemic stroke. Acta Neuropathol 2015; 129: 239-257.
29. Thalin C, Demers M, Blomgren B, et al. NETosis promotes cancer-associated arterial microthrombosis presenting as ischemic stroke with troponin elevation. Thromb Res 2016; 139: 56-64.
30. De Meyer SF, Denorme F, Langhauser F, et al. Thromboinflammation in Stroke Brain Damage. Stroke 2016; 47: 1165-1172.
31. Gunzer M. Traps and hyper inflammation -new ways that neutrophils promote or hinder survival. Br J Haematol 2014; 164: 189-199.
32. Caudrillier A, Kessenbrock K, Gilliss BM, et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122: 2661-2671.
33. Gupta S, Agrawal A. Inflammation & autoimmunity in human ageing: dendritic cells take a center stage. Indian J Med Res 2013; 138: 711-716.
34. Lindsberg PJ, Roine RO. Hyperglycemia in acute stroke. Stroke 2004; 35: 363-364.
35. Quagliaro L, Piconi L, Assaloni R, et al. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes 2003; 52: 2795-2804.
36. Rodriguez-Espinosa O, Rojas-Espinosa O, Moreno-Altamirano MM, et al. Metabolic requirements for neutrophil extracellular traps formation. Immunology 2015; 145: 213-224.
37. Menegazzo L, Ciciliot S, Poncina N, et al. NETosis is induced by high glucose and associated with type 2 diabetes. Acta Diabetol 2015; 52: 497-503.
38. Hosseinzadeh A, Thompson PR, Segal BH, Urban CF. Nicotine induces neutrophil extracellular traps. J Leukoc Biol 2016; 100: 1105-1112.
39. Lee J, Luria A, Rhodes C, et al. Nicotine drives neutrophil extracellular traps formation and accelerates collagen-induced arthritis. Rheumatology 2017; 56, 644-653.
40. Mehta H, Nazzal K, Sadikot RT. Cigarette smoking and innate immunity. Inflamm Res 2008; 57: 497-503.
41. Ali SF, Smith EE, Bhatt DL, et al. Paradoxical association of smoking with inhospital mortality among patients admitted with acute ischemic stroke. J Am Heart Assoc 2013; 2: 000171.
42. Kufner A, Nolte CH, Galinovic I, et al.Smoking-thrombolysis paradox: recanalization and reperfusion rates after intravenous tissue plasminogen activator in smokers with ischemic stroke. Stroke 2013; 44: 407-413.
43. Fekete K, Szatmari S, Szocs I, et al. Prestroke alcohol consumption and smoking are not associated with stroke severity, disability at discharge, and case fatality. J Stroke Cerebrovasc Dis 2014; 23: 31-37.
44. Engelmann MD, Svendsen JH. Inflammation in the genesis and perpetuation of atrial fibrillation. Eur Heart J 2005; 26: 2083-2092.
45. Harada M, Van Wagoner DR, Nattel S. Role of inflammation in atrial fibrillation pathophysiology and management. Circ J 2015; 79: 495-502.
46. Conway DS, Buggins P, Hughes E, et al. Prognostic significance of raised plasma levels of interleukin-6 and C-reactive protein in atrial fibrillation. Am Heart J 2004; 148: 462-466.
47. Aviles RJ, Martin DO, Apperson-Hansen C, et al. Inflammation as a risk factor for atrial fibrillation. Circulation 2003; 108: 3006-3010.
48. Boos CJ, Anderson RA, Lip GY. Is atrial fibrillation an inflammatory disorder? Eur Heart J 2006; 27: 136-149.
49. Marin F, Corral J, Roldan V, et al. Factor XIII Val34Leu polymorphism modulates the prothrombotic and inflammatory state associated with atrial fibrillation. J Mol Cell Cardiol 2004; 37: 699-704.
50. Shantsila E, Lip GY. Stroke in atrial fibrillation and improving the identification of’high-risk’ patients: the crossroads of immunity and thrombosis. J Thromb Haemost 2015; 13: 1968-1970.
51. Licata G, Tuttolomondo A, Di Raimondo D, et al. Immuno-inflammatory activation in acute cardio-embolic strokes in comparison with other subtypes of ischaemic stroke. Thromb Haemost 2009; 101: 929-937.
52. Piccardi B, Giralt D, Bustamante A, et al. Blood markers of inflammation and endothelial dysfunction in cardioembolic stroke: systematic review and metaanalysis. Biomarkers 2017; 22: 200-209.
53. Vogel B, Shinagawa H, Hofmann U, et al. Acute DNase1 treatment improves left ventricular remodeling after myocardial infarction by disruption of free chromatin. Basic Res Cardiol 2015; 110: 15,015-0472.
54. Lewis HD, Liddle J, Coote JE, et al. Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation. Nat Chem Biol 2015; 11: 189-191.