Blood markers of coagulation, fibrinolysis, endothelial dysfunction and inflammation in lacunar stroke versus non-lacunar stroke and non-stroke: Systematic review and meta-analysis

Cerebrovascular Diseases

Volumn 37, Issue 1, 2014, Pages 64-75

  Wiseman, Stewart ^a   Marlborough, Fergal ^a   Doubal, Fergus ^a   Webb, David J ^a   Wardlaw, Joanna ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Biomarker; Endothelium; Inflammation; Lacunar stroke; Stroke

Indexed keywords

BIOLOGICAL MARKERS; BLOOD COAGULATION; BLOOD PROTEINS; BRAIN ISCHEMIA; CELL ADHESION MOLECULES; CYTOKINES; ENDOTHELIUM, VASCULAR; FIBRINOLYSIS; HOMOCYSTEINE; HUMANS; INFLAMMATION; STROKE; STROKE, LACUNAR;

C REACTIVE PROTEIN; D DIMER; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FIBRINOGEN; HOMOCYSTEINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; PADGEM PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR; SELECTIN; TISSUE PLASMINOGEN ACTIVATOR; TUMOR NECROSIS FACTOR ALPHA; VON WILLEBRAND FACTOR;

BLOOD ANALYSIS; BLOOD CLOTTING; BRAIN ISCHEMIA; CARDIOEMBOLIC STROKE; CEREBROVASCULAR DISEASE; DISEASE MARKER; ENDOTHELIAL DYSFUNCTION; FIBRINOLYSIS; HUMAN; INFLAMMATION; LACUNAR STROKE; META ANALYSIS; PRIORITY JOURNAL; PROSPECTIVE STUDY; REVIEW; SYSTEMATIC REVIEW;

EID: 84891689021     PISSN: 10159770     EISSN: 14219786     Source Type: Journal    
DOI: 10.1159/000356789     Document Type: Review

References (60)

1. Knottnerus IL, Ten Cate H, Lodder J, Kessels F, Van Oostenbrugge RJ: Endothelial dysfunction in lacunar stroke: a systematic review. Cerebrovasc Dis 2009; 27: 519-526.
2. Stevenson SF, Doubal FN, Shuler K, Wardlaw JM: A systematic review of dynamic cerebral and peripheral endothelial function in lacunar stroke versus controls. Stroke 2010; 41:e434-e442.
3. Hasan N, McColgan P, Bentley P, Edwards RJ, Sharma P: Towards the identification of blood biomarkers for acute stroke in humans: a comprehensive systematic review. Br J Clin Pharmacol 2012; 74: 230-240.
4. Moher D, Liberati A, Tetzlaff J, Altman DG: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6:e1000097.
5. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB: Meta-analysis of observational studies. JAMA 2000; 283: 2008-2012.
6. Mischak H, Allmaier G, Apweiler R, Attwood T, Baumann M, Benigni A, Bennett SE, Bischoff R, Bongcam-Rudloff E, Capasso G, Coon JJ, D?Haese P, Dominiczak AF, Dakna M, Dihazi H, et al: Recommendations for biomarker identification and qualification in clinical proteomics. Sci Transl Med 2010; 2: 46ps42.
7. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM: Reporting Recommendations for Tumour Marker Prognostic Studies (REMARK). Eur J Cancer 2005; 41: 1690-1696.
8. Von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP: The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Rev Esp Salud Publica 2007; 82: 251-259.
9. Khan U, Crossley C, Kalra L, Rudd A, Wolfe CDA, Collinson P, Markus HS: Homocysteine and its relationship to stroke subtypes in a UK black population: the south London ethnicity and stroke study. Stroke 2008; 39: 2943-2949.
10. Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O?Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, et al: Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013; 12: 822-838.
11. Eikelboom JW, Hankey GJ, Anand SS, Lofthouse E, Staples N, Baker RI: Association between high homocyst(e)ine and ischemic stroke due to large- and small-artery disease but not other etiologic subtypes of ischemic stroke. Stroke 2000; 31: 1069-1075.
12. Hassan A, Hunt BJ, O?Sullivan M, Bell R, D?Souza R, Jeffery S, Bamford JM, Markus HS: Homocysteine is a risk factor for cerebral small vessel disease, acting via endothelial dysfunction. Brain 2004; 127: 212-219.
13. Hanson E, Jood K, Karlsson S, Nilsson S, Blomstrand C, Jern C: Plasma levels of von Willebrand factor in the etiologic subtypes of ischemic stroke. J Thromb Haemost 2011; 9: 275-281.
14. Higgins J, Greens S: Cochrane Handbook for Systematic Reviews of Interventions, version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011 (available from www.cochrane- handbook.org).
15. Iso H, Moriyama Y, Sato S, Kitamura A, Tanigawa T, Yamagishi K, Imano H, Ohira T, Okamura T, Naito Y, Shimamoto T: Serum total homocysteine concentrations and risk of stroke and its subtypes in Japanese. Circulation 2004; 109: 2766-2772.
16. Ohira T, Shahar E, Chambless LE, Rosamond WD, Mosley TH, Folsom AR: Risk factors for ischemic stroke subtypes: the Atherosclerosis Risk in Communities study. Stroke 2006; 37: 2493-2498.
17. Andersson J, Johansson L, Ladenvall P, Wiklund P-G, Stegmayr B, Jern C, Boman K: C-reactive protein is a determinant of firstever stroke: prospective nested case-referent study. Cerebrovasc Dis 2009; 27: 544-551.
18. Chei C-L, Yamagishi K, Kitamura A, Kiyama M, Imano H, Ohira T, Tanigawa T, Sankai T, Ishikawa Y, Sato S, Iso H: C-reactive protein levels and risk of stroke and its subtype in Japanese: the Circulatory Risk in Communities Study (CIRCS). Atherosclerosis 2011; 217: 187-193.
19. Adams HP, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE: Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 1993; 24: 35-41.
20. Kilpatrick TJ, Matkovic Z, Davis SM, Mc- Grath CM, Dauer RJ: Hematologic abnormalities occur in both cortical and lacunar infarction. Stroke 1993; 24: 1945-1950.
21. Castellanos M, Castillo J, Garcia MM, Leira R, Serena J, Chamorro A, Davalos A: Inflammation- mediated damage in progressing lacunar infarctions: a potential therapeutic target. Stroke 2002; 33: 982-987.
22. Domac FM, Somay G, Misirli H, Erenoglu NY: Tumor necrosis factor alpha serum levels and inflammatory response in acute ischemic stroke. Neurosciences 2007; 12: 25-30.
23. Beamer NB, Coull BM, Clark WM, Hazel JS, Silberger JR: Interleukin-6 and interleukin-1 antagonist in acute stroke. Ann Neurol 1995; 37: 800-805.
24. Lindgren A, Lindoff C, Norrving B, Astedt B, Johansson BB: Tissue plasminogen activator and plasminogen activator inhibitor-1 in stroke patients. Stroke 1996; 27: 1066-1071.
25. Salobir B, Sabovic M, Peternel P, Stegnar M, Grad A: Classic risk factors, hypercoagulability and migraine in young women with cerebral lacunar infarctions. Acta Neurol Scand 2002; 105: 189-195.
26. Jood K, Ladenvall P, Tjarnlund-Wolf A, Ladenvall C, Andersson M, Nilsson S, Blomstrand C, Jern C: Fibrinolytic gene polymorphism and ischemic stroke. Stroke 2005; 36: 2077-2081.
27. Tuttolomondo A, Di Sciacca R, Di Raimondo D, Serio A, D?Aguanno G, La Placa S, Pecoraro R, Arnao V, Marino L, Monaco S, Natale E, Licata G, Pinto A: Plasma levels of inflammatory and thrombotic/fibrinolytic markers in acute ischemic strokes: relationship with TOAST subtype, outcome and infarct site. J Neuroimmunol 2009; 215: 84-89.
28. Tuttolomondo A, Pinto A, Corrao S, Di Raimondo D, Fernandez P, Di Sciacca R, Arnao V, Licata G: Immuno-inflammatory and thrombotic/fibrinolytic variables associated with acute ischemic stroke diagnosis. Atherosclerosis 2009; 203: 503-508.
29. Yokokawa H, Goto A, Terui K, Funami Y, Watanabe K, Yasumura S: Prevalence of metabolic syndrome and serum marker levels in patients with four subtypes of cerebral infarction in Japan. J Clin Neurosci 2008; 15: 769-773.
30. Ilhan D, Ozbabalik D, Gulcan E, Ozdemir O, Gulbacs Z: Evaluation of platelet activation, coagulation, and fibrinolytic activation in patients with symptomatic lacunar stroke. Neurologist 2010; 16: 188-191.
31. Bath PMW, Blann A, Smith N, Butterworth RJ: Von Willebrand factor, P-selectin and fibrinogen levels in patients with acute ischaemic and haemorrhagic stroke, and their relationship with stroke sub-type and functional outcome. Platelets 1998; 9: 155-159.
32. Kataoka S, Hirose G, Hori A, Shirakawa T, Saigan T: Activation of thrombosis and fibrinolysis following brain infarction. J Neurol Sci 2000; 181: 82-88.
33. Jood K, Danielson J, Ladenvall C, Blomstrand C, Jern C: Fibrinogen gene variation and ischemic stroke. J Thromb Haemost 2008; 6: 897-904.
34. Alvarez-Perez FJ, Castelo-Branco M, Alvarez- Sabin J: Usefulness of measurement of fibrinogen, D-dimer, D-dimer/fibrinogen ratio, Creactive protein and erythrocyte sedimentation rate to assess the pathophysiology and mechanism of ischaemic stroke. J Neurol Neurosurg Psychiatry 2011; 82: 986-992.
35. Beer C, Blacker D, Hankey GJ, Puddey IB: Association of clinical and aetiologic subtype of acute ischaemic stroke and inflammation, oxidative stress and vascular function: a crosssectional observational study. Med Sci Monit 2011; 17: 467-473.
36. Zhang B, Zhang W, Li X, Pu S, Yin J, Yang N, Yi Y, Gao Q, Gao C: Admission markers predict lacunar and non-lacunar stroke in young patients. Thromb Res 2011; 128: 14-17.
37. Takano K, Yamaguchi T, Uchida K: Markers of a hypercoagulable state following acute ischemic stroke. Stroke 1992; 23: 194-198.
38. Ageno W, Finazzi S, Steidl L, Biotti MG, Mera V, Melzi D?Eril G, Venco A: Plasma measurement of D-dimer levels for the early diagnosis of ischemic stroke subtypes. Arch Intern Med 2002; 162: 2589-2593.
39. Montaner J, Perea-Gainza M, Delgado P, Ribo M, Chacon P, Rosell A, Quintana M, Palacios ME, Molina CA, Alvarez-Sabin J: Etiologic diagnosis of ischemic stroke subtypes with plasma biomarkers. Stroke 2008; 39: 2280-2287.
40. Brouns R, Van den Bossche J, De Surgeloose D, Sheorajpanday R, De Deyn PP: Clinical and biochemical diagnosis of small-vessel disease in acute ischemic stroke. J Neurol Sci 2009; 285: 185-190.
41. Isenegger J, Meier N, Lammle B, Alberio L, Fischer U, Nedeltchev K, Gralla J, Kohler H-P, Mattle HP, Arnold M: D-dimers predict stroke subtype when assessed early. Cerebrovasc Dis 2010; 29: 82-86.
42. Parnetti L, Caso V, Santucci a A, Corea F, Lanari A, Floridi A, Conte C, Bottiglieri T: Mild hyperhomocysteinemia is a risk factor in all etiological subtypes of stroke. Neurol Sci 2004; 25: 13-17.
43. Khan U, Hassan A, Vallance P, Markus HS: Asymmetric dimethylarginine in cerebral small vessel disease. Stroke 2007; 38: 411-413.
44. Jeong S-K, Kim D-H, Cho YI: Homocysteine and pulsatility index in lacunar infarction. Clin Neurol Neurosurg 2011; 113: 459-463.
45. Pavlovic AM, Pekmezovic T, Obrenovic R, Novakovic I, Tomic G, Mijajlovic M, Sternic N: Increased total homocysteine level is associated with clinical status and severity of white matter changes in symptomatic patients with subcortical small vessel disease. Clin Neurol Neurosurg 2011; 113: 711-715.
46. Kozuka K, Kohriyama T, Nomura E, Ikeda J, Kajikawa H, Nakamura S: Endothelial markers and adhesion molecules in acute ischemic stroke - sequential change and differences in stroke subtype. Atherosclerosis 2002; 161: 161-168.
47. Licata G, Tuttolomondo A, Di Raimondo D, Corrao S, Di Sciacca R, Pinto A: Immuno-inflammatory activation in acute cardio-embolic strokes in comparison with other subtypes of ischaemic stroke. Thromb Haemost 2009: 929-937.
48. Tsai N-W, Chang W-N, Shaw C-F, Jan C-R, Chang H-W, Huang C-R, Chen S-D, Chuang Y-C, Lee L-H, Wang H-C, Lee T-H, Lu C-H: Levels and value of platelet activation markers in different subtypes of acute non-cardioembolic ischemic stroke. Thromb Res 2009; 124: 213-218.
49. Turgut B, Turgut N, Celik Y, Tekgunduz E, Pamuk GE, Demir M: Differences in plateletleukocyte aggregates among subtypes of acute cerebral ischemia. J Neurol Sci 2011; 305: 126-130.
50. Hassan A, Hunt BJ, O?Sullivan M, Parmar K, Bamford JM, Briley D, Brown MM, Thomas DJ, Markus HS: Markers of endothelial dysfunction in lacunar infarction and ischaemic leukoaraiosis. Brain 2003; 126: 424-432.
51. Supanc V, Biloglav Z, Kes VB, Demarin V: Role of cell adhesion molecules in acute ischemic stroke. Ann Saudi Med 2011; 31: 365-370.
52. Ladenvall C, Jood K, Blomstrand C, Nilsson S, Jern C, Ladenvall P: Serum C-reactive protein concentration and genotype in relation to ischemic stroke subtype. Stroke 2006; 37: 2018-2023.
53. Nakase T, Yamazaki T, Ogura N, Suzuki A, Nagata K: The impact of inflammation on the pathogenesis and prognosis of ischemic stroke. J Neurol Sci 2008; 271: 104-109.
54. Vila N, Castillo J, Davalos A, Chamorro A: Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 2000; 31: 2325-2329.
55. Salobir B, Sabovic M: Possible vascular-bedspecific role of interleukin-6 in young women with a history of myocardial infarction, lacunar cerebral infarction and deep vein thrombosis. Cytokine 2004; 25: 265-272.
56. Guldiken B, Guldiken S, Turgut B, Turgut N, Demir M, Celik Y, Arikan E, Tugrul A: The roles of oxidized low-density lipoprotein and interleukin-6 levels in acute atherothrombotic and lacunar ischemic stroke. Angiology 2008; 59: 224-229.
57. Potter GM, Marlborough FJ, Wardlaw JM: Wide variation in definition, detection, and description of lacunar lesions on imaging. Stroke 2011; 42: 359-366.
58. Jackson C, Sudlow C: Are lacunar strokes really different? A systematic review of differences in risk factor profiles between lacunar and nonlacunar infarcts. Stroke 2005; 36: 891-901.
59. Fassbender K, Rossol S, Kammer T, Daffertshofer M, Wirth S, Dollman M, Hennerici M: Proinflammatory cytokines in serum of patients with acute cerebral ischemia: kinetics of secretion and relation to the extent of brain damage and outcome of disease. J Neurol Sci 1994; 122: 135-139.
60. Ahmad O, Wardlaw J, Whiteley WN: Correlation of levels of neuronal and glial markers with radiological measures of infarct volume in ischaemic stroke: a systematic review. Cerebrovasc Dis 2012; 33: 47-54.