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Semin Thromb Hemost 2016; 42(03): 223-233
DOI: 10.1055/s-0036-1572328
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Platelets as Biomarkers of Coronary Artery Disease

Leonardo Pasalic
1   Prince of Wales Clinical School, Adult Cancer Program, University of New South Wales, Sydney, Australia
2   Haematology and Sydney Centres for Thrombosis and Haemostasis, Institute of Clinical Pathology and Medical Research, Westmead Hospital, Sydney, Australia
,
Samuel S. Y. Wang
3   ANZAC Research Institute, Concord, Sydney, Australia
,
Vivien M. Y. Chen
1   Prince of Wales Clinical School, Adult Cancer Program, University of New South Wales, Sydney, Australia
3   ANZAC Research Institute, Concord, Sydney, Australia
4   Haematology, Concord Repatriation and General Hospital, Sydney, Australia
› Author Affiliations
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Publication History

Publication Date:
29 February 2016 (online)

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Abstract

Primary and secondary prevention of cardiovascular disease remain a public health priority. Effective risk stratification of patients is a central requisite for effective preventative care and several scoring systems incorporating biomarkers have been used for prognostication in patients to guide intervention decisions. Thrombosis of atherosclerotic coronary arteries is the main mechanism behind the acute coronary syndromes and since platelets play a pivotal role in the pathogenesis of thrombosis, atherogenesis, and angiogenesis, platelet-derived biomarkers are an attractive concept. This review assesses the potential and the limitations of a range of platelet-based assays as biomarkers for coronary artery disease.

Keywords

platelets - platelet function - biomarker - cardiovascular disease
 

  • References

  • 1 Lozano R, Naghavi M, Foreman K , et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380 (9859) 2095-2128
    CrossrefPubMedGoogle Scholar
  • 2 Jackson SP. Arterial thrombosis—insidious, unpredictable and deadly. Nat Med 2011; 17 (11) 1423-1436
    CrossrefPubMedGoogle Scholar
  • 3 Montgomery JE, Brown JR. Metabolic biomarkers for predicting cardiovascular disease. Vasc Health Risk Manag 2013; 9: 37-45
    PubMedGoogle Scholar
  • 4 Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation 2005; 111 (25) 3481-3488
    CrossrefPubMedGoogle Scholar
  • 5 Versteeg HH, Heemskerk JWM, Levi M, Reitsma PH. New fundamentals in hemostasis. Physiol Rev 2013; 93 (1) 327-358
    CrossrefPubMedGoogle Scholar
  • 6 Monroe DM, Hoffman M, Roberts HR. Platelets and thrombin generation. Arterioscler Thromb Vasc Biol 2002; 22 (9) 1381-1389
    CrossrefPubMedGoogle Scholar
  • 7 Monroe DM, Hoffman M. What does it take to make the perfect clot?. Arterioscler Thromb Vasc Biol 2006; 26 (1) 41-48
    CrossrefPubMedGoogle Scholar
  • 8 Hoffman M, Monroe III DM. A cell-based model of hemostasis. Thromb Haemost 2001; 85 (6) 958-965
    PubMedGoogle Scholar
  • 9 Heemskerk JWM, Mattheij NJA, Cosemans JMEM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013; 11 (1) 2-16
    PubMedGoogle Scholar
  • 10 Kuijpers MJE, Munnix IC, Cosemans JM , et al. Key role of platelet procoagulant activity in tissue factor-and collagen-dependent thrombus formation in arterioles and venules in vivo differential sensitivity to thrombin inhibition. Microcirculation 2008; 15 (4) 269-282
    CrossrefPubMedGoogle Scholar
  • 11 Bennett JS. Platelet-fibrinogen interactions. Ann N Y Acad Sci 2001; 936: 340-354
    CrossrefPubMedGoogle Scholar
  • 12 Alshehri OM, Hughes CE, Montague S , et al. Fibrin activates GPVI in human and mouse platelets. Blood 2015; 126 (13) 1601-1608
    CrossrefPubMedGoogle Scholar
  • 13 Ferroni P, Vazzana N, Riondino S, Cuccurullo C, Guadagni F, Davì G. Platelet function in health and disease: from molecular mechanisms, redox considerations to novel therapeutic opportunities. Antioxid Redox Signal 2012; 17 (10) 1447-1485
    CrossrefPubMedGoogle Scholar
  • 14 Swieringa F, Kuijpers MJE, Heemskerk JWM, van der Meijden PEJ. Targeting platelet receptor function in thrombus formation: the risk of bleeding. Blood Rev 2014; 28 (1) 9-21
    CrossrefPubMedGoogle Scholar
  • 15 Koyama H, Maeno T, Fukumoto S , et al. Platelet P-selectin expression is associated with atherosclerotic wall thickness in carotid artery in humans. Circulation 2003; 108 (5) 524-529
    CrossrefPubMedGoogle Scholar
  • 16 Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115 (12) 3378-3384
    CrossrefPubMedGoogle Scholar
  • 17 Huo Y, Schober A, Forlow SB , et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003; 9 (1) 61-67
    CrossrefPubMedGoogle Scholar
  • 18 Davì G, Patrono C. Platelet activation and atherothrombosis. N Engl J Med 2007; 357 (24) 2482-2494
    CrossrefPubMedGoogle Scholar
  • 19 Vorchheimer DA, Becker R. Platelets in atherothrombosis. Mayo Clin Proc 2006; 81 (1) 59-68
    CrossrefPubMedGoogle Scholar
  • 20 Sharma G, Berger JS. Platelet activity and cardiovascular risk in apparently healthy individuals: a review of the data. J Thromb Thrombolysis 2011; 32 (2) 201-208
    CrossrefPubMedGoogle Scholar
  • 21 D'Agostino Sr RB, Grundy S, Sullivan LM, Wilson P ; CHD Risk Prediction Group. Validation of the Framingham coronary heart disease prediction scores: results of a multiple ethnic groups investigation. JAMA 2001; 286 (2) 180-187
    CrossrefPubMedGoogle Scholar
  • 22 Lerner DJ, Kannel WB. Patterns of coronary heart disease morbidity and mortality in the sexes: a 26-year follow-up of the Framingham population. Am Heart J 1986; 111 (2) 383-390
    CrossrefPubMedGoogle Scholar
  • 23 Wilson PW, Pencina M, Jacques P, Selhub J, D'Agostino Sr R, O'Donnell CJ. C-reactive protein and reclassification of cardiovascular risk in the Framingham Heart Study. Circ Cardiovasc Qual Outcomes 2008; 1 (2) 92-97
    CrossrefPubMedGoogle Scholar
  • 24 Akosah KO, Schaper A, Cogbill C, Schoenfeld P. Preventing myocardial infarction in the young adult in the first place: how do the National Cholesterol Education Panel III guidelines perform?. J Am Coll Cardiol 2003; 41 (9) 1475-1479
    CrossrefPubMedGoogle Scholar
  • 25 Falk E, Sillesen H, Muntendam P, Fuster V. The high-risk plaque initiative: primary prevention of atherothrombotic events in the asymptomatic population. Curr Atheroscler Rep 2011; 13 (5) 359-366
    CrossrefPubMedGoogle Scholar
  • 26 Fernández-Ortiz A, Jiménez-Borreguero LJ, Peñalvo JL , et al. The Progression and Early detection of Subclinical Atherosclerosis (PESA) study: rationale and design. Am Heart J 2013; 166 (6) 990-998
    CrossrefPubMedGoogle Scholar
  • 27 Budoff MJ, Diamond GA, Raggi P , et al. Continuous probabilistic prediction of angiographically significant coronary artery disease using electron beam tomography. Circulation 2002; 105 (15) 1791-1796
    CrossrefPubMedGoogle Scholar
  • 28 Eapen DJ, Ghasemzadeh N, MacNamara JP, Quyyumi A. The evaluation of novel biomarkers and the multiple biomarker approach in the prediction of cardiovascular disease. Curr Cardiovasc Risk Rep 2014; 8: 408-411
    CrossrefPubMedGoogle Scholar
  • 29 Aldous SJ. Cardiac biomarkers in acute myocardial infarction. Int J Cardiol 2013; 164 (3) 282-294
    CrossrefPubMedGoogle Scholar
  • 30 Liuzzo G, Biasucci LM, Gallimore JR , et al. Enhanced inflammatory response in patients with preinfarction unstable angina. J Am Coll Cardiol 1999; 34 (6) 1696-1703
    CrossrefPubMedGoogle Scholar
  • 31 Arroyo-Espliguero R, Avanzas P, Cosín-Sales J, Aldama G, Pizzi C, Kaski JC. C-reactive protein elevation and disease activity in patients with coronary artery disease. Eur Heart J 2004; 25 (5) 401-408
    CrossrefPubMedGoogle Scholar
  • 32 Kervinen H, Palosuo T, Manninen V, Tenkanen L, Vaarala O, Mänttäri M. Joint effects of C-reactive protein and other risk factors on acute coronary events. Am Heart J 2001; 141 (4) 580-585
    CrossrefPubMedGoogle Scholar
  • 33 Ridker PM. High-sensitivity C-reactive protein: potential adjunct for global risk assessment in the primary prevention of cardiovascular disease. Circulation 2001; 103 (13) 1813-1818
    CrossrefPubMedGoogle Scholar
  • 34 Koenig W, Löwel H, Baumert J, Meisinger C. C-reactive protein modulates risk prediction based on the Framingham score: implications for future risk assessment: results from a large cohort study in southern Germany. Circulation 2004; 109 (11) 1349-1353
    CrossrefPubMedGoogle Scholar
  • 35 Ridker PM, Danielson E, Fonseca FA , et al; JUPITER Study Group. Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med 2008; 359 (21) 2195-2207
    CrossrefPubMedGoogle Scholar
  • 36 Kaptoge S, Di Angelantonio E, Pennells L , et al; Emerging Risk Factors Collaboration. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med 2012; 367 (14) 1310-1320
    CrossrefPubMedGoogle Scholar
  • 37 Di Angelantonio E, Gao P, Pennells L , et al; Emerging Risk Factors Collaboration. Lipid-related markers and cardiovascular disease prediction. JAMA 2012; 307 (23) 2499-2506
    PubMedGoogle Scholar
  • 38 Looney SW, Hagan JL. Statistical methods for assessing biomarkers and analyzing biomarker data. In: Rao CR, Miller J, Rao DC, eds. Handbook of Statistics. Volume 27. Elsevier: 2007: 109-147
    Google Scholar
  • 39 Mayeux R. Biomarkers: potential uses and limitations. NeuroRx 2004; 1 (2) 182-188
    CrossrefPubMedGoogle Scholar
  • 40 Strimbu K, Tavel JA. What are biomarkers?. Curr Opin HIV AIDS 2010; 5 (6) 463-466
    CrossrefPubMedGoogle Scholar
  • 41 Hoefer IE, Sels JW, Jukema JW , et al. Circulating cells as predictors of secondary manifestations of cardiovascular disease: design of the CIRCULATING CELLS study. Clin Res Cardiol 2013; 102 (11) 847-856
    CrossrefPubMedGoogle Scholar
  • 42 Kang J-G, Patino WD, Matoba S, Hwang PM. Genomic analysis of circulating cells: a window into atherosclerosis. Trends Cardiovasc Med 2006; 16 (5) 163-168
    CrossrefPubMedGoogle Scholar
  • 43 Lindsay CR, Edelstein LC. MicroRNAs in platelet physiology and function. Semin Thromb Hemost 2016; 42 (3) 215-222
    Article in Thieme ConnectPubMedGoogle Scholar
  • 44 Wykrzykowska JJ, Garcia-Garcia HM, Goedhart D, Zalewski A, Serruys PW. Differential protein biomarker expression and their time-course in patients with a spectrum of stable and unstable coronary syndromes in the Integrated Biomarker and Imaging Study-1 (IBIS-1). Int J Cardiol 2011; 149 (1) 10-16
    CrossrefPubMedGoogle Scholar
  • 45 Bahou WF. Genetic dissection of platelet function in health and disease using systems biology. Hematol Oncol Clin North Am 2013; 27 (3) 443-463
    CrossrefPubMedGoogle Scholar
  • 46 Tchebiner JZ, Nutman A, Boursi B , et al. Diagnostic and prognostic value of thrombocytosis in admitted medical patients. Am J Med Sci 2011; 342 (5) 395-401
    CrossrefPubMedGoogle Scholar
  • 47 van der Bom JG, Heckbert SR, Lumley T , et al. Platelet count and the risk for thrombosis and death in the elderly. J Thromb Haemost 2009; 7 (3) 399-405
    CrossrefPubMedGoogle Scholar
  • 48 Gary T, Pichler M, Belaj K , et al. Platelet-to-lymphocyte ratio: a novel marker for critical limb ischemia in peripheral arterial occlusive disease patients. PLoS ONE 2013; 8 (7) e67688
    CrossrefPubMedGoogle Scholar
  • 49 Ozcan Cetin EH, Cetin MS, Aras D , et al. Platelet to lymphocyte ratio as a prognostic marker of in-hospital and long-term major adverse cardiovascular events in ST-segment elevation myocardial infarction (epub ahead of print). Angiology 2015;pii: 0003319715591751; doi: 10.1177/0003319715591751
    PubMedGoogle Scholar
  • 50 Oylumlu M, Yıldız A, Oylumlu M , et al. Platelet-to-lymphocyte ratio is a predictor of in-hospital mortality patients with acute coronary syndrome. Anatol J Cardiol 2015; 15 (4) 277-283
    CrossrefPubMedGoogle Scholar
  • 51 Kurtul A, Murat SN, Yarlioglues M , et al. Association of platelet-to-lymphocyte ratio with severity and complexity of coronary artery disease in patients with acute coronary syndromes. Am J Cardiol 2014; 114 (7) 972-978
    CrossrefPubMedGoogle Scholar
  • 52 Panova-Noeva M, Schulz A, Hermanns MI, Grossmann V, Pefani E, Spronk HMH , et al. Sex-specific differences in genetic and nongenetic determinants of mean platelet volume: results from the Gutenberg Health Study. Blood 2016; 127 (2) 251-259
    CrossrefPubMedGoogle Scholar
  • 53 Goncalves SC, Labinaz M, Le May M , et al. Usefulness of mean platelet volume as a biomarker for long-term outcomes after percutaneous coronary intervention. Am J Cardiol 2011; 107 (2) 204-209
    CrossrefPubMedGoogle Scholar
  • 54 Ju HY, Kim JK, Hur SM , et al. Could mean platelet volume be a promising biomarker of progression of chronic kidney disease?. Platelets 2015; 26 (2) 143-147
    CrossrefPubMedGoogle Scholar
  • 55 Ki YJ, Park S, Ha SI, Choi DH, Song H. Usefulness of mean platelet volume as a biomarker for long-term clinical outcomes after percutaneous coronary intervention in Korean cohort: a comparable and additive predictive value to high-sensitivity cardiac troponin T and N-terminal pro-B type natriuretic peptide. Platelets 2014; 25 (6) 427-432
    CrossrefPubMedGoogle Scholar
  • 56 Lai HM, Xu R, Yang YN , et al. Association of mean platelet volume with angiographic thrombus burden and short-term mortality in patients with ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention. Catheter Cardiovasc Interv 2015; 85 (Suppl. 01) 724-733
    CrossrefPubMedGoogle Scholar
  • 57 Khandekar MM, Khurana AS, Deshmukh SD, Kakrani AL, Katdare AD, Inamdar AK. Platelet volume indices in patients with coronary artery disease and acute myocardial infarction: an Indian scenario. J Clin Pathol 2006; 59 (2) 146-149
    CrossrefPubMedGoogle Scholar
  • 58 Guthikonda S, Lev EI, Patel R , et al. Reticulated platelets and uninhibited COX-1 and COX-2 decrease the antiplatelet effects of aspirin. J Thromb Haemost 2007; 5 (3) 490-496
    CrossrefPubMedGoogle Scholar
  • 59 Guthikonda S, Alviar CL, Vaduganathan M , et al. Role of reticulated platelets and platelet size heterogeneity on platelet activity after dual antiplatelet therapy with aspirin and clopidogrel in patients with stable coronary artery disease. J Am Coll Cardiol 2008; 52 (9) 743-749
    CrossrefPubMedGoogle Scholar
  • 60 Chu SG, Becker RC, Berger PB , et al. Mean platelet volume as a predictor of cardiovascular risk: a systematic review and meta-analysis. J Thromb Haemost 2010; 8 (1) 148-156
    CrossrefPubMedGoogle Scholar
  • 61 Tavil Y, Sen N, Yazici HU, Hizal F, Abaci A, Cengel A. Mean platelet volume in patients with metabolic syndrome and its relationship with coronary artery disease. Thromb Res 2007; 120 (2) 245-250
    CrossrefPubMedGoogle Scholar
  • 62 Kamath S, Blann AD, Lip GY. Platelet activation: assessment and quantification. Eur Heart J 2001; 22 (17) 1561-1571
    CrossrefPubMedGoogle Scholar
  • 63 Zhang Y , et al. Reticulated platelets are associated with long-term outcomes of premature coronary artery disease following percutaneous coronary intervention. Experimental and Clinical Cardiology 2014; 20: 145-163
    PubMedGoogle Scholar
  • 64 Ibrahim H, Schutt RC, Hannawi B, DeLao T, Barker CM, Kleiman NS. Association of immature platelets with adverse cardiovascular outcomes. J Am Coll Cardiol 2014; 64 (20) 2122-2129
    CrossrefPubMedGoogle Scholar
  • 65 Rinder HM, Schuster JE, Rinder CS, Wang C, Schweidler HJ, Smith BR. Correlation of thrombosis with increased platelet turnover in thrombocytosis. Blood 1998; 91 (4) 1288-1294
    PubMedGoogle Scholar
  • 66 Wiviott SD, Steg PG. Clinical evidence for oral antiplatelet therapy in acute coronary syndromes. Lancet 2015; 386 (9990) 292-302
    CrossrefPubMedGoogle Scholar
  • 67 Freynhofer MK, Bruno V, Wojta J, Huber K. The role of platelets in athero-thrombotic events. Curr Pharm Des 2012; 18 (33) 5197-5214
    CrossrefPubMedGoogle Scholar
  • 68 Eikelboom JW, Hirsh J, Spencer FA, Baglin TP, Weitz JI. Antiplatelet drugs: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2012; 141 (2, Suppl): e89S-e119S
    CrossrefPubMedGoogle Scholar
  • 69 Osnabrugge RL, Head SJ, Zijlstra F , et al. A systematic review and critical assessment of 11 discordant meta-analyses on reduced-function CYP2C19 genotype and risk of adverse clinical outcomes in clopidogrel users. Genet Med 2015; 17 (1) 3-11
    CrossrefPubMedGoogle Scholar
  • 70 Patrono C, García Rodríguez LA, Landolfi R, Baigent C. Low-dose aspirin for the prevention of atherothrombosis. N Engl J Med 2005; 353 (22) 2373-2383
    CrossrefPubMedGoogle Scholar
  • 71 Antithrombotic Trialists' Collaboration. Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. BMJ 2002; 324 (7329) 71-86
    CrossrefPubMedGoogle Scholar
  • 72 Thrombosis prevention trial: randomised trial of low-intensity oral anticoagulation with warfarin and low-dose aspirin in the primary prevention of ischaemic heart disease in men at increased risk. The Medical Research Council's General Practice Research Framework. Lancet 1998; 351 (9098) 233-241
    CrossrefPubMedGoogle Scholar
  • 73 Mangiacapra F, Barbato E, Patti G , et al. Point-of-care assessment of platelet reactivity after clopidogrel to predict myonecrosis in patients undergoing percutaneous coronary intervention. JACC Cardiovasc Interv 2010; 3 (3) 318-323
    CrossrefPubMedGoogle Scholar
  • 74 Zhao XY, Wang XF, Zhang JY, Du YY, Yang HB. Effect of the composition of atherosclerotic plaques and rate of platelet aggregation on elevation of serum levels of cardiac troponin T after percutaneous coronary interventions. J Interv Cardiol 2012; 25 (5) 433-438
    CrossrefPubMedGoogle Scholar
  • 75 Zhang HZ, Kim MH, Jeong YH. Predictive values of post-clopidogrel platelet reactivity assessed by different platelet function tests on ischemic events in East Asian patients treated with PCI. Platelets 2014; 25 (4) 292-299
    CrossrefPubMedGoogle Scholar
  • 76 Patti G, Mangiacapra F, Ricottini E , et al. Correlation of platelet reactivity and C-reactive protein levels to occurrence of peri-procedural myocardial infarction in patients undergoing percutaneous coronary intervention (from the ARMYDA-CRP study). Am J Cardiol 2013; 111 (12) 1739-1744
    CrossrefPubMedGoogle Scholar
  • 77 Mangiacapra F, Bartunek J, Bijnens N , et al. Periprocedural variations of platelet reactivity during elective percutaneous coronary intervention. J Thromb Haemost 2012; 10 (12) 2452-2461
    CrossrefPubMedGoogle Scholar
  • 78 Park DW, Ahn JM, Song HG , et al. Differential prognostic impact of high on-treatment platelet reactivity among patients with acute coronary syndromes versus stable coronary artery disease undergoing percutaneous coronary intervention. Am Heart J 2013; 165 (1) 34-42.e1
    CrossrefPubMedGoogle Scholar
  • 79 Mangiacapra F, Peace A, Barbato E , et al. Thresholds for platelet reactivity to predict clinical events after coronary intervention are different in patients with and without diabetes mellitus. Platelets 2014; 25 (5) 348-356
    CrossrefPubMedGoogle Scholar
  • 80 Mehta SR, Bassand JP, Chrolavicius S , et al; CURRENT-OASIS 7 Investigators. Dose comparisons of clopidogrel and aspirin in acute coronary syndromes. N Engl J Med 2010; 363 (10) 930-942
    CrossrefPubMedGoogle Scholar
  • 81 Kim C, Ye F, Ginsberg MH. Regulation of integrin activation. Annu Rev Cell Dev Biol 2011; 27: 321-345
    CrossrefPubMedGoogle Scholar
  • 82 Kasirer-Friede A, Kahn ML, Shattil SJ. Platelet integrins and immunoreceptors. Immunol Rev 2007; 218: 247-264
    CrossrefPubMedGoogle Scholar
  • 83 Berny-Lang MA, Frelinger III AL, Barnard MR, Michelson AD, In: Michelson AD. ed. Platelets. 3rd ed. London: Academic Press; 2013: 581-602
    CrossrefGoogle Scholar
  • 84 McEver RP, Cummings RD. Perspectives series: cell adhesion in vascular biology. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 1997; 100 (3) 485-491
    CrossrefPubMedGoogle Scholar
  • 85 Varki A. Selectin ligands: will the real ones please stand up?. J Clin Invest 1997; 100 (11, Suppl): S31-S35
    PubMedGoogle Scholar
  • 86 Yang J, Furie BC, Furie B. The biology of P-selectin glycoprotein ligand-1: its role as a selectin counterreceptor in leukocyte-endothelial and leukocyte-platelet interaction. Thromb Haemost 1999; 81 (1) 1-7
    PubMedGoogle Scholar
  • 87 Evangelista V, Smyth SS. Platelets. 3rd ed. In: Michelson AD, ed. London: Academic Press; 2013: 295-312
    CrossrefGoogle Scholar
  • 88 Massaguer A, Engel P, Pérez-del-Pulgar S, Bosch J, Pizcueta P. Production and characterization of monoclonal antibodies against conserved epitopes of P-selectin (CD62P). Tissue Antigens 2000; 56 (2) 117-128
    CrossrefPubMedGoogle Scholar
  • 89 Ramström S, Södergren AL, Tynngård N, Lindahl TL. Platelet function determined by flow cytometry: new perspectives?. Semin Thromb Hemost 2016; 42 (3) 268-281
    Article in Thieme ConnectPubMedGoogle Scholar
  • 90 Klinkhardt U, Harder S. Flow cytometric measurement of platelet-leukocyte aggregates: a possible target to monitor platelet function?. Semin Thromb Hemost 2005; 31 (4) 400-403
    Article in Thieme ConnectPubMedGoogle Scholar
  • 91 Granja T, Schad J, Schüssel P , et al. Using six-colour flow cytometry to analyse the activation and interaction of platelets and leukocytes—A new assay suitable for bench and bedside conditions. Thromb Res 2015; 136 (4) 786-796
    CrossrefPubMedGoogle Scholar
  • 92 Barnard MR, Krueger LA, Frelinger AL, Furman MI, Michelson AD. Whole blood analysis of leukocyte-platelet aggregates. Current protocols in cytometry 2003; 24 6.15:6.15.1–6.15.8; DOI: 10.1002/0471142956.cy0615s24
    PubMedGoogle Scholar
  • 93 Xu XX, Gao XH, Pan R, Lu D, Dai Y. A simple adhesion assay for studying interactions between platelets and endothelial cells in vitro. Cytotechnology 2010; 62 (1) 17-22
    CrossrefPubMedGoogle Scholar
  • 94 Tantry US, Bliden KP, Suarez TA, Kreutz RP, Dichiara J, Gurbel PA. Hypercoagulability, platelet function, inflammation and coronary artery disease acuity: results of the Thrombotic RIsk Progression (TRIP) study. Platelets 2010; 21 (5) 360-367
    CrossrefPubMedGoogle Scholar
  • 95 Schultheiss HP, Tschoepe D, Esser J , et al. Large platelets continue to circulate in an activated state after myocardial infarction. Eur J Clin Invest 1994; 24 (4) 243-247
    CrossrefPubMedGoogle Scholar
  • 96 Yip H-K, Chang LT, Sun CK , et al. Platelet activity is a biomarker of cardiac necrosis and predictive of untoward clinical outcomes in patients with acute myocardial infarction undergoing primary coronary stenting. Circ J 2006; 70 (1) 31-36
    CrossrefPubMedGoogle Scholar
  • 97 Coulter SA, Cannon CP, Ault KA , et al. High levels of platelet inhibition with abciximab despite heightened platelet activation and aggregation during thrombolysis for acute myocardial infarction: results from TIMI (thrombolysis in myocardial infarction) 14. Circulation 2000; 101 (23) 2690-2695
    CrossrefPubMedGoogle Scholar
  • 98 Furman MI, Benoit SE, Barnard MR , et al. Increased platelet reactivity and circulating monocyte-platelet aggregates in patients with stable coronary artery disease. J Am Coll Cardiol 1998; 31 (2) 352-358
    CrossrefPubMedGoogle Scholar
  • 99 Kappelmayer J, Nagy Jr B, Miszti-Blasius K, Hevessy Z, Setiadi H. The emerging value of P-selectin as a disease marker. Clin Chem Lab Med 2004; 42 (5) 475-486
    PubMedGoogle Scholar
  • 100 Tschoepe D, Schultheiss HP, Kolarov P , et al. Platelet membrane activation markers are predictive for increased risk of acute ischemic events after PTCA. Circulation 1993; 88 (1) 37-42
    CrossrefPubMedGoogle Scholar
  • 101 Gawaz M, Neumann FJ, Ott I, May A, Rüdiger S, Schömig A. Role of activation-dependent platelet membrane glycoproteins in development of subacute occlusive coronary stent thrombosis. Coron Artery Dis 1997; 8 (3–4) 121-128
    CrossrefPubMedGoogle Scholar
  • 102 Kabbani SS, Watkins MW, Ashikaga T , et al. Platelet reactivity characterized prospectively: a determinant of outcome 90 days after percutaneous coronary intervention. Circulation 2001; 104 (2) 181-186
    CrossrefPubMedGoogle Scholar
  • 103 Kabbani SS, Watkins MW, Ashikaga T, Terrien EF, Sobel BE, Schneider DJ. Usefulness of platelet reactivity before percutaneous coronary intervention in determining cardiac risk one year later. Am J Cardiol 2003; 91 (7) 876-878
    CrossrefPubMedGoogle Scholar
  • 104 Ault KA, Cannon CP, Mitchell J , et al. Platelet activation in patients after an acute coronary syndrome: results from the TIMI-12 trial. Thrombolysis in myocardial infarction. J Am Coll Cardiol 1999; 33 (3) 634-639
    CrossrefPubMedGoogle Scholar
  • 105 Frelinger III AL, Michelson AD, Wiviott SD , et al. Intrinsic platelet reactivity before P2Y12 blockade contributes to residual platelet reactivity despite high-level P2Y12 blockade by prasugrel or high-dose clopidogrel. Results from PRINCIPLE-TIMI 44. Thromb Haemost 2011; 106 (2) 219-226
    Article in Thieme ConnectPubMedGoogle Scholar
  • 106 Gawaz M, Neumann FJ, Ott I, May A, Schömig A. Platelet activation and coronary stent implantation. Effect of antithrombotic therapy. Circulation 1996; 94 (3) 279-285
    CrossrefPubMedGoogle Scholar
  • 107 Neumann FJ, Gawaz M, Dickfeld T , et al. Antiplatelet effect of ticlopidine after coronary stenting. J Am Coll Cardiol 1997; 29 (7) 1515-1519
    CrossrefPubMedGoogle Scholar
  • 108 Floyd CN, Goodman T, Becker S , et al. Increased platelet expression of glycoprotein IIIa following aspirin treatment in aspirin-resistant but not aspirin-sensitive subjects. Br J Clin Pharmacol 2014; 78 (2) 320-328
    CrossrefPubMedGoogle Scholar
  • 109 Trip MD, Cats VM, van Capelle FJ, Vreeken J. Platelet hyperreactivity and prognosis in survivors of myocardial infarction. N Engl J Med 1990; 322 (22) 1549-1554
    CrossrefPubMedGoogle Scholar
  • 110 Vanschoonbeek K, Feijge MA, Keuren JF , et al. Thrombin-induced hyperactivity of platelets of young stroke patients: involvement of thrombin receptors in the subject-dependent variability in Ca2+ signal generation. Thromb Haemost 2002; 88 (6) 931-937
    PubMedGoogle Scholar
  • 111 Konstantopoulos K, Grotta JC, Sills C, Wu KK, Hellums JD. Shear-induced platelet aggregation in normal subjects and stroke patients. Thromb Haemost 1995; 74 (5) 1329-1334
    PubMedGoogle Scholar
  • 112 Yee DL, Sun CW, Bergeron AL, Dong JF, Bray PF. Aggregometry detects platelet hyperreactivity in healthy individuals. Blood 2005; 106 (8) 2723-2729
    CrossrefPubMedGoogle Scholar
  • 113 Qayyum R, Becker DM, Yanek LR , et al. Greater collagen-induced platelet aggregation following cyclooxygenase 1 inhibition predicts incident acute coronary syndromes. Clin Transl Sci 2015; 8 (1) 17-22
    CrossrefPubMedGoogle Scholar
  • 114 McBane II RD, Karnicki K, Tahirkheli N, Miller RS, Owen WG. Platelet characteristics associated with coronary artery disease. J Thromb Haemost 2003; 1 (6) 1296-1303
    CrossrefPubMedGoogle Scholar
  • 115 Chung AWY, Radomski A, Alonso-Escolano D , et al. Platelet-leukocyte aggregation induced by PAR agonists: regulation by nitric oxide and matrix metalloproteinases. Br J Pharmacol 2004; 143 (7) 845-855
    CrossrefPubMedGoogle Scholar
  • 116 von Brühl M-L, Stark K, Steinhart A , et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209 (4) 819-835
    CrossrefPubMedGoogle Scholar
  • 117 Yokoyama S, Ikeda H, Haramaki N, Yasukawa H, Murohara T, Imaizumi T. Platelet P-selectin plays an important role in arterial thrombogenesis by forming large stable platelet-leukocyte aggregates. J Am Coll Cardiol 2005; 45 (8) 1280-1286
    CrossrefPubMedGoogle Scholar
  • 118 Zhang X, Zhan D, Shin HY. Integrin subtype-dependent CD18 cleavage under shear and its influence on leukocyte-platelet binding. J Leukoc Biol 2013; 93 (2) 251-258
    CrossrefPubMedGoogle Scholar
  • 119 Zeller JA, Lenz A, Eschenfelder CC, Zunker P, Deuschl G. Platelet-leukocyte interaction and platelet activation in acute stroke with and without preceding infection. Arterioscler Thromb Vasc Biol 2005; 25 (7) 1519-1523
    CrossrefPubMedGoogle Scholar
  • 120 Naruko T, Ueda M, Haze K , et al. Neutrophil infiltration of culprit lesions in acute coronary syndromes. Circulation 2002; 106 (23) 2894-2900
    CrossrefPubMedGoogle Scholar
  • 121 Di Serafino L, Sarma J, Dierickx K , et al. Monocyte-platelets aggregates as cellular biomarker of endothelium-dependent coronary vasomotor dysfunction in patients with coronary artery disease. J Cardiovasc Transl Res 2014; 7 (1) 1-8
    CrossrefPubMedGoogle Scholar
  • 122 Rutten B, Tersteeg C, Vrijenhoek JE , et al. Increased platelet reactivity is associated with circulating platelet-monocyte complexes and macrophages in human atherosclerotic plaques. PLoS ONE 2014; 9 (8) e105019
    CrossrefPubMedGoogle Scholar
  • 123 Michelson AD, Barnard MR, Krueger LA, Valeri CR, Furman MI. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001; 104 (13) 1533-1537
    CrossrefPubMedGoogle Scholar
  • 124 Hua VM, Abeynaike L, Glaros E , et al. Necrotic platelets provide a procoagulant surface during thrombosis. Blood 2015; 126 (26) 2852-2862
    CrossrefPubMedGoogle Scholar
  • 125 Hua VM, Chen VMY. Procoagulant platelets and the pathways leading to cell death. Semin Thromb Hemost 2015; 41 (4) 405-412
    Article in Thieme ConnectPubMedGoogle Scholar
  • 126 Prodan CI, Stoner JA, Cowan LD, Dale GL. Higher coated-platelet levels are associated with stroke recurrence following nonlacunar brain infarction. J Cereb Blood Flow Metab 2013; 33 (2) 287-292
    CrossrefPubMedGoogle Scholar
  • 127 Kirkpatrick AC, Tafur AJ, Vincent AS, Dale GL, Prodan CI. Coated-platelets improve prediction of stroke and transient ischemic attack in asymptomatic internal carotid artery stenosis. Stroke 2014; 45 (10) 2995-3001
    CrossrefPubMedGoogle Scholar
  • 128 Rechner AR. Platelet function testing in clinical diagnostics. Hamostaseologie 2011; 31 (2) 79-87
    PubMedGoogle Scholar
  • 129 Gorog DA, Fuster V. Platelet function tests in clinical cardiology: unfulfilled expectations. J Am Coll Cardiol 2013; 61 (21) 2115-2129
    CrossrefPubMedGoogle Scholar
  • 130 E. Kehrel B, F. Brodde M. State of the art in platelet function testing. Transfus Med Hemother 2013; 40 (2) 73-86
    CrossrefPubMedGoogle Scholar
  • 131 Paniccia R, Priora R, Liotta AA, Abbate R. Platelet function tests: a comparative review. Vasc Health Risk Manag 2015; 11: 133-148
    PubMedGoogle Scholar
  • 132 Ghasemzadeh M, Hosseini E. Platelet-leukocyte crosstalk: Linking proinflammatory responses to procoagulant state. Thromb Res 2013; 131 (3) 191-197
    CrossrefPubMedGoogle Scholar