Drug-free platelets can act as seeds for aggregate formation during antiplatelet therapy

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 10, 2015, Pages 2122-2133

  Hoefer, Thomas ^a   Armstrong, Paul C ^a   Finsterbusch, Michaela ^a   Chan, Melissa V ^a   Kirkby, Nicholas S ^b   Warner, Timothy D ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Aspirin; Flow cytometry; P2Y12 receptor; Prasugrel; Thromboxane

Indexed keywords

ABCIXIMAB; ACETYLSALICYLIC ACID; PRASUGREL; THROMBOXANE A2; ANTITHROMBOCYTIC AGENT; THROMBOXANE;

ANTICOAGULANT THERAPY; ARTICLE; CONTROLLED STUDY; DRUG FREE PLATELET; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LIGHT TRANSMISSION AGGREGOMETRY; PLATELET AGGREGATION ASSAY; PRIORITY JOURNAL; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE RICH PLASMA; COMPARATIVE STUDY; DRUG COMBINATION; DRUG EFFECTS; IN VITRO STUDY; METABOLISM; SENSITIVITY AND SPECIFICITY;

ASPIRIN; BLOOD PLATELETS; DRUG THERAPY, COMBINATION; FLOW CYTOMETRY; HUMANS; IN VITRO TECHNIQUES; PLATELET ACTIVATION; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; PRASUGREL HYDROCHLORIDE; SENSITIVITY AND SPECIFICITY; THROMBOXANES;

EID: 84942252132     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.306219     Document Type: Article

References (47)

1. Jneid H, Anderson JL, Wright RS, Adams CD, Bridges CR, Casey DE, Jr, Ettinger SM, Fesmire FM, Ganiats TG, Lincoff AM, Peterson ED, Philippides GJ, Theroux P, Wenger NK, Zidar JP. 2012 ACCF/AHA focused update of the guideline for the management of patients with unstable angina/non-ST-elevation myocardial infarction (updating the 2007 guideline and replacing the 2011 focused update): A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2012;60:645-681. doi: 10. 1016/j. jacc. 2012. 06. 004.
2. Baigent C, Blackwell L, Collins R, Emberson J, Godwin J, Peto R, Buring J, Hennekens C, Kearney P, Meade T, Patrono C, Roncaglioni MC, Zanchetti A. Aspirin in the primary and secondary prevention of vascular disease: collaborative meta-analysis of individual participant data from randomised trials. Lancet. 2009;373:1849-1860
3. Antiplatelet 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;324:71-86
4. Patrono C. Low-dose aspirin in primary prevention: cardioprotection, chemoprevention, both, or neither? Eur Heart J. 2013;34:3403-3411. doi: 10. 1093/eurheartj/eht058.
5. Harrison P, Frelinger AL 3rd, Furman MI, Michelson AD. Measuring antiplatelet drug effects in the laboratory. Thromb Res. 2007;120:323-336. doi: 10. 1016/j. Thromres. 2006. 11. 012.
6. Bonello L, Tantry US, Marcucci R, et al; Working Group on High On-Treatment Platelet Reactivity. Consensus and future directions on the definition of high on-treatment platelet reactivity to adenosine diphosphate. J Am Coll Cardiol. 2010;56:919-933. doi: 10. 1016/j. jacc. 2010. 04. 047.
7. Gurbel PA, Tantry US. Clopidogrel response variability and the advent of personalised antiplatelet therapy. A bench to bedside journey. Thromb Haemost. 2011;106:265-271. doi: 10. 1160/TH11-03-0167.
8. Pinto Slottow TL, Bonello L, Gavini R, et al. Prevalence of aspirin and clopidogrel resistance among patients with and without drug-eluting stent thrombosis. Am J Cardiol. 2009;104:525-530. doi: 10. 1016/j. Amjcard. 2009. 04. 015.
9. Undas A, Brummel-Ziedins KE, Mann KG. Antithrombotic properties of aspirin and resistance to aspirin: beyond strictly antiplatelet actions. Blood. 2007;109:2285-2292. doi: 10. 1182/blood-2006-01-010645.
10. Tantry US, Bonello L, Aradi D, et al; Working Group on On-Treatment Platelet Reactivity. Consensus and update on the definition of on-treatment platelet reactivity to adenosine diphosphate associated with ischemia and bleeding. J Am Coll Cardiol. 2013;62:2261-2273. doi: 10. 1016/j. jacc. 2013. 07. 101.
11. Patrono C, Rocca B. Drug insight: Aspirin resistance-fact or fashion? Nat Clin Pract Cardiovasc Med. 2007;4:42-50. doi: 10. 1038/ncpcardio0728.
12. Ferreiro JL, Angiolillo DJ. Diabetes and antiplatelet therapy in acute coronary syndrome. Circulation. 2011;123:798-813. doi: 10. 1161/ CIRCULATIONAHA. 109. 913376.
13. Rocca B, Santilli F, Pitocco D, et al. The recovery of platelet cyclooxygenase activity explains interindividual variability in responsiveness to lowdose aspirin in patients with and without diabetes. J Thromb Haemost. 2012;10:1220-1230. doi: 10. 1111/j. 1538-7836. 2012. 04723. x.
14. Rocca B, Dragani A, Pagliaccia F. Identifying determinants of variability to tailor aspirin therapy. Expert Rev Cardiovasc Ther. 2013;11:365-379. doi: 10. 1586/erc. 12. 144.
15. Di Minno G, Silver MJ, Murphy S. Monitoring the entry of new platelets into the circulation after ingestion of aspirin. Blood. 1983;61:1081-1085.
16. Casado-Arroyo R, Sostres C, Lanas A. Optimizing the use of aspirin for cardiovascular prevention. Drugs. 2013;73:803-814. doi: 10. 1007/ s40265-013-0061-z.
17. Daví G, Patrono C. Platelet activation and atherothrombosis. N Engl J Med. 2007;357:2482-2494. doi: 10. 1056/NEJMra071014.
18. Cattaneo M. New P2Y12 blockers. J Thromb Haemost. 2009;7 Suppl 1:262-265. doi: 10. 1111/j. 1538-7836. 2009. 03382. x.
19. Cattaneo M. The platelet P2Y? receptor for adenosine diphosphate: congenital and drug-induced defects. Blood. 2011;117:2102-2112. doi: 10. 1182/blood-2010-08-263111.
20. Floyd CN, Passacquale G, Ferro A. Comparative pharmacokinetics and pharmacodynamics of platelet adenosine diphosphate receptor antagonists and their clinical implications. Clin Pharmacokinet. 2012;51:429-442. doi: 10. 2165/11630740-000000000-00000.
21. Zimmermann N, Wenk A, Kim U, Kienzle P, Weber AA, Gams E, SchrÖr K, Hohlfeld T. Functional and biochemical evaluation of platelet aspirin resistance after coronary artery bypass surgery. Circulation. 2003;108:542-547. doi: 10. 1161/01. CIR. 0000081770. 51929. 5A.
22. DiChiara J, Bliden KP, Tantry US, Hamed MS, Antonino MJ, Suarez TA, Bailon O, Singla A, Gurbel PA. The effect of aspirin dosing on platelet function in diabetic and nondiabetic patients: An analysis from the aspirininduced platelet effect (ASPECT) study. Diabetes. 2007;56:3014-3019. doi: 10. 2337/db07-0707.
23. Paton RC. Platelet survival in diabetes mellitus using an aspirin-labelling technique. Thromb Res. 1979;15:793-802.
24. Dassin E, Najean Y, Poirier O, Passa P, Bensoussan D. In vivo platelet kinetics in 31 diabetic patients. Correlation with the degree of vascular impairment. Thromb Haemost. 1978;40:83-88.
25. Ferguson JC, Mackay N, Philip JA, Sumner DJ. Platelet and fibrinogen kinetic studies in diabetes mellitus. Br J Haematol. 1973;25:545.
26. Spectre G, Arnetz L, Östenson CG, Brismar K, Li N, Hjemdahl P. Twice daily dosing of aspirin improves platelet inhibition in whole blood in patients with type 2 diabetes mellitus and micro-or macrovascular complications. Thromb Haemost. 2011;106:491-499. doi: 10. 1160/TH11-04-0216.
27. Capodanno D, Patel A, Dharmashankar K, Ferreiro JL, Ueno M, Kodali M, Tomasello SD, Capranzano P, Seecheran N, Darlington A, Tello-Montoliu A, Desai B, Bass TA, Angiolillo DJ. Pharmacodynamic effects of different aspirin dosing regimens in type 2 diabetes mellitus patients with coronary artery disease. Circ Cardiovasc Interv. 2011;4:180-187. doi: 10. 1161/CIRCINTERVENTIONS. 110. 960187.
28. Abrahamsen AF. Platelet survival studies in man. With special reference to thrombosis and atherosclerosis. Scand J Haematol Suppl. 1968;3:1-53.
29. Htun P, Fateh-Moghadam S, Bischofs C, Banya W, Müller K, Bigalke B, Stellos K, May AE, Flather M, Gawaz M, Geisler T. Low responsiveness to clopidogrel increases risk among CKD patients undergoing coronary intervention. J Am Soc Nephrol. 2011;22:627-633. doi: 10. 1681/ ASN. 2010020220.
30. Smith JP, Haddad EV, Taylor MB, Oram D, Blakemore D, Chen Q, Boutaud O, Oates JA. Suboptimal inhibition of platelet cyclooxygenase-1 by aspirin in metabolic syndrome. Hypertension. 2012;59:719-725. doi: 10. 1161/HYPERTENSIONAHA. 111. 181404.
31. Dragani A, Pascale S, Recchiuti A, Mattoscio D, Lattanzio S, Petrucci G, Mucci L, Ferrante E, Habib A, Ranelletti FO, Ciabattoni G, Daví G, Patrono C, Rocca B. The contribution of cyclooxygenase-1 and-2 to persistent thromboxane biosynthesis in aspirin-treated essential thrombocythemia: implications for antiplatelet therapy. Blood. 2010;115:1054-1061. doi: 10. 1182/blood-2009-08-236679.
32. Pascale S, Petrucci G, Dragani A, Habib A, Zaccardi F, Pagliaccia F, Pocaterra D, Ragazzoni E, Rolandi G, Rocca B, Patrono C. Aspirininsensitive thromboxane biosynthesis in essential thrombocythemia is explained by accelerated renewal of the drug target. Blood. 2012;119:3595-3603. doi: 10. 1182/blood-2011-06-359224.
33. Guthikonda S, Lev EI, Patel R, DeLao T, Bergeron AL, Dong JF, Kleiman NS. Reticulated platelets and uninhibited COX-1 and COX-2 decrease the antiplatelet effects of aspirin. J Thromb Haemost. 2007;5:490-496. doi: 10. 1111/j. 1538-7836. 2007. 02387. x.
34. Kuijpers MJ, Megens RT, Nikookhesal E, Feijge MA, De Mey JG, oude Egbrink MG, van Giezen JJ, Heemskerk JW. Role of newly formed platelets in thrombus formation in rat after clopidogrel treatment: comparison to the reversible binding P2Y? antagonist ticagrelor. Thromb Haemost. 2011;106:1179-1188. doi: 10. 1160/TH11-04-0252.
35. Ibrahim H, Nadipalli S, DeLao T, Guthikonda S, Kleiman NS. Immature platelet fraction (IPF) determined with an automated method predicts clopidogrel hyporesponsiveness. J Thromb Thrombolysis. 2012;33:137-142. doi: 10. 1007/s11239-011-0665-7.
36. Guthikonda S, Alviar CL, Vaduganathan M, Arikan M, Tellez A, DeLao T, Granada JF, Dong JF, Kleiman NS, Lev EI. 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;52:743-749. doi: 10. 1016/j. jacc. 2008. 05. 031.
37. Cesari F, Marcucci R, Caporale R, Paniccia R, Romano E, Gensini GF, Abbate R, Gori AM. Relationship between high platelet turnover and platelet function in high-risk patients with coronary artery disease on dual antiplatelet therapy. Thromb Haemost. 2008;99:930-935. doi: 10. 1160/ TH08-01-0002.
38. Perl L, Lerman-Shivek H, Rechavia E, Vaduganathan M, Leshem-Lev D, Zemer-Wassercug N, Dadush O, Codner P, Bental T, Battler A, Kornowski R, Lev EI. Response to prasugrel and levels of circulating reticulated platelets in patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol. 2014;63:513-517. doi: 10. 1016/j. jacc. 2013. 07. 110.
39. Gurbel PA, Bliden KP, Butler K, et al. Randomized double-blind assessment of the ONSET and OFFSET of the antiplatelet effects of ticagrelor versus clopidogrel in patients with stable coronary artery disease: the ONSET/OFFSET study. Circulation. 2009;120:2577-2585. doi: 10. 1161/ CIRCULATIONAHA. 109. 912550.
40. Cattaneo M, Cerletti C, Harrison P, Hayward CP, Kenny D, Nugent D, Nurden P, Rao AK, Schmaier AH, Watson SP, Lussana F, Pugliano MT, Michelson AD. Recommendations for the standardization of light transmission aggregometry: A consensus of the working party from the platelet physiology subcommittee of ssc/isth [published online ahead of print April 10, 2013]. J Thromb Haemost. doi: 10. 1111/jth. 12231. http:// onlinelibrary. wiley. com/doi/10. 1111/jth. 12231/abstract;jsessionid=7AFD 6DDA969FA6E02BDAE10B0766A2CB. f01t02.
41. Reilly IA, FitzGerald GA. Inhibition of thromboxane formation in vivo and ex vivo: implications for therapy with platelet inhibitory drugs. Blood. 1987;69:180-186.
42. Armstrong PC, Dhanji AR, Truss NJ, Zain ZN, Tucker AT, Mitchell JA, Warner TD. Utility of 96-well plate aggregometry and measurement of thrombi adhesion to determine aspirin and clopidogrel effectiveness. Thromb Haemost. 2009;102:772-778. doi: 10. 1160/TH09-04-0215.
43. Armstrong PC, Dhanji AR, Tucker AT, Mitchell JA, Warner TD. Reduction of platelet thromboxane A2 production ex vivo and in vivo by clopidogrel therapy. J Thromb Haemost. 2010;8:613-615. doi: 10. 1111/j. 1538-7836. 2009. 03714. x.
44. Armstrong PC, Leadbeater PD, Chan MV, Kirkby NS, Jakubowski JA, Mitchell JA, Warner TD. In the presence of strong P2Y12 receptor blockade, aspirin provides little additional inhibition of platelet aggregation. J Thromb Haemost. 2011;9:552-561. doi: 10. 1111/j. 1538-7836. 2010. 04160. x.
45. Scott JP, Montgomery RR, Retzinger GS. Dimeric ristocetin flocculates proteins, binds to platelets, and mediates von Willebrand factor-dependent agglutination of platelets. J Biol Chem. 1991;266:8149-8155.
46. Rocca B, Secchiero P, Ciabattoni G, Ranelletti FO, Catani L, Guidotti L, Melloni E, Maggiano N, Zauli G, Patrono C. Cyclooxygenase-2 expression is induced during human megakaryopoiesis and characterizes newly formed platelets. Proc Natl Acad Sci U S A. 2002;99:7634-7639. doi: 10. 1073/pnas. 112202999.
47. Grove EL, Hvas AM, Mortensen SB, Larsen SB, Kristensen SD. Effect of platelet turnover on whole blood platelet aggregation in patients with coronary artery disease. J Thromb Haemost. 2011;9:185-191. doi: 10. 1111/j. 1538-7836. 2010. 04115. x.