Genetic determinants of platelet reactivity during acetylsalicylic acid therapy in diabetic patients: Evaluation of 27 polymorphisms within candidate genes

Journal of Thrombosis and Haemostasis

Volumn 9, Issue 11, 2011, Pages 2291-2301

  Postula, M ^a   Kaplon Cieslicka, A ^a   Rosiak, M ^a   Kondracka, A ^a   Serafin, A ^a   Filipiak, K J ^a   Czlonkowski, A ^a   Opolski, G ^a   Janicki, P K ^b  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Acetylsalicylic acid; Diabetes mellitus; Genetic polymorphism; Platelet function testing; Platelet reactivity

Indexed keywords

ACETYLSALICYLIC ACID;

ADULT; AGED; ARTICLE; CAUCASIAN; FEMALE; GENOTYPE; HEART INFARCTION; HUMAN; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEOTIDE SEQUENCE; PLATELET REACTIVITY; PRIMARY PREVENTION; PRIORITY JOURNAL; SECONDARY PREVENTION; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOCYTE;

AGED; ASPIRIN; BLOOD PLATELETS; DIABETES MELLITUS; FEMALE; GENOTYPE; HUMANS; MALE; MIDDLE AGED; MUTANT PROTEINS; PLATELET ACTIVATION; PLATELET AGGREGATION INHIBITORS; PLATELET FUNCTION TESTS; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 80055116248     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2011.04482.x     Document Type: Article

References (63)

1. Yazbek N, Bapat A, Kleiman N. Platelet abnormalities in diabetes mellitus. Coron Artery Dis 2003; 14: 365-71.
2. Natarajan A, Zaman AG, Marshall SM. Platelet hyperactivity in type 2 diabetes: role of antiplatelet agents. Diab Vasc Dis Res 2008; 5: 138-44.
3. Ferroni P, Basili S, Falco A, Davi G. Platelet activation in type 2 diabetes mellitus. J Thromb Haemost 2004; 2: 1282-91.
4. 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 (Clinical research ed.) 2002; 324: 71-86.
5. 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 aspirin-induced platelet effect (ASPECT) study. Diabetes 2007; 56: 3014-9.
6. Evangelista V, De Berardis G, Totani L, Avanzini F, Giorda CB, Brero L, Levantesi G, Marelli G, Pupillo M, Iacuitti G, Pozzoli G, di Summa P, Nada E, de Simone G, Dell'Elba G, Amore C, Manarini S, Pecce R, Maione A, Tognoni G et al. Persistent platelet activation in patients with type 2 diabetes treated with low doses of aspirin. J Thromb Haemost 2007; 5: 2197-203.
7. Mortensen SB, Larsen SB, Grove EL, Kristensen SD, Hvas AM. Reduced platelet response to aspirin in patients with coronary artery disease and type 2 diabetes mellitus. Thromb Res 2010; 126: 318-22.
8. Feher G, Feher A, Pusch G, Lupkovics G, Szapary L, Papp E. The genetics of antiplatelet drug resistance. Clin Genet 2009; 75: 1-18.
9. Halushka MK, Walker LP, Halushka PV. Genetic variation in cyclooxygenase 1: effects on response to aspirin. Clin Pharmacol Ther 2003; 73: 122-30.
10. Maree AO, Curtin RJ, Chubb A, Dolan C, Cox D, O'Brien J, Crean P, Shields DC, Fitzgerald DJ. Cyclooxygenase-1 haplotype modulates platelet response to aspirin. J Thromb Haemost 2005; 3: 2340-5.
11. Lee CR, North KE, Bray MS, Couper DJ, Heiss G, Zeldin DC. Cyclooxygenase polymorphisms and risk of cardiovascular events: the Atherosclerosis Risk in Communities (ARIC) study. Clin Pharmacol Ther 2008; 83: 52-60.
12. Kunicki TJ, Williams SA, Salomon DR, Harrison P, Crisler P, Nakagawa P, Mondala TS, Head SR, Nugent DJ. Genetics of platelet reactivity in normal, healthy individuals. J Thromb Haemost 2009; 7: 2116-22.
13. Kunicki TJ, Williams SA, Nugent DJ, Harrison P, Segal HC, Syed A, Rothwell PM. Lack of association between aspirin responsiveness and seven candidate gene haplotypes in patients with symptomatic vascular disease. Thromb Haemost 2009; 101: 123-33.
14. Lepantalo A, Mikkelsson J, Resendiz JC, Viiri L, Backman JT, Kankuri E, Karhunen PJ, Lassila R. Polymorphisms of COX-1 and GPVI associate with the antiplatelet effect of aspirin in coronary artery disease patients. Thromb Haemost 2006; 95: 253-9.
15. Musunuru K, Post WS, Herzog W, Shen H, O'Connell JR, McArdle PF, Ryan KA, Gibson Q, Cheng YC, Clearfield E, Johnson AD, Tofler G, Yang Q, O'Donnell CJ, Becker DM, Yanek LR, Becker LC, Faraday N, Bielak LF, Peyser PA et al. Association of single nucleotide polymorphisms on chromosome 9p21.3 with platelet reactivity: a potential mechanism for increased vascular disease. Circulation 2010; 3: 445-53.
16. Ozdener F, Gulbas Z, Erol K, Ozdemir V. 5-Hydroxytryptamine-2A receptor gene (HTR 2 A) candidate polymorphism (T 102 C): Role for human platelet function under pharmacological challenge ex vivo. Methods Find Exp Clin Pharmacol 2005; 27: 395-400.
17. Yabe M, Matsubara Y, Takahashi S, Ishihara H, Shibano T, Miyaki K, Omae K, Watanabe G, Murata M, Ikeda Y. Identification of ADRA2A polymorphisms related to shear-mediated platelet function. Biochem Biophys Res Commun 2006; 347: 1001-5.
18. Bierend A, Rau T, Maas R, Schwedhelm E, Boger RH. P2Y12 polymorphisms and antiplatelet effects of aspirin in patients with coronary artery disease. Br J Clin Pharmacol 2008; 65: 540-7.
19. Cuisset T, Hamilos M, Delrue M, Frere C, Verhamme K, Bartunek J, Saut N, Bonnet JL, Eijgelsheim M, Wijns W, Alessi MC, Barbato E. Adrenergic receptor polymorphisms and platelet reactivity after treatment with dual antiplatelet therapy with aspirin and clopidogrel in acute coronary syndrome. Thromb Haemost 2010; 103: 774-9.
20. Fontana P, Dupont A, Gandrille S, Bachelot-Loza C, Reny JL, Aiach M, Gaussem P. Adenosine diphosphate-induced platelet aggregation is associated with P2Y12 gene sequence variations in healthy subjects. Circulation 2003; 108: 989-95.
21. Fontana P, Gandrille S, Remones V, Dupont A, Reny JL, Aiach M, Gaussem P. Identification of functional polymorphisms of the thromboxane A2 receptor gene in healthy volunteers. Thromb Haemost 2006; 96: 356-60.
22. Fontana P, Gaussem P, Aiach M, Fiessinger JN, Emmerich J, Reny JL. P2Y12 H2 haplotype is associated with peripheral arterial disease: a case-control study. Circulation 2003; 108: 2971-3.
23. Johnson AD, Yanek LR, Chen MH, Faraday N, Larson MG, Tofler G, Lin SJ, Kraja AT, Province MA, Yang Q, Becker DM, O'Donnell CJ, Becker LC. Genome-wide meta-analyses identifies seven loci associated with platelet aggregation in response to agonists. Nat Genet 2010; 42: 608-13.
24. Godeneche G, Sorel N, Ragot S, Chomel JC, Neau JP, Macchi L. Stroke and aspirin non-responder patients: relation with hypertension and platelet response to adenosine diphosphate. Platelets 2009; 20: 471-7.
25. Jones CI, Bray S, Garner SF, Stephens J, de Bono B, Angenent WG, Bentley D, Burns P, Coffey A, Deloukas P, Earthrowl M, Farndale RW, Hoylaerts MF, Koch K, Rankin A, Rice CM, Rogers J, Samani NJ, Steward M, Walker A et al. A functional genomics approach reveals novel quantitative trait loci associated with platelet signaling pathways. Blood 2009; 114: 1405-16.
26. Hetherington SL, Singh RK, Lodwick D, Thompson JR, Goodall AH, Samani NJ. Dimorphism in the P2Y1 ADP receptor gene is associated with increased platelet activation response to ADP. Arterioscler Thromb Vasc Biol 2005; 25: 252-7.
27. Soranzo N, Rendon A, Gieger C, Jones CI, Watkins NA, Menzel S, Doring A, Stephens J, Prokisch H, Erber W, Potter SC, Bray SL, Burns P, Jolley J, Falchi M, Kuhnel B, Erdmann J, Schunkert H, Samani NJ, Illig T et al. A novel variant on chromosome 7q22.3 associated with mean platelet volume, counts, and function. Blood 2009; 113: 3831-7.
28. Joutsi-Korhonen L, Smethurst PA, Rankin A, Gray E, M IJ, Onley CM, Watkins NA, Williamson LM, Goodall AH, de GrootPG, Farndale RW, Ouwehand WH. The low-frequency allele of the platelet collagen signaling receptor glycoprotein VI is associated with reduced functional responses and expression. Blood 2003; 101: 4372-9.
29. Lemaitre RN, Rice K, Marciante K, Bis JC, Lumley TS, Wiggins KL, Smith NL, Heckbert SR, Psaty BM. Variation in eicosanoid genes, non-fatal myocardial infarction and ischemic stroke. Atherosclerosis 2009; 204: e58-63.
30. Motovska Z, Kvasnicka J, Widimsky P, Petr R, Hajkova J, Bobcikova P, Osmancik P, Odvodyova D, Katina S. Platelet glycoprotein GP VI 13254C allele is an independent risk factor of premature myocardial infarction. Thromb Res 2010; 125: e61-4.
31. Kunicki TJ, Nugent DJ. The genetics of normal platelet reactivity. Blood 2010; 116: 2627-34.
32. Nielsen HL, Kristensen SD, Thygesen SS, Mortensen J, Pedersen SB, Grove EL, Hvas AM. Aspirin response evaluated by the VerifyNow Aspirin System and light transmission aggregometry. Thromb Res 2008; 123: 267-73.
33. Gurbel PA, Bliden KP, DiChiara J, Newcomer J, Weng W, Neerchal NK, Gesheff T, Chaganti SK, Etherington A, Tantry US. Evaluation of dose-related effects of aspirin on platelet function: results from the Aspirin-Induced Platelet Effect (ASPECT) study. Circulation 2007; 115: 3156-64.
34. Sestito A, Sciahbasi A, Landolfi R, Maseri A, Lanza GA, Andreotti F. A simple assay for platelet-mediated hemostasis in flowing whole blood (PFA-100): reproducibility and effects of sex and age. Cardiologia 1999; 44: 661-5.
35. Chakroun T, Addad F, Abderazek F, Ben-Farhat M, Hamdi S, Gamra H, Hassine M, Ben-Hamda K, Samama MM, Elalamy I. Screening for aspirin resistance in stable coronary artery patients by three different tests. Thromb Res 2007; 121: 413-8.
36. Crescente M, Di Castelnuovo A, Iacoviello L, Vermylen J, Cerletti C, de Gaetano G. Response variability to aspirin as assessed by the platelet function analyzer (PFA)-100. A systematic review. Thromb Haemost 2008; 99: 14-26.
37. Gonzalez-Conejero R, Rivera J, Corral J, Acuna C, Guerrero JA, Vicente V. Biological assessment of aspirin efficacy on healthy individuals: heterogeneous response or aspirin failure? Stroke; a journal of cerebral circulation 2005; 36: 276-80.
38. Reny JL, de Moerloose P, Dauzat M, Fontana P. Use of the PFA-100 closure time to predict cardiovascular events in aspirin-treated cardiovascular patients: a systematic review and meta-analysis. J Thromb Haemost 2008; 6: 444-50.
39. Hovens MM, Snoep JD, Eikenboom JC, van der Bom JG, Mertens BJ, Huisman MV. Prevalence of persistent platelet reactivity despite use of aspirin: a systematic review. Am Heart J 2007; 153: 175-81.
40. Dupont W, Plummer WD. PS power and sample size program available for free on the Internet. Control Clin Trials 1997; 18: 274.
41. Nadkarni NV, Zhao Y, Kosorok MR. Inverse regression estimation for censored data. J Am Stat Assoc 2011; 106: 178-90.
42. Manly KF, Nettleton D, Hwang JT. Genomics, prior probability, and statistical tests of multiple hypotheses. Genome Res 2004; 14: 997-1001.
43. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995; 57: 289-300.
44. Grove EL, Hvas AM, Johnsen HL, Hedegaard SS, Pedersen SB, Mortensen J, Kristensen SD. A comparison of platelet function tests and thromboxane metabolites to evaluate aspirin response in healthy individuals and patients with coronary artery disease. Thromb Haemost 2010; 103: 1245-53.
45. Henry P, Vermillet A, Boval B, Guyetand C, Petroni T, Dillinger JG, Sideris G, Sollier CB, Drouet L. 24-hour time-dependent aspirin efficacy in patients with stable coronary artery disease. Thromb Haemost 2010; 105: 336-44.
46. Santilli F, Rocca B, De Cristofaro R, Lattanzio S, Pietrangelo L, Habib A, Pettinella C, Recchiuti A, Ferrante E, Ciabattoni G, Davi G, Patrono C. Platelet cyclooxygenase inhibition by low-dose aspirin is not reflected consistently by platelet function assays: implications for aspirin "resistance". J Am Coll Cardiol 2009; 53: 667-77.
47. Patrono C, Baigent C, Hirsh J, Roth G. Antiplatelet drugs: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 2008; 133: 199S-233S.
48. Lordkipanidze M, Pharand C, Schampaert E, Turgeon J, Palisaitis DA, Diodati JG. A comparison of six major platelet function tests to determine the prevalence of aspirin resistance in patients with stable coronary artery disease. Eur Heart J 2007; 28: 1702-8.
49. Schunkert H, Gotz A, Braund P, McGinnis R, Tregouet DA, Mangino M, Linsel-Nitschke P, Cambien F, Hengstenberg C, Stark K, Blankenberg S, Tiret L, Ducimetiere P, Keniry A, Ghori MJ, Schreiber S, El Mokhtari NE, Hall AS, Dixon RJ, Goodall AH et al. Repeated replication and a prospective meta-analysis of the association between chromosome 9p21.3 and coronary artery disease. Circulation 2008; 117: 1675-84.
50. Samani NJ, Erdmann J, Hall AS, Hengstenberg C, Mangino M, Mayer B, Dixon RJ, Meitinger T, Braund P, Wichmann HE, Barrett JH, Konig IR, Stevens SE, Szymczak S, Tregouet DA, Iles MM, Pahlke F, Pollard H, Lieb W, Cambien F et al. Genomewide association analysis of coronary artery disease. N Eng J Med 2007; 357: 443-53.
51. Matarin M, Brown WM, Singleton A, Hardy JA, Meschia JF. Whole genome analyses suggest ischemic stroke and heart disease share an association with polymorphisms on chromosome 9p21. Stroke; a journal of cerebral circulation 2008; 39: 1586-9.
52. Helgadottir A, Thorleifsson G, Manolescu A, Gretarsdottir S, Blondal T, Jonasdottir A, Jonasdottir A, Sigurdsson A, Baker A, Palsson A, Masson G, Gudbjartsson DF, Magnusson KP, Andersen K, Levey AI, Backman VM, Matthiasdottir S, Jonsdottir T, Palsson S, Einarsdottir H et al. A common variant on chromosome 9p21 affects the risk of myocardial infarction. Science (New York, NY) 2007; 316: 1491-3.
53. Fujiwara T, Ikeda M, Esumi K, Fujita TD, Kono M, Tokushige H, Hatoyama T, Maeda T, Asai T, Ogawa T, Katsumata T, Sasaki S, Suzuki E, Suzuki M, Hino F, Fujita TK, Zaima H, Shimada M, Sugawara T, Tsuzuki Y et al. Exploratory aspirin resistance trial in healthy Japanese volunteers (J-ART) using platelet aggregation as a measure of thrombogenicity. Pharmacogenomics J 2007; 7: 395-403.
54. Karabina SA, Ninio E. Plasma PAF-acetylhydrolase: an unfulfilled promise? Biochim Biophys Acta 2006; 1761: 1351-8.
55. Wang Q, Hao Y, Mo X, Wang L, Lu X, Huang J, Cao J, Li H, Gu D. PLA2G7 gene polymorphisms and coronary heart disease risk: a meta-analysis. Thromb Res 2010; 126: 498-503.
56. Ninio E, Tregouet D, Carrier JL, Stengel D, Bickel C, Perret C, Rupprecht HJ, Cambien F, Blankenberg S, Tiret L. Platelet-activating factor-acetylhydrolase and PAF-receptor gene haplotypes in relation to future cardiovascular event in patients with coronary artery disease. Hum Mol Genet 2004; 13: 1341-51.
57. Wootton PT, Stephens JW, Hurel SJ, Durand H, Cooper J, Ninio E, Humphries SE, Talmud PJ. Lp-PLA2 activity and PLA2G7 A379V genotype in patients with diabetes mellitus. Atherosclerosis 2006; 189: 149-56.
58. Casas JP, Ninio E, Panayiotou A, Palmen J, Cooper JA, Ricketts SL, Sofat R, Nicolaides AN, Corsetti JP, Fowkes FG, Tzoulaki I, Kumari M, Brunner EJ, Kivimaki M, Marmot MG, Hoffmann MM, Winkler K, Marz W, Ye S, Stirnadel HA et al. PLA2G7 genotype, lipoprotein-associated phospholipase A2 activity, and coronary heart disease risk in 10 494 cases and 15 624 controls of European Ancestry. Circulation 2010; 121: 2284-93.
59. Kruse S, Mao XQ, Heinzmann A, Blattmann S, Roberts MH, Braun S, Gao PS, Forster J, Kuehr J, Hopkin JM, Shirakawa T, Deichmann KA. The Ile198Thr and Ala379Val variants of plasmatic PAF-acetylhydrolase impair catalytical activities and are associated with atopy and asthma. Am J Hum Genet 2000; 66: 1522-30.
60. Croft SA, Samani NJ, Teare MD, Hampton KK, Steeds RP, Channer KS, Daly ME. Novel platelet membrane glycoprotein VI dimorphism is a risk factor for myocardial infarction. Circulation 2001; 104: 1459-63.
61. Ollikainen E, Mikkelsson J, Perola M, Penttila A, Karhunen PJ. Platelet membrane collagen receptor glycoprotein VI polymorphism is associated with coronary thrombosis and fatal myocardial infarction in middle-aged men. Atherosclerosis 2004; 176: 95-9.
62. Snoep JD, Gaussem P, Eikenboom JC, Emmerich J, Zwaginga JJ, Holmes CE, Vos HL, de Groot PG, Herrington DM, Bray PF, Rosendaal FR, van der Bom JG. The minor allele of GP6 T13254C is associated with decreased platelet activation and a reduced risk of recurrent cardiovascular events and mortality: results from the SMILE-Platelets project. J Thromb Haemost 2010; 8: 2377-84.
63. Michelson AD. Methods for the measurement of platelet function. Am J Cardiol 2009; 103: 20A-6A.