Microfluidic thrombosis under multiple shear rates and antiplatelet therapy doses

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Li, Melissa ^a   Hotaling, Nathan A ^a   Ku, David N ^b   Forest, Craig R ^b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; EPTIFIBATIDE; HEPARIN;

ADULT; ANTICOAGULANT THERAPY; ARTICLE; BLOOD CELL COUNT; BLOOD CLOTTING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG MEGADOSE; HUMAN; HUMAN CELL; MICROFLUIDICS; QUANTITATIVE STUDY; SHEAR RATE; THROMBOCYTE FUNCTION; THROMBOSIS; VALIDATION STUDY;

ASPIRIN; BLOOD COAGULATION; BLOOD COAGULATION TESTS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROFLUIDICS; PLATELET AGGREGATION INHIBITORS; REPRODUCIBILITY OF RESULTS; THROMBOSIS;

EID: 84896752543     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082493     Document Type: Article

References (60)

1. Hofer CK, Zollinger A, Ganter MT (2010) Perioperative assessment of platelet function in patients under antiplatelet therapy. Expert Rev Med Devices 7: 625-637. doi:10.1586/erd.10.29.
2. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, et al. (n.d.) Heart Disease and Stroke Statistics-2011 Update: A Report From the American Heart Association -Roger et al. 123 (4): e18 -Circulation. Available: http://circ. ahajournals.org/cgi/content/full/123/4/e18. Accessed 2011 Mar 30.
3. Wang TH, Bhatt DL, Topol EJ (2006) Aspirin and clopidogrel resistance: an emerging clinical entity. Eur Heart J 27: 647-654. doi:10.1093/eurheartj/ ehi684.
4. Eikelboom JW, Hirsh J, Spencer FA, Baglin TP, Weitz JI (2012) Antiplatelet Drugs: Antithrombotic Therapy and Prevention of Thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 141: e89S-e119S. doi:10.1378/chest.11-2293.
5. Gasparyan AY, Watson T, Lip GYH (2008) The Role of Aspirin in Cardiovascular Prevention: Implications of Aspirin Resistance. J Am Coll Cardiol 51: 1829-1843. doi:10.1016/j.jacc.2007.11.080. (Pubitemid 351615246)
6. Maree AO, Fitzgerald DJ (2007) Variable Platelet Response to Aspirin and Clopidogrel in Atherothrombotic Disease. Circulation 115: 2196-2207. doi:10.1161/CIRCULATIONAHA.106.675991. (Pubitemid 46659072)
7. Gum PA, Kottke-Marchant K, Welsh PA, White J, Topol EJ (2003) A prospective, blinded determination of the natural history of aspirin resistance among stable patients with cardiovascular disease. J Am Coll Cardiol 41: 961-965. doi:10.1016/S0735-1097(02)03014-0. (Pubitemid 36315537)
8. Grosser T, Fries S, Lawson JA, Kapoor SC, Grant GR, et al. (2012) Drug Resistance and Pseudoresistance: An Unintended Consequence of Enteric Coating Aspirin. Circulation. Available: http://circ.ahajournals.org/content/early/2012/ 12/04/CIRCULATIONAHA.112.117283. Accessed 18 April 2013.
9. Zwaginga JJ, Sakariassen KS, Nash G, King KR, Heemskerk JWM, et al. (2006) Flow-based assays for global assessment of hemostasis. Part 2: current methods and considerations for the future. J Thromb Haemost 4: 2716-2717. doi:10.1111/j.1538-7836.2006.02178.x. (Pubitemid 44741570)
10. Breet NJ, van Werkum JW, Bouman HJ, Kelder JC, Ruven HJT, et al. (2010) Comparison of Platelet Function Tests in Predicting Clinical Outcome in Patients Undergoing Coronary Stent Implantation. JAMA 303: 754-762. doi:10.1001/jama. 2010.181.
11. Price MJ, Berger PB, Teirstein PS, Tanguay J-F, Angiolillo DJ, et al. (2011) Standard-vs High-Dose Clopidogrel Based on Platelet Function Testing After Percutaneous Coronary Intervention. JAMA J Am Med Assoc 305: 1097-1105. doi:10.1001/jama.2011.290.
12. Neeves KB, Onasoga AA, Hansen RR, Lilly JJ, Venckunaite D, et al. (2013) Sources of Variability in Platelet Accumulation on Type 1 Fibrillar Collagen in Microfluidic Flow Assays. PLoS ONE 8. Available: http://www.ncbi.nlm.nih. gov/pmc/articles/PMC3552855/. Accessed 22 April 2013.
13. Michelson AD (2004) Platelet Function Testing in Cardiovascular Diseases. Circulation 110: e489-e493. doi:10.1161/01.CIR.0000147228.29325.F9.
14. Jackson SP (2007) The growing complexity of platelet aggregation. Blood 109: 5087-5095. doi:Review. (Pubitemid 46890522)
15. Savage B, Sixma JJ, Ruggeri ZM (2002) Functional self-association of von Willebrand factor during platelet adhesion under flow. Proc Natl Acad Sci U S A 99: 425-430. (Pubitemid 34060377)
16. Bernardo A, Bergeron AL, Sun CW, Guchhait P, Cruz MA, et al. (2004) Von Willebrand factor present in fibrillar collagen enhances platelet adhesion to collagen and collagen-induced platelet aggregation. J Thromb Haemost 2: 660-669. doi:10.1111/j.1538-7836.2004.00661.x. (Pubitemid 40185692)
17. Gutierrez E, Petrich BG, Shattil SJ, Ginsberg MH, Groisman A, et al. (2008) Microfluidic devices for studies of shear-dependent platelet adhesion. Lab Chip 8: 1486. doi:10.1039/b804795b.
18. Dimov IK, Basabe-Desmonts L, Garcia-Cordero JL, Ross BM, Ricco AJ, et al. (2011) Stand-alone self-powered integrated microfluidic blood analysis system (SIMBAS). Lab Chip 11: 845-850. doi:10.1039/C0LC00403K.
19. Hosokawa K, Ohnishi T, Kondo T, Fukasawa M, Koide T, et al. (2011) A novel automated microchip flow-chamber system to quantitatively evaluate thrombus formation and antithrombotic agents under blood flow conditions. J Thromb Haemost 9: 2029-2037. doi:10.1111/j.1538-7836.2011.04464.x.
20. Neeves KB, Maloney SF, Fong KP, Schmaier AA, Kahn ML, et al. (2008) Microfluidic focal thrombosis model for measuring murine platelet deposition and stability: PAR4 signaling enhances shear-resistance of platelet aggregates. J Thromb Haemost 6: 2193-2201. doi:10.1111/j.1538-7836.2008.03188.x.
21. Kita A, Sakurai Y, Myers DR, Rounsevell R, Huang JN, et al. (2011) Microenvironmental Geometry Guides Platelet Adhesion and Spreading: A Quantitative Analysis at the Single Cell Level. PLoS ONE 6: e26437. doi:10.1371/journal.pone.0026437.
22. Tovar-Lopez FJ, Rosengarten G, Westein E, Khoshmanesh K, Jackson SP, et al. (2010) A microfluidics device to monitor platelet aggregation dynamics in response to strain rate micro-gradients in flowing blood. Lab Chip 10: 291. doi:10.1039/b916757a.
23. Conant CG, Schwartz MA, Nevill T, Ionescu-Zanetti C (2009) Platelet Adhesion and Aggregation Under Flow using Microfluidic Flow Cells. J Vis Exp JoVE. doi:10.3791/1644.
24. Para A, Bark D, Lin A, Ku D (2011) Rapid Platelet Accumulation Leading to Thrombotic Occlusion. Ann Biomed Eng 39: 1961-1971. doi:10.1007/s10439-011- 0296-3.
25. Jackson SP, Nesbitt WS, Kulkarni S (n.d.) Signaling events underlying thrombus formation. J Thromb Haemost 1: 1602-1612. doi:10.1046/j.1538-7836.2003. 00267.x.
26. Hosokawa K, Ohnishi T, Fukasawa M, Kondo T, Sameshima H, et al. (2012) A microchip flow-chamber system for quantitative assessment of the platelet thrombus formation process. Microvasc Res 83: 154-161. doi:10.1016/j.mvr.2011. 11.007.
27. Kottke-Marchant K, Powers JB, Brooks L, Kundu S, Christie DJ (1999) The effect of antiplatelet drugs, heparin, and preanalytical variables on platelet function detected by the platelet function analyzer (PFA-100). Clin Appl Thromb Off J Int Acad Clin Appl Thromb 5: 122-130. (Pubitemid 29165344)
28. Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A, et al. (2009) A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 15: 665-673. doi:10.1038/nm.1955.
29. Colace TV, Muthard RW, Diamond SL (2012) Thrombus Growth and Embolism on Tissue Factor-Bearing Collagen Surfaces Under Flow Role of Thrombin With and Without Fibrin. Arterioscler Thromb Vasc Biol 32: 1466-1476. doi:10.1161/ATVBAHA.112.249789.
30. Turner NA, Moake JL, Kamat SG, Schafer AI, Kleiman NS, et al. (1995) Comparative real-time effects on platelet adhesion and aggregation under flowing conditions of in vivo aspirin, heparin, and monoclonal antibody fragment against glycoprotein IIb-IIIa. Circulation 91: 1354-1362. doi:10.1161/01.CIR.91. 5.1354.
31. Li M, Ku DN, Forest CR (2012) Microfluidic system for simultaneous optical measurement of platelet aggregation at multiple shear rates in whole blood. Lab Chip 12: 1355-1362. doi:10.1039/C2LC21145A.
32. Storey RF, Wilcox RG, Heptinstall S (1998) Differential effects of glycoprotein IIb/IIIa antagonists on platelet microaggregate and macroaggregate formation and effect of anticoagulant on antagonist potency implications for assay methodology and comparison of different antagonists. Circulation 98: 1616-1621. doi:10.1161/01.CIR.98.16.1616. (Pubitemid 28500383)
33. Looney MR, Nguyen JX, Hu Y, Van Ziffle JA, Lowell CA, et al. (2009) Platelet depletion and aspirin treatment protect mice in a two-event model of transfusion-related acute lung injury. J Clin Invest. Available: http://www.jci.org/articles/view/38432. Accessed 29 November 2012.
34. Millenium Pharmaceuticals, Inc., Merck and Co., Inc. (2011) Integrilin (eptifibatide) injection for intravenous admninistration. Whitehouse Station, NJ 08889, USA:
35. Mueller MR, Salat A, Stangl P, Murabito M, Pulaki S, et al. (1997) Variable platelet response to low-dose ASA and the risk of limb deterioration in patients submitted to peripheral arterial angioplasty. Thromb Haemost 78: 1003-1007. (Pubitemid 27417291)
36. Eikelboom JW, Hankey GJ (2003) Aspirin resistance:a new independent predictor of vascular events?. J Am Coll Cardiol 41: 966-968. doi:10.1016/S0735-1097(02)03013-9. (Pubitemid 36315538)
37. Sodemann A, Li M, Mayor R, Forest CR (2009) Micromilling of molds for microfluidic blood diagnostic devices. Proc Annu Meet Am Soc Precis Eng: 4-9.
38. Li M, Ackerman J, Forest C (2011) Microfluidic System for Multichannel Optical Measurement of Shear Induced Platelet Thrombosis in Unfractionated Blood. Proc 15th Int Conf Miniaturized Chem Biochem Anal Syst: 541-543.
39. Dalby M, Montalescot G, Sollier CB dit, Vicaut E, Soulat T, et al. (2004) Eptifibatide provides additional platelet inhibition in Non-ST-Elevation myocardial infarction patients already treated with aspirin and clopidogrel: Results of the platelet activity extinction in Non-Q-Wave myocardial infarction with aspirin, clopidogrel, and eptifibatide (PEACE) study. J Am Coll Cardiol 43: 162-168. doi:10.1016/j.jacc.2003.08.033. (Pubitemid 38201138)
40. Hanson SR, Sakariassen KS (1998) Blood flow and antithrombotic drug effects. Am Heart J 135: S132-S145. doi:http://dx.doi.org/10.1016/S0002-8703(98) 70241-8. (Pubitemid 28237286)
41. Neeves KB, Diamond SL (2008) A membrane-based microfluidic device for controlling the flux of platelet agonists into flowing blood. Lab Chip 8: 701-709. doi:10.1039/b717824g. (Pubitemid 351585455)
42. Barstad R, Roald H, Cui Y, Turitto V, Sakariassen K (1994) A perfusion chamber developed to investigate thrombus formation and shear profiles in flowing native human blood at the apex of well-defined stenoses. Arterioscler Thromb Vasc Biol 14: 1984-1991. doi:10.1161/01.ATV.14.12.1984.
43. Magallon J, Chen J, Rabbani L, Dangas G, Yang J, et al. (2011) Humanized Mouse Model of Thrombosis Is Predictive of the Clinical Efficacy of Antiplatelet Agents. Circulation 123: 319-326. doi:10.1161/CIRCULATIONAHA. 110.951970.
44. Tsai M, Kita A, Leach J, Rounsevell R, Huang JN, et al. (2012) In vitro modeling of the microvascular occlusion and thrombosis that occur in hematologic diseases using microfluidic technology. J Clin Invest 122: 408-418. doi:10.1172/JCI58753.
45. Goto S, Tamura N, Li M, Handa M, Ikeda Y, et al. (2003) Different effects of various anti-GPIIb-IIIa agents on shear-induced platelet activation and expression of procoagulant activity. J Thromb Haemost 1: 2022-2030. doi:10.1046/j.1538-7836.2003.00349.x.
46. Giugliano RP, White JA, Bode C, Armstrong PW, Montalescot G, et al. (2009) Early versus Delayed, Provisional Eptifibatide in Acute Coronary Syndromes. N Engl J Med 360: 2176-2190. doi:10.1056/NEJMoa0901316.
47. Topol EJ (1998) Inhibition of Platelet Glycoprotein IIb/IIIa with Eptifibatide in Patients with Acute Coronary Syndromes. N Engl J Med 339: 436-443. doi:10.1056/NEJM199808133390704. (Pubitemid 28377685)
48. Vane JR, Botting RM (2003) The mechanism of action of aspirin. Thromb Res 110: 255-258. doi:http://dx.doi.org/10.1016/S0049-3848(03)00379-7. (Pubitemid 37329821)
49. Lordkipanidzé M, Pharand C, Schampaert E, Turgeon J, Palisaitis DA, et al. (2007) 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 28: 1702-1708. doi:10.1093/eurheartj/ehm226. (Pubitemid 47227104)
50. Li R, Fries S, Li X, Grosser T, Diamond SL (2013) Microfluidic Assay of Platelet Deposition on Collagen by Perfusion of Whole Blood from Healthy Individuals Taking Aspirin. Clin Chem 59: 1195-1204. doi:10.1373/clinchem. 2012.198101.
51. Barstad R, Orvim U, Hamers M, Tjonnfjord G, Brosstad F, et al. (1996) Reduced effect of aspirin on thrombus formation at high shear and disturbed laminar blood flow. Thromb Haemost 75: 827-832. (Pubitemid 26181858)
52. Roald HE, Orvim U, Bakken IJ, Barstad RM, Kierulf P, et al. (1994) Modulation of thrombotic responses in moderately stenosed arteries by cigarette smoking and aspirin ingestion. Arterioscler Thromb Vasc Biol 14: 617-621. doi:10.1161/01.ATV.14.4.617.
53. Jackson SP, Nesbitt WS, Westein E (2009) Dynamics of platelet thrombus formation. J Thromb Haemost 7: 17-20. doi:10.1111/j.1538-7836.2009.03401.x.
54. Mendolicchio GL, Zavalloni D, Bacci M, Corrada E, Marconi M, et al. (2011) Variable effect of P2Y12 inhibition on platelet thrombus volume in flowing blood. J Thromb Haemost 9: 373-382. doi:10.1111/j.1538-7836.2010.04144. x.
55. Veen G, Meyer A, Verheugt FWA, Werter CJPJ, de Swart H, et al. (1993) Culprit lesion morphology and stenosis severity in the prediction of reocclusion after coronary thrombolysis: Angiographic results of the APRICOT study. J Am Coll Cardiol 22: 1755-1762. doi:10.1016/0735-1097(93)90754-O. (Pubitemid 23359628)
56. Lucitt MB, O'Brien S, Cowman J, Meade G, Basabe-Desmonts L, et al. (2013) Assaying the efficacy of dual-antiplatelet therapy: use of a controlled-shear-rate microfluidic device with a well-defined collagen surface to track dynamic platelet adhesion. Anal Bioanal Chem 405: 4823-4834. doi:10.1007/s00216-013-6897-y.
57. Zhao R, Kameneva MV, Antaki JF (2007) Investigation of platelet margination phenomena at elevated shear stress. Biorheology 44: 161-177. (Pubitemid 350114369)
58. Barron HV, Cannon CP, Murphy SA, Braunwald E, Gibson CM (2000) Association Between White Blood Cell Count, Epicardial Blood Flow, Myocardial Perfusion, and Clinical Outcomes in the Setting of Acute Myocardial Infarction A Thrombolysis In Myocardial Infarction 10 Substudy. Circulation 102: 2329-2334. doi:10.1161/01.CIR.102.19.2329.
59. Neumann F-J, Hochholzer W, Pogatsa-Murray G, Schomig A, Gawaz M (2001) Antiplatelet effects of abciximab, tirofiban and eptifibatide in patients undergoing coronary stenting. J Am Coll Cardiol 37: 1323-1328. doi:10.1016/S0735-1097(01)01165-2. (Pubitemid 32295594)
60. Wootton DM, Ku DN (1999) Fluid mechanics of vascular systems, diseases, and thrombosis. Annu Rev Biomed Eng 1: 299-329. (Pubitemid 129740014)