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J Am Coll Cardiol, 2007; 49:1505-1516, doi:10.1016/j.jacc.2006.11.044 (Published online 26 March 2007).
© 2007 by the American College of Cardiology Foundation
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STATE-OF-THE-ART PAPER

Variability in Individual Responsiveness to Clopidogrel

Clinical Implications, Management, and Future Perspectives

Dominick J. Angiolillo, MD, PhD, FACC*,*, Antonio Fernandez-Ortiz, MD, PhD{dagger}, Esther Bernardo, BSc{dagger}, Fernando Alfonso, MD, PhD{dagger}, Carlos Macaya, MD, PhD{dagger}, Theodore A. Bass, MD, FACC* and Marco A. Costa, MD, PhD, FACC*

* Division of Cardiology, University of Florida-Shands Jacksonville, Jacksonville, Florida
{dagger} Cardiovascular Institute, San Carlos University Hospital, Madrid, Spain.

Manuscript received August 9, 2006; revised manuscript received November 13, 2006, accepted November 28, 2006.

* Reprint requests and correspondence: Dr. Dominick J. Angiolillo, Division of Cardiology, University of Florida–Shands Jacksonville, 655 West 8th Street, Jacksonville, Florida 32209. (Email: dominick.angiolillo{at}jax.ufl.edu).

Antiplatelet therapy is the cornerstone of treatment for patients with acute coronary syndromes and/or undergoing percutaneous coronary interventions. Clopidogrel, in combination with aspirin, is currently the antiplatelet treatment of choice for prevention of stent thrombosis, and clinical trials have shown that, in high-risk patients, prolonged dual antiplatelet treatment is more effective than aspirin alone in preventing major cardiovascular events. However, despite the use of clopidogrel, a considerable number of patients continue to have cardiovascular events. Numerous in vitro studies have shown that individual responsiveness to clopidogrel is not uniform in all patients and is subject to inter- and intraindividual variability. Notably, there is a growing degree of evidence that recurrence of ischemic complications may be attributed to poor response to clopidogrel. The mechanisms leading to poor clopidogrel effects are not fully elucidated and are likely multifactorial. Although the gold standard definition to assess antiplatelet drug response has not been fully established, there is sufficient evidence to support that persistence of enhanced platelet reactivity despite the use of clopidogrel is a clinically relevant entity. This paper reviews the impact of individual response variability to clopidogrel on clinical outcomes and current and future directions for its management.

Abbreviations and Acronyms
  ACS = acute coronary syndrome
  ADP = adenosine diphosphate
  ATP = adenosine triphosphate
  cAMP = cyclic adenosine monophosphate
  CYP = cytochrome P450
  GP = glycoprotein
  GTP = guanosine triphosphate
  LTA = light transmittance aggregometry
  MFI = median fluorescence intensity
  NSTE-ACS = non–ST-segment elevation acute coronary syndrome
  PCI = percutaneous coronary intervention
  PGE1 = prostaglandin E1
  STEMI = ST-segment elevation myocardial infarction
  VASP-P = vasodilator-stimulated phosphoprotein-phosphorylation




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F. Marin, R. Gonzalez-Conejero, P. Capranzano, T. A. Bass, V. Roldan, and D. J. Angiolillo
Pharmacogenetics in Cardiovascular Antithrombotic Therapy
J. Am. Coll. Cardiol., September 15, 2009; 54(12): 1041 - 1057.
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J.-P. Collet and G. Montalescot
Review: Platelet Function Testing and Implications for Clinical Practice
Journal of Cardiovascular Pharmacology and Therapeutics, September 1, 2009; 14(3): 157 - 169.
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D. Shimbo, W. Chaplin, S. Kuruvilla, L. T. Wasson, D. Abraham, and M. M. Burg
Hostility and Platelet Reactivity in Individuals Without a History of Cardiovascular Disease Events
Psychosom Med, September 1, 2009; 71(7): 741 - 747.
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A. R. Shuldiner, J. R. O'Connell, K. P. Bliden, A. Gandhi, K. Ryan, R. B. Horenstein, C. M. Damcott, R. Pakyz, U. S. Tantry, Q. Gibson, et al.
Association of Cytochrome P450 2C19 Genotype With the Antiplatelet Effect and Clinical Efficacy of Clopidogrel Therapy
JAMA, August 26, 2009; 302(8): 849 - 857.
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C. Verstuyft, T. Simon, and R. B. Kim
Personalized medicine and antiplatelet therapy: ready for prime time?
Eur. Heart J., August 2, 2009; 30(16): 1943 - 1963.
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A. Kumar and D. H. Roberts
Test Before You Stop
Arch Surg, August 1, 2009; 144(8): 787 - 787.
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G. Lindvall, U. Sartipy, S. Bjessmo, P. Svenarud, B. Lindvall, and J. van der Linden
Aprotinin reduces the antiplatelet effect of clopidogrel
Interact CardioVasc Thorac Surg, August 1, 2009; 9(2): 178 - 181.
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C. Varenhorst, S. James, D. Erlinge, J. T. Brandt, O. O. Braun, M. Man, A. Siegbahn, J. Walker, L. Wallentin, K. J. Winters, et al.
Genetic variation of CYP2C19 affects both pharmacokinetic and pharmacodynamic responses to clopidogrel but not prasugrel in aspirin-treated patients with coronary artery disease
Eur. Heart J., July 2, 2009; 30(14): 1744 - 1752.
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A. D. Michelson, A. L. Frelinger III, E. Braunwald, W. E. Downey, D. J. Angiolillo, N. P. Xenopoulos, J. A. Jakubowski, Y. Li, S. A. Murphy, J. Qin, et al.
Pharmacodynamic assessment of platelet inhibition by prasugrel vs. clopidogrel in the TRITON-TIMI 38 trial
Eur. Heart J., July 2, 2009; 30(14): 1753 - 1763.
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F. Van de Werf
New antithrombotic agents: are they needed and what can they offer to patients with a non-ST-elevation acute coronary syndrome?
Eur. Heart J., July 2, 2009; 30(14): 1695 - 1702.
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 CirculationHome page
M. Valgimigli, G. Campo, N. de Cesare, E. Meliga, P. Vranckx, A. Furgieri, D. J. Angiolillo, M. Sabate, M. Hamon, A. Repetto, et al.
Intensifying Platelet Inhibition With Tirofiban in Poor Responders to Aspirin, Clopidogrel, or Both Agents Undergoing Elective Coronary Intervention: Results From the Double-Blind, Prospective, Randomized Tailoring Treatment With Tirofiban in Patients Showing Resistance to Aspirin and/or Resistance to Clopidogrel Study
Circulation, June 30, 2009; 119(25): 3215 - 3222.
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B. T. Ivandic, M. Sausemuth, H. Ibrahim, E. Giannitsis, M. Gawaz, and H. A. Katus
Dual Antiplatelet Drug Resistance Is a Risk Factor for Cardiovascular Events after Percutaneous Coronary Intervention
Clin. Chem., June 1, 2009; 55(6): 1171 - 1176.
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 CirculationHome page
J. L. Mega, S. L. Close, S. D. Wiviott, L. Shen, R. D. Hockett, J. T. Brandt, J. R. Walker, E. M. Antman, W. L. Macias, E. Braunwald, et al.
Cytochrome P450 Genetic Polymorphisms and the Response to Prasugrel: Relationship to Pharmacokinetic, Pharmacodynamic, and Clinical Outcomes
Circulation, May 19, 2009; 119(19): 2553 - 2560.
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N. R. Desai, J. L. Mega, S. Jiang, C. P. Cannon, and M. S. Sabatine
Interaction Between Cigarette Smoking and Clinical Benefit of Clopidogrel
J. Am. Coll. Cardiol., April 14, 2009; 53(15): 1273 - 1278.
[Abstract] [Full Text] [PDF]

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D. Sibbing, J. Stegherr, W. Latz, W. Koch, J. Mehilli, K. Dorrler, T. Morath, A. Schomig, A. Kastrati, and N. von Beckerath
Cytochrome P450 2C19 loss-of-function polymorphism and stent thrombosis following percutaneous coronary intervention
Eur. Heart J., April 2, 2009; 30(8): 916 - 922.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
D. J. Angiolillo
Antiplatelet Therapy in Diabetes: Efficacy and Limitations of Current Treatment Strategies and Future Directions
Diabetes Care, April 1, 2009; 32(4): 531 - 540.
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Y.-H. Jeong, S.-W. Lee, B.-R. Choi, I.-S. Kim, M.-K. Seo, C. H. Kwak, J.-Y. Hwang, and S.-W. Park
Randomized Comparison of Adjunctive Cilostazol Versus High Maintenance Dose Clopidogrel in Patients With High Post-Treatment Platelet Reactivity: Results of the ACCEL-RESISTANCE (Adjunctive Cilostazol Versus High Maintenance Dose Clopidogrel in Patients With Clopidogrel Resistance) Randomized Study
J. Am. Coll. Cardiol., March 31, 2009; 53(13): 1101 - 1109.
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W. Kuliczkowski, A. Witkowski, L. Polonski, C. Watala, K. Filipiak, A. Budaj, J. Golanski, D. Sitkiewicz, J. Pregowski, J. Gorski, et al.
Interindividual variability in the response to oral antiplatelet drugs: a position paper of the Working Group on antiplatelet drugs resistance appointed by the Section of Cardiovascular Interventions of the Polish Cardiac Society, endorsed by the Working Group on Thrombosis of the European Society of Cardiology
Eur. Heart J., February 2, 2009; 30(4): 426 - 435.
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D. Erlinge, C. Varenhorst, O. O. Braun, S. James, K. J. Winters, J. A. Jakubowski, J. T. Brandt, A. Sugidachi, A. Siegbahn, and L. Wallentin
Patients With Poor Responsiveness to Thienopyridine Treatment or With Diabetes Have Lower Levels of Circulating Active Metabolite, but Their Platelets Respond Normally to Active Metabolite Added Ex Vivo
J. Am. Coll. Cardiol., December 9, 2008; 52(24): 1968 - 1977.
[Abstract] [Full Text] [PDF]

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 Circ Cardiovasc IntervHome page
A. Colombo and R. T. Gerber
Should dual antiplatelet therapy after drug-eluting stents be continued for more than 1 year?: Dual Antiplatelet Therapy After Drug-Eluting Stents Should Not Be Continued for More Than 1 Year and Preferably Indefinitely
Circ Cardiovasc Interv, December 1, 2008; 1(3): 226 - 232.
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P. Gladding, M. Webster, I. Zeng, H. Farrell, J. Stewart, P. Ruygrok, J. Ormiston, S. El-Jack, G. Armstrong, P. Kay, et al.
The Antiplatelet Effect of Higher Loading and Maintenance Dose Regimens of Clopidogrel: The PRINC (Plavix Response in Coronary Intervention) Trial
J. Am. Coll. Cardiol. Intv., December 1, 2008; 1(6): 612 - 619.
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 Anesth. Analg.Home page
C. Velik-Salchner, S. Maier, P. Innerhofer, W. Streif, A. Klingler, C. Kolbitsch, and D. Fries
Point-of-Care Whole Blood Impedance Aggregometry Versus Classical Light Transmission Aggregometry for Detecting Aspirin and Clopidogrel: The Results of a Pilot Study
Anesth. Analg., December 1, 2008; 107(6): 1798 - 1806.
[Abstract] [Full Text] [PDF]

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 Eur Heart J SupplHome page
G. De Luca
Adjunctive antithrombotic therapy during primary percutaneous coronary intervention
Eur. Heart J. Suppl., December 1, 2008; 10(suppl_J): J2 - J14.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
V. Fuster and M. E. Farkouh
Acute Coronary Syndromes and Diabetes Mellitus: A Winning Ticket for Prasugrel
Circulation, October 14, 2008; 118(16): 1607 - 1608.
[Full Text] [PDF]

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 J Am Coll CardiolHome page
L. Ang, V. Palakodeti, A. Khalid, S. Tsimikas, Z. Idrees, P. Tran, P. Clopton, N. Zafar, G. Bromberg-Marin, S. Keramati, et al.
Elevated Plasma Fibrinogen and Diabetes Mellitus Are Associated With Lower Inhibition of Platelet Reactivity With Clopidogrel
J. Am. Coll. Cardiol., September 23, 2008; 52(13): 1052 - 1059.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
J.-P. Collet, J. Silvain, A. Landivier, M.-L. Tanguy, G. Cayla, A. Bellemain, N. Vignolles, S. Gallier, F. Beygui, A. Pena, et al.
Dose Effect of Clopidogrel Reloading in Patients Already on 75-mg Maintenance Dose: The Reload With Clopidogrel Before Coronary Angioplasty in Subjects Treated Long Term With Dual Antiplatelet Therapy (RELOAD) Study
Circulation, September 16, 2008; 118(12): 1225 - 1233.
[Abstract] [Full Text] [PDF]

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 Eur Heart JHome page
D. J. Angiolillo, P. Capranzano, S. Goto, M. Aslam, B. Desai, R. K. Charlton, Y. Suzuki, L. C. Box, S. B. Shoemaker, M. M. Zenni, et al.
A randomized study assessing the impact of cilostazol on platelet function profiles in patients with diabetes mellitus and coronary artery disease on dual antiplatelet therapy: results of the OPTIMUS-2 study
Eur. Heart J., September 2, 2008; 29(18): 2202 - 2211.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
A. M. Gori, R. Marcucci, A. Migliorini, R. Valenti, G. Moschi, R. Paniccia, P. Buonamici, G. F. Gensini, R. Vergara, R. Abbate, et al.
Incidence and Clinical Impact of Dual Nonresponsiveness to Aspirin and Clopidogrel in Patients With Drug-Eluting Stents
J. Am. Coll. Cardiol., August 26, 2008; 52(9): 734 - 739.
[Abstract] [Full Text] [PDF]


 
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