Original Article
Genetic Determinants of Response to Clopidogrel and Cardiovascular Events
N Engl J Med 2009; 360:363-375January 22, 2009
- Abstract
Background
Pharmacogenetic determinants of the response of patients to clopidogrel contribute to variability in the biologic antiplatelet activity of the drug. The effect of these determinants on clinical outcomes after an acute myocardial infarction is unknown.
Methods
We consecutively enrolled 2208 patients presenting with an acute myocardial infarction in a nationwide French registry and receiving clopidogrel therapy. We then assessed the relation of allelic variants of genes modulating clopidogrel absorption (ABCB1), metabolic activation (CYP3A5 and CYP2C19), and biologic activity (P2RY12 and ITGB3) to the risk of death from any cause, nonfatal stroke, or myocardial infarction during 1 year of follow-up.
Results
Death occurred in 225 patients, and nonfatal myocardial infarction or stroke in 94 patients, during the follow-up period. None of the selected single-nucleotide polymorphisms (SNPs) in CYP3A5, P2RY12, or ITGB3 were associated with a risk of an adverse outcome. Patients with two variant alleles of ABCB1 (TT at nucleotide 3435) had a higher rate of cardiovascular events at 1 year than those with the ABCB1 wild-type genotype (CC at nucleotide 3435) (15.5% vs. 10.7%; adjusted hazard ratio, 1.72; 95% confidence interval [CI], 1.20 to 2.47). Patients carrying any two CYP2C19 loss-of-function alleles (*2, *3, *4, or *5), had a higher event rate than patients with none (21.5% vs. 13.3%; adjusted hazard ratio, 1.98; 95% CI, 1.10 to 3.58). Among the 1535 patients who underwent percutaneous coronary intervention during hospitalization, the rate of cardiovascular events among patients with two CYP2C19 loss-of-function alleles was 3.58 times the rate among those with none (95% CI, 1.71 to 7.51).
Conclusions
Among patients with an acute myocardial infarction who were receiving clopidogrel, those carrying CYP2C19 loss-of-function alleles had a higher rate of subsequent cardiovascular events than those who were not. This effect was particularly marked among the patients undergoing percutaneous coronary intervention. (ClinicalTrials.gov number, NCT00673036.)
Media in This Article
Figure 1
Roles in Clopidogrel Activity of Proteins with Known Genetic Polymorphisms.Figure 2
Estimated Rates of Death from Any Cause, Nonfatal Myocardial Infarction, or Stroke, According to Characteristics of Variant-Allele Polymorphisms.Article Activity
- Article
Dual antiplatelet therapy with aspirin and clopidogrel is currently recommended for the prevention of atherothrombotic events in patients after acute myocardial infarction.1,2 However, even with the use of such therapy, a substantial number of subsequent ischemic events still occur.3-6 There is interindividual variability in the response to clopidogrel.7-9 Some studies have suggested that hyporesponsiveness is associated with poorer clinical outcomes after an acute coronary syndrome, particularly after percutaneous coronary intervention (PCI).10 However, there is also variability in the identification of biologic hyporesponsiveness to clopidogrel, depending on the test or agonist used and the timing of the assessment.
The mechanisms leading to a poor response to clopidogrel have not yet been fully elucidated and are most likely multifactorial.1,2 In addition to lack of compliance, clinical factors such as obesity, insulin resistance, and the nature of the coronary event may contribute to the variability of the clopidogrel response.7 Clopidogrel is also a prodrug, requiring metabolism before it can inhibit adenosine diphosphate–induced platelet aggregation. There is growing evidence that the response to clopidogrel may be influenced by pharmacokinetic variables such as intestinal absorption and metabolic activation in the liver, both of which are affected by genetic polymorphisms (Figure 1Figure 1
Roles in Clopidogrel Activity of Proteins with Known Genetic Polymorphisms.).11-18 The relation between known polymorphisms of relevant genes and the clinical outcome after acute myocardial infarction in patients receiving clopidogrel is unknown. To address this issue, we evaluated whether previously identified polymorphisms of genes modulating clopidogrel absorption (ABCB1 17), metabolic activation (CYP3A5 19 and CYP2C19 16,18,20), and biologic activity (P2RY12 14 and ITGB3 11) were associated with death or ischemic events during a 1-year follow-up period among patients in the French Registry of Acute ST-Elevation and Non–ST-Elevation Myocardial Infarction (FAST-MI) who were receiving clopidogrel after acute myocardial infarction. A complete list of centers and investigators participating in the registry has been published elsewhere.17 Methods
Study Population
The French Registry of Acute ST-Elevation and Non–ST-Elevation Myocardial Infarction (FAST-MI) study population and methods have been described in detail elsewhere.21 Briefly, the objective of the registry was to gather complete and representative data on both care and outcomes for patients with definite acute myocardial infarction who were admitted to intensive care units (ICUs), irrespective of the type of institution (i.e., university hospitals, public hospitals, or private clinics). Patients were recruited during a period of 1 month (31 days) at each center (2 months for patients with diabetes) between October 1 and December 24, 2005. Of the 374 centers in France that at that time treated patients with acute myocardial infarction, 223 (60%) participated in the study. Written informed consent for study participation was provided by each patient. In accordance with French law, the study was reviewed by the Committee for the Protection of Human Subjects in Biomedical Research of Saint Antoine University Hospital, and the data file was approved by the Commission Nationale Informatique et Liberté.
All consecutively enrolled patients 18 years of age or older were included in the registry if they had levels of serum markers of myocardial necrosis (creatine kinase, creatine kinase MB, troponin I, or troponin T) that were more than twice the upper limit of the normal range and either symptoms consistent with acute myocardial infarction or electrocardiographic changes in at least two contiguous leads (pathologic Q waves [≥0.04 second in duration], persistent ST-segment elevation, or ST-segment depression >0.1 mV). The time from the onset of symptoms to admission to the ICU had to be less than 48 hours. Patients received care according to usual practice; treatment was not affected by participation in the registry. When blood was drawn at the time of admission, an additional 10 ml was taken for DNA banking.
Follow-up information was collected through contacts with the patients' physicians, the patients or their family, and registry offices at their places of birth. The primary outcome was the composite of death from any cause, nonfatal myocardial infarction, or stroke during 1 year of follow-up after admission. Events were adjudicated by a scientific committee whose members were unaware of patients' medications and genotypes. Follow-up information was available for 99.2% of patients initially enrolled.
The study was designed and conducted by the authors. Genotyping was performed by Integragen under the direction of two of the authors. Data collection was performed by the International Clinical Trials Association and Assistance Publique–Hôpitaux de Paris, Unité de Recherche Clinique de l'Est. The authors analyzed the data, wrote the manuscript, and made the decision to submit the manuscript for publication; they vouch for the completeness and accuracy of the data. The sponsors had no role in the design or conduct of the study, in the analysis of the results, or in the decision to publish the paper.
Genotyping
Genomic DNA was extracted from whole-blood specimens with the use of a purifier (the MagNA Pure Compact Instrument, Roche) according to the manufacturer's recommendations. Genotyping for CYP2C19, CYP3A5, ABCB1 and P2RY12 was performed with the use of an oligonucleotide ligation assay (SNPlex, Applied Biosystems) after initial amplification by means of a polymerase-chain-reaction assay involving two primers for the major variant alleles CYP2C19*2 (rs4244285), CYP2C19*3 (rs4986893), CYP3A5*3 (rs776746), ABCB1 (rs1045642), and P2RY12 (rs16846673, rs6809699, and rs6785930), as described previously22 (see the Supplementary Appendix, available with the full text of this article at NEJM.org).
Genotyping for known variants of CYP2C19 and ITGB3 with functional importance — CYP2C19*4 (rs28399504), CYP2C19*5, CYP2C19*17 (rs12248560), and ITGB3 (rs5918) — was performed with the use of an allelic discrimination assay (Custom TaqMan) (see the Supplementary Appendix) and a detection system (ABI prism 7900HT Sequence Detection System, Applied Biosystems). Base numbering and allele definitions follow the nomenclature of the Human Cytochrome P450 (CYP) Allele Nomenclature Committee (www.cypalleles.ki.se).
Statistical Analysis
All statistical tests, performed with the use of SAS software, version 9.1, or SPSS software, version 14.0, were two-sided. All single-nucleotide polymorphisms (SNPs) evaluated in our study were tested for deviation from Hardy–Weinberg equilibrium with the use of a chi-square test. A univariate Cox proportional-hazards model was used to compare baseline demographic and clinical characteristics and characteristics of treatment and therapeutic management during hospitalization between the group with and the group without outcome events. We also compared the two groups with respect to the frequencies of the ABCB1, CYP3A5, P2RY12, and ITGB3 alleles and individual variant alleles of CYP2C19, including CYP2C19*17 (associated with very rapid CYP2C19 activity18), as well as the CYP2C19 alleles known to result in a nonfunctional protein (*2, *3, *4, and *5), classified as the presence of zero, one, or two variant alleles.
Predictors identified through univariate analysis (P<0.10) and other variables considered likely to have important prognostic value were tested in a multivariable, stepwise, forward Cox proportional-hazards model for association with the primary outcome, the composite of death from any cause, nonfatal myocardial infarction, or stroke during the 1-year follow-up period. The analysis was repeated for the subgroup of patients who underwent PCI during hospitalization. We also performed a propensity analysis for the CYP2C19 loss-of-function alleles, using a multivariate logistic-regression model, and developed a matched cohort of five control patients for each patient with two variant alleles, on the basis of the propensity-analysis score.
CYP2C19 is involved in the metabolism of proton-pump inhibitors, including omeprazole, a commonly prescribed drug. We therefore tested the effect of the coprescription of omeprazole by forcing the variable into the model, although its P value in the univariate analysis was greater than 0.20. Similarly, we analyzed the effect of CYP2C19*17 and the concomitant prescription of proton-pump inhibitors, including omeprazole, by forcing these variables into another multivariable Cox model.
Results are expressed as hazard ratios from the Cox models, along with the 95% confidence intervals. Survivor-function estimates for mean values of covariates in the Cox model were generated with the use of the product-limit approach (the BASELINE statement in the PHREG procedure of SAS software). We used the likelihood-ratio test for testing gene–gene interactions for the genes identified in the Cox multivariable model as having an association with outcome events. The full model, including the interactive effect (four interaction terms corresponding to the cross-products of the two genotypes for each gene), was compared with the null model, which included only marginal effects. Under the null hypothesis of no interaction, the likelihood-ratio test follows a chi-square distribution with 4 degrees of freedom, corresponding to the difference between the full model (8 degrees of freedom) and the null model (4 degrees of freedom).
Results
Characteristics of the Patients
Of the 3670 patients enrolled in FAST-MI, 2430 patients (66%) contributed a sample to the DNA bank. Of these 2430 patients, the 2208 who received clopidogrel were included in the present analysis. The mean loading dose of clopidogrel was 300 mg per day (<300 mg per day in 36% of patients, 300 to 375 mg per day in 50%, and 450 to 900 mg per day in 15%), and the mean maintenance dose at the time of hospital discharge was 75 mg per day.
A total of 225 patients died, and 94 had a nonfatal myocardial infarction or stroke during the follow-up period. As compared with patients who did not have an outcome event, the 294 patients who had an event (13% of the study cohort) were older; more frequently had a history of hypertension, diabetes, myocardial infarction, PCI, stroke, or heart failure; and less frequently underwent reperfusion therapy consisting of primary PCI or intravenous fibrinolysis (Table 1Table 1
Baseline Characteristics and Characteristics of In-Hospital Care of the Study Patients.). The use of calcium-channel blockers, aspirin, and proton-pump inhibitors was similar in the two groups, whereas patients who had an outcome event were less likely to receive statins, beta-blockers, angiotensin-converting–enzyme inhibitors, glycoprotein IIb/IIIa inhibitors, and heparin (Table 1).Allelic Frequencies
The observed genotype distributions did not deviate from Hardy–Weinberg equilibrium and matched those reported for white populations. The allelic frequencies of CYP3A5, P2RY12, ITGB3, and the individual CYP2C19 variants did not differ significantly between the patients with and those without outcome events (Table 2Table 2
Allelic Frequencies of SNPs among the Study Patients, According to Gene.). However, the frequency of the ABCB1 variant allele and the combined CYP2C19 loss-of-function variant alleles differed significantly between the two groups (Table 2).Predictors of Death and Major Events
None of the selected SNPs in the CYP3A5, P2RY12, or ITGB3 genes were significantly associated with the risk of death, nonfatal myocardial infarction, or stroke. In contrast, there was an increase in the hazard ratio for an outcome event among patients carrying the ABCB1 variant allele (genotype CT or TT) as compared with the wild-type allele (genotype CC) (Figure 2AFigure 2
Estimated Rates of Death from Any Cause, Nonfatal Myocardial Infarction, or Stroke, According to Characteristics of Variant-Allele Polymorphisms.) or any two of the CYP2C19 loss-of-function variant alleles as compared with one or none (Figure 2B). This increase in risk remained significant after adjustment for the risk factors and treatments listed in Table 1 (Table 3Table 3
Predictors of Death from Any Cause, Nonfatal Myocardial Infarction, or Stroke among the Study Patients.). Patients with two variant alleles of ABCB1 (TT) had a higher event rate at 1 year than those with the ABCB1 wild-type genotype (CC) (15.5% vs. 10.7%; adjusted hazard ratio, 1.72; 95% confidence interval [CI], 1.20 to 2.47). Similarly, patients carrying two CYP2C19 loss-of-function variant alleles had a higher event rate than patients who did not have these alleles (21.5% vs. 13.3%; adjusted hazard ratio, 1.98; 95% CI, 1.10 to 3.58) (Table 3). After full propensity-score matching (see the Supplementary Appendix), the risk of an outcome event at 1 year among patients with two, as compared with zero, CYP2C19 deficiency alleles was even higher (hazard ratio, 2.14; 95% CI, 1.09 to 4.17). Accounting for the presence of CYP2C19*17 or the concomitant prescription of proton-pump inhibitors or calcium-channel blockers had no significant effect on these risks.No significant interaction was found between either the ABCB1 variant allele or the CYP2C19 loss-of-function variant alleles and the clinical outcome (likelihood-ratio test statistic, 0.276; P=0.99). However, the presence of both two CYP2C19 loss-of-function alleles and either one or two ABCB1 variant alleles was associated with the highest risk of events (adjusted hazard ratio for the comparison with the presence of homozygous wild-type ABCB1 and CYP2C19 alleles, 5.31; 95% CI, 2.13 to 13.20; P=0.009).
Among the 1535 patients who underwent PCI during hospitalization, the adjusted risk of death, myocardial infarction, or stroke for patients with two CYP2C19 deficiency alleles was 3.58 times the risk among patients with the wild-type genotype (95% CI, 1.71 to 7.51; P=0.005) (Table 3), whereas the ABCB1 variant allele had no significant independent effect (P=0.35).
Discussion
The present study aimed to determine whether previously identified SNPs known to alter the pharmacokinetics of clopidogrel or the ex vivo ability of platelets to aggregate were associated with clinical outcomes during the first year after acute myocardial infarction. Variant alleles of two candidate genes involved in clopidogrel absorption (ABCB1) and metabolism (CYP2C19) were linked to an increased rate of cardiovascular events. In addition, the presence of two variant alleles of CYP2C19, but not ABCB1, were found to be associated with an increase by a factor of 3.6 in the rate of cardiovascular events among the patients who underwent PCI during hospitalization as compared with those who did not. As expected, patients with an outcome event had a worse risk profile at admission for acute myocardial infarction than did those without an event. However, there was no significant difference in the risk profile or hospital care received between patients with allelic variants for clopidogrel target genes and those without such variants.
The P2RY1214 receptor for clopidogrel and its effector, glycoprotein IIb/IIIa,11 were the first pharmacogenetic targets found to explain the biologic variability in response to this antiplatelet drug. However, in subsequent studies, ex vivo antiplatelet activity after the administration of clopidogrel was not related to allelic variants in these proteins.15,23-25 We found no association between polymorphisms of P2RY12 and ITGB3 (the gene encoding the beta subunit of glycoprotein IIb/IIIa) and clinical outcomes in patients with acute myocardial infarction who were treated with clopidogrel.
Clopidogrel is a prodrug that must be metabolized in the liver by several CYP proteins, including CYP3A and CYP2C19, to become active.26 Suh et al.19 reported an increased frequency of atherothrombotic events within 6 months after coronary angioplasty among patients with the CYP3A5 nonexpression genotype (CYP3A5*3) who were receiving clopidogrel therapy. Further studies, however, showed no association between the CYP3A5 genetic polymorphism and the antiplatelet effect of clopidogrel ex vivo, either in patients13,23 or in healthy subjects.14 Likewise, the results of the present study do not support a role of the CYP3A5 genetic polymorphism in the clinical response to clopidogrel. It is unlikely that concomitant drug use blunted a putative effect of the CYP3A5 genetic polymorphism, since most of the patients were not treated with strong or even moderate CYP3A inhibitors, as defined by current Food and Drug Administration guidelines (www.fda.gov/cder/drug/drugInteractions/default.htm).
Genetic polymorphisms of CYP2C19 modulate clopidogrel pharmacokinetics13 and pharmacodynamics in healthy volunteers,13,16 as well as in patients.15,18,27 As compared with subjects with no CYP2C19 variant allele, subjects carrying one or two CYP2C19 loss-of-function alleles have been shown to have lower plasma concentrations of the active metabolite of clopidogrel and a decrease in the antiplatelet effect of clopidogrel in ex vivo aggregation tests.13 Our results support and extend these findings from previous studies by showing a worse clinical outcome in patients carrying two CYP2C19 loss-of-function alleles who were treated with clopidogrel after acute myocardial infarction. This effect was particularly marked in the subgroup of patients who underwent PCI. In contrast, patients with one CYP2C19 variant allele did not have an increased risk (and actually had a slightly lower risk in the overall population), as compared with those who had no CYP2C19 variant alleles.
The antiplatelet activity of clopidogrel has been shown to be reduced in patients receiving omeprazole, a CYP2C19 inhibitor.28 In the present study, the use of omeprazole, or any other proton-pump inhibitor, had no effect on the clinical response to clopidogrel. This is an important clinical observation, considering the high frequency of coprescription of proton-pump inhibitors and dual antiplatelet therapy. It is possible that biologic differences detected by platelet-function tests are not large enough to have clinical relevance. This possibility would account for the absence of a discernible effect of omeprazole or the CYP2C19*17 allele, which slightly increases CYP2C19 expression, on clinical outcomes after clopidogrel therapy.
The drug-efflux transporter, P-glycoprotein (encoded by the ABCB1 gene), is a physiologic intestinal barrier against the absorption of several drugs, including clopidogrel.17 The relation between the noncoding ABCB1 C3435T SNP and P-glycoprotein expression or activity remains controversial.29-34 Discrepancies in the reported effect of C3435T may reflect differences in ABCB1 SNP frequencies among ethnic groups,35 complex effects of various polymorphisms along the same gene within a haplotype,36 or confounding by environmental factors.31,32 In the present study, patients with the ABCB1 TT and CT genotypes had worse clinical outcomes than those with a CC genotype. There was no interaction between the ABCB1 polymorphism and CYP2C19 loss-of-function variant alleles and the clinical outcome, but the association of two CYP2C19-deficient alleles and either one or two ABCB1 variant alleles was associated with a rate of events that was more than five times the rate among patients with the wild-type genotypes. Regardless of the exact link between the ABCB1 C3435T polymorphism and P-glycoprotein expression, the results of our study are consistent with the finding in a previous study that plasma concentrations of clopidogrel and its active metabolite were reduced in patients carrying the TT genotype.17 However, since the ABCB1 polymorphism was not an independent predictor of the outcome in the subgroup of patients undergoing PCI in our study, these results should be interpreted with caution and considered exploratory findings that need to be replicated.
The use of clopidogrel with aspirin is recommended for reducing recurrent atherothrombotic events after acute myocardial infarction and is deemed mandatory after stent placement.1,2 Although the optimal duration of clopidogrel therapy is uncertain, a duration of 1 year is common in patients with myocardial infarction, particularly those who undergo PCI.1,2 As a consequence, the prevalence of clopidogrel use in this population is substantial and increasing.37 Among patients for whom clopidogrel therapy is indicated, genotyping rather than repeated platelet monitoring could be an affordable and suitable strategy to identify patients at high risk for atherothrombotic events.
The observational nature of our study does not allow us to investigate cause-and-effect relationships. We cannot rule out the possibility that both ABCB1 and CYP2C19 polymorphisms affect atherothrombosis directly rather than acting as modulators of the clopidogrel response. However, no such effect was seen in the subgroup of 222 patients who contributed a blood sample to the DNA bank but who did not receive clopidogrel (event rate at 1 year for patients with the CYP2C19 wild-type genotype, those with one deficient allele, and those with two deficient alleles, 33%, 46%, and 25%, respectively; P=0.17). In addition, the patients in our study simultaneously received drugs other than clopidogrel that are known to prevent the recurrence of atherothrombotic events, including aspirin, statins, angiotensin-converting–enzyme inhibitors, and beta-blockers, and we cannot exclude the possibility that the influence of genetic factors on the response to clopidogrel would have been different in the absence of these other medications. However, current management of acute myocardial infarction includes the concomitant prescription of these drugs. Therefore, the results of this nationwide observational study reflect that which can be expected from the pharmacogenetics of clopidogrel in clinical practice.
In summary, in a study of 2208 patients with acute myocardial infarction who were treated with clopidogrel, we evaluated the relationship between genetic determinants of the response to clopidogrel and subsequent cardiovascular events. Genetic variants in CYP2C19 that result in loss of function were associated with an increase in the risk of death, myocardial infarction, or stroke, especially among patients undergoing PCI.
Supported by unrestricted grants from Pfizer and Servier for FAST-MI, a registry of the French Society of Cardiology, and a research grant from the French Caisse Nationale d'Assurance Maladie.
Dr. Simon reports receiving consulting fees from Bayer–Schering, Pfizer and Eli Lilly, lecture fees from Bayer–Schering, and grant support from Pfizer and Servier; Dr. Steg, consulting fees from Astellas, AstraZeneca, Bayer, Boehringer Ingelheim, Bristol-Myers Squibb, Endotis, GlaxoSmithKline, Medtronic, Merck Sharp & Dohme, Nycomed, Sanofi-Aventis, Servier, and the Medicines Company, lecture fees from Boehringer Ingelheim, Bristol-Myers Squibb, GlaxoSmithKline, Medtronic, Nycomed, Sanofi-Aventis, Servier, and the Medicines Company, and grant support from Sanofi-Aventis; Dr. Danchin, consulting fees from Servier, Sanofi-Aventis, Eli Lilly, and AstraZeneca, lecture fees from Servier, Sanofi-Aventis, and Bristol-Myers Squibb, and grant support from Pfizer and Servier; and Dr. Becquemont, consulting fees from Sanofi-Aventis, Pfizer, and Servier and lecture fees from GlaxoSmithKline.
No other potential conflict of interest relevant to this article was reported.
Drs. Danchin and Becquemont contributed equally to this article.
This article (10.1056/NEJMoa0808227) was published at NEJM.org on December 22, 2008.
We thank the physicians who cared for the patients at the participating institutions, E. Martin and F. Rousseau (IntegraGene, Paris), the International Clinical Trials Association Contract Research Organization (Fontaine-lès-Dijon, France), Liliane Dubert (Department of Pharmacology, Université Pierre et Marie Curie [UPMC] Paris 06), the Clinical Research Assistant team of Unité de Recherche Clinique de l'Est Parisien (Assistance Publique–Hôpitaux de Paris and UPMC Paris 06), and Benoît Pace and Geneviève Mulak (French Society of Cardiology) for their assistance in designing the electronic case-record form and data management during the follow-up period.
Source Information
From Assistance Publique–Hôpitaux de Paris (AP-HP), Hôpital Saint-Antoine, and Université Pierre et Marie Curie (UPMC) Paris 06 (T.S., L.Q., E.D.); AP-HP, Hôpital Bicètre, Université Paris Sud 11 (C.V., L.B.); INSERM, Unite 720 (M.M.-K.); AP-HP, Hôpital Bichat; INSERM, Unite 698; and Université Paris 07 (P.G.S.); and AP-HP, Hôpital Européen Georges Pompidou, Université Rene Descartes Paris 05 (N.D.) — all in Paris; Centre Hospitalier Universitaire Besançon, Besançon (N.M.); and INSERM, Unite 558, Toulouse (J.F.) — all in France.
Address reprint requests to Dr. Simon at the Department of Pharmacology, UPMC, 27 Rue Chaligny, 75012 Paris, France, or at tabassome.simon@sat.aphp.fr.
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