Platelet reactivity in response to aspirin and ticagrelor in African-Americans and European-Americans.


Journal

Journal of thrombosis and thrombolysis
ISSN: 1573-742X
Titre abrégé: J Thromb Thrombolysis
Pays: Netherlands
ID NLM: 9502018

Informations de publication

Date de publication:
Feb 2021
Historique:
accepted: 30 10 2020
pubmed: 8 11 2020
medline: 26 10 2021
entrez: 7 11 2020
Statut: ppublish

Résumé

Platelet gene polymorphisms are associated with variable on-treatment platelet reactivity and vary by race. Whether differences in platelet reactivity and aspirin or ticagrelor exist between African-American and European-Americans remains poorly understood. Biological samples from three prior prospective antiplatelet challenge studies at the Duke Clinical Research Unit were used to compare platelet reactivity between African-American and European-American subjects. Platelet reactivity at baseline, on-aspirin, on-ticagrelor, and the treatment effect of aspirin or ticagrelor were compared between groups using an adjusted mixed effects model. Compared with European-Americans (n = 282; 50% female; mean ± standard deviation age, 50 ± 16), African-Americans (n = 209; 67% female; age 48 ± 12) had lower baseline platelet reactivity with platelet function analyzer-100 (PFA-100) (p < 0.01) and with light transmission aggregometry (LTA) in response to arachidonic acid (AA), adenosine diphosphate (ADP), and epinephrine agonists (p < 0.05). African-Americans had lower platelet reactivity on aspirin in response to ADP, epinephrine, and collagen (p < 0.05) and on ticagrelor in response to AA, ADP, and collagen (p < 0.05). The treatment effect of aspirin was greater in European-Americans with an AA agonist (p = 0.002). Between-race differences with in vitro aspirin mirrored those seen in vivo. The treatment effect of ticagrelor was greater in European-Americans in response to ADP (p < 0.05) but with collagen, the treatment effect was greater for African-Americans (p < 0.05). Platelet reactivity was overall lower in African-Americans off-treatment, on aspirin, and on ticagrelor. European-Americans experienced greater platelet suppression on aspirin and on ticagrelor. The aspirin response difference in vivo and in vitro suggests a mechanism intrinsic to the platelet. Whether the absolute level of platelet reactivity or the degree of platelet suppression after treatment is more important for clinical outcomes is uncertain.

Identifiants

pubmed: 33159252
doi: 10.1007/s11239-020-02327-w
pii: 10.1007/s11239-020-02327-w
pmc: PMC7889728
mid: NIHMS1644827
doi:

Substances chimiques

Platelet Aggregation Inhibitors 0
Ticagrelor GLH0314RVC
Aspirin R16CO5Y76E

Types de publication

Comparative Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

249-259

Subventions

Organisme : Duke-National University Singapore
ID : 2012/0003R
Organisme : National Institutes of General Medical Sciences
ID : 5RC1GM091083
Organisme : NHLBI NIH HHS
ID : R01 HL118049
Pays : United States
Organisme : NCBDD CDC HHS
ID : U01 DD000014
Pays : United States
Organisme : CDC HHS
ID : 5U01DD000014
Pays : United States
Organisme : NIGMS NIH HHS
ID : RC1 GM091083
Pays : United States
Organisme : NCRR NIH HHS
ID : UL1 RR024128
Pays : United States
Organisme : Foundation for the National Institutes of Health
ID : R01HL118049
Organisme : NCRR NIH HHS
ID : 5UL1RR024128
Pays : United States

Références

Patrono C, Morais J, Baigent C et al (2017) Antiplatelet agents for the treatment and prevention of coronary atherothrombosis. J Am Coll Cardiol 70(14):1760–1776
pubmed: 28958334 doi: 10.1016/j.jacc.2017.08.037
ISIS-2 (Second International Study of Infarct Survival) Collaborative Group (1988) Randomised trial of intravenous streptokinase, oral aspirin, both, or neither among 17,187 cases of suspected acute myocardial infarction: ISIS-2. Lancet 2(8607):349–360
Antithrombotic TC (2002) Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. BMJ 324(7329):71–86
doi: 10.1136/bmj.324.7329.71
Stone GW, Witzenbichler B, Weisz G et al (2013) Platelet reactivity and clinical outcomes after coronary artery implantation of drug-eluting stents (ADAPT-DES): a prospective multicentre registry study. Lancet 382(9892):614–623
pubmed: 23890998 doi: 10.1016/S0140-6736(13)61170-8
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(6):961–965
pubmed: 12651041 doi: 10.1016/S0735-1097(02)03014-0
Wenaweser P, Dorffler-Melly J, Imboden K et al (2005) Stent thrombosis is associated with an impaired response to antiplatelet therapy. J Am Coll Cardiol 45(11):1748–1752
pubmed: 15936599 doi: 10.1016/j.jacc.2005.01.058
Snoep JD, Hovens MM, Eikenboom JC, van der Bom JG, Huisman MV (2007) Association of laboratory-defined aspirin resistance with a higher risk of recurrent cardiovascular events: a systematic review and meta-analysis. Arch Intern Med 167(15):1593–1599
pubmed: 17698681 doi: 10.1001/archinte.167.15.1593
Cuisset T, Cayla G, Frere C et al (2009) Predictive value of post-treatment platelet reactivity for occurrence of post-discharge bleeding after non-ST elevation acute coronary syndrome Shifting from antiplatelet resistance to bleeding risk assessment? EuroIntervention 5(3):325–329
pubmed: 19736156 doi: 10.4244/51
Tantry US, Bonello L, Aradi D et al (2013) Consensus and update on the definition of on-treatment platelet reactivity to adenosine diphosphate associated with ischemia and bleeding. J Am Coll Cardiol 62(24):2261–2273
pubmed: 24076493 doi: 10.1016/j.jacc.2013.07.101
Aradi D, Kirtane A, Bonello L et al (2015) Bleeding and stent thrombosis on P2Y12-inhibitors: collaborative analysis on the role of platelet reactivity for risk stratification after percutaneous coronary intervention. Eur Heart J 36(27):1762–1771
pubmed: 25896078 doi: 10.1093/eurheartj/ehv104
Faraday N, Yanek LR, Mathias R et al (2007) Heritability of platelet responsiveness to aspirin in activation pathways directly and indirectly related to cyclooxygenase-1. Circulation 115(19):2490–2496
pubmed: 17470694 doi: 10.1161/CIRCULATIONAHA.106.667584
Frelinger AL 3rd, Furman MI, Linden MD et al (2006) Residual arachidonic acid-induced platelet activation via an adenosine diphosphate-dependent but cyclooxygenase-1- and cyclooxygenase-2-independent pathway: a 700-patient study of aspirin resistance. Circulation 113(25):2888–2896
pubmed: 16785341 doi: 10.1161/CIRCULATIONAHA.105.596627
Verdoia M, Sartori C, Pergolini P et al (2016) Prevalence and predictors of high-on treatment platelet reactivity with ticagrelor in ACS patients undergoing stent implantation. Vasc Pharmacol 77:48–53
doi: 10.1016/j.vph.2015.04.014
Siller-Matula JM, Akca B, Neunteufl T et al (2016) Inter-patient variability of platelet reactivity in patients treated with prasugrel and ticagrelor. Platelets 27(4):373–377
pubmed: 26555925 doi: 10.3109/09537104.2015.1095874
Yee DL, Sun CW, Bergeron AL, Dong JF, Bray PF (2005) Aggregometry detects platelet hyperreactivity in healthy individuals. Blood 106(8):2723–2729
pubmed: 15972447 pmcid: 1634759 doi: 10.1182/blood-2005-03-1290
Gaxiola B, Friedl W, Propping P (1984) Epinephrine-induced platelet aggregation. A twin study. Clin Genet 26(6):543–548
pubmed: 6541984 doi: 10.1111/j.1399-0004.1984.tb01101.x
O’Donnell CJ, Larson MG, Feng D et al (2001) Genetic and environmental contributions to platelet aggregation: the Framingham heart study. Circulation 103(25):3051–3056
pubmed: 11425767 doi: 10.1161/01.CIR.103.25.3051
Bray PF, Mathias RA, Faraday N et al (2007) Heritability of platelet function in families with premature coronary artery disease. J Thromb Haemost 5(8):1617–1623
pubmed: 17663734 doi: 10.1111/j.1538-7836.2007.02618.x
Edelstein LC, Simon LM, Montoya RT et al (2013) Racial differences in human platelet PAR4 reactivity reflect expression of PCTP and miR-376c. Nat Med 19(12):1609–1616
pubmed: 24216752 pmcid: 3855898 doi: 10.1038/nm.3385
Kim HO, Jin Y, Kickler TS, Blakemore K, Kwon OH, Bray PF (1995) Gene frequencies of the five major human platelet antigens in African-American, white, and Korean populations. Transfusion 35(10):863–867
pubmed: 7570918 doi: 10.1046/j.1537-2995.1995.351096026369.x
Ramsey G, Salamon DJ (1986) Frequency of PLA1 in blacks. Transfusion 26(6):531–532
pubmed: 3775837 doi: 10.1046/j.1537-2995.1986.26687043619.x
Ulrich CM, Carlson CS, Sibert J et al (2005) Thromboxane synthase (TBXAS1) polymorphisms in African-American and Caucasian populations: evidence for selective pressure. Hum Mutat 26(4):394–395
pubmed: 16134166 doi: 10.1002/humu.9371
Weng Z, Li X, Li Y, Lin J, Peng F, Niu W (2013) The association of four common polymorphisms from four candidate genes (COX-1, COX-2, ITGA2B, ITGA2) with aspirin insensitivity: a meta-analysis. PLoS ONE 8(11):e78093
pubmed: 24244288 pmcid: 3828324 doi: 10.1371/journal.pone.0078093
Wallentin L, Becker RC, Budaj A et al (2009) Ticagrelor versus clopidogrel in patients with acute coronary syndromes. N Engl J Med 361(11):1045–1057
pubmed: 19717846 doi: 10.1056/NEJMoa0904327
Alexopoulos D, Xanthopoulou I, Gkizas V et al (2012) Randomized assessment of ticagrelor versus prasugrel antiplatelet effects in patients with ST-segment-elevation myocardial infarction. Circ Cardiovasc Interv 5(6):797–804
pubmed: 23169985 doi: 10.1161/CIRCINTERVENTIONS.112.972323
Parodi G, Valenti R, Bellandi B et al (2013) Comparison of prasugrel and ticagrelor loading doses in ST-segment elevation myocardial infarction patients: RAPID (Rapid Activity of Platelet Inhibitor Drugs) primary PCI study. J Am Coll Cardiol 61(15):1601–1606
pubmed: 23500251 doi: 10.1016/j.jacc.2013.01.024
Ibrahim K, Christoph M, Schmeinck S et al (2014) High rates of prasugrel and ticagrelor non-responder in patients treated with therapeutic hypothermia after cardiac arrest. Resuscitation 85(5):649–656
pubmed: 24555950 doi: 10.1016/j.resuscitation.2014.02.004
Vang JJ, Nilsson L, Berntsson P et al (2009) Ticagrelor binds to human P2Y(12) independently from ADP but antagonizes ADP-induced receptor signaling and platelet aggregation. J Thromb Haemost 7(9):1556–1565
doi: 10.1111/j.1538-7836.2009.03527.x
Wadowski PP, Eichelberger B, Kopp CW et al (2017) Disaggregation following agonist-induced platelet activation in patients on dual antiplatelet therapy. J Cardiovasc Transl Res 10(4):359–367
pubmed: 28425039 pmcid: 5585279 doi: 10.1007/s12265-017-9746-0
Elwood PC, Cochrane AL, Burr ML et al (1974) A randomized controlled trial of acetyl salicylic acid in the secondary prevention of mortality from myocardial infarction. Br Med J 1(5905):436–440
pubmed: 4593555 pmcid: 1633246 doi: 10.1136/bmj.1.5905.436
The RISC Group (1990) Risk of myocardial infarction and death during treatment with low dose aspirin and intravenous heparin in men with unstable coronary artery disease. Lancet 336(8719):827–830
doi: 10.1016/0140-6736(90)92336-G
Ford ES (2013) Trends in predicted 10-year risk of coronary heart disease and cardiovascular disease among U.S. adults from 1999 to 2010. J Am Coll Cardiol 61(22):2249–2252
pubmed: 23563124 pmcid: 4571185 doi: 10.1016/j.jacc.2013.03.023
Mozaffarian D, Benjamin EJ, Go AS et al (2015) Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation 131(4):e29-322
pubmed: 25520374
Albright KC, Huang L, Blackburn J et al (2018) Racial differences in recurrent ischemic stroke risk and recurrent stroke case fatality. Neurology 91(19):e1741–e1750
pubmed: 30282770 pmcid: 6251602 doi: 10.1212/WNL.0000000000006467
Voora D, Ortel TL, Lucas JE et al (2012) Time-dependent changes in non-COX-1-dependent platelet function with daily aspirin therapy. J Thromb Thrombolysis 33(3):246–257
pubmed: 22294277 pmcid: 3337886 doi: 10.1007/s11239-012-0683-0
Ortel TL, James AH, Thames EH et al (2000) Assessment of primary hemostasis by PFA-100 analysis in a tertiary care center. Thromb Haemost 84(1):93–97
pubmed: 10928477
Valenti R, Cantini G, Marcucci R et al (2015) Prognostic impact of high residual platelet reactivity after chronic total occlusion percutaneous coronary intervention in patients with diabetes mellitus. Int J Cardiol 201:561–567
pubmed: 26334380 doi: 10.1016/j.ijcard.2015.04.052
Meade TW, Vickers MV, Thompson SG, Stirling Y, Haines AP, Miller GJ (1985) Epidemiological characteristics of platelet aggregability. Br Med J (Clin Res Ed) 290(6466):428–432
doi: 10.1136/bmj.290.6466.428
Trip MD, Cats VM, van Capelle FJ, Vreeken J (1990) Platelet hyperreactivity and prognosis in survivors of myocardial infarction. N Engl J Med 322(22):1549–1554
pubmed: 2336086 doi: 10.1056/NEJM199005313222201
Thaulow E, Erikssen J, Sandvik L, Stormorken H, Cohn PF (1991) Blood platelet count and function are related to total and cardiovascular death in apparently healthy men. Circulation 84(2):613–617
pubmed: 1860204 doi: 10.1161/01.CIR.84.2.613
Terres W, Lund GK, Hubner A, Ehlert A, Reuter H, Hamm CW (1995) Endogenous tissue plasminogen activator and platelet reactivity as risk factors for reocclusion after recanalization of chronic total coronary occlusions. Am Heart J 130(4):711–716
pubmed: 7572577 doi: 10.1016/0002-8703(95)90068-3
Elwood PC, Renaud S, Beswick AD, O’Brien JR, Sweetnam PM (1998) Platelet aggregation and incident ischaemic heart disease in the Caerphilly cohort. Heart 80(6):578–582
pubmed: 10065026 pmcid: 1728885 doi: 10.1136/hrt.80.6.578
Meade TW, Cooper JA, Miller GJ (1997) Platelet counts and aggregation measures in the incidence of ischaemic heart disease (IHD). Thromb Haemost 78(2):926–929
pubmed: 9268196 doi: 10.1055/s-0038-1657653
Gaglia MA Jr, Lipinski MJ, Lhermusier T et al (2017) Comparison of platelet reactivity in black versus white patients with acute coronary syndromes after treatment with ticagrelor. Am J Cardiol 119(8):1135–1140
pubmed: 28202132 doi: 10.1016/j.amjcard.2017.01.002
Husted S, van Giezen JJ (2009) Ticagrelor: the first reversibly binding oral P2Y1P2Y12 receptor antagonist. Cardiovasc Ther 27(4):259–274
pubmed: 19604248 doi: 10.1111/j.1755-5922.2009.00096.x
Zhao P, Metcalf M, Bunnett NW (2014) Biased signaling of protease-activated receptors. Front Endocrinol (Lausanne) 5:67
doi: 10.3389/fendo.2014.00067
Tourdot BE, Conaway S, Niisuke K, Edelstein LC, Bray PF, Holinstat M (2014) Mechanism of race-dependent platelet activation through the protease-activated receptor-4 and Gq signaling axis. Arterioscler Thromb Vasc Biol 34(12):2644–2650
pubmed: 25278289 pmcid: 4239175 doi: 10.1161/ATVBAHA.114.304249
Thomas KL, Honeycutt E, Shaw LK, Peterson ED (2010) Racial differences in long-term survival among patients with coronary artery disease. Am Heart J 160(4):744–751
pubmed: 20934570 doi: 10.1016/j.ahj.2010.06.014
Fernandez-Jimenez R, Wang TJ, Fuster V, Blot WJ (2019) Low-dose aspirin for primary prevention of cardiovascular disease: use patterns and impact across race and ethnicity in the southern community cohort study. J Am Heart Assoc 8(24):e013404
pubmed: 31822218 pmcid: 6951082 doi: 10.1161/JAHA.119.013404
Collins SD, Torguson R, Gaglia MA Jr et al (2010) Does black ethnicity influence the development of stent thrombosis in the drug-eluting stent era? Circulation 122(11):1085–1090
pubmed: 20805432 doi: 10.1161/CIRCULATIONAHA.109.907998
Urban P, Mehran R, Colleran R et al (2019) Defining high bleeding risk in patients undergoing percutaneous coronary intervention. Circulation 140(3):240–261
pubmed: 31116032 pmcid: 6636810 doi: 10.1161/CIRCULATIONAHA.119.040167
Casto AM, Feldman MW (2011) Genome-wide association study SNPs in the human genome diversity project populations: does selection affect unlinked SNPs with shared trait associations? PLoS Genet 7(1):e1001266
pubmed: 21253569 pmcid: 3017115 doi: 10.1371/journal.pgen.1001266
Tourdot BE, Stoveken H, Trumbo D et al (2018) Genetic variant in human PAR (protease-activated receptor) 4 enhances thrombus formation resulting in resistance to antiplatelet therapeutics. Arterioscler Thromb Vasc Biol 38(7):1632–1643
pubmed: 29748334 pmcid: 6023764 doi: 10.1161/ATVBAHA.118.311112
Edelstein LC, Simon LM, Lindsay CR et al (2014) Common variants in the human platelet PAR4 thrombin receptor alter platelet function and differ by race. Blood 124(23):3450–3458
pubmed: 25293779 pmcid: 4246040 doi: 10.1182/blood-2014-04-572479
Faraday N, Yanek LR, Yang XP et al (2011) Identification of a specific intronic PEAR1 gene variant associated with greater platelet aggregability and protein expression. Blood 118(12):3367–3375
pubmed: 21791418 pmcid: 3179402 doi: 10.1182/blood-2010-11-320788
Qayyum R, Becker LC, Becker DM et al (2015) Genome-wide association study of platelet aggregation in African-Americans. BMC Genet 16:58
pubmed: 26024889 pmcid: 4448541 doi: 10.1186/s12863-015-0217-9
Kambayashi J, Shinoki N, Nakamura T et al (1996) Prevalence of impaired responsiveness to epinephrine in platelets among Japanese. Thromb Res 81(1):85–90
pubmed: 8747523 doi: 10.1016/0049-3848(95)00216-2
Siffert W, Forster P, Jockel KH et al (1999) Worldwide ethnic distribution of the G protein beta3 subunit 825T allele and its association with obesity in European-American, Chinese, and Black African individuals. J Am Soc Nephrol 10(9):1921–1930
pubmed: 10477144
Dusse F, Frey UH, Bilalic A et al (2012) The GNB3 C825T polymorphism influences platelet aggregation in human whole blood. Pharmacogenet Genom 22(1):43–49
doi: 10.1097/FPC.0b013e32834e1674
Yee DL, Bergeron AL, Sun CW, Dong JF, Bray PF (2006) Platelet hyperreactivity generalizes to multiple forms of stimulation. J Thromb Haemost 4(9):2043–2050
pubmed: 16961612 doi: 10.1111/j.1538-7836.2006.02089.x
Naber C, Hermann BL, Vietzke D et al (2000) Enhanced epinephrine-induced platelet aggregation in individuals carrying the G protein beta3 subunit 825T allele. FEBS Lett 484(3):199–201
pubmed: 11078878 doi: 10.1016/S0014-5793(00)02158-X
Strisciuglio T, Franco D, Di Gioia G et al (2018) Impact of genetic polymorphisms on platelet function and response to anti platelet drugs. Cardiovasc Diagn Ther 8(5):610–620
pubmed: 30498685 pmcid: 6232354 doi: 10.21037/cdt.2018.05.06
Morange PE, Simon C, Alessi MC et al (2004) Endothelial cell markers and the risk of coronary heart disease: the Prospective Epidemiological Study of Myocardial Infarction (PRIME) study. Circulation 109(11):1343–1348
pubmed: 15023872 doi: 10.1161/01.CIR.0000120705.55512.EC
Conlan MG, Folsom AR, Finch A et al (1993) Associations of factor VIII and von Willebrand factor with age, race, sex, and risk factors for atherosclerosis. The Atherosclerosis Risk in Communities (ARIC) Study. Thromb Haemost 70(3):380–385
pubmed: 8259533 doi: 10.1055/s-0038-1649589
Folsom AR, Aleksic N, Sanhueza A, Boerwinkle E (2009) Risk factor correlates of platelet and leukocyte markers assessed by flow cytometry in a population-based sample. Atherosclerosis 205(1):272–278
pubmed: 19124123 doi: 10.1016/j.atherosclerosis.2008.11.005
Lev EI, Bliden KP, Jeong YH et al (2014) Influence of race and sex on thrombogenicity in a large cohort of coronary artery disease patients. J Am Heart Assoc 3(5):e001167
pubmed: 25332180 pmcid: 4323822 doi: 10.1161/JAHA.114.001167
Wilson JF, Weale ME, Smith AC et al (2001) Population genetic structure of variable drug response. Nat Genet 29(3):265–269
pubmed: 11685208 doi: 10.1038/ng761
Rosenberg NA, Pritchard JK, Weber JL et al (2002) Genetic structure of human populations. Science 298(5602):2381–2385
pubmed: 12493913 doi: 10.1126/science.1078311
Tang H, Quertermous T, Rodriguez B et al (2005) Genetic structure, self-identified race/ethnicity, and confounding in case-control association studies. Am J Hum Genet 76(2):268–275
pubmed: 15625622 doi: 10.1086/427888
Carson P, Ziesche S, Johnson G, Cohn JN (1999) Racial differences in response to therapy for heart failure: analysis of the vasodilator-heart failure trials. Vasodilator-Heart Failure Trial Study Group. J Card Fail 5(3):178–187
pubmed: 10496190 doi: 10.1016/S1071-9164(99)90001-5
Jamerson K, DeQuattro V (1996) The impact of ethnicity on response to antihypertensive therapy. Am J Med 101(3A):22S-32S
pubmed: 8876472 doi: 10.1016/S0002-9343(96)00265-3
Ramamoorthy A, Pacanowski MA, Bull J, Zhang L (2015) Racial/ethnic differences in drug disposition and response: review of recently approved drugs. Clin Pharmacol Ther 97(3):263–273
pubmed: 25669658 doi: 10.1002/cpt.61
Teng R, Butler K (2014) Pharmacokinetics, pharmacodynamics, and tolerability of single and multiple doses of ticagrelor in Japanese and European-American volunteers. Int J Clin Pharmacol Ther 52(6):478–491
pubmed: 24755129 doi: 10.5414/CP202017

Auteurs

Margaret Infeld (M)

Division of Cardiology, Department of Medicine, Larner College of Medicine, University of Vermont, Burlington, VT, USA.

Kevin A Friede (KA)

Division of Cardiology, Department of Medicine, Duke University, Durham, NC, USA.

Tan Ru San (TR)

Department of Cardiology, National Heart Centre, Singapore, Singapore.

Holly J Knickerbocker (HJ)

Center for Applied Genomics & Precision Medicine, Duke University, 2187 CIEMAS, Campus Box 3382, Durham, NC, 27708, USA.

Geoffrey S Ginsburg (GS)

Center for Applied Genomics & Precision Medicine, Duke University, 2187 CIEMAS, Campus Box 3382, Durham, NC, 27708, USA.
Division of Cardiology, Department of Medicine, Duke University, Durham, NC, USA.

Thomas L Ortel (TL)

Division of Hematology, Duke University, Durham, NC, USA.

Deepak Voora (D)

Center for Applied Genomics & Precision Medicine, Duke University, 2187 CIEMAS, Campus Box 3382, Durham, NC, 27708, USA. deepak.voora@duke.edu.
Division of Cardiology, Department of Medicine, Duke University, Durham, NC, USA. deepak.voora@duke.edu.

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