Is atrial fibrillation in HFpEF a distinct phenotype? Insights from multiparametric MRI and circulating biomarkers.

Atrial fibrillation Biomarkers Cardiovascular magnetic resonance Cluster analysis Heart failure Phenotype

Journal

BMC cardiovascular disorders
ISSN: 1471-2261
Titre abrégé: BMC Cardiovasc Disord
Pays: England
ID NLM: 100968539

Informations de publication

Date de publication:
07 Feb 2024
Historique:
received: 29 06 2023
accepted: 17 01 2024
medline: 8 2 2024
pubmed: 8 2 2024
entrez: 7 2 2024
Statut: epublish

Résumé

Heart failure with preserved ejection fraction (HFpEF) and atrial fibrillation (AF) frequently co-exist. There is a limited understanding on whether this coexistence is associated with distinct alterations in myocardial remodelling and mechanics. We aimed to determine if patients with atrial fibrillation (AF) and heart failure with preserved ejection fraction (HFpEF) represent a distinct phenotype. In this secondary analysis of adults with HFpEF (NCT03050593), participants were comprehensively phenotyped with stress cardiac MRI, echocardiography and plasma fibroinflammatory biomarkers, and were followed for the composite endpoint (HF hospitalisation or death) at a median of 8.5 years. Those with AF were compared to sinus rhythm (SR) and unsupervised cluster analysis was performed to explore possible phenotypes. 136 subjects were included (SR = 75, AF = 61). The AF group was older (76 ± 8 vs. 70 ± 10 years) with less diabetes (36% vs. 61%) compared to the SR group and had higher left atrial (LA) volumes (61 ± 30 vs. 39 ± 15 mL/m Presence of AF in HFpEF is associated with cardiac structural and functional changes together with altered expression of several fibro-inflammatory biomarkers. Distinct phenotypes exist in HFpEF which may have differing clinical outcomes.

Sections du résumé

BACKGROUND BACKGROUND
Heart failure with preserved ejection fraction (HFpEF) and atrial fibrillation (AF) frequently co-exist. There is a limited understanding on whether this coexistence is associated with distinct alterations in myocardial remodelling and mechanics. We aimed to determine if patients with atrial fibrillation (AF) and heart failure with preserved ejection fraction (HFpEF) represent a distinct phenotype.
METHODS METHODS
In this secondary analysis of adults with HFpEF (NCT03050593), participants were comprehensively phenotyped with stress cardiac MRI, echocardiography and plasma fibroinflammatory biomarkers, and were followed for the composite endpoint (HF hospitalisation or death) at a median of 8.5 years. Those with AF were compared to sinus rhythm (SR) and unsupervised cluster analysis was performed to explore possible phenotypes.
RESULTS RESULTS
136 subjects were included (SR = 75, AF = 61). The AF group was older (76 ± 8 vs. 70 ± 10 years) with less diabetes (36% vs. 61%) compared to the SR group and had higher left atrial (LA) volumes (61 ± 30 vs. 39 ± 15 mL/m
CONCLUSIONS CONCLUSIONS
Presence of AF in HFpEF is associated with cardiac structural and functional changes together with altered expression of several fibro-inflammatory biomarkers. Distinct phenotypes exist in HFpEF which may have differing clinical outcomes.

Identifiants

pubmed: 38326736
doi: 10.1186/s12872-024-03734-0
pii: 10.1186/s12872-024-03734-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

94

Informations de copyright

© 2024. The Author(s).

Références

Samson R, Jaiswal A, Ennezat PV, Cassidy M, Jemtel THL. Clinical phenotypes in heart failure with preserved ejection fraction. J Am Heart Assoc. 2016;5:e002477. https://doi.org/10.1161/JAHA.115.002477 .
doi: 10.1161/JAHA.115.002477 pubmed: 26811159 pmcid: 4859363
Tromp J, Ouwerkerk W, Demissei BG, et al. Novel endotypes in heart failure: effects on guideline-directed medical therapy. Eur Heart J. 2018;39:4269–76. https://doi.org/10.1093/eurheartj/ehy712 .
doi: 10.1093/eurheartj/ehy712 pubmed: 30551207
Zakeri R, Chamberlain AM, Roger VL, Redfield MM. Temporal relationship and prognostic significance of atrial fibrillation in heart failure patients with preserved ejection fraction: a community-based study. Circulation. 2013;128:1085–93. https://doi.org/10.1161/circulationaha.113.001475 .
doi: 10.1161/circulationaha.113.001475 pubmed: 23908348 pmcid: 3910441
Reddy YNV, Carter RE, Obokata M, Redfield MM, Borlaug BA. A simple, evidence-based approach to help guide diagnosis of heart failure with preserved ejection fraction. Circulation. 2018;138:861–70. https://doi.org/10.1161/CIRCULATIONAHA.118.034646 .
doi: 10.1161/CIRCULATIONAHA.118.034646 pubmed: 29792299 pmcid: 6202181
Kao DP, Lewsey JD, Anand IS, et al. Characterization of subgroups of heart failure patients with preserved ejection fraction with possible implications for prognosis and treatment response. Eur J Heart Fail. 2015;17:925–35. https://doi.org/10.1002/ejhf.327 .
doi: 10.1002/ejhf.327 pubmed: 26250359
Zafrir B, Lund LH, Laroche C, et al. Prognostic implications of atrial fibrillation in heart failure with reduced, mid-range, and preserved ejection fraction: a report from 14 964 patients in the European Society of Cardiology Heart Failure Long-Term Registry. Eur Heart J. 2018;39:4277–84. https://doi.org/10.1093/eurheartj/ehy626 .
doi: 10.1093/eurheartj/ehy626 pubmed: 30325423
Sartipy U, Dahlström U, Fu M, Lund LH. Atrial fibrillation in heart failure with preserved, mid-range, and reduced ejection fraction. JACC: Heart Fail. 2017;5:565–74. https://doi.org/10.1016/j.jchf.2017.05.001 .
doi: 10.1016/j.jchf.2017.05.001 pubmed: 28711451
Santema BT, Kloosterman M, Van Gelder IC, et al. Comparing biomarker profiles of patients with heart failure: atrial fibrillation vs. sinus rhythm and reduced vs. preserved ejection fraction. Eur Heart J. 2018;39:3867–75. https://doi.org/10.1093/eurheartj/ehy421 .
doi: 10.1093/eurheartj/ehy421 pubmed: 30137304
Packer M, Lam CSP, Lund LH, Redfield MM. Interdependence of atrial fibrillation and heart failure with a preserved ejection fraction reflects a common underlying atrial and ventricular myopathy. Circulation. 2020;141:4–6. https://doi.org/10.1161/CIRCULATIONAHA.119.042996 .
doi: 10.1161/CIRCULATIONAHA.119.042996 pubmed: 31887078
Galli E, Bourg C, Kosmala W, Oger E, Donal E. Phenomapping heart failure with preserved ejection fraction using machine learning cluster analysis: prognostic and therapeutic implications. Heart Fail Clin. 2021;17:499–518. https://doi.org/10.1016/j.hfc.2021.02.010 .
doi: 10.1016/j.hfc.2021.02.010 pubmed: 34051979
Ripley DP, Musa TA, Dobson LE, Plein S, Greenwood JP. Cardiovascular magnetic resonance imaging: what the general cardiologist should know. Heart. 2016;102:1589–603. https://doi.org/10.1136/heartjnl-2015-307896 .
doi: 10.1136/heartjnl-2015-307896 pubmed: 27559093
Arnold JR, Kanagala P, Budgeon CA, et al. Prevalence and prognostic significance of microvascular dysfunction in heart failure with preserved ejection fraction. JACC Cardiovasc Imaging. 2022;15(6):1001–11. https://doi.org/10.1016/j.jcmg.2021.11.022 .
doi: 10.1016/j.jcmg.2021.11.022 pubmed: 35033490
Chamsi-Pasha MA, Zhan Y, Debs D, Shah DJ. CMR in the evaluation of diastolic dysfunction and phenotyping of HFpEF: current role and future perspectives. JACC Cardiovasc Imaging. 2020;13:283–96. https://doi.org/10.1016/j.jcmg.2019.02.031 .
doi: 10.1016/j.jcmg.2019.02.031 pubmed: 31202753
Schönbauer R, Duca F, Kammerlander AA, et al. Persistent atrial fibrillation in heart failure with preserved ejection fraction: prognostic relevance and association with clinical, imaging and invasive haemodynamic parameters. Eur J Clin Investig. 2020;50:e13184. https://doi.org/10.1111/eci.13184 .
doi: 10.1111/eci.13184
Schönbauer R, Kammerlander AA, Duca F, et al. Prognostic impact of left atrial function in heart failure with preserved ejection fraction in sinus rhythm vs. persistent atrial fibrillation. ESC Heart Fail. 2022;9:465–75. https://doi.org/10.1002/ehf2.13723 .
doi: 10.1002/ehf2.13723 pubmed: 34866363
Kanagala P, Cheng ASH, Singh A, et al. Relationship between focal and diffuse fibrosis assessed by CMR and clinical outcomes in heart failure with preserved ejection fraction. JACC Cardiovasc Imaging. 2019;12:2291–301. https://doi.org/10.1016/j.jcmg.2018.11.031 .
doi: 10.1016/j.jcmg.2018.11.031 pubmed: 30772227
Kanagala P, Arnold JR, Singh A, et al. Prevalence of right ventricular dysfunction and prognostic significance in heart failure with preserved ejection fraction. Int J Cardiovasc Imaging. 2021;37:255–66. https://doi.org/10.1007/s10554-020-01953-y .
doi: 10.1007/s10554-020-01953-y pubmed: 32737707
Singh A, Chan DCS, Greenwood JP, et al. Symptom onset in aortic stenosis: relation to sex differences in left ventricular remodeling. JACC Cardiovasc Imaging. 2019;12:96–105. https://doi.org/10.1016/j.jcmg.2017.09.019 .
doi: 10.1016/j.jcmg.2017.09.019 pubmed: 29248646
Napier R, McNulty SE, Eton DT, et al. Comparing measures to assess health-related quality of life in heart failure with preserved ejection fraction. JACC Heart Fail. 2018;6:552–60. https://doi.org/10.1016/j.jchf.2018.02.006 .
doi: 10.1016/j.jchf.2018.02.006 pubmed: 29885952 pmcid: 6026057
Picard MH, Adams D, Bierig SM, et al. American Society of Echocardiography recommendations for quality echocardiography laboratory operations. J Am Soc Echocardiogr. 2011;24:1–10. https://doi.org/10.1016/j.echo.2010.11.006 .
doi: 10.1016/j.echo.2010.11.006 pubmed: 21172594
Singh A, Horsfield MA, Bekele S, et al. Myocardial T1 and extracellular volume fraction measurement in asymptomatic patients with aortic stenosis: reproducibility and comparison with age-matched controls. Eur Heart J Cardiovasc Imaging. 2015;16:763–70. https://doi.org/10.1093/ehjci/jev007 .
doi: 10.1093/ehjci/jev007 pubmed: 25680382
Gulsin GS, Henson J, Brady EM, et al. Cardiovascular determinants of aerobic exercise capacity in adults with type 2 diabetes. Diabetes Care. 2020;43:2248–56. https://doi.org/10.2337/dc20-0706 .
doi: 10.2337/dc20-0706 pubmed: 32680830 pmcid: 7440912
Flachskampf FA, Biering-Sørensen T, Solomon SD, et al. Cardiac imaging to evaluate left ventricular diastolic function. JACC Cardiovasc Imaging. 2015;8:1071–93. https://doi.org/10.1016/j.jcmg.2015.07.004 .
doi: 10.1016/j.jcmg.2015.07.004 pubmed: 26381769
Haaf P, Garg P, Messroghli DR, et al. Cardiac T1 mapping and extracellular volume (ECV) in clinical practice: a comprehensive review. J Cardiovasc Magn Reson. 2016;18:89. https://doi.org/10.1186/s12968-016-0308-4 .
doi: 10.1186/s12968-016-0308-4 pubmed: 27899132 pmcid: 5129251
Lloyd S. Least squares quantization in PCM. IEEE Trans Inf Theory. 1982;28:129–37. https://doi.org/10.1109/TIT.1982.1056489 .
doi: 10.1109/TIT.1982.1056489
van Buuren S, Groothuis-Oudshoorn K. Mice: multivariate imputation by chained equations in R. J Stat Softw. 2011;45:1–67. https://doi.org/10.18637/jss.v045.i03 .
doi: 10.18637/jss.v045.i03
Alghofaili Y. Interpretable K-Means: Clusters Feature Importances. Understand your K-Means clusters by extracting each cluster’s most important features. https://towardsdatascience.com/interpretable-k-means-clusters-feature-importances-7e516eeb8d3c (2022).
Claus P, Omar AMS, Pedrizzetti G, Sengupta PP, Nagel E. Tissue tracking Technology for Assessing Cardiac Mechanics: principles, Normal values, and clinical applications. JACC Cardiovasc Imaging. 2015;8:1444–60. https://doi.org/10.1016/j.jcmg.2015.11.001 .
doi: 10.1016/j.jcmg.2015.11.001 pubmed: 26699113
DeVore AD, McNulty S, Alenezi F, et al. Impaired left ventricular global longitudinal strain in patients with heart failure with preserved ejection fraction: insights from the RELAX trial. Eur J Heart Fail. 2017;19:893–900. https://doi.org/10.1002/ejhf.754 .
doi: 10.1002/ejhf.754 pubmed: 28194841
Augustine D, Lewandowski AJ, Lazdam M, et al. Global and regional left ventricular myocardial deformation measures by magnetic resonance feature tracking in healthy volunteers: comparison with tagging and relevance of gender. J Cardiovasc Magn Reson. 2013;15:8. https://doi.org/10.1186/1532-429X-15-8 .
doi: 10.1186/1532-429X-15-8 pubmed: 23331550 pmcid: 3621526
Schuster A, Morton G, Hussain ST, et al. The intra-observer reproducibility of cardiovascular magnetic resonance myocardial feature tracking strain assessment is independent of field strength. Eur J Radiol. 2013;82:296–301. https://doi.org/10.1016/j.ejrad.2012.11.012 .
doi: 10.1016/j.ejrad.2012.11.012 pubmed: 23246014
Morton G, Schuster A, Jogiya R, et al. Inter-study reproducibility of cardiovascular magnetic resonance myocardial feature tracking. J Cardiovasc Magn Reson. 2012;14:43. https://doi.org/10.1186/1532-429X-14-43 .
doi: 10.1186/1532-429X-14-43 pubmed: 22721175 pmcid: 3461471
Ayton SL, Alfuhied A, Gulsin GS, et al. The Interfield strength agreement of left ventricular strain measurements at 1.5 T and 3 T using cardiac MRI feature tracking. J Magn Reson Imaging. 2022;57:1250–61. https://doi.org/10.1002/jmri.28328 .
doi: 10.1002/jmri.28328 pubmed: 35767224
Nazir SA, Shetye AM, Khan JN, et al. Inter-study repeatability of circumferential strain and diastolic strain rate by CMR tagging, feature tracking and tissue tracking in ST-segment elevation myocardial infarction. Int J Cardiovasc Imaging. 2020;36:1133–46. https://doi.org/10.1007/s10554-020-01806-8 .
doi: 10.1007/s10554-020-01806-8 pubmed: 32152811 pmcid: 7228913
Iwano H, Pu M, Upadhya B, et al. Delay of left ventricular longitudinal expansion with diastolic dysfunction: impact on load dependence of e′ and longitudinal strain rate. Physiol Rep. 2014;2:e12082. https://doi.org/10.14814/phy2.12082 .
doi: 10.14814/phy2.12082 pubmed: 25035279 pmcid: 4187544
van Grootel RWJ, Kauling RM, Menting ME, et al. Influence of age and sex on left ventricular diastolic strain analysis. Int J Cardiovasc Imaging. 2019;35:491–8. https://doi.org/10.1007/s10554-018-1480-4 .
doi: 10.1007/s10554-018-1480-4 pubmed: 30377894
Vinereanu D, Nicolaides E, Tweddel AC, Fraser AG. "Pure" diastolic dysfunction is associated with long-axis systolic dysfunction. Implications for the diagnosis and classification of heart failure. Eur J Heart Fail. 2005;7:820–8. https://doi.org/10.1016/j.ejheart.2005.02.003 .
doi: 10.1016/j.ejheart.2005.02.003 pubmed: 15921957
Diao S-L, Xu H-P, Zhang B, Ma B-X, Liu X-L. Associations of MMP-2, BAX, and Bcl-2 mRNA and protein expressions with development of atrial fibrillation. Med Sci Monit. 2016;22:1497–507. https://doi.org/10.12659/msm.895715 .
doi: 10.12659/msm.895715 pubmed: 27141955 pmcid: 4915330
de Boer RA, De Keulenaer G, Bauersachs J, et al. Towards better definition, quantification and treatment of fibrosis in heart failure. A scientific roadmap by the Committee of Translational Research of the heart failure association (HFA) of the European Society of Cardiology. Eur J Heart Fail. 2019;21:272–85. https://doi.org/10.1002/ejhf.1406 .
doi: 10.1002/ejhf.1406 pubmed: 30714667
Krebber MM, van Dijk CGM, Vernooij RWM, et al. Matrix Metalloproteinases and tissue inhibitors of Metalloproteinases in extracellular matrix remodeling during left ventricular diastolic dysfunction and heart failure with preserved ejection fraction: a systematic review and Meta-analysis. Int J Mol Sci. 2020;21:6742. https://doi.org/10.3390/ijms21186742 .
doi: 10.3390/ijms21186742 pubmed: 32937927 pmcid: 7555240
DeCoux A, Lindsey ML, Villarreal F, Garcia RA, Schulz R. Myocardial matrix metalloproteinase-2: inside out and upside down. J Mol Cell Cardiol. 2014;77:64–72. https://doi.org/10.1016/j.yjmcc.2014.09.016 .
doi: 10.1016/j.yjmcc.2014.09.016 pubmed: 25261607
Ali MAM, Cho WJ, Hudson B, et al. Titin is a target of matrix Metalloproteinase-2. Circulation. 2010;122:2039–47. https://doi.org/10.1161/CIRCULATIONAHA.109.930222 .
doi: 10.1161/CIRCULATIONAHA.109.930222 pubmed: 21041693 pmcid: 3057897
Freestone B, Chong AY, Lim HS, Blann A, Lip GYH. Angiogenic factors in atrial fibrillation: a possible role in thrombogenesis? Ann Med. 2005;37:365–72. https://doi.org/10.1080/07853890510037392 .
doi: 10.1080/07853890510037392 pubmed: 16179272
Tsai Y-C, Lee C-S, Chiu Y-W, et al. Angiopoietin-2, Angiopoietin-1 and subclinical cardiovascular disease in chronic kidney disease. Sci Rep. 2016;6:39400. https://doi.org/10.1038/srep39400 .
doi: 10.1038/srep39400 pubmed: 27991547 pmcid: 5171919
de Oliveira AAA, de Oliveira TA, de Oliveira LA, et al. Association between angiopoietin-2 and functional cardiac remodeling in hemodialysis patients with normal left ventricular ejection. J Clin Hypertens. 2022;24:502–12. https://doi.org/10.1111/jch.14465 .
doi: 10.1111/jch.14465
Chang F-C, Chiang W-C, Tsai M-H, et al. Angiopoietin-2–induced arterial stiffness in CKD. J Am Soc Nephrol. 2014;25:1198–209. https://doi.org/10.1681/asn.2013050542 .
doi: 10.1681/asn.2013050542 pubmed: 24511140 pmcid: 4033368
Chow B, Rabkin SW. The relationship between arterial stiffness and heart failure with preserved ejection fraction: a systemic meta-analysis. Heart Fail Rev. 2015;20:291–303. https://doi.org/10.1007/s10741-015-9471-1 .
doi: 10.1007/s10741-015-9471-1 pubmed: 25716909
Soeki T, Bando S, Uematsu E, et al. Pentraxin 3 is a local inflammatory marker in atrial fibrillation. Heart Vessel. 2014;29:653–8. https://doi.org/10.1007/s00380-013-0400-8 .
doi: 10.1007/s00380-013-0400-8
Ristagno G, Fumagalli F, Bottazzi B, et al. Pentraxin 3 in cardiovascular disease. Front Immunol. 2019;10:823. https://doi.org/10.3389/fimmu.2019.00823 .
doi: 10.3389/fimmu.2019.00823 pubmed: 31057548 pmcid: 6481278
Shah SJ, Katz DH, Selvaraj S, et al. Phenomapping for novel classification of heart failure with preserved ejection fraction. Circulation. 2015;131:269–79. https://doi.org/10.1161/circulationaha.114.010637 .
doi: 10.1161/circulationaha.114.010637 pubmed: 25398313
Hedman ÅK, Hage C, Sharma A, et al. Identification of novel pheno-groups in heart failure with preserved ejection fraction using machine learning. Heart. 2020;106:342–9. https://doi.org/10.1136/heartjnl-2019-315481 .
doi: 10.1136/heartjnl-2019-315481 pubmed: 31911501
Segar MW, Patel KV, Ayers C, et al. Phenomapping of patients with heart failure with preserved ejection fraction using machine learning-based unsupervised cluster analysis. Eur J Heart Fail. 2020;22:148–58. https://doi.org/10.1002/ejhf.1621 .
doi: 10.1002/ejhf.1621 pubmed: 31637815
Guo Y, Liu L, Wang J. Adiponectin and the risk of new-onset atrial fibrillation: a meta-analysis of prospective cohort studies. Biosci Rep. 2019;39:BSR20182284. https://doi.org/10.1042/bsr20182284 .
doi: 10.1042/bsr20182284 pubmed: 31088901 pmcid: 6558722
Hopkins TA, Ouchi N, Shibata R, Walsh K. Adiponectin actions in the cardiovascular system. Cardiovasc Res. 2007;74:11–8. https://doi.org/10.1016/j.cardiores.2006.10.009 .
doi: 10.1016/j.cardiores.2006.10.009 pubmed: 17140553
Rodríguez-Calvo R, Girona J, Alegret JM, et al. Role of the fatty acid-binding protein 4 in heart failure and cardiovascular disease. J Endocrinol. 2017;233:R173–r184. https://doi.org/10.1530/joe-17-0031 .
doi: 10.1530/joe-17-0031 pubmed: 28420707
Patten RD, Konstam MA. Ventricular remodeling and the renin angiotensin aldosterone system. Congestive Heart Failure. 2000;6:187–92. https://doi.org/10.1111/j.1527-5299.2000.80159.x .
doi: 10.1111/j.1527-5299.2000.80159.x pubmed: 12147951
Rusinaru D, Leborgne L, Peltier M, Tribouilloy C. Effect of atrial fibrillation on long-term survival in patients hospitalised for heart failure with preserved ejection fraction☆. Eur J Heart Fail. 2008;10:566–72. https://doi.org/10.1016/j.ejheart.2008.04.002 .
doi: 10.1016/j.ejheart.2008.04.002 pubmed: 18456551

Auteurs

Abhishek Dattani (A)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK. ad530@leicester.ac.uk.

Emer M Brady (EM)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Prathap Kanagala (P)

University of Liverpool, Liverpool, UK.

Svetlana Stoma (S)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Kelly S Parke (KS)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Anna-Marie Marsh (AM)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Anvesha Singh (A)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Jayanth R Arnold (JR)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Alastair J Moss (AJ)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Lei Zhao (L)

Bristol Myers Squibb, Princeton, NJ, USA.

Mary Ellen Cvijic (ME)

Bristol Myers Squibb, Princeton, NJ, USA.

Matthew Fronheiser (M)

Bristol Myers Squibb, Princeton, NJ, USA.

Shuyan Du (S)

Bristol Myers Squibb, Princeton, NJ, USA.

Philippe Costet (P)

Bristol Myers Squibb, Princeton, NJ, USA.

Peter Schafer (P)

Bristol Myers Squibb, Princeton, NJ, USA.

Leon Carayannopoulos (L)

Bristol Myers Squibb, Princeton, NJ, USA.

Ching-Pin Chang (CP)

Bristol Myers Squibb, Princeton, NJ, USA.

David Gordon (D)

Bristol Myers Squibb, Princeton, NJ, USA.

Francisco Ramirez-Valle (F)

Bristol Myers Squibb, Princeton, NJ, USA.

Michael Jerosch-Herold (M)

Brigham and Women's Hospital and Harvard Medical School, Boston, USA.

Christopher P Nelson (CP)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Iain B Squire (IB)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Leong L Ng (LL)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Gaurav S Gulsin (GS)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Gerry P McCann (GP)

Department of Cardiovascular Sciences, University of Leicester and the National Institute for Health Research Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

Classifications MeSH