Enhancing rare variant interpretation in inherited arrhythmias through quantitative analysis of consortium disease cohorts and population controls.


Journal

Genetics in medicine : official journal of the American College of Medical Genetics
ISSN: 1530-0366
Titre abrégé: Genet Med
Pays: United States
ID NLM: 9815831

Informations de publication

Date de publication:
01 2021
Historique:
received: 01 06 2020
accepted: 11 08 2020
revised: 03 08 2020
pubmed: 8 9 2020
medline: 3 6 2021
entrez: 7 9 2020
Statut: ppublish

Résumé

Stringent variant interpretation guidelines can lead to high rates of variants of uncertain significance (VUS) for genetically heterogeneous disease like long QT syndrome (LQTS) and Brugada syndrome (BrS). Quantitative and disease-specific customization of American College of Medical Genetics and Genomics/Association for Molecular Pathology (ACMG/AMP) guidelines can address this false negative rate. We compared rare variant frequencies from 1847 LQTS (KCNQ1/KCNH2/SCN5A) and 3335 BrS (SCN5A) cases from the International LQTS/BrS Genetics Consortia to population-specific gnomAD data and developed disease-specific criteria for ACMG/AMP evidence classes-rarity (PM2/BS1 rules) and case enrichment of individual (PS4) and domain-specific (PM1) variants. Rare SCN5A variant prevalence differed between European (20.8%) and Japanese (8.9%) BrS patients (p = 5.7 × 10 Large case-control data sets enable quantitative implementation of ACMG/AMP guidelines and increased sensitivity for inherited arrhythmia genetic testing.

Identifiants

pubmed: 32893267
doi: 10.1038/s41436-020-00946-5
pii: S1098-3600(21)02504-1
pmc: PMC7790744
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

47-58

Subventions

Organisme : Medical Research Council
ID : MC_UP_1102/20
Pays : United Kingdom
Organisme : NHLBI NIH HHS
ID : R01 HL152201
Pays : United States

Investigateurs

Alain Al Arnaout (AA)
Mathieu Amelot (M)
Frédéric Anselme (F)
Olivier Billon (O)
Pascal Defaye (P)
Jean-Marc Dupuis (JM)
Laurence Jesel (L)
Gabriel Laurent (G)
Philippe Maury (P)
Jean-Luc Pasquie (JL)
Francois Wiart (F)

Références

Walsh R, Thomson KL, Ware JS, et al. Reassessment of Mendelian gene pathogenicity using 7,855 cardiomyopathy cases and 60,706 reference samples. Genet Med. 2017;19:192–203.
doi: 10.1038/gim.2016.90
Hosseini SM, Kim R, Udupa S, et al. Reappraisal of reported genes for sudden arrhythmic death. Circulation. 2018;138:1195–1205.
doi: 10.1161/CIRCULATIONAHA.118.035070
Richards S, Aziz N, Bale S, et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med. 2015;17:405–423.
doi: 10.1038/gim.2015.30
Walsh R, Mazzarotto F, Whiffin N, et al. Quantitative approaches to variant classification increase the yield and precision of genetic testing in Mendelian diseases: the case of hypertrophic cardiomyopathy. Genome Med. 2019;11:5.
doi: 10.1186/s13073-019-0616-z
Ackerman MJ, Priori SG, Willems S, et al. HRS/EHRA expert consensus statement on the state of genetic testing for the channelopathies and cardiomyopathies this document was developed as a partnership between the Heart Rhythm Society (HRS) and the European Heart Rhythm Association (EHRA). Heart Rhythm. 2011;8:1308–1339.
doi: 10.1016/j.hrthm.2011.05.020
Denham NC, Pearman CM, Ding WY, et al. Systematic re-evaluation of SCN5A variants associated with Brugada syndrome. J Cardiovasc Electrophysiol. 2019;30:118–127.
doi: 10.1111/jce.13740
Harrison SM, Biesecker LG, Rehm HL. Overview of specifications to the ACMG/AMP variant interpretation guidelines. Curr Protoc Hum Genet. 2019;103:e93.
pubmed: 31479589 pmcid: 6885382
Kapa S, Tester DJ, Salisbury BA, et al. Genetic testing for long-QT syndrome: distinguishing pathogenic mutations from benign variants. Circulation. 2009;120:1752–1760.
doi: 10.1161/CIRCULATIONAHA.109.863076
Kapplinger JD, Tseng AS, Salisbury BA, et al. Enhancing the predictive power of mutations in the C-terminus of the KCNQ1-encoded Kv7.1 voltage-gated potassium channel. J Cardiovasc Transl Res. 2015;8:187–197.
doi: 10.1007/s12265-015-9622-8
Kapplinger JD, Giudicessi JR, Ye D, et al. Enhanced classification of Brugada syndrome–associated and long-QT syndrome–associated genetic variants in the SCN5A-encoded Na(v)1.5 cardiac sodium channel. Circ Cardiovasc Genet. 2015;8:582–595.
doi: 10.1161/CIRCGENETICS.114.000831
Lahrouchi N, Tadros R, Crotti L, et al. Transethnic genome-wide association study provides insights in the genetic architecture and heritability of long QT syndrome. Circulation. 2020;142:324–338.
doi: 10.1161/CIRCULATIONAHA.120.045956
Whiffin N, Minikel E, Walsh R, et al. Using high-resolution variant frequencies to empower clinical genome interpretation. Genet Med. 2017;19:1151–1158.
doi: 10.1038/gim.2017.26
Whiffin N, Walsh R, Govind R, et al. CardioClassifier: disease- and gene-specific computational decision support for clinical genome interpretation. Genet Med. 2018;20:1246–1254.
doi: 10.1038/gim.2017.258
Abou Tayoun AN, Pesaran T, DiStefano MT, et al. Recommendations for interpreting the loss of function PVS1 ACMG/AMP variant criterion. Hum Mutat. 2018;39:1517–1524.
doi: 10.1002/humu.23626
Glazer AM, Wada Y, Li B, et al. High-throughput reclassification of SCN5A variants. Am J Hum Genet. 2020;107:111–123.
doi: 10.1016/j.ajhg.2020.05.015
Probst V, Wilde AAM, Barc J, et al. SCN5A mutations and the role of genetic background in the pathophysiology of Brugada syndrome. Circ Cardiovasc Genet. 2009;2:552–557.
doi: 10.1161/CIRCGENETICS.109.853374
Tavtigian SV, Greenblatt MS, Harrison SM, et al. Modeling the ACMG/AMP variant classification guidelines as a Bayesian classification framework. Genet Med. 2018;20:1054–1060.
doi: 10.1038/gim.2017.210
Kapplinger JD, Tester DJ, Salisbury BA, et al. Spectrum and prevalence of mutations from the first 2,500 consecutive unrelated patients referred for the FAMILION long QT syndrome genetic test. Heart Rhythm. 2009;6:1297–1303.
doi: 10.1016/j.hrthm.2009.05.021
Lahrouchi N, Raju H, Lodder EM, et al. Utility of post-mortem genetic testing in cases of sudden arrhythmic death syndrome. J Am Coll Cardiol. 2017;69:2134–2145.
doi: 10.1016/j.jacc.2017.02.046
Landry LG, Rehm HL. Association of racial/ethnic categories with the ability of genetic tests to detect a cause of cardiomyopathy. JAMA Cardiol. 2018;3:341–345.
doi: 10.1001/jamacardio.2017.5333

Auteurs

Roddy Walsh (R)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands. r.t.walsh@amsterdamumc.nl.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands. r.t.walsh@amsterdamumc.nl.

Najim Lahrouchi (N)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.

Rafik Tadros (R)

Department of Medicine, Cardiovascular Genetics Center, Montreal Heart Institute and Faculty of Medicine, Université de Montréal, Montreal, QC, Canada.

Florence Kyndt (F)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CHU Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

Charlotte Glinge (C)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Cardiology, The Heart Centre, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.

Pieter G Postema (PG)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.

Ahmad S Amin (AS)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.

Eline A Nannenberg (EA)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Clinical Genetics, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

James S Ware (JS)

National Heart and Lung Institute, Imperial College London, London, United Kingdom.
Cardiovascular Research Centre, Royal Brompton and Harefield NHS Foundation Trust, London, United Kingdom.
MRC London Institute of Medical Sciences, Imperial College London, London, United Kingdom.

Nicola Whiffin (N)

National Heart and Lung Institute, Imperial College London, London, United Kingdom.
Cardiovascular Research Centre, Royal Brompton and Harefield NHS Foundation Trust, London, United Kingdom.
MRC London Institute of Medical Sciences, Imperial College London, London, United Kingdom.

Francesco Mazzarotto (F)

National Heart and Lung Institute, Imperial College London, London, United Kingdom.
Cardiovascular Research Centre, Royal Brompton and Harefield NHS Foundation Trust, London, United Kingdom.
Cardiomyopathy Unit, Careggi University Hospital, Florence, Italy.
Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.

Doris Škorić-Milosavljević (D)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.

Christian Krijger (C)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.

Elena Arbelo (E)

Arrhythmia Section, Cardiology Department, Hospital Clínic, Universitat de Barcelona, Barcelona, Spain.
IDIBAPS, Institut d'Investigació August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares (CIBERCV), Madrid, Spain.

Dominique Babuty (D)

CHU Tours, Service de Cardiologie, Tours, France.

Hector Barajas-Martinez (H)

Lankenau Institute for Medical Research, Wynnewood, PA, USA.

Britt M Beckmann (BM)

Department of Internal Medicine I, LMU Klinikum, Klinikum der Ludwig Maximilians Universität München, München, Germany.

Stéphane Bézieau (S)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CHU Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

J Martijn Bos (JM)

Department of Cardiovascular Medicine, Division of Heart Rhythm Services, Mayo Clinic, Rochester, MN, USA.

Jeroen Breckpot (J)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Human Genetics, University Hospitals Leuven, Leuven, Belgium.

Oscar Campuzano (O)

Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares (CIBERCV), Madrid, Spain.
Cardiovascular Genetics Center, University of Girona-IDIBGI, Girona, Spain.
Medical Science Department, School of Medicine, University of Girona, Girona, Spain.
Biochemistry and Molecular Genetics Department, Hospital Clinic, University of Barcelona-IDIBAPS, Barcelona, Spain.

Silvia Castelletti (S)

Istituto Auxologico Italiano, IRCCS-Center for Cardiac Arrhythmias of Genetic Origin, Milan, Italy.

Candan Celen (C)

Department of Cardiology, Ege University School of Medicine, Izmir, Turkey.

Sebastian Clauss (S)

Department of Internal Medicine I, LMU Klinikum, Klinikum der Ludwig Maximilians Universität München, München, Germany.
German Centre for Cardiovascular Research (DZHK), Partner Site Munich, Munich Heart Alliance (MHA), Munich, Germany.
Walter Brendel Centre of Experimental Medicine, Ludwig-Maximilians University Munich (LMU), Munich, Germany.

Anniek Corveleyn (A)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Center for Human Genetics, University Hospitals Leuven, Leuven, Belgium.

Lia Crotti (L)

Istituto Auxologico Italiano, IRCCS-Center for Cardiac Arrhythmias of Genetic Origin, Milan, Italy.
Istituto Auxologico Italiano, IRCCS, Department of Cardiovascular, Neural and Metabolic Sciences, San Luca Hospital, Milan, Italy.
Department of Medicine and Surgery, University of Milano-Bicocca, Milan, Italy.
Istituto Auxologico Italiano, IRCCS-Laboratory of Cardiovascular Genetics, Cusano Milanino, MI, Italy.

Federica Dagradi (F)

Istituto Auxologico Italiano, IRCCS-Center for Cardiac Arrhythmias of Genetic Origin, Milan, Italy.

Carlo de Asmundis (C)

Heart Rhythm Management Center, Postgraduate program in Cardiac Electrophysiology and Pacing Universitair Ziekenhuis, Brussel-Vrije Universiteit Brussel, ERN Heart Guard Center, Brussels, Belgium.

Isabelle Denjoy (I)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
CNMR Maladies Cardiaques Héréditaires Rares, Hôpital Bichat, Université de Paris, Paris, France.
AP-HP, Service de Cardiologie, Hôpital Bichat, Paris, France.

Sven Dittmann (S)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Institute for Genetics of Heart Diseases, University Hospital Münster, Münster, Germany.

Patrick T Ellinor (PT)

Cardiac Arrhythmia Service and Cardiovascular Research Center, Massachusetts General Hospital, Boston, MA, USA.
Cardiovascular Disease Initiative, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA, USA.

Cristina Gil Ortuño (CG)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Cardiogenetic Laboratory, Inherited Cardiac Disease Unit, University Hospital Virgen de la Arrixaca-IMIB, Murcia, Spain.

Carla Giustetto (C)

Division of Cardiology, University of Torino, Department of Medical Sciences, "Città della Salute e della Scienza" Hospital, Torino, Italy.

Jean-Baptiste Gourraud (JB)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CHU Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

Daisuke Hazeki (D)

Department of Pediatrics, Kagoshima City Hospital, Kagoshima, Japan.

Minoru Horie (M)

Center for Epidemiologic Research in Asia, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Japan.

Taisuke Ishikawa (T)

Omics Research Center, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan.

Hideki Itoh (H)

Division of Patient Safety, Hiroshima University Hospital, Minami-ku, Hiroshima, Japan.

Yoshiaki Kaneko (Y)

Department of Cardiovascular Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan.

Jørgen K Kanters (JK)

Laboratory of Experimental Cardiology, Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark.

Hiroki Kimoto (H)

Department of Molecular Physiology, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan.

Maria-Christina Kotta (MC)

Istituto Auxologico Italiano, IRCCS-Center for Cardiac Arrhythmias of Genetic Origin, Milan, Italy.
Istituto Auxologico Italiano, IRCCS-Laboratory of Cardiovascular Genetics, Cusano Milanino, MI, Italy.

Ingrid P C Krapels (IPC)

Department of Clinical Genetics, Maastricht University Medical Center+, Maastricht, Netherlands.

Masahiko Kurabayashi (M)

Department of Cardiovascular Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan.

Julieta Lazarte (J)

Department of Medicine and Robarts Research Institute, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.

Antoine Leenhardt (A)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
CNMR Maladies Cardiaques Héréditaires Rares, Hôpital Bichat, Université de Paris, Paris, France.
AP-HP, Service de Cardiologie, Hôpital Bichat, Paris, France.

Bart L Loeys (BL)

Center of Medical Genetics, Faculty of Medicine and Health Sciences, University of Antwerp and Antwerp University Hospital, Antwerp, Belgium.

Catarina Lundin (C)

Department of Clinical Genetics and Pathology, Lund University, Lund, Sweden.

Takeru Makiyama (T)

Department of Cardiovascular Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Jacques Mansourati (J)

CHU Brest, Service de Cardiologie, Brest, France.

Raphaël P Martins (RP)

Univ Rennes, CHU Rennes, INSERM, Rennes, France.

Andrea Mazzanti (A)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular Cardiology, ICS Maugeri, IRCCS and Department of Molecular Medicine, University of Pavia, Pavia, Italy.

Stellan Mörner (S)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Centre for Cardiovascular Genetics, Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden.

Carlo Napolitano (C)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular Cardiology, ICS Maugeri, IRCCS and Department of Molecular Medicine, University of Pavia, Pavia, Italy.

Kimie Ohkubo (K)

Department of Cardiovascular Medicine, Nihon University, Tokyo, Japan.

Michael Papadakis (M)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular and Clinical Sciences Research Institute, St. George's, University of London, London, United Kingdom.
Cardiology Clinical Academic Group, St. George's University Hospitals' NHS Foundation Trust, London, United Kingdom.

Boris Rudic (B)

Department of Medicine, University Medical Center Mannheim, Mannheim, Germany.
German Center for Cardiovascular Research (DZHK), Partner Site Heidelberg/Mannheim, Mannheim, Germany.

Maria Sabater Molina (MS)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Cardiogenetic Laboratory, Inherited Cardiac Disease Unit, University Hospital Virgen de la Arrixaca-IMIB, Murcia, Spain.

Frédéric Sacher (F)

Hôpital Cardiologique du Haut-Lévêque, LIRYC Institute, Université Bordeaux, Bordeaux, France.

Hatice Sahin (H)

Department of Cardiology, Ege University School of Medicine, Izmir, Turkey.

Georgia Sarquella-Brugada (G)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Medical Science Department, School of Medicine, University of Girona, Girona, Spain.
Arrhythmias Unit, Hospital Sant Joan de Déu, University of Barcelona, Barcelona, Spain.

Regina Sebastiano (R)

Medical Genetics, San Luigi Univesity Hospital, Orbassano, TO, Italy.

Sanjay Sharma (S)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular and Clinical Sciences Research Institute, St. George's, University of London, London, United Kingdom.
Cardiology Clinical Academic Group, St. George's University Hospitals' NHS Foundation Trust, London, United Kingdom.

Mary N Sheppard (MN)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular and Clinical Sciences Research Institute, St. George's, University of London, London, United Kingdom.
Cardiology Clinical Academic Group, St. George's University Hospitals' NHS Foundation Trust, London, United Kingdom.

Keiko Shimamoto (K)

Department of Cardiovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Japan.

M Benjamin Shoemaker (MB)

Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.

Birgit Stallmeyer (B)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Institute for Genetics of Heart Diseases, University Hospital Münster, Münster, Germany.

Johannes Steinfurt (J)

Department of Cardiology and Angiology I, Heart Center University of Freiburg, Medical Faculty, Freiburg, Germany.

Yuji Tanaka (Y)

Department of Pediatrics, National Hospital Organization Kagoshima Medical Center, Kagoshima, Japan.

David J Tester (DJ)

Department of Cardiovascular Medicine, Division of Heart Rhythm Services, Mayo Clinic, Rochester, MN, USA.

Keisuke Usuda (K)

Department of Cardiovascular Medicine, Kanazawa University Graduate School of Medical Sciences, Kanazawa, Japan.

Paul A van der Zwaag (PA)

Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, Netherlands.

Sonia Van Dooren (S)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Centre for Medical Genetics, research group Reproduction and Genetics, research cluster Reproduction, Genetics and Regenerative Medicine, Vrije Universiteit Brussel (VUB), Universitair Ziekenhuis Brussel (UZ Brussel), Brussels, Belgium.

Lut Van Laer (L)

Center of Medical Genetics, Faculty of Medicine and Health Sciences, University of Antwerp and Antwerp University Hospital, Antwerp, Belgium.

Annika Winbo (A)

Department of Physiology, University of Auckland, Auckland, New Zealand.

Bo G Winkel (BG)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Cardiology, The Heart Centre, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.

Kenichiro Yamagata (K)

Department of Cardiovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Japan.

Sven Zumhagen (S)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Institute for Genetics of Heart Diseases, University Hospital Münster, Münster, Germany.

Paul G A Volders (PGA)

Department of Cardiology, CARIM, Maastricht University Medical Center+, Maastricht, Netherlands.

Steven A Lubitz (SA)

Cardiac Arrhythmia Service and Cardiovascular Research Center, Massachusetts General Hospital, Boston, MA, USA.
Cardiovascular Disease Initiative, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA, USA.

Charles Antzelevitch (C)

Lankenau Institute for Medical Research, Wynnewood, PA, USA.

Pyotr G Platonov (PG)

Department of Cardiology, Clinical Sciences, Lund University, Lund, Sweden.

Katja E Odening (KE)

Department of Cardiology and Angiology I, Heart Center University of Freiburg, Medical Faculty, Freiburg, Germany.
Department of Cardiology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland.

Dan M Roden (DM)

Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
Department of Biomedical Informatics, Vanderbilt University Medical Center, Nashville, TN, USA.
Department of Pharmacology, Vanderbilt University Medical Center, Nashville, TN, USA.

Jason D Roberts (JD)

Section of Cardiac Electrophysiology, Division of Cardiology, Department of Medicine, Western University, London, ON, Canada.

Jonathan R Skinner (JR)

Cardiac Inherited Disease Group, Starship Childrens Hospital, Auckland, New Zealand.

Jacob Tfelt-Hansen (J)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Cardiology, The Heart Centre, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
Department of Forensic Medicine, Faculty of Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Maarten P van den Berg (MP)

Department of Cardiology, University of Groningen, University Medical Center Groningen, Groningen, Netherlands.

Morten S Olesen (MS)

Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark.

Pier D Lambiase (PD)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Barts Heart Centre, Barts Health NHS Trust & Institute of Cardiovascular Science, University College London, London, United Kingdom.

Martin Borggrefe (M)

Department of Medicine, University Medical Center Mannheim, Mannheim, Germany.
German Center for Cardiovascular Research (DZHK), Partner Site Heidelberg/Mannheim, Mannheim, Germany.

Kenshi Hayashi (K)

Department of Cardiovascular Medicine, Kanazawa University Graduate School of Medical Sciences, Kanazawa, Japan.

Annika Rydberg (A)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Clinical Sciences, Paediatrics, Umeå University, Umeå, Sweden.

Tadashi Nakajima (T)

Department of Cardiovascular Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan.

Masao Yoshinaga (M)

Department of Pediatrics, National Hospital Organization Kagoshima Medical Center, Kagoshima, Japan.

Johan B Saenen (JB)

Department of Cardiology, University of Antwerp, Antwerp University Hospital, Antwerp, Belgium.

Stefan Kääb (S)

Department of Internal Medicine I, LMU Klinikum, Klinikum der Ludwig Maximilians Universität München, München, Germany.
German Centre for Cardiovascular Research (DZHK), Partner Site Munich, Munich Heart Alliance (MHA), Munich, Germany.

Pedro Brugada (P)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Heart Rhythm Management Center, UZ Brussel-VUB, Brussels, Belgium.

Tomas Robyns (T)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Department of Cardiovascular Diseases, University Hospitals Leuven, Leuven, Belgium.

Daniela F Giachino (DF)

Medical Genetics, San Luigi Univesity Hospital, Orbassano, TO, Italy.
Medical Genetics Department, Clinical and Biological Sciences, Univestity of Torino, Orbassano, TO, Italy.

Michael J Ackerman (MJ)

Department of Cardiovascular Medicine, Division of Heart Rhythm Services, Mayo Clinic, Rochester, MN, USA.

Ramon Brugada (R)

Hospital Trueta, CiberCV, University of Girona, IDIBGI, Girona, Spain.

Josep Brugada (J)

Cardiovascular Institute, Hospital Clinic, University of Barcelona, Barcelona, Spain.

Juan R Gimeno (JR)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Inherited Cardiac Disease Unit, Cardiology Department, University Hospital Virgen de la Arrixaca, Murcia, Spain.

Can Hasdemir (C)

Department of Cardiology, Ege University School of Medicine, Izmir, Turkey.

Pascale Guicheney (P)

INSERM, Sorbonne University, UMRS 1166, Institute of Cardiometabolism and Nutrition (ICAN), Paris, France.

Silvia G Priori (SG)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular Cardiology, ICS Maugeri, IRCCS and Department of Molecular Medicine, University of Pavia, Pavia, Italy.

Eric Schulze-Bahr (E)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Institute for Genetics of Heart Diseases, University Hospital Münster, Münster, Germany.

Naomasa Makita (N)

Omics Research Center, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan.

Peter J Schwartz (PJ)

Istituto Auxologico Italiano, IRCCS-Center for Cardiac Arrhythmias of Genetic Origin, Milan, Italy.
Istituto Auxologico Italiano, IRCCS-Laboratory of Cardiovascular Genetics, Cusano Milanino, MI, Italy.

Wataru Shimizu (W)

Department of Cardiovascular Medicine, Nippon Medical School, Tokyo, Japan.

Takeshi Aiba (T)

Department of Cardiovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Japan.

Jean-Jacques Schott (JJ)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CHU Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

Richard Redon (R)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CHU Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

Seiko Ohno (S)

Department of Bioscience and Genetics, National Cerebral and Cardiovascular Center, Suita, Japan.

Vincent Probst (V)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CHU Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

Elijah R Behr (ER)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Molecular and Clinical Sciences Research Institute, St. George's, University of London, London, United Kingdom.
Cardiology Clinical Academic Group, St. George's University Hospitals' NHS Foundation Trust, London, United Kingdom.

Julien Barc (J)

Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.
Université de Nantes, CNRS, INSERM, l'institut du thorax, Nantes, France.

Connie R Bezzina (CR)

Department of Clinical and Experimental Cardiology, Heart Centre, Amsterdam Cardiovascular Sciences, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Member of the European Reference Network for rare, low prevalence and/or complex diseases of the heart: ERN GUARD-Heart, Amsterdam, Netherlands.

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