Transethnic Genome-Wide Association Study Provides Insights in the Genetic Architecture and Heritability of Long QT Syndrome


Por: Lahrouchi N, Tadros R, Crotti L, Mizusawa Y, Postema PG, Beekman L, Walsh R, Hasegawa K, Barc J, Ernsting M, Turkowski KL, Mazzanti A, Beckmann BM, Shimamoto K, Diamant UB, Wijeyeratne YD, Kucho Y, Robyns T, Ishikawa T, Arbelo E, Christiansen M, Winbo A, Jabbari R, Lubitz SA, Steinfurt J, Rudic B, Loeys B, Shoemaker MB, Weeke PE, Pfeiffer R, Davies B, Andorin A, Hofman N, Dagradi F, Pedrazzini M, Tester DJ, Bos JM, Sarquella-Brugada G, Campuzano Ó, Platonov PG, Stallmeyer B, Zumhagen S, Nannenberg EA, Veldink JH, van den Berg LH, Al-Chalabi A, Shaw CE, Shaw PJ, Morrison KE, Andersen PM, Müller-Nurasyid M, Cusi D, Barlassina C, Galan P, Lathrop M, Munter M, Werge T, Ribasés M, Aung T, Khor CC, Ozaki M, Lichtner P, Meitinger T, van Tintelen JP, Hoedemaekers Y, Denjoy I, Leenhardt A, Napolitano C, Shimizu W, Schott JJ, Gourraud JB, Makiyama T, Ohno S, Itoh H, Krahn AD, Antzelevitch C, Roden DM, Saenen J, Borggrefe M, Odening KE, Ellinor PT, Tfelt-Hansen J, Skinner JR, van den Berg MP, Olesen MS, Brugada-Terradellas J, Brugada R, Makita N, Breckpot J, Yoshinaga M, Behr ER, Rydberg A, Aiba T, Kääb S, Priori SG, Guicheney P, Tan HL, Newton-Cheh C, Ackerman MJ, Schwartz PJ, Schulze-Bahr E, Probst V, Horie M, Wilde AA, Tanck MWT and Bezzina CR

Publicada: 28 jul 2020 Ahead of Print: 20 may 2020
Resumen:
Background: Long QT syndrome (LQTS) is a rare genetic disorder and a major preventable cause of sudden cardiac death in the young. A causal rare genetic variant with large effect size is identified in up to 80% of probands (genotype positive) and cascade family screening shows incomplete penetrance of genetic variants. Furthermore, a proportion of cases meeting diagnostic criteria for LQTS remain genetically elusive despite genetic testing of established genes (genotype negative). These observations raise the possibility that common genetic variants with small effect size contribute to the clinical picture of LQTS. This study aimed to characterize and quantify the contribution of common genetic variation to LQTS disease susceptibility. Methods: We conducted genome-wide association studies followed by transethnic meta-analysis in 1656 unrelated patients with LQTS of European or Japanese ancestry and 9890 controls to identify susceptibility single nucleotide polymorphisms. We estimated the common variant heritability of LQTS and tested the genetic correlation between LQTS susceptibility and other cardiac traits. Furthermore, we tested the aggregate effect of the 68 single nucleotide polymorphisms previously associated with the QT-interval in the general population using a polygenic risk score. Results: Genome-wide association analysis identified 3 loci associated with LQTS at genome-wide statistical significance (P<5x10(-8)) nearNOS1AP,KCNQ1, andKLF12, and 1 missense variant inKCNE1(p.Asp85Asn) at the suggestive threshold (P<10(-6)). Heritability analyses showed that approximate to 15% of variance in overall LQTS susceptibility was attributable to common genetic variation (h2SNP0.148; standard error 0.019). LQTS susceptibility showed a strong genome-wide genetic correlation with the QT-interval in the general population (r(g)=0.40;P=3.2x10(-3)). The polygenic risk score comprising common variants previously associated with the QT-interval in the general population was greater in LQTS cases compared with controls (P<10-13), and it is notable that, among patients with LQTS, this polygenic risk score was greater in patients who were genotype negative compared with those who were genotype positive (P<0.005). Conclusions: This work establishes an important role for common genetic variation in susceptibility to LQTS. We demonstrate overlap between genetic control of the QT-interval in the general population and genetic factors contributing to LQTS susceptibility. Using polygenic risk score analyses aggregating common genetic variants that modulate the QT-interval in the general population, we provide evidence for a polygenic architecture in genotype negative LQTS.

Filiaciones:
Lahrouchi N:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Tadros R:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

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

Crotti L:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

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

 Istituto Auxologico Italiano, IRCCS, Laboratory of Cardiovascular Genetics, 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

Mizusawa Y:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Postema PG:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Beekman L:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Walsh R:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Hasegawa K:
 Department of Cardiovascular Medicine, Shiga University of Medical Science, Otsu, Japan

 Department of Cardiovascular Medicine, Faculty of Medical Sciences, University of Fukui, Fukui, Japan

Barc J:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 l'institut du thorax, INSERM, CNRS, Univ Nantes, Nantes, France

Ernsting M:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Institute for Genetics of Heart Diseases, Department of Cardiovascular Medicine, University Hospital Muenster, Muenster, Germany

Turkowski KL:
 Departments of Cardiovascular Medicine (Division of Heart Rhythm Services and the Windland Smith Rice Genetic Heart Rhythm Clinic), Pediatric and Adolescent Medicine (Division of Pediatric Cardiology), and Molecular Pharmacology & Experimental Therapeutics (Windland Smith Rice Sudden Death Genomics Laboratory), Mayo Clinic, Rochester, MN

Mazzanti A:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Molecular Cardiology, ICS Maugeri, IRCCS and Department of Molecular Medicine, University of Pavia, Pavia, Italy

Beckmann BM:
 Department of Internal Medicine I, University Hospital of the Ludwig Maximilians University, Munich, Germany

Shimamoto K:
 Department of Cardiovascular Medicine, National Cerebral and Cardiovascular Center, Osaka, Japan

Diamant UB:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Department of Clinical Sciences, Unit of Paediatrics, Umeå University, Umeå, Sweden

Wijeyeratne YD:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 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

Kucho Y:
 National Hospital Organization Kagoshima Medical Center, Japan

Robyns T:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Department of Cardiovascular Diseases, University Hospitals Leuven, Belgium

 Department of cardiovascular sciences, KU Leuven, Belgium

Ishikawa T:
 Omics Research Center, National Cerebral and Cardiovascular Center, Osaka, Japan

Arbelo E:
 Cardiovascular Institute, Hospital Clinic de Barcelona, Universitat de Barcelona, Spain. Institut d'Investigació August Pi i Sunyer (IDIBAPS). Centro de Investigacion Biomedica en Red de Enfermedades Cardiovasculares (CIBERCV), Barcelona, Spain

Christiansen M:
 Department of Congenital Disorders, Statens Serum Institute, Copenhagen, Denmark

 The Lundbeck Foundation Initiative for Integrative Psychiatric Research, iPSYCH, Copenhagen, Denmark

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

Winbo A:
 Department of Physiology, The University of Auckland, Auckland, New Zealand

Jabbari R:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 The Department of Cardiology, The Heart Centre, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark

Lubitz SA:
 Cardiac Arrhythmia Service, Massachusetts General Hospital, Boston, MA

 Cardiovascular Disease Initiative and Program in Medical and Population Genetics, Broad Institute, Cambridge, Boston, MA

Steinfurt J:
 Department of Cardiology and Angiology I, Heart Center University of Freiburg, Medical Faculty, Freiburg, Germany

Rudic B:
 Department of Medicine, University Medical Center Mannheim, Mannheim, Germany

 German Center for Cardiovascular Research (DZHK), Partner Site Heidelberg/Mannheim, Germany

Loeys B:
 Department of Clinical Genetics, Antwerp University Hospital, Antwerp, Belgium

Shoemaker MB:
 Department of Medicine, Vanderbilt University Medical Center, Nashville, TN

Weeke PE:
 The Department of Cardiology, The Heart Centre, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark

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

Pfeiffer R:
 Masonic Medical Research Institute, Utica, NY

Davies B:
 Heart Rhythm Services, Division of Cardiology, Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada

Andorin A:
 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

 l'institut du thorax, CHU Nantes, Service de Cardiologie, Nantes, France

Hofman N:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Dagradi F:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

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

Pedrazzini M:
 Istituto Auxologico Italiano, IRCCS, Laboratory of Cardiovascular Genetics, Milan, Italy

Tester DJ:
 Departments of Cardiovascular Medicine (Division of Heart Rhythm Services and the Windland Smith Rice Genetic Heart Rhythm Clinic), Pediatric and Adolescent Medicine (Division of Pediatric Cardiology), and Molecular Pharmacology & Experimental Therapeutics (Windland Smith Rice Sudden Death Genomics Laboratory), Mayo Clinic, Rochester, MN

Bos JM:
 Departments of Cardiovascular Medicine (Division of Heart Rhythm Services and the Windland Smith Rice Genetic Heart Rhythm Clinic), Pediatric and Adolescent Medicine (Division of Pediatric Cardiology), and Molecular Pharmacology & Experimental Therapeutics (Windland Smith Rice Sudden Death Genomics Laboratory), Mayo Clinic, Rochester, MN

Sarquella-Brugada G:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Arrhythmia, Inherited Heart Disease and Sudden Death Unit, Hospital Sant Joan de Déu, European Reference Center at the ERN GUARD-Heart Reference Network for Rare Cardiac Diseases, Barcelona, Spain

 Medical Science Department, School of Medicine, University of Girona, Girona, Spain

 Cardiovascular Program, Research Institute of Sant Joan de Déu (IRSJD), Barcelona, Spain

Campuzano Ó:
 Cardiovascular Program, Research Institute of Sant Joan de Déu (IRSJD), Barcelona, Spain

 Center for Biomedical Diagnosis, Hospital Clinic de Barcelona, Universitat de Barcelona, Spain. Institut d'Investigació August Pi i Sunyer (IDIBAPS). Cardiovascular Genetics Center, University of Girona-IDIBGI, Girona (Spain). Medical Science Department, School of Medicine, University of Girona, Girona, Spain

 Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares (CIBERCV), Madrid, Spain

Platonov PG:
 Center for Integrative Electrocardiology (CIEL), Department of Cardiology, Clinical Sciences, Lund University, Lund, Sweden

Stallmeyer B:
 Institute for Genetics of Heart Diseases, Department of Cardiovascular Medicine, University Hospital Muenster, Muenster, Germany

Zumhagen S:
 Institute for Genetics of Heart Diseases, Department of Cardiovascular Medicine, University Hospital Muenster, Muenster, Germany

Nannenberg EA:
 Department of Clinical Genetics, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands

Veldink JH:
 Department of Neurology, UMC Utrecht Brain Center, University Medical Center Utrecht, Utrecht, The Netherlands

van den Berg LH:
 Department of Neurology, UMC Utrecht Brain Center, University Medical Center Utrecht, Utrecht, The Netherlands

Al-Chalabi A:
 King's College Hospital, Bessemer Road, London, SE5 9RS, UK

 Department of Basic and Clinical Neuroscience, King's College London, Maurice Wohl Clinical Neuroscience Institute, London, UK

Shaw CE:
 Department of Basic and Clinical Neuroscience, King's College London, Maurice Wohl Clinical Neuroscience Institute, London, UK

 UK Dementia Research Institute, King's College London, London, UK

Shaw PJ:
 Sheffield Institute for Translational Neuroscience, University of Sheffield, Sheffield, UK

Morrison KE:
 Faculty of Medicine, University of Southampton, University Hospital Southampton, Southampton, UK

Andersen PM:
 Department of Neurology, Ulm University, 89081 Ulm, Germany

 and Department of Pharmacology and Clinical Neuroscience, Umeå University, 90187 Umeå, Sweden

Müller-Nurasyid M:
 Department of Internal Medicine I, University Hospital of the Ludwig Maximilians University, Munich, Germany

 Institute of Genetic Epidemiology, Helmholtz Zentrum München-German Research Center for Environmental Health, Neuherberg, Germany

 Chair of Genetic Epidemiology, IBE, Faculty of Medicine, LMU Munich, Germany

Cusi D:
 Department of Health Sciences, University of Milan, Milan, Italy

 Bio4Dreams - business nursery for life sciences, Milan, Italy

Barlassina C:
 Department of Health Sciences, University of Milan, Milan, Italy

 Bio4Dreams - business nursery for life sciences, Milan, Italy

Galan P:
 Equipe de Recherche en Epidémiologie Nutritionnelle, Centre d'Epidémiologie et Statistiques Paris Cité, Université Paris 13, Inserm (U1153), Inra (U1125), COMUE SorbonneParis-Cité, Bobigny, France

Lathrop M:
 McGill University and Génome Québec Innovation Centre, Montréal, Québec, Canada

Munter M:
 McGill University and Génome Québec Innovation Centre, Montréal, Québec, Canada

Werge T:
 The Lundbeck Foundation Initiative for Integrative Psychiatric Research, iPSYCH, Copenhagen, Denmark

 Institute of Biological Psychiatry, Mental Health Centre Sct Hans, Copenhagen University Hospital, Roskilde, Denmark

 Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

Ribasés M:
 Psychiatric Genetics Unit, Institute Vall d'Hebron Research (VHIR), Universitat Autònoma de Barcelona, Barcelona, Spain

Aung T:
 Singapore Eye Research Institute, Singapore, Singapore

Khor CC:
 Genome Institute of Singapore, Singapore, Singapore

Ozaki M:
 Ozaki Eye Hospital, 1-15, Kamezaki, Hyuga, Miyazaki 883-0066 Japan

Lichtner P:
 Institute of Human Genetics, Helmholtz Zentrum München, Neuherberg, Germany

Meitinger T:
 Institute of Human Genetics, Helmholtz Zentrum München, Neuherberg, Germany

van Tintelen JP:
 Department of Clinical Genetics, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands

 Department of Clinical Genetics, University Medical Centre Groningen, Groningen, The Netherlands

 Department of Clinical Genetics, University Medical Centre Utrecht, University of Utrecht, Utrecht, The Netherlands

Hoedemaekers Y:
 Department of Clinical Genetics, University Medical Centre Groningen, Groningen, The Netherlands

Denjoy I:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 AP-HP, Hôpital Bichat, Département de Cardiologie et Centre de Référence des Maladies Cardiaques Héréditaires, F-75018 Paris, France, Université de Paris INSERM U1166, F-75013 Paris, France

Leenhardt A:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 AP-HP, Hôpital Bichat, Département de Cardiologie et Centre de Référence des Maladies Cardiaques Héréditaires, F-75018 Paris, France, Université de Paris INSERM U1166, F-75013 Paris, France

Napolitano C:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Molecular Cardiology, ICS Maugeri, IRCCS and Department of Molecular Medicine, University of Pavia, Pavia, Italy

Shimizu W:
 Department of Cardiovascular Medicine, National Cerebral and Cardiovascular Center, Osaka, Japan

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

Schott JJ:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 l'institut du thorax, INSERM, CNRS, Univ Nantes, Nantes, France

 l'institut du thorax, CHU Nantes, Service de Cardiologie, Nantes, France

Gourraud JB:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 l'institut du thorax, INSERM, CNRS, Univ Nantes, Nantes, France

 l'institut du thorax, CHU Nantes, Service de Cardiologie, Nantes, France

Makiyama T:
 Department of Cardiovascular Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan

Ohno S:
 Department of Cardiovascular Medicine, Shiga University of Medical Science, Otsu, Japan

 Center for Epidemiologic Research in Asia, Shiga University of Medical Science, Otsu, Japan

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

Itoh H:
 Department of Cardiovascular Medicine, Shiga University of Medical Science, Otsu, Japan

 Center for Epidemiologic Research in Asia, Shiga University of Medical Science, Otsu, Japan

Krahn AD:
 Heart Rhythm Services, Division of Cardiology, Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada

Antzelevitch C:
 Lankenau Institute for Medical Research, Wynnewood, PA

 Lankenau Heart Institute, Wynnewood, PA

 Sidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, PA

Roden DM:
 Department of Biomedical Informatics, Vanderbilt University Medical Center, Nashville, TN

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

 Department of Pharmacology, Vanderbilt University Medical Center, Nashville, TN

Saenen J:
 Department of Cardiology, Antwerp University Hospital, Belgium

Borggrefe M:
 Department of Medicine, University Medical Center Mannheim, Mannheim, Germany

 German Center for Cardiovascular Research (DZHK), Partner Site Heidelberg/Mannheim, Germany

Odening KE:
 Department of Cardiology and Angiology I, Heart Center University of Freiburg, Medical Faculty, Freiburg, Germany

Ellinor PT:
 Cardiac Arrhythmia Service, Massachusetts General Hospital, Boston, MA

 Cardiovascular Disease Initiative and Program in Medical and Population Genetics, Broad Institute, Cambridge, Boston, MA

Tfelt-Hansen J:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 The 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

Skinner JR:
 Cardiac Inherited Disease Group, Starship Childrens Hospital, Auckland, New Zealand

van den Berg MP:
 Department of cardiology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

Olesen MS:
 Laboratory for Molecular Cardiology, Department of Cardiology, The Heart Centre, Rigshospitalet (Copenhagen University Hospital), Copenhagen, Denmark

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

Brugada-Terradellas J:
 Arrhythmia Unit, Hospital Sant Joan de Déu, University of Barcelona, Barcelona,Spain

 Cardiovascular Institute, Hospital Clinic de Barcelona, Universitat de Barcelona, Spain

 Institut d'Investigació August Pi i Sunyer (IDIBAPS)

Brugada R:
 Center for Biomedical Diagnosis, Hospital Clinic de Barcelona, Universitat de Barcelona, Spain. Institut d'Investigació August Pi i Sunyer (IDIBAPS). Cardiovascular Genetics Center, University of Girona-IDIBGI, Girona (Spain). Medical Science Department, School of Medicine, University of Girona, Girona, Spain

 Cardiovascular Genetics Center, University of Girona-IDIBGI, Girona, Spain. Medical Science Department, School of Medicine, University of Girona, Girona, Spain

 Cardiology Service, Hospital Josep Trueta, Girona, Spain

Makita N:
 National Cerebral and Cardiovascular Center Research Institute, Osaka, Japan

Breckpot J:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Centre for human genetics, university hospitals Leuven, Belgium

Yoshinaga M:
 National Hospital Organization Kagoshima Medical Center, Japan

Behr ER:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 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

Rydberg A:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Department of Clinical Sciences, Unit of Paediatrics, Umeå University, Umeå, Sweden

Aiba T:
 Department of Cardiovascular Medicine, National Cerebral and Cardiovascular Center, Osaka, Japan

Kääb S:
 Department of Internal Medicine I, University Hospital of the Ludwig Maximilians University, Munich, Germany

Priori SG:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Molecular Cardiology, ICS Maugeri, IRCCS and Department of Molecular Medicine, University of Pavia, Pavia, Italy

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

Tan HL:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Netherlands Heart Institute, Utrecht, The Netherlands

Newton-Cheh C:
 Cardiovascular Research Center and Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA

Ackerman MJ:
 Departments of Cardiovascular Medicine (Division of Heart Rhythm Services and the Windland Smith Rice Genetic Heart Rhythm Clinic), Pediatric and Adolescent Medicine (Division of Pediatric Cardiology), and Molecular Pharmacology & Experimental Therapeutics (Windland Smith Rice Sudden Death Genomics Laboratory), Mayo Clinic, Rochester, MN

Schwartz PJ:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

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

 Istituto Auxologico Italiano, IRCCS, Laboratory of Cardiovascular Genetics, Milan, Italy

Schulze-Bahr E:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 Institute for Genetics of Heart Diseases, Department of Cardiovascular Medicine, University Hospital Muenster, Muenster, Germany

Probst V:
 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

 l'institut du thorax, INSERM, CNRS, Univ Nantes, Nantes, France

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

Horie M:
 Department of Cardiovascular Medicine, Shiga University of Medical Science, Otsu, Japan

 Center for Epidemiologic Research in Asia, Shiga University of Medical Science, Otsu, Japan

Wilde AA:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart

Tanck MWT:
 Department of Clinical Epidemiology, Biostatistics and Bioinformatics, Amsterdam UMC, University of Amsterdam. Amsterdam, The Netherlands

Bezzina CR:
 Amsterdam UMC, University of Amsterdam, Heart Center

 Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, Amsterdam, The Netherlands

 Member of the European Reference Network for rare, low prevalence and complex diseases of the heart - ERN GUARD-Heart
ISSN: 00097322





CIRCULATION
Editorial
LIPPINCOTT WILLIAMS & WILKINS, TWO COMMERCE SQ, 2001 MARKET ST, PHILADELPHIA, PA 19103, Estados Unidos America
Tipo de documento: Article
Volumen: 142 Número: 4
Páginas: 324-338
WOS Id: 000562745400012
ID de PubMed: 32429735
imagen Green Submitted, Green Accepted, Green Published, hybrid

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