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Multi-ancestry GWAS of the electrocardiographic PR interval identifies 202 loci underlying cardiac conduction

Author

Listed:
  • Ioanna Ntalla

    (Queen Mary University of London)

  • Lu-Chen Weng

    (Massachusetts General Hospital
    The Broad Institute of MIT and Harvard)

  • James H. Cartwright

    (Queen Mary University of London)

  • Amelia Weber Hall

    (Massachusetts General Hospital
    The Broad Institute of MIT and Harvard)

  • Gardar Sveinbjornsson

    (deCODE genetics/Amgen, Inc.)

  • Nathan R. Tucker

    (Massachusetts General Hospital
    The Broad Institute of MIT and Harvard)

  • Seung Hoan Choi

    (The Broad Institute of MIT and Harvard)

  • Mark D. Chaffin

    (The Broad Institute of MIT and Harvard)

  • Carolina Roselli

    (The Broad Institute of MIT and Harvard
    University of Groningen, University Medical Center Groningen)

  • Michael R. Barnes

    (Queen Mary University of London
    Barts Cardiovascular Biomedical Research Centre, Queen Mary University of London)

  • Borbala Mifsud

    (Queen Mary University of London
    Hamad Bin Khalifa University, Education City)

  • Helen R. Warren

    (Queen Mary University of London
    Barts Cardiovascular Biomedical Research Centre, Queen Mary University of London)

  • Caroline Hayward

    (Institute of Genetics and Molecular Medicine, University of Edinburgh)

  • Jonathan Marten

    (Institute of Genetics and Molecular Medicine, University of Edinburgh)

  • James J. Cranley

    (Queen Mary University of London)

  • Maria Pina Concas

    (Institute for Maternal and Child Health-IRCCS ‘Burlo Garofolo’)

  • Paolo Gasparini

    (Institute for Maternal and Child Health-IRCCS ‘Burlo Garofolo’
    University of Trieste)

  • Thibaud Boutin

    (Institute of Genetics and Molecular Medicine, University of Edinburgh)

  • Ivana Kolcic

    (University of Split School of Medicine)

  • Ozren Polasek

    (University of Split School of Medicine
    Clinical Hospital Centre Split
    Psychiatric Hospital Sveti Ivan)

  • Igor Rudan

    (University of Edinburgh)

  • Nathalia M. Araujo

    (Universidade Federal de Minas Gerais, Belo Horizonte)

  • Maria Fernanda Lima-Costa

    (Oswaldo Cruz Foundation, Belo Horizonte)

  • Antonio Luiz P. Ribeiro

    (Hospital das Clínicas e Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte)

  • Renan P. Souza

    (Universidade Federal de Minas Gerais, Belo Horizonte)

  • Eduardo Tarazona-Santos

    (Universidade Federal de Minas Gerais, Belo Horizonte)

  • Vilmantas Giedraitis

    (Geriatrics, Uppsala University)

  • Erik Ingelsson

    (Stanford University School of Medicine
    Stanford University
    Stanford University
    Molecular Epidemiology and Science for Life Laboratory, Uppsala University)

  • Anubha Mahajan

    (University of Oxford)

  • Andrew P. Morris

    (University of Oxford
    University of Liverpool
    University of Manchester)

  • Fabiola Del Greco M

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Luisa Foco

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Martin Gögele

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Andrew A. Hicks

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • James P. Cook

    (University of Liverpool)

  • Lars Lind

    (Uppsala University Hospital)

  • Cecilia M. Lindgren

    (Li Ka Shing Centre for Health Information and Discovery, Big Data Institute, University of Oxford
    The Wellcome Centre for Human Genetics, University of Oxford
    The Broad Institute of MIT and Harvard)

  • Johan Sundström

    (Uppsala University)

  • Christopher P. Nelson

    (Cardiovascular Research Centre, Glenfield Hospital, University of Leicester
    NIHR Leicester Biomedical Research Centre, Glenfield Hospital)

  • Muhammad B. Riaz

    (Cardiovascular Research Centre, Glenfield Hospital, University of Leicester
    NIHR Leicester Biomedical Research Centre, Glenfield Hospital)

  • Nilesh J. Samani

    (Cardiovascular Research Centre, Glenfield Hospital, University of Leicester
    NIHR Leicester Biomedical Research Centre, Glenfield Hospital)

  • Gianfranco Sinagra

    (Azienda Ospedaliera Universitaria Integrata of Trieste)

  • Sheila Ulivi

    (Institute for Maternal and Child Health-IRCCS ‘Burlo Garofolo’)

  • Mika Kähönen

    (Tampere University Hospital
    Faculty of Medicine and Health Technology, Finnish Cardiovascular Research Center Tampere University)

  • Pashupati P. Mishra

    (Fimlab Laboratories
    Faculty of Medicine and Health Technology, Finnish Cardiovascular Research Center, Tampere University)

  • Nina Mononen

    (Fimlab Laboratories
    Faculty of Medicine and Health Technology, Finnish Cardiovascular Research Center, Tampere University)

  • Kjell Nikus

    (Heart Center, Tampere University Hospital
    Finnish Cardiovascular Research Center, Faculty of Medicine and Health Technology, Tampere University)

  • Mark J. Caulfield

    (Queen Mary University of London
    Barts Cardiovascular Biomedical Research Centre, Queen Mary University of London)

  • Anna Dominiczak

    (University of Glasgow)

  • Sandosh Padmanabhan

    (University of Glasgow
    University of Glasgow)

  • May E. Montasser

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Jeff R. O’Connell

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Kathleen Ryan

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Alan R. Shuldiner

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Stefanie Aeschbacher

    (University Hospital)

  • David Conen

    (University Hospital
    McMaster University)

  • Lorenz Risch

    (Inselspital Bern, University Hospital, University of Bern
    Labormedizinisches Zentrum Dr. Risch
    Private University of the Principality of Liechtenstein)

  • Sébastien Thériault

    (McMaster University
    Medical Biochemistry and Pathology, Laval University)

  • Nina Hutri-Kähönen

    (Tampere University Hospital
    Tampere University)

  • Terho Lehtimäki

    (Fimlab Laboratories
    Faculty of Medicine and Health Technology, Finnish Cardiovascular Research Center, Tampere University)

  • Leo-Pekka Lyytikäinen

    (Fimlab Laboratories
    Faculty of Medicine and Health Technology, Finnish Cardiovascular Research Center, Tampere University
    Heart Center, Tampere University Hospital)

  • Olli T. Raitakari

    (Turku University Hospital
    University of Turku
    University of Turku and Turku University Hospital)

  • Catriona L. K. Barnes

    (University of Edinburgh)

  • Harry Campbell

    (University of Edinburgh)

  • Peter K. Joshi

    (University of Edinburgh)

  • James F. Wilson

    (Institute of Genetics and Molecular Medicine, University of Edinburgh
    University of Edinburgh)

  • Aaron Isaacs

    (CARIM School for Cardiovascular Diseases, Maastricht Center for Systems Biology (MaCSBio), Department of Biochemistry, and Department of Physiology, Maastricht University)

  • Jan A. Kors

    (University Medical Center Rotterdam)

  • Cornelia M. Duijn

    (Erasmus University Medical Center)

  • Paul L. Huang

    (Massachusetts General Hospital)

  • Vilmundur Gudnason

    (Icelandic Heart Association
    University of Iceland)

  • Tamara B. Harris

    (Laboratory of Epidemiology and Population Sciences, National Institute on Aging, NIH)

  • Lenore J. Launer

    (Laboratory of Epidemiology and Population Sciences, National Institute on Aging, NIH)

  • Albert V. Smith

    (Icelandic Heart Association
    University of Michigan)

  • Erwin P. Bottinger

    (The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai)

  • Ruth J. F. Loos

    (The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai
    The Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai)

  • Girish N. Nadkarni

    (The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai)

  • Michael H. Preuss

    (The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai)

  • Adolfo Correa

    (Jackson Heart Study, Department of Medicine, University of Mississippi Medical Center)

  • Hao Mei

    (University of Mississippi Medical Center)

  • James Wilson

    (University of Mississippi Medical Center)

  • Thomas Meitinger

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    Institute of Human Genetics, Helmholtz Zentrum München - German Research Center for Environmental Health
    Technische Universität München)

  • Martina Müller-Nurasyid

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health
    IBE, Faculty of Medicine, LMU Munich
    Hospital of the Ludwig-Maximilians-University (LMU) Munich)

  • Annette Peters

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    German Center for Diabetes Research
    Institute of Epidemiology, Helmholtz Zentrum München—German Research Center for Environmental Health)

  • Melanie Waldenberger

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    Institute of Epidemiology, Helmholtz Zentrum München—German Research Center for Environmental Health
    Research Unit of Molecular Epidemiology, Helmholtz Zentrum München—German Research Center for Environmental Health)

  • Massimo Mangino

    (Kings College London
    NIHR Biomedical Research Centre at Guy’s and St Thomas’ Foundation Trust)

  • Timothy D. Spector

    (Kings College London)

  • Michiel Rienstra

    (University of Groningen, University Medical Center Groningen)

  • Yordi J. Vegte

    (University of Groningen, University Medical Center Groningen)

  • Pim Harst

    (University of Groningen, University Medical Center Groningen)

  • Niek Verweij

    (University of Groningen, University Medical Center Groningen
    Genomics plc)

  • Stefan Kääb

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    Hospital of the Ludwig-Maximilians-University (LMU) Munich)

  • Katharina Schramm

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health
    Hospital of the Ludwig-Maximilians-University (LMU) Munich)

  • Moritz F. Sinner

    (DZHK (German Centre for Cardiovascular Research), Munich Heart Alliance
    Hospital of the Ludwig-Maximilians-University (LMU) Munich)

  • Konstantin Strauch

    (Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health
    IBE, Faculty of Medicine, LMU Munich)

  • Michael J. Cutler

    (Intermountain Medical Center)

  • Diane Fatkin

    (Molecular Cardiology and Biophysics Division, Victor Chang Cardiac Research Institute
    St. Vincent’s Hospital
    St Vincent’s Clinical School, Faculty of Medicine, UNSW Sydney)

  • Barry London

    (University of Iowa)

  • Morten Olesen

    (University Hospital of Copenhagen
    University of Copenhagen)

  • Dan M. Roden

    (Pharmacology, and Biomedical Informatics, Vanderbilt University Medical Center)

  • M. Benjamin Shoemaker

    (Vanderbilt University Medical Center)

  • J. Gustav Smith

    (Clinical Sciences, Wallenberg Center for Molecular Medicine, Lund University Diabetes Center, Lund University and Skane University Hospital)

  • Mary L. Biggs

    (Cardiovascular Health Research Unit, Department of Medicine, University of Washington
    University of Washington)

  • Joshua C. Bis

    (Cardiovascular Health Research Unit, Department of Medicine, University of Washington)

  • Jennifer A. Brody

    (Cardiovascular Health Research Unit, Department of Medicine, University of Washington)

  • Bruce M. Psaty

    (Cardiovascular Health Research Unit, Department of Medicine, University of Washington
    University of Washington
    Kaiser Permanente Washington Health Research Institute)

  • Kenneth Rice

    (University of Washington)

  • Nona Sotoodehnia

    (Cardiovascular Health Research Unit, Department of Medicine, University of Washington
    University of Washington
    Cardiology Division, University of Washington)

  • Alessandro Grandi

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Christian Fuchsberger

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Cristian Pattaro

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Peter P. Pramstaller

    (Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck)

  • Ian Ford

    (Robertson Center for Biostatistics, University of Glasgow)

  • J. Wouter Jukema

    (Leiden University Medical Center
    Einthoven Laboratory for Experimental Vascular Medicine, Leiden University Medical Center)

  • Peter W. Macfarlane

    (Institute of Health and Wellbeing, College of Medical, Veterinary and Life Sciences, University of Glasgow)

  • Stella Trompet

    (Leiden University Medical Center)

  • Marcus Dörr

    (DZHK (German Centre for Cardiovascular Research)
    Pneumology, Infectious Diseases, Intensive Care Medicine, University Medicine Greifswald)

  • Stephan B. Felix

    (DZHK (German Centre for Cardiovascular Research)
    Pneumology, Infectious Diseases, Intensive Care Medicine, University Medicine Greifswald)

  • Uwe Völker

    (DZHK (German Centre for Cardiovascular Research)
    Interfaculty Institute for Genetics and Functional Genomics; Department of Functional Genomics; University Medicine and University of Greifswald)

  • Stefan Weiss

    (DZHK (German Centre for Cardiovascular Research)
    Interfaculty Institute for Genetics and Functional Genomics; Department of Functional Genomics; University Medicine and University of Greifswald)

  • Aki S. Havulinna

    (Finnish Institute for Health and Welfare
    Institute for Molecular Medicine Finland (FIMM), HiLIFE, University of Helsinki)

  • Antti Jula

    (Finnish Institute for Health and Welfare)

  • Katri Sääksjärvi

    (Finnish Institute for Health and Welfare)

  • Veikko Salomaa

    (Finnish Institute for Health and Welfare)

  • Xiuqing Guo

    (Institute for Translational Genomics and Population Sciences and Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Susan R. Heckbert

    (Cardiovascular Health Research Unit and Department of Epidemiology, University of Washington)

  • Henry J. Lin

    (Institute for Translational Genomics and Population Sciences and Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Jerome I. Rotter

    (Institute for Translational Genomics and Population Sciences and Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Kent D. Taylor

    (Institute for Translational Genomics and Population Sciences and Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Jie Yao

    (Institute for Translational Genomics and Population Sciences, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Renée Mutsert

    (Leiden University Medical Center)

  • Arie C. Maan

    (Leiden University Medical Center)

  • Dennis O. Mook-Kanamori

    (Leiden University Medical Center
    Leiden University Medical Center)

  • Raymond Noordam

    (Leiden University Medical Center)

  • Francesco Cucca

    (University of Sassari)

  • Jun Ding

    (Laboratory of Genetics and Genomics, NIA/NIH)

  • Edward G. Lakatta

    (Laboratory of Cardiovascular Science, NIA/NIH)

  • Yong Qian

    (Laboratory of Genetics and Genomics, NIA/NIH)

  • Kirill V. Tarasov

    (Laboratory of Cardiovascular Science, NIA/NIH)

  • Daniel Levy

    (Population Sciences Branch, Division of Intramural Research, National Heart, Lung, and Blood Institute
    National Heart Lung and Blood Institute’s and Boston University’s Framingham Heart Study)

  • Honghuang Lin

    (National Heart Lung and Blood Institute’s and Boston University’s Framingham Heart Study
    Boston University School of Medicine)

  • Christopher H. Newton-Cheh

    (The Broad Institute of MIT and Harvard
    Harvard Medical School and Massachusetts General Hospital)

  • Kathryn L. Lunetta

    (National Heart Lung and Blood Institute’s and Boston University’s Framingham Heart Study
    Boston University School of Public Health)

  • Alison D. Murray

    (The Institute of Medical Sciences, Aberdeen Biomedical Imaging Centre, University of Aberdeen)

  • David J. Porteous

    (Centre for Genomic and Experimental Medicine, Institute of Genetics & Molecular Medicine, University of Edinburgh, Western General Hospital
    Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh)

  • Blair H. Smith

    (Division of Population Health and Genomics, Ninewells Hospital and Medical School, University of Dundee)

  • Bruno H. Stricker

    (University Medical Center Rotterdam)

  • André Uitterlinden

    (Human Genotyping Facility Erasmus MC University Medical Center Rotterdam)

  • Marten E. Berg

    (University Medical Center Rotterdam)

  • Jeffrey Haessler

    (Fred Hutchinson Cancer Research Center, Division of Public Health Sciences)

  • Rebecca D. Jackson

    (Ohio State University)

  • Charles Kooperberg

    (Fred Hutchinson Cancer Research Center, Division of Public Health Sciences)

  • Ulrike Peters

    (Fred Hutchinson Cancer Research Center, Division of Public Health Sciences)

  • Alexander P. Reiner

    (Fred Hutchinson Cancer Research Center, Division of Public Health Sciences
    University of Washington)

  • Eric A. Whitsel

    (University of North Carolina)

  • Alvaro Alonso

    (Rollins School of Public Health, Emory University)

  • Dan E. Arking

    (McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine)

  • Eric Boerwinkle

    (Human Genetics Center, University of Texas Health Science Center at Houston)

  • Georg B. Ehret

    (Cardiology, Geneva University Hospitals)

  • Elsayed Z. Soliman

    (Epidemiological Cardiology Research Center, Wake Forest School of Medicine)

  • Christy L. Avery

    (University of North Carolina
    University of North Carolina)

  • Stephanie M. Gogarten

    (University of Washington)

  • Kathleen F. Kerr

    (University of Washington)

  • Cathy C. Laurie

    (University of Washington)

  • Amanda A. Seyerle

    (Division of Pharmaceutical Outcomes and Policy, University of North Carolina)

  • Adrienne Stilp

    (University of Washington)

  • Solmaz Assa

    (University of Groningen, University Medical Center Groningen)

  • M. Abdullah Said

    (University of Groningen, University Medical Center Groningen)

  • M. Yldau van der Ende

    (University of Groningen, University Medical Center Groningen)

  • Pier D. Lambiase

    (Barts Heart Centre, St Bartholomews Hospital
    University College London)

  • Michele Orini

    (Barts Heart Centre, St Bartholomews Hospital
    University College London)

  • Julia Ramirez

    (Queen Mary University of London
    University College London)

  • Stefan Duijvenboden

    (Queen Mary University of London
    University College London)

  • David O. Arnar

    (deCODE genetics/Amgen, Inc.
    University of Iceland
    Landspitali University Hospital)

  • Daniel F. Gudbjartsson

    (deCODE genetics/Amgen, Inc.
    University of Iceland)

  • Hilma Holm

    (deCODE genetics/Amgen, Inc.)

  • Patrick Sulem

    (deCODE genetics/Amgen, Inc.)

  • Gudmar Thorleifsson

    (deCODE genetics/Amgen, Inc.)

  • Rosa B. Thorolfsdottir

    (deCODE genetics/Amgen, Inc.
    University of Iceland)

  • Unnur Thorsteinsdottir

    (deCODE genetics/Amgen, Inc.
    University of Iceland)

  • Emelia J. Benjamin

    (National Heart Lung and Blood Institute’s and Boston University’s Framingham Heart Study
    Section of Cardiovascular Medicine and Section of Preventive Medicine, Department of Medicine, Boston University School of Medicine
    Boston University School of Public Health)

  • Andrew Tinker

    (Queen Mary University of London
    Barts Cardiovascular Biomedical Research Centre, Queen Mary University of London)

  • Kari Stefansson

    (deCODE genetics/Amgen, Inc.
    University of Iceland)

  • Patrick T. Ellinor

    (Massachusetts General Hospital
    The Broad Institute of MIT and Harvard
    Cardiac Arrhythmia Service, Massachusetts General Hospital)

  • Yalda Jamshidi

    (Genetics Research Centre, Molecular and Clinical Sciences Institute, St George’s, University of London)

  • Steven A. Lubitz

    (Massachusetts General Hospital
    The Broad Institute of MIT and Harvard
    Cardiac Arrhythmia Service, Massachusetts General Hospital)

  • Patricia B. Munroe

    (Queen Mary University of London
    Barts Cardiovascular Biomedical Research Centre, Queen Mary University of London)

Abstract

The electrocardiographic PR interval reflects atrioventricular conduction, and is associated with conduction abnormalities, pacemaker implantation, atrial fibrillation (AF), and cardiovascular mortality. Here we report a multi-ancestry (N = 293,051) genome-wide association meta-analysis for the PR interval, discovering 202 loci of which 141 have not previously been reported. Variants at identified loci increase the percentage of heritability explained, from 33.5% to 62.6%. We observe enrichment for cardiac muscle developmental/contractile and cytoskeletal genes, highlighting key regulation processes for atrioventricular conduction. Additionally, 8 loci not previously reported harbor genes underlying inherited arrhythmic syndromes and/or cardiomyopathies suggesting a role for these genes in cardiovascular pathology in the general population. We show that polygenic predisposition to PR interval duration is an endophenotype for cardiovascular disease, including distal conduction disease, AF, and atrioventricular pre-excitation. These findings advance our understanding of the polygenic basis of cardiac conduction, and the genetic relationship between PR interval duration and cardiovascular disease.

Suggested Citation

  • Ioanna Ntalla & Lu-Chen Weng & James H. Cartwright & Amelia Weber Hall & Gardar Sveinbjornsson & Nathan R. Tucker & Seung Hoan Choi & Mark D. Chaffin & Carolina Roselli & Michael R. Barnes & Borbala M, 2020. "Multi-ancestry GWAS of the electrocardiographic PR interval identifies 202 loci underlying cardiac conduction," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15706-x
    DOI: 10.1038/s41467-020-15706-x
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    Cited by:

    1. Shaan Khurshid & Julieta Lazarte & James P. Pirruccello & Lu-Chen Weng & Seung Hoan Choi & Amelia W. Hall & Xin Wang & Samuel F. Friedman & Victor Nauffal & Kiran J. Biddinger & Krishna G. Aragam & Pu, 2023. "Clinical and genetic associations of deep learning-derived cardiac magnetic resonance-based left ventricular mass," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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